Advertisement
Mayo Clinic Proceedings Home

Coffee Intake of Colorectal Cancer Patients and Prognosis According to Histopathologic Lymphocytic Reaction and T-Cell Infiltrates

  • Tomotaka Ugai
    Correspondence
    Correspondence: Address to Tomotaka Ugai, MD, PhD, Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, 221 Longwood Ave, EBRC Rm 404, Boston, MA 02115; or Shuji Ogino, MD, PhD, MS, Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, 221 Longwood Ave, EBRC Rm 404A, Boston, MA 02115 .
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

    Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA
    Search for articles by this author
  • Koichiro Haruki
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Juha P. Väyrynen
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

    Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA

    Cancer and Translational Medicine Research Unit, Medical Research Center Oulu, Oulu University Hospital, and University of Oulu, Oulu, Finland
    Search for articles by this author
  • Jennifer Borowsky
    Affiliations
    Conjoint Gastroenterology Department, QIMR Berghofer Medical Research Institute, Queensland, Australia
    Search for articles by this author
  • Kenji Fujiyoshi
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Mai Chan Lau
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Naohiko Akimoto
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Rong Zhong
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

    Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA
    Search for articles by this author
  • Junko Kishikawa
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Kota Arima
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Shan-shan Shi
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Melissa Zhao
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Charles S. Fuchs
    Affiliations
    Yale Cancer Center, New Haven, CT

    Department of Medicine, Yale School of Medicine, New Haven, CT

    Smilow Cancer Hospital, New Haven, CT
    Search for articles by this author
  • Xuehong Zhang
    Affiliations
    Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA
    Search for articles by this author
  • Marios Giannakis
    Affiliations
    Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

    Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA

    Broad Institute of MIT and Harvard, Cambridge, MA
    Search for articles by this author
  • Mingyang Song
    Affiliations
    Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA

    Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston

    Division of Gastroenterology, Massachusetts General Hospital, Boston
    Search for articles by this author
  • Hongmei Nan
    Affiliations
    Department of Global Health, Richard M. Fairbanks School of Public Health, Indiana University, Indianapolis

    Department of Epidemiology, Richard M. Fairbanks School of Public Health, Indiana University, Indianapolis
    Search for articles by this author
  • Jeffrey A. Meyerhardt
    Affiliations
    Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Molin Wang
    Affiliations
    Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

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

    Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA
    Search for articles by this author
  • Jonathan A. Nowak
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
    Search for articles by this author
  • Shuji Ogino
    Correspondence
    Correspondence: Address to Tomotaka Ugai, MD, PhD, Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, 221 Longwood Ave, EBRC Rm 404, Boston, MA 02115; or Shuji Ogino, MD, PhD, MS, Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, 221 Longwood Ave, EBRC Rm 404A, Boston, MA 02115 .
    Affiliations
    Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA

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

    Cancer Immunology and Cancer Epidemiology Programs, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA

    Broad Institute of MIT and Harvard, Cambridge, MA
    Search for articles by this author

      Abstract

      Given previous biologic evidence of immunomodulatory effects of coffee, we hypothesized that the association between coffee intake of colorectal cancer patients and survival differs by immune responses. Using a molecular pathologic epidemiology database of 4465 incident colorectal cancer cases, including 1262 cases with molecular data, in the Nurses’ Health Study and the Health Professionals Follow-up Study, we examined the association between coffee intake of colorectal cancer patients and survival in strata of levels of histopathologic lymphocytic reaction and T-cell infiltrates in tumor tissue. We did not observe a significant association of coffee intake with colorectal cancer–specific mortality (multivariable-adjusted hazard ratio [HR] for 1-cup increase of coffee intake per day, 0.93; 95% CI, 0.84 to 1.03). Although statistical significance was not reached at the stringent level (α=.005), the association of coffee intake with colorectal cancer–specific mortality differed by Crohn disease–like lymphoid reaction (Pinteraction=.007). Coffee intake was associated with lower colorectal cancer–specific mortality in patients with high Crohn disease–like reaction (multivariable HR for 1-cup increase of coffee intake per day, 0.55; 95% CI, 0.37 to 0.81; Ptrend=.002) but not in patients with intermediate Crohn disease–like reaction (the corresponding HR, 1.02; 95% CI, 0.72 to 1.44) or negative/low Crohn disease–like reaction (the corresponding HR, 0.95; 95% CI, 0.83 to 1.07). The associations of coffee intake with colorectal cancer–specific mortality did not significantly differ by levels of other lymphocytic reaction or any T-cell subset (Pinteraction>.18). There is suggestive evidence for differential prognostic effects of coffee intake by Crohn disease–like lymphoid reaction in colorectal cancer.

      Abbreviations and Acronyms:

