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Dietary Patterns and Risk of Colorectal Cancer: Analysis by Tumor Location and Molecular Subtypes

  • Author Footnotes
    ∗ Authors share co-first authorship
    Raaj S. Mehta
    Footnotes
    ∗ Authors share co-first authorship
    Affiliations
    Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

    Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
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  • Author Footnotes
    ∗ Authors share co-first authorship
    Mingyang Song
    Footnotes
    ∗ Authors share co-first authorship
    Affiliations
    Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

    Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts
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  • Author Footnotes
    ∗ Authors share co-first authorship
    Reiko Nishihara
    Footnotes
    ∗ Authors share co-first authorship
    Affiliations
    Division of MPE Molecular Pathological Epidemiology, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, Massachusetts

    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts

    Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts

    Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts

    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • David A. Drew
    Affiliations
    Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

    Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
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  • Kana Wu
    Affiliations
    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts
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  • Zhi Rong Qian
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Teresa T. Fung
    Affiliations
    Program in Dietetics, Simmons College, Boston, Massachusetts
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  • Tsuyoshi Hamada
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Yohei Masugi
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Annacarolina da Silva
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Yan Shi
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Wanwan Li
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Mancang Gu
    Affiliations
    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Walter C. Willett
    Affiliations
    Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts
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  • Charles S. Fuchs
    Affiliations
    Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts

    Yale Cancer Center, Smilow Cancer Hospital and Yale School of Medicine, New Haven, Connecticut
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  • Edward L. Giovannucci
    Affiliations
    Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts

    Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts
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  • Author Footnotes
    § Authors share co-senior authorship.
    Shuji Ogino
    Correspondence
    Reprint requests Address requests for reprints to: Shuji Ogino, MD, PhD, MS, Division of MPE Molecular Pathological Epidemiology, Brigham and Women’s Hospital, 450 Brookline Ave., DFCI Room SM1036, Boston, Massachusetts 02215. fax: (617) 582-8558.
    Footnotes
    § Authors share co-senior authorship.
    Affiliations
    Division of MPE Molecular Pathological Epidemiology, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts

    Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts
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  • Author Footnotes
    § Authors share co-senior authorship.
    Andrew T. Chan
    Correspondence
    Andrew T. Chan, MD, MPH, Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, 55 Fruit St., Boston, Massachusetts 02114. fax: (617) 726-3673.
    Footnotes
    § Authors share co-senior authorship.
    Affiliations
    Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

    Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

    Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, Massachusetts
    Search for articles by this author
  • Author Footnotes
    ∗ Authors share co-first authorship
    § Authors share co-senior authorship.
Published:February 26, 2017DOI:https://doi.org/10.1053/j.gastro.2017.02.015

      Background & Aims

      Western and prudent dietary patterns have been associated with higher and lower risks of colorectal cancer (CRC), respectively. However, little is known about the associations between dietary patterns and specific anatomic subsites or molecular subtypes of CRC.

      Methods

      We used multivariable Cox proportional hazards models to examine the associations between Western and prudent dietary patterns and CRC risk in the Health Professionals Follow-up Study and Nurses’ Health Study.

      Results

      After up to 32 years of follow-up of 137,217 men and women, we documented 3260 cases of CRC. Among individuals from whom subsite data were available, we observed 1264 proximal colon, 866 distal colon, and 670 rectal tumors. Western diet was associated with an increased incidence of CRC (Ptrend < .0001), with a relative risk (RR) of 1.31 (95% CI, 1.15–1.48, comparing the highest to lowest quartile). The association of Western diet with CRC was evident for tumors of the distal colon (RR, 1.55; 95% CI, 1.22–1.96; Ptrend = .0004) and rectum (RR, 1.35; 95% CI, 1.03–1.77; Ptrend = .01) but not proximal colon (RR, 1.11; 95% CI, 0.91–1.35; Ptrend = .51) when we comparing extreme quartiles. In contrast, for the prudent pattern, we observed a RR of 0.86 for overall CRC (95% CI, 0.77–0.95; Ptrend = .01), with similar trends at anatomic subsites. However, the trend appeared stronger among men than women. Among 1285 cases (39%) with tissue available for molecular profiling, Western diet appeared to be more strongly associated with some CRC molecular subtypes (no mutations in KRAS [KRAS wildtype] or BRAF [BRAF wildtype], no or a low CpG island methylator phenotype, and microsatellite stability), although formal tests for heterogeneity did not produce statistically significant results.

      Conclusions

      Western dietary patterns are associated with an increased risk of CRC, particularly distal colon and rectal tumors. Western dietary patterns also appear more strongly associated with tumors that are KRAS wildtype, BRAF wildtype, have no or a low CpG island methylator phenotype, and microsatellite stability. In contrast, prudent dietary patterns are associated with a lower risk of CRC that does not vary according to anatomic subsite or molecular subtype.

      Keywords

      Abbreviations used in this paper:

      BMI (body mass index), CI (confidence interval), CIMP (CpG Island Methylator Phenotype), CRC (colorectal cancer), FFQ (food frequency questionnaire), HPFS (Health Professionals Follow-up Study), MSI (microsatellite instability), MSS (microsatellite stable), NHS (Nurses’ Health Study), RR (relative risk)
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