Investigation of superspreading COVID-19 outbreak events in meat and poultry processing plants in Germany: A cross-sectional study

Roman Pokora; Susan Kutschbach; Matthias Weigl; Detlef Braun; Annegret Epple; Eva Lorenz; Stefan Grund; Juergen Hecht; Helmut Hollich; Peter Rietschel; Frank Schneider; Roland Sohmen; Katherine Taylor; Isabel Dienstbuehl

doi:10.1371/journal.pone.0242456

Peer Review History

Original SubmissionDecember 17, 2020
9 Feb 2021 Decision Letter - Sergio A. Useche, Editor PONE-D-20-37878 Investigation of superspreading COVID-19 outbreaks events in meat and poultry processing plants in Germany: A cross-sectional study PLOS ONE Dear Dr. Pokora, 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. Your paper has been scientifically assessed, and the comments provided by our reviewer provide good account of the good quality of the work you submitted, However, the reviewer asks for some improvements and clarifications (most of them relatively minor) before considering suggesting the acceptance of the paper in PLOS ONE. Please ensure to respond all them with enough level of detail and seiousness during your revisions. Therefore, I will be able to make an editorial decision as soon as I receive the second reviewer's report. Please submit your revised manuscript by Mar 26 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 We look forward to receiving your revised manuscript. Kind regards, Sergio A. Useche, Ph.D. Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1) Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. 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) Please include additional information regarding the survey or questionnaire used in the study and ensure that you have provided sufficient details that others could replicate the analyses. For instance, if you developed a questionnaire as part of this study and it is not under a copyright more restrictive than CC-BY, please include a copy, in both the original language and English, as Supporting Information, or include a citation if it has been published previously. 3) In the Methods, please discuss whether and how the questionnaire was validated and/or pre-tested. If these did not occur, please provide the rationale for not doing so. 4) Please provide further details on sample size and power calculations. 5) In statistical methods, please refer to any post-hoc corrections to correct for multiple comparisons during your statistical analyses. If these were not performed please justify the reasons. Please refer to our statistical reporting guidelines for assistance (https://journals.plos.org/plosone/s/submission-guidelines.#loc-statistical-reporting). 6) In your statistical analyses, please state whether you accounted for clustering by locality, i.e, processing plant. For example, did you consider using multilevel models? 7) In your discussions and conclusions please take care to avoid statements implying causality from correlational research. For example, avoid the use of terms such as “effect of” or “resulted in." Instead consistently use terms such as "associated with" or "associations." 8) We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially identifying or sensitive patient information) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. Please see http://www.bmj.com/content/340/bmj.c181.long for guidelines on how to de-identify and prepare clinical data for publication. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. We will update your Data Availability statement on your behalf to reflect the information you provide. [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 authors have conducted a cross-sectional analysis of meat processing plants to assess factors associated with risk for transmission of COVID-19. They surveyed 26 plants and included 7 companies with more than 10 cases in their analyses. The results identified lack of social distancing, cool temperature and lack of air exchange as factors associated with higher rates of transmission. These findings are consistent with other reports and provide companies with guidance for reducing the risk of transmission in their facilities. While useful, there are several issues that need to be addressed. The survey identified plants with a range of infection rates. There was no comparison to identify differences between plants with high infection rates versus low infection rates. It seems that this could have been useful, and there should be some comment about why this wasn’t pursued, or if it was pursued, why it wasn’t reported. Line 61-64. It is not clear how contract workers mentioned here relate to the temporary or contract workers who comprised the main study population. It is somewhat confusing throughout to understand the differences between permanent, contract and temporary workers. Please elaborate. Lines 110-111 The distribution of companies by cases is based on the interval June-September? Line 112 What is “paper and pencil questionnaire”? Is this just to distinguish from an online survey? Line 142 “point prevalence” seems really to be more of a period-based incidence measure. Line 147 Why were there no comparisons between plants with different categories of infection? Line 150 Is the difference between fixed breaks with or with time shifts a reflection on whether every takes a break at the same time or not? This could be clarified. Line 162 The calculation assumes that all shifts have the same number of employees. Is that correct? Lines 191-194 Are these calculations manipulations of the model to predict outcomes for defined exposure levels? This warrants a bit more description. Line 210 What does it mean that one plant took part although it was not contacted? Table 1 Why were employees excluded? In Table 1 there is a column heading for contract workers. In Table 3 the corresponding column headings mentions regular workers. These appear to be the same and should be called the same. ****** 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 [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.0242456.r001
Revision 1
