Estimating the impact of missed colorectal cancer diagnoses on life expectancy in Minamisoma City following the 2011 triple disaster

Hiroaki Saito; Michio Murakami; Akihiko Ozaki; Yoshitaka Nishikawa; Toyoaki Sawano; Yuki Shimada; Sho Fujioka; Tianchen Zhao; Tomoyoshi Oikawa; Yukio Kanazawa; Masaharu Tsubokura

doi:10.1371/journal.pone.0324822

Peer Review History

Original SubmissionMay 16, 2024
16 May 2024 Author Response https://doi.org/10.1371/journal.pone.0324822.r001
23 Sep 2024 Decision Letter - Belgin Sever, Editor Dear Dr. Saito, 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 Nov 07 2024 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. 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'. 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[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? 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 Reviewer #1: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English??> Reviewer #1: Yes ****** Reviewer #1: Your manuscript provides a valuable contribution to the field of disaster medicine and public health. The modeling approach and analysis are rigorous, and the policy implications of your findings are clear. To further strengthen your paper, consider addressing the points mentioned in the editor's recommendation, particularly expanding on the limitations of your assumptions and the potential impact of missed screenings on precancerous lesions. I recommend accepting the manuscript with minor revisions, particularly focusing on the following areas: 1. Enhance the discussion of limitations: Expand on the limitations related to the assumptions made in the LLE calculations and the generalizability of the findings to other populations. 2. Clarify the impact of screening on precancerous lesions: Address the potential impact of missed CRC screenings on the detection and removal of precancerous lesions, which could further influence the study's conclusions. 3. Include a brief mention of limitations in the abstract: Add a sentence in the abstract that briefly acknowledges the study's limitations. Overall, this is a well-executed study that has the potential to inform public health policies in disaster-affected regions. I look forward to seeing the final version of your manuscript. ****** 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: Yes: NIKOLAOS GOUVAS ******** [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 https://doi.org/10.1371/journal.pone.0324822.r002
Revision 1
12 Nov 2024 Author Response Response to the comments Reviewers' comments: Reviewer #1: Your manuscript provides a valuable contribution to the field of disaster medicine and public health. The modeling approach and analysis are rigorous, and the policy implications of your findings are clear. To further strengthen your paper, consider addressing the points mentioned in the editor's recommendation, particularly expanding on the limitations of your assumptions and the potential impact of missed screenings on precancerous lesions. Response We appreciate your comments. We have modified the manuscript according to the editor’s comments and reviewer’s comments. Comments I recommend accepting the manuscript with minor revisions, particularly focusing on the following areas: 1. Enhance the discussion of limitations: Expand on the limitations related to the assumptions made in the LLE calculations and the generalizability of the findings to other populations. Response Thank you for this helpful comment. We have added to the limitations section a discussion of our assumption that the proportion of colorectal cancers detected through screening in our study population would match national statistics. We acknowledge that this assumption may not hold true for other populations. To address the generalizability of our findings, we further elaborated on the need to consider key process indicators related to colorectal cancer screening, such as population risk, primary screening positive rate, and secondary screening attendance rate. When applying our methodology to other populations, these factors should be carefully evaluated and adjustments made as needed to ensure the validity of the results. We have added the following sentences. Page35 Lines109-120 This study has several limitations. First, in calculating LLE, we assumed that the proportion of CRC cases detected through the fecal occult blood method in the study population would match the national statistics for Japan. This assumption implies that if the population risk is equivalent, and the primary screening positive rate and secondary screening attendance rate are stable, the number of CRC diagnoses can be predicted for any population undergoing the screening. However, this may not hold true for other populations. Notably, Japan has a known low colonoscopy screening attendance rate, which could be higher in populations with better educational approaches to CRC screening. When considering the generalizability of this research method to other populations, it is crucial to evaluate whether the population's CRC risk and indicators for each screening process are comparable to this study. Adjusting these factors as needed may enhance the generalizability of this study. Comments 2. Clarify the impact of screening on precancerous lesions: Address the potential impact of missed CRC screenings on the detection and removal of precancerous lesions, which could further influence the study's conclusions. Response Thank you for your valuable comment. As you pointed out, one of the limitations of this study is that it does not include the therapeutic effect of precancerous lesions as a cancer prevention effect. We have added further details regarding this point to the limitations section. In this model, we calculated the effect on the LEE of detected colorectal cancer over a 10-year