{"doi":"10.1136/bmjonc-2025-000787","title":"Smoking habit and long-term colorectal cancer incidence by exome-wide mutational and neoantigen loads: evidence based on the prospective cohort incident-tumour biobank method","abstract":"Objective To test the hypothesis that the association of smoking with long-term colorectal cancer incidence may be stronger for tumours with higher mutational and neoantigen loads. Methods and analysis In the Nurses’ Health Study (1980–2012) and the Health Professionals Follow-up Study (1986–2012), our novel prospective cohort incident-tumour biobank method (PCIBM) used 3053 incident colorectal carcinoma cases including 752 cases with whole-exome sequencing data. Using the multivariable duplication-method Cox regression model with the inverse probability weighting to adjust for the selection bias due to tissue availability, we assessed a differential association of cigarette smoking with colorectal carcinoma incidence by an exome-wide tumour mutational burden (e-TMB) or neoantigen load. Results The association of pack-years smoked with colorectal cancer incidence differed by e-TMB (P heterogeneity <0.001). Multivariable-adjusted HRs for e-TMB-high (≥10 mutations/megabase) tumours were 1.28 (95% CI 0.72 to 2.28) and 2.56 (95% CI 1.61 to 4.07) for 1–19 and ≥20 pack-years (vs 0 pack-years; P trend <0.001), respectively. In contrast, pack-years smoked were not associated with e-TMB-low tumour incidence (P trend =0.67). A similar differential association was observed for the neoantigen load (P heterogeneity =0.017). The differential association by e-TMB appeared consistent in the strata of CpG island methylator phenotype status, BRAF mutation or lymphocytic infiltrates. Conclusions Smoking is more strongly associated with the long-term incidence of colorectal carcinoma harbouring higher mutational and neoantigen loads. Our PCIBM-based evidence supports the immunosuppressive effect of smoking and the potential of smoking cessation in improving antitumour immunity for cancer prevention and treatment.","journal":"BMJ Oncology","year":2025,"id":516252,"datarank":0.3856809148539515,"base_score":2.3978952727983707,"endowment":2.3978952727983707,"self_citation_contribution":0.3596842909197557,"citation_network_contribution":0.025996623934195807,"self_endowment_contribution":0.3596842909197557,"citer_contribution":0.025996623934195807,"corpus_percentile":52.87382996828344,"corpus_rank":6093,"citation_count":10,"citer_count":6,"citers_with_citation_signal":2,"citers_with_endowment":2,"datacite_reuse_total":0,"is_dataset":true,"is_dataset_confidence":0.6177,"is_data_producer":false,"deposit_databanks":null,"is_oa":true,"file_count":0,"downloads":0,"has_version_chain":false,"published_date":"2025-01-01","fair_score":4.1667,"fair_percentile":4.891470498318557,"algorithm_id":"datarank_citation_only_1hop_v6","ranking_scope":"data_only","authors":[{"id":241016,"name":"Tomotaka Ugai","orcid":"0000-0003-0182-5269","position":1,"is_corresponding":false},{"id":3720,"name":"Carino Gurjao","orcid":"0000-0002-4813-5460","position":2,"is_corresponding":false},{"id":1093432,"name":"Satoko Ugai","orcid":"0009-0001-9661-9363","position":3,"is_corresponding":false},{"id":269896,"name":"Xuehong Zhang","orcid":"0000-0002-8260-8508","position":4,"is_corresponding":false},{"id":241004,"name":"Koichiro Haruki","orcid":"0000-0002-1686-3228","position":5,"is_corresponding":false},{"id":665246,"name":"Yasutoshi Takashima","orcid":"0009-0009-0430-454X","position":6,"is_corresponding":false},{"id":241015,"name":"Naohiko Akimoto","orcid":"0000-0001-9880-4143","position":7,"is_corresponding":false},{"id":241005,"name":"Mai Chan Lau","orcid":"0000-0002-7698-4697","position":8,"is_corresponding":false},{"id":1381591,"name":"Kosuke Matsuda","orcid":"0009-0009-2847-0251","position":9,"is_corresponding":false},{"id":1381592,"name":"Nobuhiro Nakazawa","orcid":"0000-0001-8705-2150","position":10,"is_corresponding":false},{"id":1381593,"name":"Mayu