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

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 associatio...

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Main Authors: 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
Format: Article
Language:English
Published: MDPI AG 2023-06-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/13/6/744
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author 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
author_facet 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
author_sort Dong Hoon Lee
collection DOAJ
description 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.
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spelling doaj.art-34123ceeec9e45459a6aadec9c90b2c02023-11-18T11:35:07ZengMDPI AGMetabolites2218-19892023-06-0113674410.3390/metabo13060744Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal CancerDong Hoon Lee0Qi Jin1Ni Shi2Fenglei Wang3Alaina M. Bever4Jun Li5Liming Liang6Frank B. Hu7Mingyang Song8Oana A. Zeleznik9Xuehong Zhang10Amit Joshi11Kana Wu12Justin Y. Jeon13Jeffrey A. Meyerhardt14Andrew T. Chan15A. Heather Eliassen16Clary B. Clish17Steven K. Clinton18Edward L. Giovannucci19Fred K. Tabung20Department of Sport Industry Studies, Yonsei University, Seoul 03722, Republic of KoreaDepartment of Exercise and Nutrition Sciences, Moyes College of Education, Weber State University, Ogden, UT 84408, USAComprehensive Cancer Center, The Ohio State University, Columbus, OH 43210, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USAChanning Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USAChanning Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USAClinical and Translational Epidemiology Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Sport Industry Studies, Yonsei University, Seoul 03722, Republic of KoreaDepartment of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USAChanning Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USAComprehensive Cancer Center, The Ohio State University, Columbus, OH 43210, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USADepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USAThe 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.https://www.mdpi.com/2218-1989/13/6/744empirical dietary inflammatory patterninflammation biomarkersempirical dietary index for hyperinsulinemiaC-peptideplasma metabolomic profilescolorectal cancer
spellingShingle 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
Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer
Metabolites
empirical dietary inflammatory pattern
inflammation biomarkers
empirical dietary index for hyperinsulinemia
C-peptide
plasma metabolomic profiles
colorectal cancer
title Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer
title_full Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer
title_fullStr Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer
title_full_unstemmed Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer
title_short Dietary Inflammatory and Insulinemic Potentials, Plasma Metabolome and Risk of Colorectal Cancer
title_sort dietary inflammatory and insulinemic potentials plasma metabolome and risk of colorectal cancer
topic empirical dietary inflammatory pattern
inflammation biomarkers
empirical dietary index for hyperinsulinemia
C-peptide
plasma metabolomic profiles
colorectal cancer
url https://www.mdpi.com/2218-1989/13/6/744
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