Association Between Inflammatory Diet Pattern and Risk of Colorectal Carcinoma Subtypes Classified by Immune Responses to Tumor

Li Liu, Reiko Nishihara, Zhi Rong Qian, Fred K. Tabung, Daniel Nevo, Xuehong Zhang, Mingyang Song, Yin Cao, Kosuke Mima, Yohei Masugi, Yan Shi, Annacarolina da Silva, Tyler Twombly, Mancang Gu, Wanwan Li, Tsuyoshi Hamada, Keisuke Kosumi, Kentaro Inamura, Jonathan A. Nowak, David A. Drew & 9 others Paul Lochhead, Katsuhiko Nosho, Kana Wu, Molin Wang, Wendy S. Garrett, Andrew T. Chan, Charles S. Fuchs, Edward L. Giovannucci, Shuji Ogino

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Background & Aims Dietary patterns affect systemic and local intestinal inflammation, which have been linked to colorectal carcinogenesis. Chronic inflammation can interfere with the adaptive immune response. We investigated whether the association of a diet that promotes intestinal inflammation with risk of colorectal carcinoma was stronger for tumors with lower lymphocytic reactions than tumors with higher lymphocytic reactions. Methods We collected data from the molecular pathological epidemiology databases of 2 prospective cohort studies: the Nurses’ Health Study (since 1976) and the Health Professionals Follow-Up Study (since 1986). We used duplication-method time-varying Cox proportional cause-specific hazards regression to assess the association of empirical dietary inflammatory pattern (EDIP) score (derived from food frequency questionnaire data) with colorectal carcinoma subtype. Foods that contribute to high EDIP scores include red and processed meats, refined grains, carbonated beverages, and some vegetables; foods that contribute to low EDIP scores include beer, wine, coffee, tea, yellow and leafy vegetables, and fruit juice. Colorectal tissue samples were analyzed histologically for patterns of lymphocytic reactions (Crohn's-like lymphoid reaction, peritumoral lymphocytic reaction, intratumoral periglandular reaction, and tumor-infiltrating lymphocytes). Results During follow-up of 124,433 participants, we documented 1311 incident colon and rectal cancer cases with available tissue data. The association between the EDIP and colorectal cancer risk was significant (Ptrend =.02), and varied with degree of peritumoral lymphocytic reaction (Pheterogeneity <.001). Higher EDIP scores were associated with increased risk of colorectal cancer with an absent or low peritumoral lymphocytic reaction (highest vs lowest EDIP score quintile hazard ratio, 2.60; 95% confidence interval, 1.60−4.23; Ptrend <.001), but not risk of tumors with intermediate or high peritumoral lymphocytic reaction (Ptrend >.80). Conclusions In 2 prospective cohort studies, we associated inflammatory diets with a higher risk of colorectal cancer subtype that contains little or no peritumoral lymphocytic reaction. These findings suggest that diet-related inflammation might contribute to development of colorectal cancer, by suppressing the adaptive anti-tumor immune response.

Original languageEnglish
Pages (from-to)1517-1530.e14
JournalGastroenterology
Volume153
Issue number6
DOIs
Publication statusPublished - 2017 Dec 1
Externally publishedYes

Fingerprint

Colorectal Neoplasms
Diet
Inflammation
Neoplasms
Food
Cohort Studies
Prospective Studies
Tumor-Infiltrating Lymphocytes
Carbonated Beverages
Molecular Epidemiology
Coffee
Health
Adaptive Immunity
Tea
Wine
Rectal Neoplasms
Vegetables
Colonic Neoplasms
Carcinogenesis
Nurses

Keywords

  • Adaptive Immune Cells
  • BRAF
  • CpG Island Methylator Phenotype
  • Cyclooxygenase-2

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Association Between Inflammatory Diet Pattern and Risk of Colorectal Carcinoma Subtypes Classified by Immune Responses to Tumor. / Liu, Li; Nishihara, Reiko; Qian, Zhi Rong; Tabung, Fred K.; Nevo, Daniel; Zhang, Xuehong; Song, Mingyang; Cao, Yin; Mima, Kosuke; Masugi, Yohei; Shi, Yan; da Silva, Annacarolina; Twombly, Tyler; Gu, Mancang; Li, Wanwan; Hamada, Tsuyoshi; Kosumi, Keisuke; Inamura, Kentaro; Nowak, Jonathan A.; Drew, David A.; Lochhead, Paul; Nosho, Katsuhiko; Wu, Kana; Wang, Molin; Garrett, Wendy S.; Chan, Andrew T.; Fuchs, Charles S.; Giovannucci, Edward L.; Ogino, Shuji.

In: Gastroenterology, Vol. 153, No. 6, 01.12.2017, p. 1517-1530.e14.