span. On the other hand, it is generally considered that it takes at least 10-15 years for an adenoma to lead to colorectal cancer death, so we believe it is acceptable not to include it in this model. Certainly, a model that measures the long-term effects of these treatments is needed, and we have indicated the need for further research. Page35-6 Lines121-132 Second, this study does not account for the effect of identifying and excising colorectal polyps, which are precancerous CRC lesions. The impact of CRC screening encompasses both early CRC detection to suppress cancer progression and the prevention of CRC development by detecting and removing precancerous lesions. Our estimations only include the effect of reduced life expectancy due to CRC detected through screening and do not consider the preventive effect of identifying and treating precancerous lesions. Consequently, the increase in LLE due to the decline in CRC screening participation may be underestimated. However, the time from advanced adenoma to CRC death is estimated to be 10-15 years [31], suggesting a negligible impact within our model's timeframe. To estimate the effect of LLE, including the treatment effect of precancerous lesions, a model that evaluates long-term impacts such as microsimulation models [32], needs to be constructed. Comments 3. Include a brief mention of limitations in the abstract: Add a sentence in the abstract that briefly acknowledges the study's limitations. Response We appreciate your comment. We have modified the abstract as follows. Page 37 Lines 149-159 Conclusions: Although these data could be used to determine health policy goals following a catastrophic disaster, they should be interpreted with caution because they may underestimate the impact of CRC screening. This study has limitations, including the assumption of uniform national CRC screening and treatment performance and the exclusion of the preventive effect of polyp removal. Attachments Attachment Submitted filename: Response to the comments.docx https://doi.org/10.1371/journal.pone.0324822.r003
12 Mar 2025 Decision Letter - Ahmed Abdel Moneim, Editor Dear Dr. Saito, 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 Apr 26 2025 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. 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'. 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We look forward to receiving your revised manuscript. Kind regards, Ahmed E. Abdel Moneim 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 Reviewer #2: (No Response) Reviewer #3: All comments have been addressed Reviewer #4: All comments have been addressed ******** 2. Is the manuscript technically sound, and do the data support the conclusions??> Reviewer #2: Partly Reviewer #3: Yes Reviewer #4: No ****** 3. Has the statistical analysis been performed appropriately and rigorously? -->?> Reviewer #2: Yes Reviewer #3: Yes Reviewer #4: Yes ****** 4. Have the authors made all data underlying the findings in their manuscript fully available??> The PLOS Data policy Reviewer #2: No Reviewer #3: Yes Reviewer #4: No ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English??> Reviewer #2: Yes Reviewer #3: Yes Reviewer #4: No ****** Reviewer #2: Overall representation is good, the novelty, description and paper sections are managed well. Only few things need to be considered to make it more valuable: • Lack of Crystal Ball software Tool configuration • Also include the limitations of Estimated shift of CRC stage in case of reduced screening. • The visualization is not enough (recommendations: Bar Plotting OR Spider Plotting) Reviewer #3: Very nice and methodologically sound and transparent paper on missed cancer cases in screening program due to a national disaster. I recommend it for publication. Reviewer #4: I don’t like the abstract I will look review detail if you give go ahead ( no response) Importsnt topic very much in my field. I was a silent academic interacting w the interested screeners I don’t like the abstract However ,Yes, I appreciate and very much sympathize w the authors cultural requirements The abstract is 1.overloaded details re methods Results 2. This will be dangerously lost (misled)on reader uncertain sbout colonoscopy in their practices (expert opinion public heslth actor needs to go to text) 3.Please it needs lacks clear statements- tech jargon is not for abstract section A)how many cancers were discovered at later staged updtsged (what stage 4,3,2 /10000 adults B)which population is target for extra intervention (young or elderly define age cut C)How many otherwise avoidable deaths !! D)Is this enough evidence health loss , to support which/ sny salvage intervention ? Whose (why do) criteria support a special intervention ? E) did they adjust for real - world routine non compliance If they are concerned that they underestimated the impsct this is a very concerning message ( this is a point for limitations not abstract ) Do They by extension dangerously downplay screening ( I don’t like that To msny doubt provokers come across my desk! History changing tech makes them wrong advice going forward ****** 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 #2: Yes: Muhammad Arshad Reviewer #3: Yes: Benjamin Benzon Reviewer #4: 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 Attachments Attachment Submitted filename: PlosOne Comment.pdf https://doi.org/10.1371/journal.pone.0324822.r004
Revision 2
