SARS-CoV-2 infections among Australian passengers on the Diamond Princess cruise ship: A retrospective cohort study

Liz J. Walker; Tudor A. Codreanu; Paul K. Armstrong; Sam Goodwin; Abigail Trewin; Emma Spencer; Samantha M. Colquhoun; Dianne M. Stephens; Rob W. Baird; Nicholas M. Douglas; Danielle Cribb; Rhonda Owen; Paul Kelly; Martyn D. Kirk

doi:10.1371/journal.pone.0255401

Peer Review History

Original SubmissionFebruary 9, 2021
30 Mar 2021 Decision Letter - Eric HY Lau, Editor PONE-D-20-38119 SARS-CoV-2 infections among Australian passengers on the Diamond Princess cruise ship: a retrospective cohort study. PLOS ONE Dear Dr. Walker, 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 Authors are expected to address all the criticisms by all Reviewers. In particular, please provide the rationale of the modelling strategy, potential impact of non-response (Reviewers #1), the impact of asymptomatic infections in the results and conclusion, and further clarify the timing and type of actions carried out in Japan or Australia (Reviewer #2). In additional to the above comments, please address, Could the authors add more discussion on how the results will inform infection control policy while we expect cruise ship is likely to resume in the near future, where various non-pharmaceutical interventions are now more widely accepted and some passengers are vaccinated. Line 179-180. “The median time-to-clearance of SARS-CoV-2 infection was lower for asymptomatic cases.” Please replace the word “lower” with “shorter”. Table 2. Range, please clarify the meaning of “1 -> 14” Please submit your revised manuscript by May 14 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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The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. Thank you for including your ethics statement: "The Australian National University Human Research Ethics Committee (Protocol 2017/909) has a standing approval for outbreak investigations involving staff and students. The investigation was consistent with routine Australian public health activities during outbreaks of infectious disease.". Please provide additional details regarding participant consent. As your study also involves a retrospective analysis of medical records or archived samples, please ensure that you have discussed whether all data were fully anonymized before you accessed them and/or whether the IRB or ethics committee waived the requirement for informed consent. If patients provided informed written consent to have data from their medical records used in research, please include this information. Once you have amended this statement in the Methods section of the manuscript, please add the same text to the “Ethics Statement” field of the submission form (via “Edit Submission”). For additional information about PLOS ONE ethical requirements for human subjects research, please refer to http://journals.plos.org/plosone/s/submission-guidelines#loc-human-subjects-research. 3. We note that you have included the phrase “data not shown” in your manuscript. Unfortunately, this does not meet our data sharing requirements. PLOS does not permit references to inaccessible data. We require that authors provide all relevant data within the paper, Supporting Information files, or in an acceptable, public repository. Please add a citation to support this phrase or upload the data that corresponds with these findings to a stable repository (such as Figshare or Dryad) and provide and URLs, DOIs, or accession numbers that may be used to access these data. Or, if the data are not a core part of the research being presented in your study, we ask that you remove the phrase that refers to these data. Additional Editor Comments (if provided): The Authors are expected to address all the criticisms by all Reviewers. In particular, please provide the rationale of the modelling strategy, potential impact of non-response (Reviewers #1), the impact of asymptomatic infections in the results and conclusion, and further clarify the timing and type of actions carried out in Japan or Australia (Reviewer #2). In additional to the above comments, please address, 1. Could the authors add more discussion on how the results will inform infection control policy while we expect cruise ship is likely to resume in the near future, where various non-pharmaceutical interventions are now more widely accepted and some passengers are vaccinated. 2. Line 179-180. “The median time-to-clearance of SARS-CoV-2 infection was lower for asymptomatic cases.” Please replace the word “lower” with “shorter”. 3. Table 2. Range, please clarify the meaning of “1 -> 14” [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: Yes 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: This is a retrospective cohort study about Australian passengers on the Diamond Princess which shows the natural history of COVID-19. This study highlighted challenges of cruise ship-related COVID-19 outbreak and the tips they learned are worth publishing. However, I have some comments to improve the manuscript before publication. Major comments: 1. The authors conducted Cox proportional hazards regression analysis for the prediction of time-to-clearance of SARS-CoV-2, but little is discussed or shown about the model. This explanation will facilitate readers to understand the findings of the study, including why the authors categorize the age as a binary variable. 2. Age, gender and race may influence the development of COVID-19. It is better to describe their distribution among those who censored (who did not respond to the questionnaire), if the information is available. Minor comment: Line 226. “Viral culture suggest” → “Results of viral culture suggest”. Reviewer #2: The authors presented the retrospective cohort data from Australian passengers in the Diamond Princess outbreak. The authors characterized and classified the passengers into groups and determined the factors that could affect COVID-19 transmissibility and infectivity. It is clear that the information presented in the manuscript is important to the control of COVID-19. Nevertheless, the event happened in the early period of the pandemic. The epidemic and observational data in the manuscript have been thoroughly covered and discussed in many COVID-19 articles. Areas for improvement: 1. Considering the available published papers on the Diamond Princess cohort, the Introduction and Discussion sections could be significantly improved by citing and discussing those findings. 