Diagnostic activity impacts lifetime risk of prostate cancer diagnosis more strongly than life expectancy

Andri Wilberg Orrason; Marcus Westerberg; Peter Albertsen; Johan Styrke; David Robinson; Hans Garmo; Pär Stattin

doi:10.1371/journal.pone.0277784

Peer Review History

Original SubmissionAugust 18, 2022
12 Sep 2022 Decision Letter - Donovan Anthony McGrowder, Editor PONE-D-22-23181Diagnostic activity impacts lifetime risk of prostate cancer diagnosis more strongly than life expectancyPLOS ONE Dear Dr. Orrason, 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. ============================== ACADEMIC EDITOR: Please submit your revised manuscript by October 27, 2022. 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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Additional Editor Comments: Dear Dr. Orrason, Your manuscript “Diagnostic activity impacts lifetime risk of prostate cancer diagnosis more strongly than life expectancy” has been assessed by our reviewers. They have raised a number of points which we believe would improve the manuscript and may allow a revised version to be published in PLOS ONE. Their reports, together with any other comments, are below. If you are able to fully address these points, we would encourage you to submit a revised manuscript to PLOS ONE. Regards, Dr. Donovan McGrowder Associate Editor 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: No Reviewer #3: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: No Reviewer #3: 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: No Reviewer #3: No ****** 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 Reviewer #3: 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 very good paper -- and well-written. The authors have shown convincingly that the lifetime risk of a prostate cancer diagnosis is strongly influenced by diagnostic activity and to a lesser degree by life expectancy. I think this information will be useful to a broad segment of medical practitioners. Reviewer #2: In this paper, the authors use their newly developed Proxy‐based Risk‐stratified Incidence Simulation Model (PRISM) to validate this obvious truth, and to describe the interplay between age, incidence, mortality, and diagnostic activity in Swedish men between ages 40-100 to quantify the effect of diagnostic activity and life expectancy on the lifetime risk of a prostate cancer (PCa) diagnosis overall and by risk categories. Overall, this is a simulation study, where the factors being simulated have not been described very well. 1. It is quite clear what the risk categories are – and how the patients were classified. However, it is not quite clear how the ‘diagnostic activity’ was quantified. Greater clarity as to how some men were classified as ‘low diagnostic activity’ vs ‘intermediate’ vs ‘high’ is warranted. 2. Similarly, please explain how ‘life expectancy’ was calculated. 3. Instead of simply a simulated follow up, the authors would benefit from comparing the simulation to a real life follow up, and determine whether that real life experience follows that of the simulation. Reviewer #3: In this manuscript, authors examined the impact of diagnostic activity and life expectancy on the lifetime risk of prostate cancer diagnosis. They employed a state transition simulation model based on Swedish population based data and simulated life trajectories of a large cohort of men from ages 40-100 to estimate the lifetime risk of a prostate cancer diagnosis. Their analyses determined that the lifetime risk of prostate cancer diagnosis is influenced by diagnostic activity. Higher exposure to diagnostic activity resulted in more prostate cancer diagnosis. Men exposed to high diagnostic activity were found to have five fold increased risk of low or intermediate risk prostate cancer and half the risk of high risk prostate cancer as compared to men with low diagnostic activity. Overall, it is a comprehensive study using a large cohort of men with interesting findings. ******** [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
17 Sep 2022 Author Response 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 very good paper -- and well-written. The authors have shown convincingly that the lifetime risk of a prostate cancer diagnosis is strongly influenced by diagnostic activity and to a lesser degree by life expectancy. I think this information will be useful to a broad segment of medical practitioners. RE: We thank reviewer #1 for his/her positive feedback. Reviewer #2: In this paper, the authors use their newly developed Proxy‐based Risk‐stratified Incidence Simulation Model (PRISM) to validate this obvious truth, and to describe the interplay between age, incidence, mortality, and diagnostic activity in Swedish men between ages 40-100 to quantify the effect of diagnostic activity and life expectancy on the lifetime risk of a prostate cancer (PCa) diagnosis overall and by risk categories. Overall, this is a simulation study, where the factors being simulated have not been described very well. 1. It is quite clear what the risk categories are – and how the patients were classified. However, it is not quite clear how the ‘diagnostic activity’ was quantified. Greater clarity as to how some men were classified as ‘low diagnostic activity’ vs ‘intermediate’ vs ‘high’ is warranted. 2. Similarly, please explain how ‘life expectancy’ was calculated. 3. Instead of simply a simulated follow up, the authors would benefit from comparing the simulation to a real life follow up and determine whether that real life experience follows that of the simulation. RE: We thank the reviewer for valuable remarks. The principles of the PRISM-PC simulation model has previously been thoroughly described (reference 8 and 11). We provide a reference to this methods paper and in addition we also provide a brief description of the model under Methods. We argue that a more detailed review of the model components is beyond the scope of this article and would be of little benefit for the readers of PLOSONE. However, if the editor still wants a more detailed description of the model we are of course willing to provide such a paragraph. 