Higashioka","orcid":"0000-0002-3846-0470","position":11,"is_corresponding":false},{"id":1381594,"name":"Satoshi Miyahara","orcid":"0000-0001-8522-860X","position":12,"is_corresponding":false},{"id":333370,"name":"Keisuke Kosumi","orcid":"0000-0003-4028-1137","position":13,"is_corresponding":false},{"id":416222,"name":"Yohei Masugi","orcid":"0000-0002-6952-4043","position":14,"is_corresponding":false},{"id":945969,"name":"Li Liu","orcid":"0000-0002-0504-418X","position":15,"is_corresponding":false},{"id":261915,"name":"Yin Cao","orcid":"0000-0001-9835-7662","position":16,"is_corresponding":false},{"id":537632,"name":"Daniel Nevo","orcid":"0000-0002-9770-827X","position":17,"is_corresponding":false},{"id":131778,"name":"Molin Wang","orcid":"0000-0003-1951-8961","position":18,"is_corresponding":false},{"id":241019,"name":"Reiko Nishihara","orcid":"0000-0002-2579-9141","position":19,"is_corresponding":false},{"id":1885,"name":"Sachet A. Shukla","orcid":"0000-0003-2445-3584","position":20,"is_corresponding":false},{"id":3263,"name":"Catherine J. Wu","orcid":"0000-0002-3348-5054","position":21,"is_corresponding":false},{"id":5604,"name":"Levi A. Garraway","orcid":"0000-0003-3739-0471","position":22,"is_corresponding":false},{"id":6441,"name":"Jeffrey A. Meyerhardt","orcid":"0000-0002-1120-0898","position":23,"is_corresponding":false},{"id":86230,"name":"Edward L. Giovannucci","orcid":"0000-0002-6123-0219","position":24,"is_corresponding":false},{"id":3733,"name":"Jonathan A. Nowak","orcid":"0000-0002-0943-7407","position":25,"is_corresponding":false},{"id":75990,"name":"Charles S. Fuchs","orcid":"0000-0003-1582-9842","position":26,"is_corresponding":false},{"id":41038,"name":"Andrew T. Chan","orcid":"0000-0001-7284-6767","position":27,"is_corresponding":false},{"id":104568,"name":"Mingyang Song","orcid":"0000-0002-1324-0316","position":28,"is_corresponding":false},{"id":3011,"name":"Marios Giannakis","orcid":"0000-0001-9012-6982","position":29,"is_corresponding":false},{"id":3732,"name":"Shuji Ogino","orcid":"0000-0002-3909-2323","position":30,"is_corresponding":false},{"id":333371,"name":"Tsuyoshi Hamada","orcid":"0000-0002-3937-2755","position":0,"is_corresponding":true}],"reference_count":60,"raw_metadata":null,"created_at":"2026-07-19T02:48:49.486328Z","pmid":"40519220","pmcid":"PMC12164326","fwci":null,"citation_percentile":null,"influential_citations":0,"oa_status":null,"license":null,"views":0,"total_file_size_bytes":0,"version_count":0,"fair_f":11.1111,"fair_a":6.25,"fair_i":0.0,"fair_r":25.0,"fair_zscore":-1.1986,"fair_rationale":{"fair_score":4.17,"has_llm":true,"taxonomy_version":"fair_taxonomy_v5","dimensions":{"F":{"name":"Findable","score":11.11,"criteria":[{"key":"f_dataset_pid","label":"Persistent identifier for the data","kind":"llm","weight":2.0,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"No persistent identifier string (DOI, Handle, ARK, URN, or repository accession) is given for the dataset.","anchors":["RDA-F1-01D — FAIR Data Maturity Model: 'Data is identified by a persistent identifier' (priorit","RDA-F1-02D — FAIR Data Maturity Model: 'Data is identified by a globally unique identifier'","FsF-F1-02D — F-UJI/FAIRsFAIR: 'Data is assigned a persistent identifier'"],"scored":true,"signal":null},{"key":"f_repository_named","label":"Named repository","kind":"llm","weight":2.0,"fraction":0.0,"verdict":"no","evidence":"\"guidelines are available on our website for outside users to access the resources of our study ( http://www.nurseshealthstudy.org/ , http://www.hsph.harvard.edu/hpfs/ ).\"","grounded":false,"rationale":"The host is an institutional website, not a curated data repository. 