2. Line 105: the lack of RT-PCR testing in the repatriated group without known symptoms is a major concern since the majority of the infected individuals might not be symptomatic. This could mean that the findings were biased toward symptomatic cases only, which would negate all the conclusions. It will be helpful for the authors to address this point and rewrite the manuscript accordingly. 3. Line 178: it appears here that there is the data from asymptomatic infected individuals. This is in contrary to point #2 that RT-PCR testing was not done in this group. Is the data from Japan or obtained after repatriation? Please also list the criteria for clearance used in Australia at that time. 4. The Discussion section has several points on the best practice for COVID-19 prevention (examples in Line 257, 258 and 262). However, they are not related to the data shown in the manuscript. If they are presented, the data leading to these points will be needed. 5. In the Methods section, it is difficult to fully understand which activities were done in Australia or in Japan and when they were performed. The authors can clarify them in the text or introduce the information in either Figure 1 or Figure 2. 6. Line 89: the name of the document is incorrect. Please use its full name. ****** 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: No Reviewer #2: 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. 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Revision 1
23 May 2021 Author Response Reviewer 1 comments: 1. The authors conducted Cox proportional hazards regression analysis for the prediction of time-to-clearance of SARS-CoV-2, but little is discussed or shown about the model. This explanation will facilitate readers to understand the findings of the study, including why the authors categorize the age as a binary variable. Response: This was a very simple survival analysis to account for censoring. Evidence at the time of the outbreak indicated older age may have been a risk factor for infection and longer shedding. Due to the small sample size we were unable to separate age into broader age group, so elected for a binary age group category. Our model found age was not statistically significant and this is likely due to the intensive social mixing that occurs on a cruise ship. 2. Age, gender and race may influence the development of COVID-19. It is better to describe their distribution among those who censored (who did not respond to the questionnaire), if the information is available. Response: Unfortunately, we do not know the date of symptom onset for individuals who were unable to be contacted or declined participation, therefore we are unable to include all positive SARS-CoV-2 Australian cases in the Cox regression. Our response rate from SARS-CoV-2 cases was high (78%) and we believe the current model would not differ much if we had data on the 12 censored individuals. 3. Line 226. “Viral culture suggest” → “Results of viral culture suggest”. Response: Sentence has been amended to ‘Results of viral culture suggest…’ Reviewer 2 comments: 1. Considering the available published papers on the Diamond Princess cohort, the Introduction and Discussion sections could be significantly improved by citing and discussing those findings. Response: A literature review was conducted on 29 April 2021 using search term Diamond Princess. The introduction and discussion have been updated to incorporate findings from other studies of the Diamond Princess cohort. 2. Line 105: the lack of RT-PCR testing in the repatriated group without known symptoms is a major concern since the majority of the infected individuals might not be symptomatic. This could mean that the findings were biased toward symptomatic cases only, which would negate all the conclusions. It will be helpful for the authors to address this point and rewrite the manuscript accordingly. Response: At the time of this outbreak, routine screening was not conducted of the entire cohort that was repatriated. However, all passengers were screened on board the Diamond Princess prior to their repatriation. At the quarantine facility, there was a sensitive screening system based on daily temperature checks and symptoms. There may have been a bias towards toward symptomatic cases. However, this is normal in outbreak investigations for infectious agents where screening of entire cohorts is rare. Our findings and conclusions would be biased toward the null. We have noted this in the discussion. 3. Line 178: it appears here that there is the data from asymptomatic infected individuals. This is incontrary to point #2 that RT-PCR testing was not done in this group. Is the data from Japan or obtained after repatriation? Please also list the criteria for clearance used in Australia at that time. Response: As we mentioned in the manuscript, all passengers were screened for SARS-CoV-2 on board the Diamond Princess. The criteria for clearance are listed in the methods. We have added text to clarify that this applied to both passengers in Japan and Australia. 4. The Discussion section has several points on the best practice for COVID-19 prevention (examples in Line 257, 258 and 262). However, they are not related to the data shown in the manuscript. If they are presented, the data leading to these points will be needed. Response: We disagree, these are our reflections on the findings from the experience of investigating this outbreak. These are public health practices that prevent infections on board cruise ships. Where possible, we have referenced our statements. 