16 Apr 2021 Author Response Comments of the editor and our replies: 1) Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. 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 Thank you. We revised the headings and tables. 2) Please include additional information regarding the survey or questionnaire used in the study and ensure that you have provided sufficient details that others could replicate the analyses. For instance, if you developed a questionnaire as part of this study and it is not under a copyright more restrictive than CC-BY, please include a copy, in both the original language and English, as Supporting Information, or include a citation if it has been published previously. We have added both the original questionnaire in German in the first and final version and a translated version of the final questionnaire as supporting information. 3) In the Methods, please discuss whether and how the questionnaire was validated and/or pre-tested. If these did not occur, please provide the rationale for not doing so. After analyzing the answers for the questionnaire 1, we discovered that we were not able to distinguish between regular, contract and temporary workers and added therefore a new column in a revised version of the questionnaire. Additionally, we adapted the questions about the air conditioning. In version 1 we just collected the proportion of outdoor air and air circulation. After carefully reading the literature we decided that it would be more appropriate to collect information on outdoor air flow and to use this information. After that decision we contacted again the organizations and collected this additional information. We included this in the manuscript in line 135ff. 4) Please provide further details on sample size and power calculations. The first version of the questionnaire was developed to collect information on the outbreaks to better support the organizations we insure. In the second step, we considered whether the data could be analyzed combined. Until this point in time we knew about three of four outbreak events in meat and poultry plants in Germany and could not assess the future extent. Therefore, we did not calculate a sample size calculation. At the time point of the analysis the sample size was sufficiently large, that no formal power analysis was carried out. 5) In statistical methods, please refer to any post-hoc corrections to correct for multiple comparisons during your statistical analyses. If these were not performed please justify the reasons. Please refer to our statistical reporting guidelines for assistance. We understand the concerns from PLOS ONE and agree with the request. For that reason, we do not report P values anywhere in the manuscript. The reasons for doing so: 1. The sample size is sufficiently large that even seemingly trivial differences are likely to be statistically significant. 2. P-values are commonly misinterpreted as the probability that the test hypothesis is true, or as the probability that observed association is due to chance alone. Both are false. In sum, in the present study we do not believe that adding P values or corrected P values would help readers to get a better sense of whether or not the reported characteristics differ across working groups, or that P values and significance testing would add valuable information beyond what is already reported in the manuscript. We hope that the explanations will satisfy you and that you will appreciate our efforts to conform with the STROBE statement and the position of the American Statistical Association (2016). 6) In your statistical analyses, please state whether you accounted for clustering by locality, i.e, processing plant. For example, did you consider using multilevel models? That is a very interesting point and we considered using multilevel models. In our understanding, hierarchical data in our study would be individual data of the workers, such as nationality or the disease status, (subordinate level 1) in the different departments or companies (parent level 2). In our evaluation, we have 2 levels, where level 2 is the parent level and level 1 is the child level. The predictors (UVs) can be at different levels and can be used for predictions. The dependent variable, on the other hand, is always at level 1. Since all the predictors are at level 2 in our study, we decided to evaluate a classical statistical method. 7) In your discussions and conclusions please take care to avoid statements implying causality from correlational research. For example, avoid the use of terms such as “effect of” or “resulted in." Instead consistently use terms such as "associated with" or "associations." Thank you! It was not in our interest to create this impression and we carefully went through the manuscript again and changed the wording. 8) We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially identifying or sensitive patient information) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. Thank you. We made the dataset for the main analysis available and changed our statement: Availability of data and material: All relevant data are within the manuscript and the dataset is available under https://doi.org/10.5281/zenodo.4692642. The legal basis for the collection of the study data is section 1, section 9 paragraph 8, section 14 and 207 of the Social Code (SGB VII) and the statutes of the BGN. All persons involved in the project are subject to the obligation to maintain confidentiality in accordance with Section 35 SGB I. The analysis presents insurance data collected during the legal mandate with ongoing follow-up data collection. Original questionnaires and measurement reports are not made available for the scientific community outside the established and controlled workflows and algorithms. To meet the general idea of verification and reproducibility of scientific findings, we offer access to the original data at the local database in accordance with the data protection protocol upon request at any time. The study team, which constitutes a member of each involved department and the coordinating principal investigator of the study (Dr Pokora) decides on internal and external access of researchers and use of the data based on a research proposal to be supplied by the researcher. Interested researchers make their requests to the coordinating principal investigator of the study (roman.pokora@bgn.de). Comments of the reviewer and our replies: 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 authors have