Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort

Joseph A. Rothwell; Neil Murphy; Jelena Bešević; Nathalie Kliemann; Mazda Jenab; Pietro Ferrari; David Achaintre; Audrey Gicquiau; Béatrice Vozar; Augustin Scalbert; Inge Huybrechts; Heinz Freisling; Cornelia Prehn; Jerzy Adamski; Amanda J. Cross; Valeria Maria Pala; Marie Christine Boutron-Ruault; Christina C. Dahm; Kim Overvad; Inger Torhild Gram; Torkjel M. Sandanger; Guri Skeie; Paula Jakszyn; Kostas K. Tsilidis; Krasimira Aleksandrova; Matthias B. Schulze; David J. Hughes; Bethany van Guelpen; Stina Bodén; Maria José Sánchez; Julie A. Schmidt; Verena Katzke; Tilman Kühn; Sandra Colorado-Yohar; Rosario Tumino; Bas Bueno-de-Mesquita; Paolo Vineis; Giovanna Masala; Salvatore Panico; Anne Kirstine Eriksen; Anne Tjønneland; Dagfinn Aune; Elisabete Weiderpass; Gianluca Severi; Véronique Chajès; Marc J. Gunter

doi:10.1016/j.cgh.2020.11.045

Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort

Joseph A. Rothwell, Neil Murphy, Jelena Bešević, Nathalie Kliemann, Mazda Jenab, Pietro Ferrari, David Achaintre, Audrey Gicquiau, Béatrice Vozar, Augustin Scalbert, Inge Huybrechts, Heinz Freisling, Cornelia Prehn, Jerzy Adamski, Amanda J. Cross, Valeria Maria Pala, Marie Christine Boutron-Ruault, Christina C. Dahm, Kim Overvad, Inger Torhild GramTorkjel M. Sandanger, Guri Skeie, Paula Jakszyn, Kostas K. Tsilidis, Krasimira Aleksandrova, Matthias B. Schulze, David J. Hughes, Bethany van Guelpen, Stina Bodén, Maria José Sánchez, Julie A. Schmidt, Verena Katzke, Tilman Kühn, Sandra Colorado-Yohar, Rosario Tumino, Bas Bueno-de-Mesquita, Paolo Vineis, Giovanna Masala, Salvatore Panico, Anne Kirstine Eriksen, Anne Tjønneland, Dagfinn Aune, Elisabete Weiderpass, Gianluca Severi, Véronique Chajès, Marc J. Gunter

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Abstract

Background & Aims: Colorectal cancer risk can be lowered by adherence to the World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) guidelines. We derived metabolic signatures of adherence to these guidelines and tested their associations with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition cohort. Methods: Scores reflecting adherence to the WCRF/AICR recommendations (scale, 1–5) were calculated from participant data on weight maintenance, physical activity, diet, and alcohol among a discovery set of 5738 cancer-free European Prospective Investigation into Cancer and Nutrition participants with metabolomics data. Partial least-squares regression was used to derive fatty acid and endogenous metabolite signatures of the WCRF/AICR score in this group. In an independent set of 1608 colorectal cancer cases and matched controls, odds ratios (ORs) and 95% CIs were calculated for colorectal cancer risk per unit increase in WCRF/AICR score and per the corresponding change in metabolic signatures using multivariable conditional logistic regression. Results: Higher WCRF/AICR scores were characterized by metabolic signatures of increased odd-chain fatty acids, serine, glycine, and specific phosphatidylcholines. Signatures were inversely associated more strongly with colorectal cancer risk (fatty acids: OR, 0.51 per unit increase; 95% CI, 0.29–0.90; endogenous metabolites: OR, 0.62 per unit change; 95% CI, 0.50–0.78) than the WCRF/AICR score (OR, 0.93 per unit change; 95% CI, 0.86–1.00) overall. Signature associations were stronger in male compared with female participants. Conclusions: Metabolite profiles reflecting adherence to WCRF/AICR guidelines and additional lifestyle or biological risk factors were associated with colorectal cancer. Measuring a specific panel of metabolites representative of a healthy or unhealthy lifestyle may identify strata of the population at higher risk of colorectal cancer.

