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PCLM-D-23-00217

Climate factors associated with cancer incidence: an ecological study covering 33 cancers from population-based registries in 37 countries

PLOS Climate

Dear Dr. Ji,

Thank you for submitting your manuscript to PLOS Climate. After careful consideration, we feel that it has merit but does not fully meet PLOS Climate’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.

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I have completed my evaluation of your manuscript. The reviewers and myself recommend reconsideration of your manuscript following major revision.

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Please submit your revised manuscript by Feb 05 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 climate@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pclm/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

We look forward to receiving your revised manuscript.

Kind regards,

Noureddine Benkeblia, Dr. Sci., Dr. Agr.

Academic Editor

PLOS Climate

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1. Please provide separate figure files in .tif or .eps format.

For more information about figure files please see our guidelines:  LINK

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Additional Editor Comments (if provided):

I have completed my evaluation of your manuscript. The reviewers and myself recommend reconsideration of your manuscript following major revision.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Climate’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

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3. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Climate 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

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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: Overall interesting study and well-written. Some findings such as melanoma incidence which positively correlated with UV and temperature were expected given the strong association between UV exposure and cutaneous malignancy and that animal models have historically demonstrated heat enhances cutaneous carcinogenesis. Other findings are less intuitive, but the overall lack of a relationship between the rate of change in climate factors and the incidence of cancer for 30 out of 43 of the malignancy categories, coupled with several limitations listed below, calls into question the generalizability and applicability of the data.

Major Comments:

Throughout, the authors refer to ozone levels/concentrations. To be crystal clear, they need to specify each time they are measuring stratospheric ozone that filters UVB and is being degraded by CFCs and related compounds, and not tropospheric or ground-level ozone which is an important secondary pollutant that has multiple health impacts and carcinogenic potential. My advice is to perform control F function and insert 'stratospheric' in front of the word ozone in each instance of use to eliminate any potential for confusion.

I find figure 5 less helpful without knowing the number of cases of each type of cancer analyzed. Was no difference seen in 30 cancer types because the n was low for those particular cancers or was there truly no effect? The authors should include a table listing the average total cancer cases by cancer type.

I see a number of limitations to this study as outlined below:

Of the 37 nations represented, only 9 are middle income countries and none are low-income. Of the 9 MICs, 7 are considered upper middle-income nations and 2 are considered lower middle income. No low-income nations are represented and there is zero data from the African continent. More than 81% of the cancer cases analyzed are from high-income nations including the US, UK, countries within the EU, Japan, Australia and New Zealand. Given that 85% of the world's population live in LMICs and LMICs are disproportionately impacted by climate change, I don't think the authors have adequately acknowledged this considerable limitation to the generalizability and inherent equity of this data, especially in populations residing outside of high-income nations.

Only ages 45-74 were examined. Yet, a recent study published in BMJ Oncology found that the global incidence of new, early-onset cancer cases among individuals aged 14 to 49 years increased by approximately 80% from 1990 to 2019. Because of the older age ranges examined, this study fails to capture the influence of climate variables on the rising incidence of cancer in younger populations globally.

Additionally, broader impacts of climate change on immunity, food supply and nutrition, and viral pathogens are not considered but likely also contribute to the multifactorial etiology of carcinogenesis. Moreover, it is clear that climate variables play a synergistic role with air pollution in cancer pathogenesis. This is particularly true of cutaneous malignancies where UV + air pollution (PM2.5, PAHs) enhance cancer induction. Climate change and air pollution share the same root cause – combustion of fossil fuels. Their combined influence on disease is likely greater than any one variable’s contributions. Because air pollution exposure was included as a covariate in the models to account for confounding, it is possible that the association between climate variables and cancer incidence was diluted, as the potential for synergy between these related anthropogenic environmental impacts was not examined.

Minor Comments:

Abstract: NDVI is used in the abstract without defining what this acronym is. Need to spell out normalized difference vegetation index (NDVI).

Lines 152-153: Delete 'we performed'

Line 160: Delete 'and' preceding bij

Line 171: Needs a space to separate 95% and Cis

Line 220: Should be colorectal cancer, not colorectum. Also needs to be changed in several figures.

Line 289-290: Currently reads "This suggests that solar radiation may influence cancer risk more directly, possibly by directly impacting genetic mutations." The use of words like 'may' and 'possibly' lack definitiveness. UVR is well-established to be a complete carcinogen due to its ability to act as mutagen and promote and initiate tumor formation without inducement by another agent. Of course it directly impacts cancer incidence as a mutagen when compared to a variable such as greenness.

Line 295 : Extra spaces within sentence need to be removed.

Reviewer #2: Understanding the association between climate change and cancer risk is an important contribution to the field.

My main concern stems from the choice of the environmental hazards evaluated.

For example, the rationale for choosing each environmental hazard, including its connection with climate change, must be explained. Ozone layer depletion is not directly connected to climate change, while PM2.5, which does have a direct connection with climate change, is only included as a covariate.

Most importantly, the authors should clarify throughout the manuscript that only some climate hazards are included. Proximity to fossil fuel infrastructure, a major root cause of climate chance and increased cancer risk, can be evaluated using satellite data, but is not included.

The language used to describe the methods and results needs to be corrected. The authors did not "adjust for smoking status" for example.

The differences between the sizes, population density, data collection (completeness and accuracy), and geographic boundaries used by different registries need to be better explained, including the limitations inherent with combining such variable data into single estimates.

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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.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

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Climate factors associated with cancer incidence: an ecological study covering 33 cancers from population-based registries in 37 countries

PCLM-D-23-00217R1

Dear Dr. Ji,

We are pleased to inform you that your manuscript 'Climate factors associated with cancer incidence: an ecological study covering 33 cancers from population-based registries in 37 countries' has been provisionally accepted for publication in PLOS Climate.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow-up email from a member of our team. 

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

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 climate@plos.org.

Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Climate.

Best regards,

Noureddine Benkeblia, Dr. Sci., Dr. Agr.

Academic Editor

PLOS Climate

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Reviewer Comments (if any, and for reference):

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

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2. Does this manuscript meet PLOS Climate’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: (No Response)

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: (No Response)

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4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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 Response)

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Climate 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: (No Response)

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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: Th authors have adequately addressed reviewers’ concerns.

Reviewer #2: (No Response)

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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.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Eva Rawlings Parker, MD, DTMH, FAAD

Reviewer #2: No

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