23 Apr 2025 Author Response 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. Reply For the following cited papers, minor corrections to the terminology description in the abstract have been declared, but not retraceted. We therefore cited the article. Satoh H, Ohira T, Hosoya M, Sakai A, Watanabe T, Ohtsuru A, et al. Evacuation after the Fukushima Daiichi Nuclear Power Plant Accident Is a Cause of Diabetes: Results from the Fukushima Health Management Survey. J Diabetes Res. 2015;2015:627390. Epub 2015/06/25. doi: 10.1155/2015/627390. PubMed PMID: 26106625; PubMed Central PMCID: PMCPMC4461763. Comments Reviewer #2: Overall representation is good, the novelty, description and paper sections are managed well. Only few things need to be considered to make it more valuable: • Lack of Crystal Ball software Tool configuration Reply Thank you for your comment. We have amended the description of the Monte Carlo simulation with Crystal Ball as follows. Page 19 line 325-338 To estimate uncertainty, Monte Carlo simulation was performed using Crystal Ball software (Oracle, Redwood City, CA, USA). For screening participation rates in Minamisoma City and national colorectal cancer detection rates, we calculated standard errors and defined probability distributions. For 10-year relative mortality rates of colorectal cancer, we utilized the reported 95% confidence intervals (S1, S2 tables). The simulation was conducted with 10,000 iterations for each age group and sex category. For each iteration, the model randomly sampled values from the defined probability distributions for all input parameters and calculated the resulting outcomes (number of missed CRC cases, stage distributions, and associated LLEs). The 95% uncertainty intervals (UIs) reported throughout our results represent the 2.5th and 97.5th percentiles of the output distributions from these 10,000 iterations. For key outputs such as the number of missed CRC diagnoses, the additional LLE due to stage progression, and the cost per life-year saved (CPLYS), we reported both the point estimates (based on the mean of the simulation results) and the 95% UIs. Comments • Also include the limitations of Estimated shift of CRC stage in case of reduced screening. Reply Thank you for your suggestion. We have added this issue in the limitation as follows. Page 37, line 143-150 Fourth, information regarding the progression of colorectal cancer stages due to a one-year delay in diagnosis is based on limited literature. The assumption that 10% of early-stage (I and II) colorectal cancers would progress to more advanced stages within one year may not fully capture the complex nature of cancer progression, which can vary significantly between individuals and cancer subtypes. Future research with more robust data on stage progression rates specific to the Japanese population would strengthen our estimation. Comments • The visualization is not enough (recommendations: Bar Plotting OR Spider Plotting) Reply In addition to the Table, additional loss of life expectancy resulting from changes in colorectal cancer stage due to a 1-year diagnostic delay has been added to the S1 figure. Comments Reviewer #3: Very nice and methodologically sound and transparent paper on missed cancer cases in screening program due to a national disaster. I recommend it for publication. Reply We appreciate your review and comments. Comments Reviewer #4: I don’t like the abstract I will look review detail if you give go ahead (no response) Importsnt topic very much in my field. I was a silent academic interacting w the interested screeners I don’t like the abstract However ,Yes, I appreciate and very much sympathize w the authors cultural requirements The abstract is 1.overloaded details re methods Results Reply We appreciate your comments. We have modified the abstract as follows. Background: After the 2011 Great East Japan Earthquake, participation in colorectal cancer (CRC) screening significantly decreased in Minamisoma City, Fukushima Prefecture. However, the long-term health effects of this decline in screening participation have not been quantified. This study aims to construct a model to evaluate the impact of post-disaster decreases in CRC screening participation on population health. Methods: We utilized the population and CRC screening data targeting 40-74 years-old residents in Minamisoma City. We compared the actual screening participation in 2011 with projected participation rates based on pre-disaster levels to estimate the number of residents who missed screening due to the disaster. Based on national CRC screening performance data and stage-specific survival rates in Japan, we estimated the number of missed CRC cases and modeled the additional the loss of life expectancy (LLE) due to CRC resulting from a one-year delay in diagnosis. Results: The estimated number of colorectal cancer cases that might have been missed due to decreased screening participation was 1.794 (95% uncertainty interval: 1.597 to 1.994) for men and 1.203 (0.931 to 1.491) for women. The missed detection opportunities estimated result in 0.428 (0.282 to 0.582) person-years [2.684 (1.793 to 3.604) years per 10,000 persons] and 0.229 (0.103 to 0.372) person-years [0.993 (0.450 to 1.608) years per 10,000 persons] of additional LLE for men and women, respectively. The estimated cost per life-year saved was 1.12×10^6 (0.81×10^6 to 1.62×10^6 ) yen for men and 3.65×10^6 (2.02×10^6 to 7.19×10^6 ) yen for women, respectively. Conclusions: The calculated additional LLE due to missed CRC screening was relatively small but suggests preventive health services should be considered in disaster response planning. These findings provide a quantitative framework for evaluating health impacts of service disruptions. Comments 2. This will be dangerously lost (misled)on reader uncertain sbout colonoscopy in their practices (expert opinion public heslth actor needs to go to text) Reply Colonoscopy is generally recommended in all cases of positive feacal immunochemical test (FIT). The administration repeatedly contacts and recommends those who have not undergone it to undergo colonoscopy. In this estimation, the impact is estimated by using statistics from Japan on the number of colorectal cancers diagnosed from people who have undergone the FIT. The average colonoscopy compliance rate and the percentage of cancers detected in the process are factored in. The following has been added to the method regarding the usual response. Page 9 Line 142-144 Colorectal cancer screening data of Minamisoma is compiled for those who participated in the annually recommended faecal immunochemical test (FIT). Colonoscopy is recommended if FIT is positive. 