conducted a cross-sectional analysis of meat processing plants to assess factors associated with risk for transmission of COVID-19. They surveyed 26 plants and included 7 companies with more than 10 cases in their analyses. The results identified lack of social distancing, cool temperature and lack of air exchange as factors associated with higher rates of transmission. These findings are consistent with other reports and provide companies with guidance for reducing the risk of transmission in their facilities. While useful, there are several issues that need to be addressed. The survey identified plants with a range of infection rates. There was no comparison to identify differences between plants with high infection rates versus low infection rates. It seems that this could have been useful, and there should be some comment about why this wasn’t pursued, or if it was pursued, why it wasn’t reported. Line 61-64. It is not clear how contract workers mentioned here relate to the temporary or contract workers who comprised the main study population. It is somewhat confusing throughout to understand the differences between permanent, contract and temporary workers. Please elaborate. We have clarified our wording and the problems with the wording. After the evaluation of the first version of the questionnaire we decided to combine contract and temporary workers. The definition and the exact difference of the two groups of temporary and contract workers is not selective and we tried to clarify our use in the method section and added a section in the method part in line 141ff. Lines 110-111 The distribution of companies by cases is based on the interval June-September? Yes, data was collected between June and September 2020. Earliest outbreak by a participant plant was May 2020 and was the first outbreak in a meat processing facility in Germany. Line 112 What is “paper and pencil questionnaire”? Is this just to distinguish from an online survey? Since the companies were given a word document to fill out, we changed this word to “questionnaire”. Line 142 “point prevalence” seems really to be more of a period-based incidence measure. We agree with the reviewer that the wording is here a little bit problematic. The best description is maybe to describe each outbreak as a “point prevalence” and the combined prevalence from all companies a “period-based prevalence”. We clarified that in the manuscript. Line 147 Why were there no comparisons between plants with different categories of infection? We analyzed the differences across plants with different categories of infection. The comparison is unfortunately a little bit problematic because we had to analyze free text and put it in categories. Also, the occupational safety measures display safety measures at different time points. Now we included some intervention and prevention efforts of the facilities (line 234ff) and put a new section in the method part as well in the discussion section. Line 150 Is the difference between fixed breaks with or with time shifts a reflection on whether every takes a break at the same time or not? This could be clarified. Yes. We clarified that and added an explanation: “Fixed breaks without time shift mean that all workers have their breaks at the same time. Fixed breaks with time shift mean that there is a break pattern where different working groups, departments or divisions have different time windows for their break.” Line 162 The calculation assumes that all shifts have the same number of employees. Is that correct? Yes, the assumption is that each shift in a company has the same number of employees. Like we wrote in the discussion the visits in the companies confirmed our assumption about the actual number of potentially exposed subjects during a shift. Lines 191-194 Are these calculations manipulations of the model to predict outcomes for defined exposure levels? This warrants a bit more description. Exactly. These calculations are based on the same model and only the amount of fresh air has been changed. We excluded this from the manuscript, because it does not add any further knowledge to the association of the variables. Line 210 What does it mean that one plant took part although it was not contacted? It means that the parent company has distributed the questionnaire to all of its companies and all companies of the parent company have answered the questionnaire. Therefore, we received one questionnaire from a company we did not write to. Table 1 Why were employees excluded? Employees were excluded when information was missing. We discussed the possibility of imputation, but because our analysis was only possible because working areas in the meat processing area are clearly distinct, we decided that we don’t want to impute missing values, for example for the cleaning personal. Our procedure is explained at the end of the statistical analysis part. In Table 1 there is a column heading for contract workers. In Table 3 the corresponding column headings mentions regular workers. These appear to be the same and should be called the same. We agree and clarified our wording into regular, contract and temporary workers. Thank you for this advice. Attachments Attachment Submitted filename: Reponese to reviewers_20210326.docx https://doi.org/10.1371/journal.pone.0242456.r002
24 May 2021 Decision Letter - Sergio A. Useche, Editor Investigation of superspreading COVID-19 outbreak events in meat and poultry processing plants in Germany: A cross-sectional study PONE-D-20-37878R1 Dear Dr. Pokora, 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, Sergio A. Useche, 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 ******** 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 addressed all relevant comments. The manuscript can now be accepted for 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.0242456.r003
Formally Accepted
28 May 2021 Acceptance Letter - Sergio A. Useche, Editor PONE-D-20-37878R1 Investigation of superspreading COVID-19 outbreak events in meat and poultry processing plants in Germany: A cross-sectional study Dear Dr. Pokora: 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. Sergio A. Useche Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0242456.r004

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