Original language	English
Pages (from-to)	e1061-e1082
Journal	Clinical Gastroenterology and Hepatology
Volume	20
Issue number	5
DOIs	https://doi.org/10.1016/j.cgh.2020.11.045
Publication status	Published - 1 May 2022

Keywords

Colorectal Neoplasm
Risk Factors
Targeted Metabolomics
World Cancer Research Fund/American Institute for Cancer Research Recommendations

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10.1016/j.cgh.2020.11.045

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Rothwell, J. A., Murphy, N., Bešević, J., Kliemann, N., Jenab, M., Ferrari, P., Achaintre, D., Gicquiau, A., Vozar, B., Scalbert, A., Huybrechts, I., Freisling, H., Prehn, C., Adamski, J., Cross, A. J., Pala, V. M., Boutron-Ruault, M. C., Dahm, C. C., Overvad, K., ... Gunter, M. J. (2022). Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort. Clinical Gastroenterology and Hepatology, 20(5), e1061-e1082. https://doi.org/10.1016/j.cgh.2020.11.045

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title = "Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort",

abstract = "Background & Aims: Colorectal cancer risk can be lowered by adherence to the World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) guidelines. We derived metabolic signatures of adherence to these guidelines and tested their associations with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition cohort. Methods: Scores reflecting adherence to the WCRF/AICR recommendations (scale, 1–5) were calculated from participant data on weight maintenance, physical activity, diet, and alcohol among a discovery set of 5738 cancer-free European Prospective Investigation into Cancer and Nutrition participants with metabolomics data. Partial least-squares regression was used to derive fatty acid and endogenous metabolite signatures of the WCRF/AICR score in this group. In an independent set of 1608 colorectal cancer cases and matched controls, odds ratios (ORs) and 95% CIs were calculated for colorectal cancer risk per unit increase in WCRF/AICR score and per the corresponding change in metabolic signatures using multivariable conditional logistic regression. Results: Higher WCRF/AICR scores were characterized by metabolic signatures of increased odd-chain fatty acids, serine, glycine, and specific phosphatidylcholines. Signatures were inversely associated more strongly with colorectal cancer risk (fatty acids: OR, 0.51 per unit increase; 95% CI, 0.29–0.90; endogenous metabolites: OR, 0.62 per unit change; 95% CI, 0.50–0.78) than the WCRF/AICR score (OR, 0.93 per unit change; 95% CI, 0.86–1.00) overall. Signature associations were stronger in male compared with female participants. Conclusions: Metabolite profiles reflecting adherence to WCRF/AICR guidelines and additional lifestyle or biological risk factors were associated with colorectal cancer. Measuring a specific panel of metabolites representative of a healthy or unhealthy lifestyle may identify strata of the population at higher risk of colorectal cancer.",

keywords = "Colorectal Neoplasm, Risk Factors, Targeted Metabolomics, World Cancer Research Fund/American Institute for Cancer Research Recommendations",

author = "Rothwell, {Joseph A.} and Neil Murphy and Jelena Be{\v s}evi{\'c} and Nathalie Kliemann and Mazda Jenab and Pietro Ferrari and David Achaintre and Audrey Gicquiau and B{\'e}atrice Vozar and Augustin Scalbert and Inge Huybrechts and Heinz Freisling and Cornelia Prehn and Jerzy Adamski and Cross, {Amanda J.} and Pala, {Valeria Maria} and Boutron-Ruault, {Marie Christine} and Dahm, {Christina C.} and Kim Overvad and Gram, {Inger Torhild} and Sandanger, {Torkjel M.} and Guri Skeie and Paula Jakszyn and Tsilidis, {Kostas K.} and Krasimira Aleksandrova and Schulze, {Matthias B.} and Hughes, {David J.} and {van Guelpen}, Bethany and Stina Bod{\'e}n and S{\'a}nchez, {Maria Jos{\'e}} and Schmidt, {Julie A.} and Verena Katzke and Tilman K{\"u}hn and Sandra Colorado-Yohar and Rosario Tumino and Bas Bueno-de-Mesquita and Paolo Vineis and Giovanna Masala and Salvatore Panico and Eriksen, {Anne Kirstine} and Anne Tj{\o}nneland and Dagfinn Aune and Elisabete Weiderpass and Gianluca Severi and V{\'e}ronique Chaj{\`e}s and Gunter, {Marc J.}",