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[downgraded to 'no' — no verifiable quote from the paper]","anchors":["RDA-F2-01M — 'Rich metadata is provided to allow discovery' (priority Essential)","FsF-F2-01M — F-UJI: 'Metadata includes descriptive core elements to support data findability'","FsF-R1-01MD — F-UJI: 'Metadata specifies the content of the data'"],"scored":false,"signal":null},{"key":"f_dataset_cited","label":"Dataset formally cited","kind":"llm","weight":1.0,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"No identifier or link for the dataset appears anywhere in the reference list or body text.","anchors":["FORCE11 Joint Declaration of Data Citation Principles (2014) — data should be cited as a first-","RDA-F3-01M — metadata clearly and explicitly includes the identifier of the data it describes","FsF-F3-01M — F-UJI: 'Metadata includes the identifier of the data it describes'"],"scored":true,"signal":null}]},"A":{"name":"Accessible","score":6.25,"criteria":[{"key":"a_data_openly_accessible","label":"Access route free of preconditions","kind":"llm","weight":2.0,"fraction":0.0,"verdict":"no","evidence":"\"Data are available on reasonable request.\"","grounded":false,"rationale":"The only route offered is a discretionary request to a person, which is not a followable precondition.","anchors":["RDA-A1.1-01D — 'Data is accessible through a free access protocol'","FsF-A1-01M — F-UJI: 'Metadata contains access level and access conditions of the data'","NSTC Desirable Characteristics of Data Repositories (2022) — 'Free and Easy Access'"],"scored":true,"signal":null},{"key":"a_access_conditions_stated","label":"Access level labelled","kind":"llm","weight":1.0,"fraction":0.0,"verdict":"no","evidence":"\"With input from and approval of the External Advisory Committees for the two cohorts (the Nurses’ Health Study (NHS) and the Health Professionals Follow-up Study (HPFS)), we have adopted a data enclave approach to data sharing. Along with a general description of the NHS and HPFS cohorts as well as all questionnaires that have been used since 1976 in the NHS and since 1986 in the HPFS, for both the blood repository and the questionnaire data, guidelines are available on our website for outside users to access the resources of our study ( http://www.nurseshealthstudy.org/ , http://www.hsph.harvard.edu/hpfs/ ). Typically, an outside user prepares a brief proposal that is reviewed by the NHS and HPFS investigator groups to identify a local investigator to assist the outside investigator.\"","grounded":false,"rationale":"The text describes an access action (proposal review) but does not label the access level with a standard term. [downgraded to 'no' — no verifiable quote from the paper] [majority verdict 'no' (3/5 passes agreed)]","anchors":["FsF-A1-01M — F-UJI: 'Metadata contains access level and access conditions of the data'","RDA-A1-01M — metadata contains information to enable the user to get access to the data","COAR Controlled Vocabularies — Access Rights v1.0 (open / embargoed / restricted / metadata-onl"],"scored":false,"signal":null},{"key":"a_controlled_access_for_sensitive","label":"Gatekeeper for sensitive data","kind":"llm","weight":0.5,"fraction":0.5,"verdict":"partial","evidence":"\"Typically, an outside user prepares a brief proposal that is reviewed by the NHS and HPFS investigator groups to identify a local investigator to assist the outside investigator.\"","grounded":false,"rationale":"An institutional gatekeeper (investigator groups and committees) is named for accessing human-subject data. [downgraded to 'partial' — no verifiable quote from the paper] [majority verdict 'partial' (3/5 passes agreed)]","anchors":["NIH Genomic Data Sharing Policy (NOT-OD-14-124) — controlled-access via a Data Access Committee","RDA-A1.2-01D — 'Data is accessible through an access protocol that supports authentication and ","NIH DMS Policy Element 5 (NOT-OD-21-014) — Access, Distribution, or Reuse Considerations (conse"],"scored":false,"signal":null},{"key":"a_timeline_retention","label":"Availability timing & retention","kind":"llm","weight":0.5,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"Neither a persistence commitment nor an availability timing statement is given for the data.","anchors":["NIH DMS