Research output: Contribution to journalArticle

Liu, L, Nishihara, R, Qian, ZR, Tabung, FK, Nevo, D, Zhang, X, Song, M, Cao, Y, Mima, K, Masugi, Y, Shi, Y, da Silva, A, Twombly, T, Gu, M, Li, W, Hamada, T, Kosumi, K, Inamura, K, Nowak, JA, Drew, DA, Lochhead, P, Nosho, K, Wu, K, Wang, M, Garrett, WS, Chan, AT, Fuchs, CS, Giovannucci, EL & Ogino, S 2017, 'Association Between Inflammatory Diet Pattern and Risk of Colorectal Carcinoma Subtypes Classified by Immune Responses to Tumor', Gastroenterology, vol. 153, no. 6, pp. 1517-1530.e14. https://doi.org/10.1053/j.gastro.2017.08.045
Liu, Li ; Nishihara, Reiko ; Qian, Zhi Rong ; Tabung, Fred K. ; Nevo, Daniel ; Zhang, Xuehong ; Song, Mingyang ; Cao, Yin ; Mima, Kosuke ; Masugi, Yohei ; Shi, Yan ; da Silva, Annacarolina ; Twombly, Tyler ; Gu, Mancang ; Li, Wanwan ; Hamada, Tsuyoshi ; Kosumi, Keisuke ; Inamura, Kentaro ; Nowak, Jonathan A. ; Drew, David A. ; Lochhead, Paul ; Nosho, Katsuhiko ; Wu, Kana ; Wang, Molin ; Garrett, Wendy S. ; Chan, Andrew T. ; Fuchs, Charles S. ; Giovannucci, Edward L. ; Ogino, Shuji. / Association Between Inflammatory Diet Pattern and Risk of Colorectal Carcinoma Subtypes Classified by Immune Responses to Tumor. In: Gastroenterology. 2017 ; Vol. 153, No. 6. pp. 1517-1530.e14.
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abstract = "Background & Aims Dietary patterns affect systemic and local intestinal inflammation, which have been linked to colorectal carcinogenesis. Chronic inflammation can interfere with the adaptive immune response. We investigated whether the association of a diet that promotes intestinal inflammation with risk of colorectal carcinoma was stronger for tumors with lower lymphocytic reactions than tumors with higher lymphocytic reactions. Methods We collected data from the molecular pathological epidemiology databases of 2 prospective cohort studies: the Nurses’ Health Study (since 1976) and the Health Professionals Follow-Up Study (since 1986). We used duplication-method time-varying Cox proportional cause-specific hazards regression to assess the association of empirical dietary inflammatory pattern (EDIP) score (derived from food frequency questionnaire data) with colorectal carcinoma subtype. Foods that contribute to high EDIP scores include red and processed meats, refined grains, carbonated beverages, and some vegetables; foods that contribute to low EDIP scores include beer, wine, coffee, tea, yellow and leafy vegetables, and fruit juice. Colorectal tissue samples were analyzed histologically for patterns of lymphocytic reactions (Crohn's-like lymphoid reaction, peritumoral lymphocytic reaction, intratumoral periglandular reaction, and tumor-infiltrating lymphocytes). Results During follow-up of 124,433 participants, we documented 1311 incident colon and rectal cancer cases with available tissue data. The association between the EDIP and colorectal cancer risk was significant (Ptrend =.02), and varied with degree of peritumoral lymphocytic reaction (Pheterogeneity <.001). Higher EDIP scores were associated with increased risk of colorectal cancer with an absent or low peritumoral lymphocytic reaction (highest vs lowest EDIP score quintile hazard ratio, 2.60; 95{\%} confidence interval, 1.60−4.23; Ptrend <.001), but not risk of tumors with intermediate or high peritumoral lymphocytic reaction (Ptrend >.80). Conclusions In 2 prospective cohort studies, we associated inflammatory diets with a higher risk of colorectal cancer subtype that contains little or no peritumoral lymphocytic reaction. These findings suggest that diet-related inflammation might contribute to development of colorectal cancer, by suppressing the adaptive anti-tumor immune response.",
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author = "Li Liu and Reiko Nishihara and Qian, {Zhi Rong} and Tabung, {Fred K.} and Daniel Nevo and Xuehong Zhang and Mingyang Song and Yin Cao and Kosuke Mima and Yohei Masugi and Yan Shi and {da Silva}, Annacarolina and Tyler Twombly and Mancang Gu and Wanwan Li and Tsuyoshi Hamada and Keisuke Kosumi and Kentaro Inamura and Nowak, {Jonathan A.} and Drew, {David A.} and Paul Lochhead and Katsuhiko Nosho and Kana Wu and Molin Wang and Garrett, {Wendy S.} and Chan, {Andrew T.} and Fuchs, {Charles S.} and Giovannucci, {Edward L.} and Shuji Ogino",
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T1 - Association Between Inflammatory Diet Pattern and Risk of Colorectal Carcinoma Subtypes Classified by Immune Responses to Tumor

AU - Liu, Li

AU - Nishihara, Reiko

AU - Qian, Zhi Rong

AU - Tabung, Fred K.