note = "Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = may,

day = "1",

doi = "10.1016/j.cgh.2020.11.045",

language = "English",

volume = "20",

pages = "e1061--e1082",

journal = "Clinical Gastroenterology and Hepatology",

issn = "1542-3565",

number = "5",

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Rothwell, JA, Murphy, N, Bešević, J, Kliemann, N, Jenab, M, Ferrari, P, Achaintre, D, Gicquiau, A, Vozar, B, Scalbert, A, Huybrechts, I, Freisling, H, Prehn, C, Adamski, J, Cross, AJ, Pala, VM, Boutron-Ruault, MC, Dahm, CC, Overvad, K, Gram, IT, Sandanger, TM, Skeie, G, Jakszyn, P, Tsilidis, KK, Aleksandrova, K, Schulze, MB, Hughes, DJ, van Guelpen, B, Bodén, S, Sánchez, MJ, Schmidt, JA, Katzke, V, Kühn, T, Colorado-Yohar, S, Tumino, R, Bueno-de-Mesquita, B, Vineis, P, Masala, G, Panico, S, Eriksen, AK, Tjønneland, A, Aune, D, Weiderpass, E, Severi, G, Chajès, V & Gunter, MJ 2022, 'Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort', Clinical Gastroenterology and Hepatology, vol. 20, no. 5, pp. e1061-e1082. https://doi.org/10.1016/j.cgh.2020.11.045

TY - JOUR

T1 - Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort

AU - Rothwell, Joseph A.

AU - Murphy, Neil

AU - Bešević, Jelena

AU - Kliemann, Nathalie

AU - Jenab, Mazda

AU - Ferrari, Pietro

AU - Achaintre, David

AU - Gicquiau, Audrey

AU - Vozar, Béatrice

AU - Scalbert, Augustin

AU - Huybrechts, Inge

AU - Freisling, Heinz

AU - Prehn, Cornelia

AU - Adamski, Jerzy

AU - Cross, Amanda J.

AU - Pala, Valeria Maria

AU - Boutron-Ruault, Marie Christine

AU - Dahm, Christina C.

AU - Overvad, Kim

AU - Gram, Inger Torhild

AU - Sandanger, Torkjel M.

AU - Skeie, Guri

AU - Jakszyn, Paula

AU - Tsilidis, Kostas K.

AU - Aleksandrova, Krasimira

AU - Schulze, Matthias B.

AU - Hughes, David J.

AU - van Guelpen, Bethany

AU - Bodén, Stina

AU - Sánchez, Maria José

AU - Schmidt, Julie A.

AU - Katzke, Verena

AU - Kühn, Tilman

AU - Colorado-Yohar, Sandra

AU - Tumino, Rosario

AU - Bueno-de-Mesquita, Bas

AU - Vineis, Paolo

AU - Masala, Giovanna

AU - Panico, Salvatore

AU - Eriksen, Anne Kirstine

AU - Tjønneland, Anne

AU - Aune, Dagfinn

AU - Weiderpass, Elisabete

AU - Severi, Gianluca

AU - Chajès, Véronique

AU - Gunter, Marc J.

