Ranking lifestyle risk factors for cervical cancer among Black women: A case-control study from Johannesburg, South Africa

Mwiza Gideon Singini; Freddy Sitas; Debbie Bradshaw; Wenlong Carl Chen; Melitah Motlhale; Abram Bunya Kamiza; Chantal Babb de Villiers; Cathryn M. Lewis; Christopher G. Mathew; Tim Waterboer; Robert Newton; Mazvita Muchengeti; Elvira Singh

doi:10.1371/journal.pone.0260319

Peer Review History

Original SubmissionJune 9, 2021
10 Sep 2021 Decision Letter - Nülüfer Erbil, Editor PONE-D-21-18984Ranking lifestyle risk factors for cervical cancer among Black women: A Case-Control study from Johannesburg, South AfricaPLOS ONE Dear Dr. Singh, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Oct 25 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. 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Specifically, 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. 4. Please include your actual numerical p-values in Table 2 5. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability. 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We will update your Data Availability statement to reflect the information you provide in your cover letter. Additional Editor Comments (if provided): [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ******** 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: Dear Authors, Although the manuscript is well statistics, according to previous references, all information that we had known with the lifestyle risk factors for cervical cancer among Black women, like these related references that authors cited, so for more contribution, suggest authors clarify and mentation what these JCS data that the medical system or policy-related cervical cancer could improve. Thank you for your effort. Reviewer #2: This is a good study to determine the risk factors for cervical cancer, one of the most common cancer types in women.It is a case-control study on a large sample that will contribute to the literature. ****** 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. 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.0260319.r001
Revision 1
27 Sep 2021 Author Response 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. Response : Thank you for your comment: The manuscript has been formatted and meets PLOSE ONE’s style requirement. 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 the survey or 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. If the questionnaire is published, please provide a citation to the (1) questionnaire and/or (2) original publication associated with the questionnaire. Response: Thank you for your comment: Additional information regarding the questionnaire has been added to the manuscript line 141-147. Page 5, as follows: The questionnaire included questions on the following: socio-demographic factors such as; place of birth and residence, marital status, education, the home language of parents. Enviromental exposures such as method of cooking and heating. Lifestyle factors such as; smoking by type of tobacco and amounts smoked, snuff (sniffed tobacco) use, alcohol consumption by type, parity, use of oral and injectable contraceptives, number of sexual partners. On occupations, self-reported use of Anti-Retroviral Therapy (ART) (since 2005), PAP smear (2001) and self-reported history of diabetes. The questionnaire has also been included as a Supplementary material. 3. In your ethics statement in the Methods section and in the online submission form, please provide additional information about the data used in your retrospective study. Specifically, 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. Response: Thank you for your comment: Information on data anonymization has been discussed in the revised manuscript lines 147-152 page 5 as follows: The JCS and the current study were approved by the University of the Witwatersrand Human Research Ethics Committee (Medical) (certificate number for the current study. M200252). In the JCS, participants gave written informed or wittnessd consent to once-off interview and optional blood draw and to have their information and blood sample anonymized. Any future investigations require approval of the University of the Witwatersrand Human Research Ethics Committee HREC [16]. The information has also been included in the online submission form. 4. Please include your actual numerical p-values in Table 2. Response: Thank you for your comment: The actual numerical p-values in Table 2 have been added. Pages 13-15 5. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability. Response: Data cannot be shared publicly because of ethics policy at University of Witwatersrand, whereby any new analyses require Human Research Ethics Committee approval. Data are available from the SA-NCR /National Health Laboratory Services. (contact : elviras@nicd.ac.za) for researchers who meet the relevant ethics criteria for access to these data. Reviewer 1: Although the manuscript is well statistics, according to previous references, all information that we had known with the lifestyle risk factors for cervical cancer among Black women, like these related references that authors cited, so for more contribution, suggest authors clarify and mentation what these JCS data that the medical system or policy-related cervical cancer could improve. Thank you for your effort. Response: Thank you very much for your question: Our findings have important policy implications. Firstly, ranking of lifestyle risk factors for cervical cancer can inform medical systems on which key risk factors to integrate in cervical cancer education programmes. This would help health care personnel that are involved in advising women about cervical cancer screening, to understand the public-health gains that result by minimizing the risk of each factor. Second, most of the previous studies were conducted in women of European ancestry. We have amended the concluding sentence as follows: In conclusion, in order of importance, HIV-positivity, educational attainment, parity, hormonal contraceptive use, alcohol, smoking and residing in rural area were associated with cervical cancer among black South African women. These women should be prioritized in opportunistic or planned cervical cancer screening programs. Our findings confirm previosuly known cofactors of cervical cancer and provide a rank order of risks that could be used locally to target educational messaging and appropriate interventions. Reviewer #2: This is a good study to determine the risk factors for cervical cancer, one of the most common cancer types in women. It is a case-control study on a large sample that will contribute to the literature. We thank the reviewer for their comments. Attachments Attachment Submitted filename: Response to the reviewers.docx https://doi.org/10.1371/journal.pone.0260319.r002
