Evidence map›Paper›PMID 30312431›Full record

ArticleJournal of the National Cancer Institute2019

Smoking and Risk of Colorectal Cancer Sub-Classified by Tumor-Infiltrating T Cells.

Tsuyoshi Hamada, Jonathan A Nowak, Yohei Masugi, David A Drew, Mingyang Song, Yin Cao, Keisuke Kosumi, Kosuke Mima, Tyler S Twombly, Li Liu and 16 more

Erratum issuedOpen access · bronzeAbstract read
In one paragraph

Article in Journal of the National Cancer Institute, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 32 papers.

0numbers the graph read from it
0cells of the map it votes in
32citing papers in PubMed
1.6field-weighted citation impact, top 13% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

32 citing papers in PubMed, 48 citations in OpenAlex.

  1. Trial
  2. Article
  3. Smoking promotes colorectal cancer via the CKAP2L/AREG axis.International journal of oncology · 2026
    Article
  4. Review
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  13. Genome-wide Interaction Study with Smoking for Colorectal Cancer Risk Identifies Novel Genetic Loci Related to Tumor Suppression, Inflammation, and Immune Response.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2023
    Article
  14. Lifetime Exposure to Cigarette Smoke and Risk of Ovarian Cancer by T-cell Tumor Immune Infiltration.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2023
    Article
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4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

26 authors at 11 institutions in 5 countries.

Tsuyoshi HamadaDepartment of Oncologic Pathology.
Jonathan A NowakDepartment of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA.
Yohei MasugiDepartment of Oncologic Pathology.
David A DrewClinical and Translational Epidemiology Unit, and Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
Mingyang SongClinical and Translational Epidemiology Unit, and Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
Yin CaoClinical and Translational Epidemiology Unit, and Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
Keisuke KosumiDepartment of Oncologic Pathology.
Kosuke MimaDepartment of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA.
Tyler S TwomblyDepartment of Oncologic Pathology.
Li LiuDepartment of Oncologic Pathology.
Yan ShiDepartment of Oncologic Pathology.
Annacarolina da SilvaDepartment of Oncologic Pathology.
Mancang GuDepartment of Oncologic Pathology.
Wanwan LiDepartment of Oncologic Pathology.
Katsuhiko NoshoDepartment of Gastroenterology, Rheumatology, and Clinical Immunology, Sapporo Medical University School of Medicine, Sapporo, Japan.
NaNa KeumDepartment of Nutrition.
Marios GiannakisDepartment of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA.
Jeffrey A Meyerhardt
Kana WuDepartment of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
Molin WangDepartment of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
Andrew T ChanDepartment of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
Edward L GiovannucciDepartment of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
Charles S FuchsYale Cancer Center, New Haven, CT.
Reiko NishiharaDepartment of Oncologic Pathology.
Xuehong ZhangDepartment of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
Shuji OginoDepartment of Oncologic Pathology.
Harvard University · USDana-Farber Cancer Institute · USBrigham and Women's Hospital · USBroad Institute · USChinese PLA General Hospital · CNDongguk University · KRPathological Society · GBSapporo Medical University · JPSmilow Cancer Hospital · USWashington University in St. Louis · USZhejiang Chinese Medical University · CN