PY - 2022/5/1

Y1 - 2022/5/1

N2 - Background & Aims: Colorectal cancer risk can be lowered by adherence to the World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) guidelines. We derived metabolic signatures of adherence to these guidelines and tested their associations with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition cohort. Methods: Scores reflecting adherence to the WCRF/AICR recommendations (scale, 1–5) were calculated from participant data on weight maintenance, physical activity, diet, and alcohol among a discovery set of 5738 cancer-free European Prospective Investigation into Cancer and Nutrition participants with metabolomics data. Partial least-squares regression was used to derive fatty acid and endogenous metabolite signatures of the WCRF/AICR score in this group. In an independent set of 1608 colorectal cancer cases and matched controls, odds ratios (ORs) and 95% CIs were calculated for colorectal cancer risk per unit increase in WCRF/AICR score and per the corresponding change in metabolic signatures using multivariable conditional logistic regression. Results: Higher WCRF/AICR scores were characterized by metabolic signatures of increased odd-chain fatty acids, serine, glycine, and specific phosphatidylcholines. Signatures were inversely associated more strongly with colorectal cancer risk (fatty acids: OR, 0.51 per unit increase; 95% CI, 0.29–0.90; endogenous metabolites: OR, 0.62 per unit change; 95% CI, 0.50–0.78) than the WCRF/AICR score (OR, 0.93 per unit change; 95% CI, 0.86–1.00) overall. Signature associations were stronger in male compared with female participants. Conclusions: Metabolite profiles reflecting adherence to WCRF/AICR guidelines and additional lifestyle or biological risk factors were associated with colorectal cancer. Measuring a specific panel of metabolites representative of a healthy or unhealthy lifestyle may identify strata of the population at higher risk of colorectal cancer.

AB - Background & Aims: Colorectal cancer risk can be lowered by adherence to the World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) guidelines. We derived metabolic signatures of adherence to these guidelines and tested their associations with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition cohort. Methods: Scores reflecting adherence to the WCRF/AICR recommendations (scale, 1–5) were calculated from participant data on weight maintenance, physical activity, diet, and alcohol among a discovery set of 5738 cancer-free European Prospective Investigation into Cancer and Nutrition participants with metabolomics data. Partial least-squares regression was used to derive fatty acid and endogenous metabolite signatures of the WCRF/AICR score in this group. In an independent set of 1608 colorectal cancer cases and matched controls, odds ratios (ORs) and 95% CIs were calculated for colorectal cancer risk per unit increase in WCRF/AICR score and per the corresponding change in metabolic signatures using multivariable conditional logistic regression. Results: Higher WCRF/AICR scores were characterized by metabolic signatures of increased odd-chain fatty acids, serine, glycine, and specific phosphatidylcholines. Signatures were inversely associated more strongly with colorectal cancer risk (fatty acids: OR, 0.51 per unit increase; 95% CI, 0.29–0.90; endogenous metabolites: OR, 0.62 per unit change; 95% CI, 0.50–0.78) than the WCRF/AICR score (OR, 0.93 per unit change; 95% CI, 0.86–1.00) overall. Signature associations were stronger in male compared with female participants. Conclusions: Metabolite profiles reflecting adherence to WCRF/AICR guidelines and additional lifestyle or biological risk factors were associated with colorectal cancer. Measuring a specific panel of metabolites representative of a healthy or unhealthy lifestyle may identify strata of the population at higher risk of colorectal cancer.

KW - Colorectal Neoplasm

KW - Risk Factors

KW - Targeted Metabolomics

KW - World Cancer Research Fund/American Institute for Cancer Research Recommendations

UR - http://www.scopus.com/inward/record.url?scp=85109819565&partnerID=8YFLogxK

U2 - 10.1016/j.cgh.2020.11.045

DO - 10.1016/j.cgh.2020.11.045

M3 - Article

C2 - 33279777

AN - SCOPUS:85109819565

SN - 1542-3565

VL - 20

SP - e1061-e1082

JO - Clinical Gastroenterology and Hepatology

JF - Clinical Gastroenterology and Hepatology

IS - 5

ER -

Metabolic Signatures of Healthy Lifestyle Patterns and Colorectal Cancer Risk in a European Cohort

Abstract

Keywords

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