Plan Element 4 (NOT-OD-21-014) — Data Preservation, Access, and Associated Timelines","NSTC Desirable Characteristics (2022), Organizational Infrastructure: 'Retention Policy'","RDA-A2-01M — 'Metadata is guaranteed to remain available after data is no longer available'"],"scored":false,"signal":null}]},"I":{"name":"Interoperable","score":0.0,"criteria":[{"key":"i_open_nonproprietary_format","label":"Open file format","kind":"llm","weight":1.0,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"No file format token of any kind is named for the released data.","anchors":["FsF-R1.3-02D — F-UJI: 'Data is available in a file format recommended by the target research co","RDA-R1.3-02D — data is expressed in a machine-understandable community standard","RDA-I1-01D — data uses a knowledge representation expressed in a standardised format"],"scored":true,"signal":null},{"key":"i_community_standard_vocabulary","label":"Community standard / vocabulary","kind":"llm","weight":1.0,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"No data or metadata community standard (e.g., MIAME, BIDS, an ontology) is named; only molecular pathology markers are used.","anchors":["RDA-R1.3-01M — 'Metadata complies with a community standard' (priority Essential)","RDA-R1.3-01D — 'Data complies with a community standard'","RDA-I2-01M — '(Meta)data use vocabularies that follow FAIR principles'"],"scored":false,"signal":null},{"key":"i_qualified_references","label":"Identifiers for the resources the data depend on","kind":"llm","weight":0.5,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"No identifier (accession, DOI, RRID, build ID) for an external resource is provided in the text.","anchors":["RDA-I3-01M — '(meta)data include references to other (meta)data'","RDA-I3-03M — 'metadata includes qualified references to other metadata'","FsF-I3-01M — F-UJI: 'Metadata includes links between the data and its related entities'"],"scored":false,"signal":null}]},"R":{"name":"Reusable","score":25.0,"criteria":[{"key":"r_reuse_license","label":"Reuse licence","kind":"llm","weight":2.0,"fraction":0.0,"verdict":"no","evidence":null,"grounded":false,"rationale":"No license or terms document is named for the data; the CC BY 4.0 license applies to the article only.","anchors":["RDA-R1.1-01M — 'Metadata includes information about the licence under which the data can be reu","RDA-R1.1-02M — 'Metadata refers to a standard reuse licence'","RDA-R1.1-03M — 'Metadata refers to a machine-understandable reuse licence'"],"scored":true,"signal":null},{"key":"r_provenance_methods","label":"Provenance of the data","kind":"llm","weight":1.0,"fraction":1.0,"verdict":"yes","evidence":"To further filter out spurious single-nucleotide variant calls, we used BWA (Burrows-Wheeler Aligner)-MEM ( http://bio-bwa.sourceforge.net/ ) to realign sequenced reads associated with the mutations to a set of sequences derived from the human reference assembly.","grounded":true,"rationale":"The text names specific software (BWA-MEM) and also mentions NetMHCpan V.4.1, qualifying as class 1 (proper nouns). 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For clinical / human-subjects data, deposit in dbGaP or the European Genome-phenome Archive (EGA).","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":null,"why":"No persistent identifier string (DOI, Handle, ARK, URN, or repository accession) is given for the dataset.","gain":16.67,"priority":"essential","scored":true},{"key":"f_repository_named","dimension":"F","label":"Named repository","action":"Deposit the data in a repository registered in re3data/FAIRsharing (a domain repository such as GEO, SRA, dbGaP, PRIDE, or a generalist such as Zenodo, Dryad, Dataverse) and name it explicitly in the paper. A lab website is not an archive: it has no retention commitment and no accession. 