AU - Nevo, Daniel

AU - Zhang, Xuehong

AU - Song, Mingyang

AU - Cao, Yin

AU - Mima, Kosuke

AU - Masugi, Yohei

AU - Shi, Yan

AU - da Silva, Annacarolina

AU - Twombly, Tyler

AU - Gu, Mancang

AU - Li, Wanwan

AU - Hamada, Tsuyoshi

AU - Kosumi, Keisuke

AU - Inamura, Kentaro

AU - Nowak, Jonathan A.

AU - Drew, David A.

AU - Lochhead, Paul

AU - Nosho, Katsuhiko

AU - Wu, Kana

AU - Wang, Molin

AU - Garrett, Wendy S.

AU - Chan, Andrew T.

AU - Fuchs, Charles S.

AU - Giovannucci, Edward L.

AU - Ogino, Shuji

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Background & Aims Dietary patterns affect systemic and local intestinal inflammation, which have been linked to colorectal carcinogenesis. Chronic inflammation can interfere with the adaptive immune response. We investigated whether the association of a diet that promotes intestinal inflammation with risk of colorectal carcinoma was stronger for tumors with lower lymphocytic reactions than tumors with higher lymphocytic reactions. Methods We collected data from the molecular pathological epidemiology databases of 2 prospective cohort studies: the Nurses’ Health Study (since 1976) and the Health Professionals Follow-Up Study (since 1986). We used duplication-method time-varying Cox proportional cause-specific hazards regression to assess the association of empirical dietary inflammatory pattern (EDIP) score (derived from food frequency questionnaire data) with colorectal carcinoma subtype. Foods that contribute to high EDIP scores include red and processed meats, refined grains, carbonated beverages, and some vegetables; foods that contribute to low EDIP scores include beer, wine, coffee, tea, yellow and leafy vegetables, and fruit juice. Colorectal tissue samples were analyzed histologically for patterns of lymphocytic reactions (Crohn's-like lymphoid reaction, peritumoral lymphocytic reaction, intratumoral periglandular reaction, and tumor-infiltrating lymphocytes). Results During follow-up of 124,433 participants, we documented 1311 incident colon and rectal cancer cases with available tissue data. The association between the EDIP and colorectal cancer risk was significant (Ptrend =.02), and varied with degree of peritumoral lymphocytic reaction (Pheterogeneity <.001). Higher EDIP scores were associated with increased risk of colorectal cancer with an absent or low peritumoral lymphocytic reaction (highest vs lowest EDIP score quintile hazard ratio, 2.60; 95% confidence interval, 1.60−4.23; Ptrend <.001), but not risk of tumors with intermediate or high peritumoral lymphocytic reaction (Ptrend >.80). Conclusions In 2 prospective cohort studies, we associated inflammatory diets with a higher risk of colorectal cancer subtype that contains little or no peritumoral lymphocytic reaction. These findings suggest that diet-related inflammation might contribute to development of colorectal cancer, by suppressing the adaptive anti-tumor immune response.

AB - Background & Aims Dietary patterns affect systemic and local intestinal inflammation, which have been linked to colorectal carcinogenesis. Chronic inflammation can interfere with the adaptive immune response. We investigated whether the association of a diet that promotes intestinal inflammation with risk of colorectal carcinoma was stronger for tumors with lower lymphocytic reactions than tumors with higher lymphocytic reactions. Methods We collected data from the molecular pathological epidemiology databases of 2 prospective cohort studies: the Nurses’ Health Study (since 1976) and the Health Professionals Follow-Up Study (since 1986). We used duplication-method time-varying Cox proportional cause-specific hazards regression to assess the association of empirical dietary inflammatory pattern (EDIP) score (derived from food frequency questionnaire data) with colorectal carcinoma subtype. Foods that contribute to high EDIP scores include red and processed meats, refined grains, carbonated beverages, and some vegetables; foods that contribute to low EDIP scores include beer, wine, coffee, tea, yellow and leafy vegetables, and fruit juice. Colorectal tissue samples were analyzed histologically for patterns of lymphocytic reactions (Crohn's-like lymphoid reaction, peritumoral lymphocytic reaction, intratumoral periglandular reaction, and tumor-infiltrating lymphocytes). Results During follow-up of 124,433 participants, we documented 1311 incident colon and rectal cancer cases with available tissue data. The association between the EDIP and colorectal cancer risk was significant (Ptrend =.02), and varied with degree of peritumoral lymphocytic reaction (Pheterogeneity <.001). Higher EDIP scores were associated with increased risk of colorectal cancer with an absent or low peritumoral lymphocytic reaction (highest vs lowest EDIP score quintile hazard ratio, 2.60; 95% confidence interval, 1.60−4.23; Ptrend <.001), but not risk of tumors with intermediate or high peritumoral lymphocytic reaction (Ptrend >.80). Conclusions In 2 prospective cohort studies, we associated inflammatory diets with a higher risk of colorectal cancer subtype that contains little or no peritumoral lymphocytic reaction. These findings suggest that diet-related inflammation might contribute to development of colorectal cancer, by suppressing the adaptive anti-tumor immune response.

KW - Adaptive Immune Cells

KW - BRAF

KW - CpG Island Methylator Phenotype

KW - Cyclooxygenase-2

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