5. In the Methods section, it is difficult to fully understand which activities were done in Australia or in Japan and when they were performed. The authors can clarify them in the text or introduce the information in either Figure 1 or Figure 2. Response: The majority of work for this investigation was conducted in Australia. The exceptions were the laboratory work, where some of this occurred in Japan, which is identified. We have noted in the manuscript that interviews were conducted on-site at the quarantine facility or via telephone for people remaining in Japan. 6. Line 89: the name of the document is incorrect. Please use its full name. Response: The name of the document has been correct to ‘The first few X cases and contacts (FFX) investigation protocol for coronavirus disease 2019 (COVID-19)‎’. Editors comments: 1. Could the authors add more discussion on how the results will inform infection control policy while we expect cruise ship is likely to resume in the near future, where various nonpharmaceutical interventions are now more widely accepted, and some passengers are vaccinated. Response: We have added the following paragraph to the final part of the discussion: ‘The results of this investigation show the highly infectious nature of SARS-CoV-2 on cruise ships and the consequences in an older vulnerable population. In the future, non-pharmaceutical interventions along with vaccination of travellers will prove important requirments for resumption of cruises.’ 2. Line 179-180. “The median time-to- clearance of SARS-CoV-2 infection was lower for asymptomatic cases.” Please replace the word “lower” with “shorter”. Response: The sentence has been amended to read ‘The median time-to- clearance of SARS-CoV-2 infection was shorter for asymptomatic cases.’ 3. Table 2. Range, please clarify the meaning of “1 -> 14” Response: >14 days indicates the symptom was still experienced at the time of the questionnaire. A footnote has been added to Table 2. 4. Please provide additional details regarding participant consent. As your study also involves a retrospective analysis of medical records or archived samples, please ensure that you have discussed whether all data were fully anonymized before you accessed them and/or whether the IRB or ethics committee waived the requirement for informed consent. If patients provided informed written consent to have data from their medical records used in research, please include this information. Once you have amended this statement in the Methods section of the manuscript, please add the same text to the “Ethics Statement” field of the submission form (via “Edit Submission”). Response: This paper details the Australian response to an outbreak of SARS-CoV-2 conducted under public health legislation. We have detailed that in manuscript. SARS-CoV-2 pathology results conducted in Japan were obtained under the International Health Regulations (2005) between the Japanese IHR focal point to the Australian IHR focal point. SARS-CoV-2 pathology results conducted in Australia were obtained under the National Health Security Act (2007), states and territories have agreed data sharing for the national surveillance of diseases on the National Notifiable Disease List (NNDL) with the Australian Government. All investigators participated in this as part of their role as public health professionals and operated under public health legislation. The lead author was a Master of Applied Epidemiology scholar at the Australian National University at the time of this investigation. The Australian National University has a standing approval for MAE scholars to investigate outbreaks and evaluate surveillance, which is already documented in the manuscript. Participation was voluntary and participants provided verbal consent at the time of the survey, which we have detailed in the manuscript and the ‘ethics statement’. No medical records were obtained, information regarding medical treatment (x-ray, CT-scans) were obtained verbally from each case’s recall. 5. We note that you have included the phrase “data not shown” in your manuscript. Unfortunately, this does not meet our data sharing requirements. PLOS does not permit references to inaccessible data. We require that authors provide all relevant data within the paper, Supporting Information files, or in an acceptable, public repository. Please add a citation to support this phrase or upload the data that corresponds with these findings to a stable repository (such as Figshare or Dryad) and provide and URLs, DOIs, or accession numbers that may be used to access these data. Or, if the data are not a core part of the research being presented in your study, we ask that you remove the phrase that refers to these data. Response:We have deleted the sentences that references ‘data not shown’ from the manuscript. Attachments Attachment Submitted filename: PONE-D-20-38119 Response to reviewers and editor_FINAL.docx https://doi.org/10.1371/journal.pone.0255401.r002
16 Jul 2021 Decision Letter - Eric HY Lau, Editor SARS-CoV-2 infections among Australian passengers on the Diamond Princess cruise ship: a retrospective cohort study. PONE-D-20-38119R1 Dear Dr. Walker, 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, Eric HY Lau, Ph.D. 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 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: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: 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 Reviewer #2: 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 Reviewer #2: 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: (No Response) Reviewer #2: The manuscript has been satisfactorily revised. I would like to thank the authors for conducting this important study. ****** 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 Reviewer #2: No https://doi.org/10.1371/journal.pone.0255401.r003
Formally Accepted
27 Aug 2021 Acceptance Letter - Eric HY Lau, Editor PONE-D-20-38119R1 SARS-CoV-2 infections among Australian passengers on the Diamond Princess cruise ship: a retrospective cohort study. Dear Dr. Walker: 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. Eric HY Lau Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0255401.r004

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