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Archive the analysis code in a versioned repository (GitHub + a Zenodo release DOI).","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":null,"why":"No code locator (repository URL, DOI, or package identifier) is given; only SAS software is mentioned as a tool, not the study's custom code.","gain":8.33,"priority":"important","scored":true},{"key":"r_versioning","dimension":"R","label":"Snapshot identified","action":"Version the deposit and cite the exact version analysed (a version-specific DOI, or an accession with its version suffix). 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[downgraded to 'no' — no verifiable quote from the paper]","gain":0.0,"priority":"essential","scored":false},{"key":"a_access_conditions_stated","dimension":"A","label":"Access level labelled","action":"State the access level in words, using the standard vocabulary: 'These data are open access' / 'These data are controlled access'. A reader — and a harvester — should not have to infer the access level from the presence of a download link.","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":"\"With input from and approval of the External Advisory Committees for the two cohorts (the Nurses’ Health Study (NHS) and the Health Professionals Follow-up Study (HPFS)), we have adopted a data enclave approach to data sharing. Along with a general description of the NHS and HPFS cohorts as well as all questionnaires that have been used since 1976 in the NHS and since 1986 in the HPFS, for both the blood repository and the questionnaire data, guidelines are available on our website for outside users to access the resources of our study ( http://www.nurseshealthstudy.org/ , http://www.hsph.harvard.edu/hpfs/ ). Typically, an outside user prepares a brief proposal that is reviewed by the NHS and HPFS investigator groups to identify a local investigator to assist the outside investigator.\"","why":"The text describes an access action (proposal review) but does not label the access level with a standard term. [downgraded to 'no' — no verifiable quote from the paper] [majority verdict 'no' (3/5 passes agreed)]","gain":0.0,"priority":"important","scored":false},{"key":"i_community_standard_vocabulary","dimension":"I","label":"Community standard / vocabulary","action":"Adopt and NAME your domain's data standard — the minimum-information checklist, metadata schema, or ontology your community uses (MIAME/MINSEQE, ISA-Tab, BIDS, an OBO ontology, HL7 FHIR/OMOP) — and say which one you followed. A reporting checklist standardises your paper; it does nothing for your data. In clinical / human-subjects, describe the data with OMOP CDM, CDISC SDTM or HL7 FHIR.","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":null,"why":"No data or metadata community standard (e.g., MIAME, BIDS, an ontology) is named; only molecular pathology markers are used.","gain":0.0,"priority":"important","scored":false},{"key":"r_documentation_codebook","dimension":"R","label":"Documentation / codebook","action":"Ship a README and a data dictionary IN the deposit — every file, every variable, its units, its allowed values, its missing-value codes. It is the cheapest single thing that makes a dataset usable by someone who was not in the lab, and a table buried in the article does not travel with the data.","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":null,"why":"No documentation object (README, codebook) is said to accompany the data, and no variable-definition table exists inside the article.","gain":0.0,"priority":"important","scored":false},{"key":"a_controlled_access_for_sensitive","dimension":"A","label":"Gatekeeper for sensitive data","action":"Route sensitive data through an institutional gatekeeper — deposit in a controlled- access repository (dbGaP, EGA) with a Data Access Committee and a published DUA — rather than through the corresponding author's inbox. An author-gated dataset dies with the author's email address, and 'on reasonable request' has been shown repeatedly not to yield data. For sensitive/human clinical / human-subjects data, use a controlled-access repository such as dbGaP or EGA.","anchors":["yes","partial","no"],"verdict":"partial","current":0.5,"evidence":"\"Typically, an outside user prepares a brief proposal that is reviewed by the NHS and HPFS investigator groups to identify a local investigator to assist the outside investigator.