3.Please it needs lacks clear statements- tech jargon is not for abstract section A)how many cancers were discovered at later staged updtsged (what stage 4,3,2 /10000 adults Reply The estimated missed cancers in relation to men and women are listed in the abstract as follows. Detailed estimates of the number of missed cancers per stage have been omitted from the abstract, as they are listed in table 3. Abstract Methods: We utilized the population and CRC screening data targeting 40-74 years-old residents in Minamisoma City. We compared the actual screening participation in 2011 with projected participation rates based on pre-disaster levels to estimate the number of residents who missed screening due to the disaster. Based on national CRC screening performance data and stage-specific survival rates in Japan, we estimated the number of missed CRC cases and modeled the additional the loss of life expectancy (LLE) due to CRC resulting from a one-year delay in diagnosis. B)which population is target for extra intervention (young or elderly define age cut Reply We appreciate your comments. We have added the eli Page 9 Line 139-140 We focused on individuals aged 40–74 years who were eligible for municipal CRC screening in Minamisoma in 2011. C)How many otherwise avoidable deaths !! Reply The extent to which death occurs is not calculated in this simulation. In this case, life expectancy lost is calculated as an assessment of the risk caused by not undergoing screening. Although there are methods to calculate lost life expectancy from additional deaths that occur, we believe that these are not optimal when estimating the short-term impact in a small population such as in this case. D)Is this enough evidence health loss , to support which/ sny salvage intervention ? Whose (why do) criteria support a special intervention ? Reply We appreciate your important question. There are no clear criteria on whether intervention should be undertaken, and efforts should be made by disaster-affected areas to regain the effectiveness of their peacetime screening programmes compared to the priorities of other issues. As we describe in our discussion, the results of this simulation can be used for comparison with other health effects that have occurred since the disaster. From the perspective of lost life expectancy, we can conclude that the administrative priority should be on diabetes control, as the burden of diabetes is higher compared to the increase in diabetes that occurred after the disaster. On the other hand, from the CPLYS perspective, measures to increase participation in colorectal cancer screening are cost-effective, so it is reasonable to take measures to increase the declining participation rate. We should explore the desired intervention method, but it would be desirable to consider implementing a reintroduction of screening awareness and enhanced follow-up programmes to restore screening participation rates. We have added this issue as follows. Page 31 Line 31-33 The desired intervention is a subject for future research, but it would be desirable to consider implementing a reintroduction of screening awareness and enhanced follow-up programmes to restore screening participation rates. E) did they adjust for real - world routine non compliance Reply This is a important topic. In colorectal cancer screening, participation rates vary by region. The genelalizabitity in this regard is described in the limitaion below. Page 38 Line 150-151 Finally, the Minamisoma City population was < 70,000 at the time of the disaster, which is a relatively small target population. This was compounded by the fact that the CRC screening participation rate was low (in the 10% range) before the disaster, suggesting a potentially limited number of study participants. These factors introduced significant limitations during the verification process. However, to mitigate these limitations, we employed Monte Carlo analysis to enhance the validity of our research. Comments If they are concerned that they underestimated the impsct this is a very concerning message ( this is a point for limitations not abstract ) Do They by extension dangerously downplay screening ( I don’t like that To msny doubt provokers come across my desk! History changing tech makes them wrong advice going forward Reply Our interpretation is also that the decline in colorectal cancer screening after the disaster should not be underestimated. We do not underestimate the impact of screening. We are only adding a note that the impact shown may be a numerical underestimation. In other words, the actual impact of the drop in screening uptake may be greater than that simulated here, and may require more vigilance. This is a Simulation study and there are usual limitations to the estimates. Attachments Attachment Submitted filename: Response letter.docx https://doi.org/10.1371/journal.pone.0324822.r005
2 May 2025 Decision Letter - Ahmed Abdel Moneim, Editor <p>Estimating the Impact of Missed Colorectal Cancer Diagnoses on Life Expectancy in Minamisoma City Following the 2011 Triple Disaster PONE-D-24-16149R2 Dear Dr. Saito, 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, 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, Ahmed E. Abdel Moneim Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0324822.r006
Formally Accepted
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