1. The diagnostic activity is difficult to quantify as the reviewer correctly points out. Diagnostic activity is based on a broad set of factors, such as uptake and intensity of PSA testing, biopsy frequency, number of biopsy cores taken and more recently use of MRT prostate etc. Long time series of such data are not available for the entire Swedish population. However, the result of high diagnostic activity is earlier diagnosis with increased proportion of men diagnosed with low an intermediate-risk prostate cancer. This proportion was therefore used as a proxy for diagnostic activity. Due to the lack of data on the above factors, the proxy is difficult to translate e.g., PSA testing rates. Instead, we use historical and geographical variations in the proxy due to similar variations in the underlying diagnostic activity from real life scenarios. These were based on ours and others qualitative knowledge of the historical diagnostic activity, motivating the names of the scenarios: low as in Sweden 1992, intermediate as in Sweden 2016 and high as in Stockholm 2014. The relative differences in diagnostic activity are shown in the figure below for clarification: Three levels of the proxy for diagnostic activity; low as in Sweden 1992 (green), intermediate as in Sweden 2016 (blue) and high as in Stockholm 2014 (red). 2. The age-conditional life expectancy of men without a prostate cancer diagnosis was calculated using comparator men without a prostate cancer diagnosis in PCBaSe using an age-period-cohort model using age, calendar period and birth cohort data. Age-period-cohort (APC) models are frequently used to estimate life expectancy (Fay et al. Age-conditional probabilities of developing cancer. Statistics in medicine. 2003, Smittenaar et al. Cancer incidence and mortality projections in the UK until 2035. British journal of cancer. 2016). One of the strengths of our model is that a prostate cancer-free comparator cohort in PCBaSe was used to calculate the life expectancy of men without a prostate cancer diagnosis, whereas most studies are limited to general population life table data which also includes men with prostate cancer. Also, the model allowed us to extrapolate outside of observed calendar periods in order to explore hypothetical improvements in life-expectancy. 3. Correct. Real-life data would certainly be the ideal choice for our study hypothesis. However, this is almost impossible to achieve since both diagnostic activity and life expectancy are continuously changing for each birth cohort. The important time horizon is also very long since the risk of prostate cancer becomes non-negligible after age 40 and is elevated throughout the rest of a man’s lifetime. We are not aware of any high-quality data with follow-up that extends that long. Modeling techniques are therefore essential to test these factors independently. To underline this we have added a sentence to the last paragraph in Discussion. In our previous paper, the output of the simulation model was compared with observed data of incidence and mortality, with good agreement between the two (reference 8). Additional external validation based on data from other countries would be desirable if the appropriate data would be made available e.g., through collaborations. Reviewer #3: In this manuscript, authors examined the impact of diagnostic activity and life expectancy on the lifetime risk of prostate cancer diagnosis. They employed a state transition simulation model based on Swedish population based data and simulated life trajectories of a large cohort of men from ages 40-100 to estimate the lifetime risk of a prostate cancer diagnosis. Their analyses determined that the lifetime risk of prostate cancer diagnosis is influenced by diagnostic activity. Higher exposure to diagnostic activity resulted in more prostate cancer diagnosis. Men exposed to high diagnostic activity were found to have five fold increased risk of low or intermediate risk prostate cancer and half the risk of high risk prostate cancer as compared to men with low diagnostic activity. Overall, it is a comprehensive study using a large cohort of men with interesting findings. RE: We thank the reviewer for a positive comment. Attachments Attachment Submitted filename: Lifetime_risk_PLOSOne_Answer_to_reviewers.docx https://doi.org/10.1371/journal.pone.0277784.r002
3 Nov 2022 Decision Letter - Donovan Anthony McGrowder, Editor Diagnostic activity impacts lifetime risk of prostate cancer diagnosis more strongly than life expectancy PONE-D-22-23181R1 Dear Dr. Orrason, 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, Donovan Anthony McGrowder, PhD., MA., MSc Academic Editor PLOS ONE Additional Editor: Dear Dr. Orrason, The manuscript entitled “Diagnostic activity impacts lifetime risk of prostate cancer diagnosis more strongly than life expectancy” was revised in accordance with the reviewers’ comments and is provisionally accepted pending final checks for formatting and technical requirements. Regards, Dr. Donovan McGrowder (Academic Editor) https://doi.org/10.1371/journal.pone.0277784.r003
Formally Accepted
14 Nov 2022 Acceptance Letter - Donovan Anthony McGrowder, Editor PONE-D-22-23181R1 Diagnostic activity impacts lifetime risk of prostate cancer diagnosis more strongly than life expectancy Dear Dr. Orrason: 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. Donovan Anthony McGrowder Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0277784.r004

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