\"","why":"An institutional gatekeeper (investigator groups and committees) is named for accessing human-subject data. [downgraded to 'partial' — no verifiable quote from the paper] [majority verdict 'partial' (3/5 passes agreed)]","gain":0.0,"priority":"useful","scored":false},{"key":"i_qualified_references","dimension":"I","label":"Identifiers for the resources the data depend on","action":"Cite by identifier every resource the data depend on — the source datasets' accessions, the reference build (GRCh38 / GCA_000001405.28), the cohort application number, the code DOI — and register those relations on the dataset record (IsDerivedFrom, IsSupplementTo). A name is not a link: it cannot be resolved, versioned, or followed by a machine.","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":null,"why":"No identifier (accession, DOI, RRID, build ID) for an external resource is provided in the text.","gain":0.0,"priority":"useful","scored":false},{"key":"a_timeline_retention","dimension":"A","label":"Availability timing & retention","action":"State when the data become available AND how long they will be retained — cite the repository's preservation policy. NIH DMS Element 4 asks for both; most papers give neither.","anchors":["yes","partial","no"],"verdict":"no","current":0.0,"evidence":null,"why":"Neither a persistence commitment nor an availability timing statement is given for the data.","gain":0.0,"priority":"useful","scored":false}],"suggestions":["Mint or cite a persistent identifier for the dataset — a repository DOI or an accession from a registered repository — and print it in the paper. A bare URL is not persistent: it is the single most common cause of a dead data link five years after publication. For clinical / human-subjects data, deposit in dbGaP or the European Genome-phenome Archive (EGA).","Deposit the data in a repository registered in re3data/FAIRsharing (a domain repository such as GEO, SRA, dbGaP, PRIDE, or a generalist such as Zenodo, Dryad, Dataverse) and name it explicitly in the paper. A lab website is not an archive: it has no retention commitment and no accession. For clinical / human-subjects data, deposit in dbGaP or the European Genome-phenome Archive (EGA).","Remove the precondition or justify it. Release the data at publication with no embargo, no registration wall, and no approval step — NIH's zero-embargo public- access rule (NOT-OD-25-101) has already made 'available at publication' the federal baseline for the article; the data should not lag behind it. For clinical / human-subjects data, deposit in dbGaP or the European Genome-phenome Archive (EGA).","Attach a standard, machine-readable open licence to the deposit — CC0 or CC BY, which is what Horizon Europe and most funders expect — and print the licence identifier in the paper. 'Free to use' is not a licence: it grants nothing a reuser's institution can rely on.","Cite the dataset in the reference list like a publication — creator, year, title, repository, DOI/accession — and cite it in-text where it is used. Only a reference- list entry is machine-readable to Crossref/DataCite, and only a citation lets the data earn credit. Cite the clinical / human-subjects repository accession (e.g. from dbGaP or the European Genome-phenome Archive (EGA)) in the reference list."],"model":"deepseek/deepseek-v4-flash","agent_version":"fair_agent_v8","fulltext_source":"epmc_xml"},"fair_model":"deepseek/deepseek-v4-flash","fair_agent_version":"fair_agent_v8","fair_fulltext_source":"epmc_xml","fair_has_llm":true,"fair_computed_at":"2026-07-20T12:25:10.692945Z","clinical_trials":[],"software_tools":[],"db_accessions":[],"linked_datasets":[],"topics":[]}