Funding

Statistical MethodsP01CA087969 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ROSNER, BERNARD A · 2000 to 2019
$77.8M
Validity of Diet and Activity Measures in WomenP01CA055075 · NCI · HARVARD UNIVERSITY (SCH OF PUBLIC HLTH) · PI SMITH-WARNER, STEPHANIE A · 1991 to 2009
$41.8M
Pilot & Feasibility ProgramP30DK043351 · NIDDK · MASSACHUSETTS GENERAL HOSPITAL · PI RAYMOND T CHUNG · 1991 to 2026
$35.3M
Tissue and Pathology ResourcesP50CA127003 · NCI · DANA-FARBER CANCER INST · PI BASS, ADAM JOEL · 2007 to 2023
$33.2M
Long Term Multidisciplinary Study of Cancer in Women: The Nurses Health StudyUM1CA186107 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ELIASSEN, A. HEATHER, STAMPFER, MEIR · 2014 to 2023
$22.3M
Training Program in Cancer EpidemiologyT32CA009001 · NCI · HARVARD UNIVERSITY (SCH OF PUBLIC HLTH) · PI A. Heather Eliassen, Meir Stampfer · 1985 to 2026
$17.3M
Cancer Epidemiology Cohort in Male Health ProfessionalsU01CA167552 · NCI · HARVARD UNIVERSITY D/B/A HARVARD SCHOOL OF PUBLIC HEALTH · PI Lorelei Mucci, Walter C. Willett · 2017 to 2026
$17.0M
Cancer Epidemiology Cohort in Male Health ProfessionalsUM1CA167552 · NCI · HARVARD SCHOOL OF PUBLIC HEALTH · PI WILLETT, WALTER C. · 2012 to 2016
$11.5M
Inflammation and Colorectal NeoplasiaR01CA137178 · NCI · MASSACHUSETTS GENERAL HOSPITAL · PI CHAN, ANDREW T · 2009 to 2019
$6.5M
Accelerating Transdisciplinary Epidemiology of Colorectal CancerR35CA197735 · NCI · DANA-FARBER CANCER INST · PI OGINO, SHUJI · 2015 to 2021
$6.0M
Dietary And Lifestyle Determinants Of Colon Cancer Recurrence and SurvivalR01CA118553 · NCI · YALE UNIVERSITY · PI FUCHS, CHARLES S · 2007 to 2019
$4.4M
Impact of Celecoxib and Inflammation on Survival in Stage III Colon CancerR01CA169141 · NCI · YALE UNIVERSITY · PI FUCHS, CHARLES S · 2013 to 2018
$3.9M
NCI NIH HHS K07 CA188126NCI NIH HHS K07 CA190673NCI NIH HHS L30 CA209764NCI NIH HHS P01 CA055075NCI NIH HHS P01 CA087969NCI NIH HHS P50 CA127003NCI NIH HHS R00 CA215314NCI NIH HHS R01 CA118553NCI NIH HHS R01 CA137178NCI NIH HHS R01 CA151993NCI NIH HHS R01 CA169141NCI NIH HHS R35 CA197735NCI NIH HHS T32 CA009001NCI NIH HHS U01 CA167552NCI NIH HHS UM1 CA167552NCI NIH HHS UM1 CA186107NIDDK NIH HHS K24 DK098311NIDDK NIH HHS P30 DK043351
6 · The paper itself

Abstract

Background: Evidence indicates not only carcinogenic effect of cigarette smoking but also its immunosuppressive effect. We hypothesized that the association of smoking with colorectal cancer risk might be stronger for tumors with lower anti-tumor adaptive immune response. Methods: During follow-up of 134 981 participants (3 490 851 person-years) in the Nurses' Health Study and Health Professionals Follow-up Study, we documented 729 rectal and colon cancer cases with available data on T-cell densities in tumor microenvironment. Using the duplication-method Cox regression model, we examined a differential association of smoking status with risk of colorectal carcinoma subclassified by densities of CD3+ cells, CD8+ cells, CD45RO (PTPRC)+ cells, or FOXP3+ cells. All statistical tests were two-sided. Results: The association of smoking status with colorectal cancer risk differed by CD3+ cell density (Pheterogeneity = .007). Compared with never smokers, multivariable-adjusted hazard ratios for CD3+ cell-low colorectal cancer were 1.38 (95% confidence interval = 1.09 to 1.75) in former smokers and 1.59 (95% confidence interval = 1.14 to 2.23) in current smokers (Ptrend = .002, across smoking status categories). In contrast, smoking status was not associated with CD3+ cell-high cancer risk (Ptrend = .52). This differential association appeared consistent in strata of microsatellite instability, CpG island methylator phenotype, or BRAF mutation status. There was no statistically significant differential association according to densities of CD8+ cells, CD45RO+ cells, or FOXP3+ cells (Pheterogeneity > .04, with adjusted α of 0.01). Conclusions: Colorectal cancer risk increased by smoking was stronger for tumors with lower T-lymphocyte response, suggesting an interplay of smoking and immunity in colorectal carcinogenesis.

Indexed as

AdultAgedCD8-Positive T-LymphocytesColorectal NeoplasmsFemaleFollow-Up StudiesHumansLymphocytes, Tumor-InfiltratingMaleMiddle AgedPrognosisProspective StudiesTobacco SmokingTumor Microenvironment

Identifiers

PMID30312431
PMCPMC6335108
OpenAlexW2896691366

What OpenQuestion holds

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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.