      FFQ (food frequency questionnaire), HPFS (Health Professionals Follow-up Study), HR (hazard ratio), IPW (inverse probability weighting), NHS (Nurses’ Health Study)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Mayo Clinic Proceedings
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Paucek R.D.
        • Baltimore D.
        • Li G.
        The cellular immunotherapy revolution: arming the immune system for precision therapy.
        Trends Immunol. 2019; 40: 292-309
        • Pages F.
        • Berger A.
        • Camus M.
        • et al.
        Effector memory T cells, early metastasis, and survival in colorectal cancer.
        N Engl J Med. 2005; 353: 2654-2666
        • Song M.
        • Zhang X.
        • Meyerhardt J.A.
        • et al.
        Marine omega-3 polyunsaturated fatty acid intake and survival after colorectal cancer diagnosis.
        Gut. 2017; 66: 1790-1796
        • Hamada T.
        • Liu L.
        • Nowak J.A.
        • et al.
        Vitamin D status after colorectal cancer diagnosis and patient survival according to immune response to tumour.
        Eur J Cancer. 2018; 103: 98-107
        • Guercio B.J.
        • Sato K.
        • Niedzwiecki D.
        • et al.
        Coffee intake, recurrence, and mortality in stage III colon cancer: results from CALGB 89803 (Alliance).
        J Clin Oncol. 2015; 33: 3598-3607
        • Hu Y.
        • Ding M.
        • Yuan C.
        • et al.
        Association between coffee intake after diagnosis of colorectal cancer and reduced mortality.
        Gastroenterology. 2018; 154: 916-926.e9
        • Sharif K.
        • Watad A.
        • Bragazzi N.L.
        • Adawi M.
        • Amital H.
        • Shoenfeld Y.
        Coffee and autoimmunity: more than a mere hot beverage!.
        Autoimmun Rev. 2017; 16: 712-721
        • Horrigan L.A.
        • Kelly J.P.
        • Connor T.J.
        Immunomodulatory effects of caffeine: friend or foe?.
        Pharmacol Ther. 2006; 111: 877-892
        • Zou T.
        • Yang Y.
        • Xia F.
        • et al.
        Resveratrol inhibits CD4+ T cell activation by enhancing the expression and activity of Sirt1.
        PLoS One. 2013; 8: e75139
        • Zitvogel L.
        • Pietrocola F.
        • Kroemer G.
        Nutrition, inflammation and cancer.
        Nat Immunol. 2017; 18: 843-850
        • Willett W.C.
        • Sampson L.
        • Stampfer M.J.
        • et al.
        Reproducibility and validity of a semiquantitative food frequency questionnaire.
        Am J Epidemiol. 1985; 122: 51-65
        • Rimm E.B.
        • Giovannucci E.L.
        • Stampfer M.J.
        • Colditz G.A.
        • Litin L.B.
        • Willett W.C.
        Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals.
        Am J Epidemiol. 1992; 135 (discussion 1127-1136): 1114-1126
        • Haruki K.
        • Kosumi K.
        • Li P.
        • et al.
        An integrated analysis of lymphocytic reaction, tumour molecular characteristics and patient survival in colorectal cancer.
        Br J Cancer. 2020; 122: 1367-1377
        • Fujiyoshi K.
        • Vayrynen J.P.
        • Borowsky J.
        • et al.
        Tumour budding, poorly differentiated clusters, and T-cell response in colorectal cancer.
        EBioMedicine. 2020; 57: 102860
        • Ogino S.
        • Nosho K.
        • Irahara N.
        • et al.
        Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype.
        Clin Cancer Res. 2009; 15: 6412-6420
        • Chan A.T.
        • Ogino S.
        • Fuchs C.S.
        Aspirin and the risk of colorectal cancer in relation to the expression of COX-2.
        N Engl J Med. 2007; 356: 2131-2142
        • Borowsky J.
        • Haruki K.
        • Lau M.C.
        • et al.
        Association of Fusobacterium nucleatum with specific T-cell subsets in the colorectal carcinoma microenvironment.
        Clin Cancer Res. 2021; 27: 2816-2826
        • Fujiyoshi K.
        • Bruford E.A.
        • Mroz P.
        • et al.
        Opinion: standardizing gene product nomenclature—a call to action.
        Proc Natl Acad Sci U S A. 2021; 118 (e2025207118)
        • Nosho K.
        • Irahara N.
        • Shima K.
        • et al.
        Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample.
        PLoS One. 2008; 3: e3698
        • Liu L.
        • Nevo D.
        • Nishihara R.
        • et al.
        Utility of inverse probability weighting in molecular pathological epidemiology.
        Eur J Epidemiol. 2018; 33: 381-392
        • Ogino S.
        • Nowak J.A.
        • Hamada T.
        • et al.
        Integrative analysis of exogenous, endogenous, tumour and immune factors for precision medicine.
        Gut. 2018; 67: 1168-1180
        • Ogino S.
        • Nowak J.A.
        • Hamada T.
        • Milner Jr., D.A.
        • Nishihara R.
        Insights into pathogenic interactions among environment, host, and tumor at the crossroads of molecular pathology and epidemiology.
        Annu Rev Pathol. 2019; 14: 83-103
        • Koh H.
        • Hamada T.
        • Song M.
        • et al.
        Physical activity and colorectal cancer prognosis according to tumor-infiltrating T cells.
        JNCI Cancer Spectr. 2018; 2: pky058
        • Sautes-Fridman C.
        • Petitprez F.
        • Calderaro J.
        • Fridman W.H.
        Tertiary lymphoid structures in the era of cancer immunotherapy.
        Nat Rev Cancer. 2019; 19: 307-325
        • Helmink B.A.
        • Reddy S.M.
        • Gao J.
        • et al.
        B cells and tertiary lymphoid structures promote immunotherapy response.
        Nature. 2020; 577: 549-555

      Linked Article

      • Colorectal Cancer, Crohn-Like Lymphoid Reactions, Survival — And the Power of a Good Cup of Coffee!
        Mayo Clinic ProceedingsVol. 97Issue 1
        • Preview
          “Never underestimate the power of a good cup of coffee.”1 Indeed, over the past 40 years, coffee’s reputation has changed for the better. In 1981, a 369-patient case control study reported on an unforeseen “strong association between coffee consumption and pancreatic cancer.”2 Since then, other studies have cited uncontrolled for confounders to explain this earlier, unexpected observation, drawing very different conclusions of their own: coffee now seems to confer health benefits, reduce cancer risk, and improve cancer outcomes.
        • Full-Text
        • PDF