22 Oct 2021 Decision Letter - Nülüfer Erbil, Editor PONE-D-21-18984R1Ranking lifestyle risk factors for cervical cancer among Black women: A Case-Control study from Johannesburg, South AfricaPLOS ONE Dear Dr. Singh, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Dec 06 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: 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, Nülüfer Erbil, Ph.D, Prof. 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) 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: 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: Dear authors, The revised manuscript is better, but Result section, “A total of, 26,263 participants were enrolled in the JCS between 1995 to 2016. A total of 9,249 women were included in this study of whom 3,540 (38.3%) had invasive cervical cancer (cases) and 5,709 were designated as controls, (61.7%) as described in Figure 1.”The figure is vague, not easy to read follow the authors’ context, please clarify. Thank you. Reviewer #2: An original study done in a special group. It is a good work that will contribute to the literature. ****** 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 [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.0260319.r003
Revision 2
29 Oct 2021 Author Response Please review your reference list to ensure that it is complete and correct. Response: Reference list has been reviewed, it is complete and correct Reviewer #1: Dear authors, The revised manuscript is better, but Result section, “A total of, 26,263 participants were enrolled in the JCS between 1995 to 2016. A total of 9,249 women were included in this study of whom 3,540 (38.3%) had invasive cervical cancer (cases) and 5,709 were designated as controls, (61.7%) as described in Figure 1.”The figure is vague, not easy to read follow the authors’ context, please clarify. Thank you. Response: Thank you so much for your question: Figure 1 has been revised for easy to read. The information on the results section regarding figure 1, has been placed in the methods section where the description of exclusion was done. (lines 161-184 of the manuscript). A total of, 26,263 participants were enrolled in the JCS between 1995 to 2016. We excluded 8,677 (33.0%) males, 3,105 (17.6%) women older than 65 years or younger than 25 years, 663 (4.6%) non-cancer participants, 945(6.9%) non-South Africans, 1 with missing data, 640 (5.0%) with missing HIV-status and 691 (5.7%) with primary site unknown malignancy. From those with cancer of the cervix, we excluded International Classification of Diseases for Oncology (ICD-O) codes such as ( ICD-O morphology: 8010-8050 epithelial neoplasm (n=98, 2.6%), (ICD-O morphology: 8000 and 8001) not otherwise specified (n=9, 0.2%), (ICD-O morphology: 8560, 8570 and 8574) complex epithelial neoplasms (n=108, 2.8%) and other minor histological types (ICD-O morphology: 8098,8170, 8200, 8272, 8310, 8441,8460, 8480-8490, 8500,8650 and 8931-9100) (n=64, 1.7%) Figure 1. Figure 1 also outlines the criteria used to select cases and controls. The control groups were arranged into four sets. Each set comprised of women diagnosed with different cancer types that are unrelated to the exposures of interest (these being infection, smoking, alcohol, parity, number of sexual partners and use of hormonal contraceptives) [16–18] Figure 1. Cancer controls unrelated to infection constituted the highest number of controls S1 Table. The demographic analyses excluded 2,009 (26.0%) women with cancers related to infections. Analyses relating to smoking excluded 2,218 (28.7%) women with cancers related to smoking and infections. Analyses relating to alcohol excluded 6,800 (60.4%) women with cancers related to alcohol and infections. Analyses relating to hormonal contraceptives excluded 6,458 (57.4%) women with cancers related to hormonal contraceptives and infections. Of the remaining 9,249 women, 3,540 (38.3%) had invasive cervical cancer (defined as cases) and 5,709 (61.7%) had other cancers (defined as controls) that were not related to the exposure of interest Figure1. Reviewer #2: An original study done in a special group. It is a good work that will contribute to the literature. We thank the reviewer for their comments. Attachments Attachment Submitted filename: Response to the reviewers_25 October 2021.docx https://doi.org/10.1371/journal.pone.0260319.r004
8 Nov 2021 Decision Letter - Nülüfer Erbil, Editor Ranking lifestyle risk factors for cervical cancer among Black women: A Case-Control study from Johannesburg, South Africa PONE-D-21-18984R2 Dear Dr. Singh, 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, Nülüfer Erbil, Ph.D, Prof. 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: (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: (No Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: (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 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: (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: DEAR Author, The title with "Ranking lifestyle risk factors for cervical cancer among Black women: A Case-Control study from Johannesburg, South Africa. " revised manuscript is much better. I have no other comments. Thank you. ****** 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.0260319.r005
Formally Accepted
17 Nov 2021 Acceptance Letter - Nülüfer Erbil, Editor PONE-D-21-18984R2 Ranking lifestyle risk factors for cervical cancer among Black women: A Case-Control study from Johannesburg, South Africa Dear Dr. Singh: 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. Nülüfer Erbil Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0260319.r006

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