Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer

Dong Hoon Lee; Qi Jin; Ni Shi; Fenglei Wang; Alaina M Bever; Jun Li; Liming Liang; Frank B Hu; Mingyang Song; Oana A Zeleznik; Xuehong Zhang; Amit Joshi; Kana Wu; Justin Y Jeon; Jeffrey A Meyerhardt; Andrew T Chan; A Heather Eliassen; Clary B Clish; Steven K Clinton; Edward L Giovannucci; Fred K Tabung

doi:10.3390/metabo13060744

Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer

Metabolites. 2023 Jun 12;13(6):744. doi: 10.3390/metabo13060744.

Authors

Dong Hoon Lee^{1

2}, Qi Jin^{3

4

5}, Ni Shi^{4

6}, Fenglei Wang², Alaina M Bever^{7

8}, Jun Li^{2

7}, Liming Liang^{7

9

10}, Frank B Hu^{2

7

10}, Mingyang Song^{2

7

11

12}, Oana A Zeleznik¹⁰, Xuehong Zhang¹⁰, Amit Joshi^{11

12}, Kana Wu², Justin Y Jeon^{1

13}, Jeffrey A Meyerhardt¹⁴, Andrew T Chan^{10

11

12

15

16}, A Heather Eliassen^{2

7

10}, Clary B Clish¹⁶, Steven K Clinton^{4

5

6}, Edward L Giovannucci^{2

7}, Fred K Tabung^{2

4

5

6

17}

Affiliations

¹ Department of Sport Industry Studies, Yonsei University, Seoul 03722, Republic of Korea.
² Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
³ Department of Exercise and Nutrition Sciences, Moyes College of Education, Weber State University, Ogden, UT 84408, USA.
⁴ Comprehensive Cancer Center, The Ohio State University, Columbus, OH 43210, USA.
⁵ Interdisciplinary Ph.D. Program in Nutrition, The Ohio State University, Columbus, OH 43210, USA.
⁶ Division of Medical Oncology, Department of Internal Medicine, College of Medicine, The Ohio State University, Columbus, OH 43210, USA.
⁷ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
⁸ Harvard-MIT Division of Health Sciences and Technology, Harvard Medical School, Boston, MA 02115, USA.
⁹ Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹⁰ Channing Division of Network Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
¹¹ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
¹² Division of Gastroenterology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
¹³ Cancer Prevention Center, Yonsei Cancer Center, Seoul 03722, Republic of Korea.
¹⁴ Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA.
¹⁵ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
¹⁶ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹⁷ Division of Epidemiology, College of Public Health, The Ohio State University, Columbus, OH 43220, USA.

Abstract

The inflammatory and insulinemic potentials of diets have been associated with colorectal cancer risk. However, it is unknown whether the plasma metabolite profiles related to inflammatory diets, or to insulinemic diets, underlie this association. The aim of this study was to evaluate the association between metabolomic profile scores related to the food-based empirical dietary inflammatory patterns (EDIP), the empirical dietary index for hyperinsulinemia (EDIH), and plasma inflammation (CRP, IL-6, TNFα-R2, adiponectin) and insulin (C-peptide) biomarkers, and colorectal cancer risk. Elastic net regression was used to derive three metabolomic profile scores for each dietary pattern among 6840 participants from the Nurses' Health Study and Health Professionals Follow-up Study, and associations with CRC risk were examined using multivariable-adjusted logistic regression, in a case-control study of 524 matched pairs nested in both cohorts. Among 186 known metabolites, 27 were significantly associated with both the EDIP and inflammatory biomarkers, and 21 were significantly associated with both the EDIH and C-peptide. In men, odds ratios (ORs) of colorectal cancer, per 1 standard deviation (SD) increment in metabolomic score, were 1.91 (1.31-2.78) for the common EDIP and inflammatory-biomarker metabolome, 1.12 (0.78-1.60) for EDIP-only metabolome, and 1.65 (1.16-2.36) for the inflammatory-biomarkers-only metabolome. However, no association was found for EDIH-only, C-peptide-only, and the common metabolomic signatures in men. Moreover, the metabolomic signatures were not associated with colorectal cancer risk among women. Metabolomic profiles reflecting pro-inflammatory diets and inflammation biomarkers were associated with colorectal cancer risk in men, while no association was found in women. Larger studies are needed to confirm our findings.

Keywords: C-peptide; colorectal cancer; empirical dietary index for hyperinsulinemia; empirical dietary inflammatory pattern; inflammation biomarkers; plasma metabolomic profiles.

Abstract

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