Pan-cancer analysis of pre-diagnostic blood metabolite concentrations in the European Prospective Investigation into Cancer and Nutrition.


Journal

BMC medicine
ISSN: 1741-7015
Titre abrégé: BMC Med
Pays: England
ID NLM: 101190723

Informations de publication

Date de publication:
19 10 2022
Historique:
received: 30 03 2022
accepted: 05 09 2022
entrez: 18 10 2022
pubmed: 19 10 2022
medline: 21 10 2022
Statut: epublish

Résumé

Epidemiological studies of associations between metabolites and cancer risk have typically focused on specific cancer types separately. Here, we designed a multivariate pan-cancer analysis to identify metabolites potentially associated with multiple cancer types, while also allowing the investigation of cancer type-specific associations. We analysed targeted metabolomics data available for 5828 matched case-control pairs from cancer-specific case-control studies on breast, colorectal, endometrial, gallbladder, kidney, localized and advanced prostate cancer, and hepatocellular carcinoma nested within the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. From pre-diagnostic blood levels of an initial set of 117 metabolites, 33 cluster representatives of strongly correlated metabolites and 17 single metabolites were derived by hierarchical clustering. The mutually adjusted associations of the resulting 50 metabolites with cancer risk were examined in penalized conditional logistic regression models adjusted for body mass index, using the data-shared lasso penalty. Out of the 50 studied metabolites, (i) six were inversely associated with the risk of most cancer types: glutamine, butyrylcarnitine, lysophosphatidylcholine a C18:2, and three clusters of phosphatidylcholines (PCs); (ii) three were positively associated with most cancer types: proline, decanoylcarnitine, and one cluster of PCs; and (iii) 10 were specifically associated with particular cancer types, including histidine that was inversely associated with colorectal cancer risk and one cluster of sphingomyelins that was inversely associated with risk of hepatocellular carcinoma and positively with endometrial cancer risk. These results could provide novel insights for the identification of pathways for cancer development, in particular those shared across different cancer types.

Sections du résumé

BACKGROUND
Epidemiological studies of associations between metabolites and cancer risk have typically focused on specific cancer types separately. Here, we designed a multivariate pan-cancer analysis to identify metabolites potentially associated with multiple cancer types, while also allowing the investigation of cancer type-specific associations.
METHODS
We analysed targeted metabolomics data available for 5828 matched case-control pairs from cancer-specific case-control studies on breast, colorectal, endometrial, gallbladder, kidney, localized and advanced prostate cancer, and hepatocellular carcinoma nested within the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. From pre-diagnostic blood levels of an initial set of 117 metabolites, 33 cluster representatives of strongly correlated metabolites and 17 single metabolites were derived by hierarchical clustering. The mutually adjusted associations of the resulting 50 metabolites with cancer risk were examined in penalized conditional logistic regression models adjusted for body mass index, using the data-shared lasso penalty.
RESULTS
Out of the 50 studied metabolites, (i) six were inversely associated with the risk of most cancer types: glutamine, butyrylcarnitine, lysophosphatidylcholine a C18:2, and three clusters of phosphatidylcholines (PCs); (ii) three were positively associated with most cancer types: proline, decanoylcarnitine, and one cluster of PCs; and (iii) 10 were specifically associated with particular cancer types, including histidine that was inversely associated with colorectal cancer risk and one cluster of sphingomyelins that was inversely associated with risk of hepatocellular carcinoma and positively with endometrial cancer risk.
CONCLUSIONS
These results could provide novel insights for the identification of pathways for cancer development, in particular those shared across different cancer types.

Identifiants

pubmed: 36258205
doi: 10.1186/s12916-022-02553-4
pii: 10.1186/s12916-022-02553-4
pmc: PMC9580145
doi:

Substances chimiques

Sphingomyelins 0
Lysophosphatidylcholines 0
Glutamine 0RH81L854J
Histidine 4QD397987E
Phosphatidylcholines 0
Proline 9DLQ4CIU6V

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

351

Subventions

Organisme : Cancer Research UK
ID : 24390
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M012190/1
Pays : United Kingdom

Informations de copyright

© 2022. The Author(s).

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Auteurs

Marie Breeur (M)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Pietro Ferrari (P)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Laure Dossus (L)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Mazda Jenab (M)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Mattias Johansson (M)

Genetics Branch, International Agency for Research on Cancer, 69372 CEDEX 08, Lyon, France.

Sabina Rinaldi (S)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Ruth C Travis (RC)

Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, OX3 7LF, UK.

Mathilde His (M)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Tim J Key (TJ)

Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, OX3 7LF, UK.

Julie A Schmidt (JA)

Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, OX3 7LF, UK.
Department of Clinical Epidemiology, Department of Clinical Medicine, Aarhus University Hospital and Aarhus University, DK-8200, Aarhus N, Denmark.

Kim Overvad (K)

Department of Public Health, Aarhus University, DK-8000, Aarhus C, Denmark.

Anne Tjønneland (A)

Danish Cancer Society Research Center Diet, Genes and Environment Nutrition and Biomarkers, DK-2100, Copenhagen, Denmark.

Cecilie Kyrø (C)

Danish Cancer Society Research Center Diet, Genes and Environment Nutrition and Biomarkers, DK-2100, Copenhagen, Denmark.

Joseph A Rothwell (JA)

Université Paris-Saclay, UVSQ, Inserm, CESP U1018, "Exposome and Heredity" team, Gustave Roussy, 94800, Villejuif, France.

Nasser Laouali (N)

Université Paris-Saclay, UVSQ, Inserm, CESP U1018, "Exposome and Heredity" team, Gustave Roussy, 94800, Villejuif, France.

Gianluca Severi (G)

Université Paris-Saclay, UVSQ, Inserm, CESP U1018, "Exposome and Heredity" team, Gustave Roussy, 94800, Villejuif, France.

Rudolf Kaaks (R)

Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), 69120, Heidelberg, Germany.

Verena Katzke (V)

Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), 69120, Heidelberg, Germany.

Matthias B Schulze (MB)

Department of Molecular Epidemiology, German Institute of Human Nutrition, 14558, Nuthetal, Germany.

Fabian Eichelmann (F)

Department of Molecular Epidemiology, German Institute of Human Nutrition, 14558, Nuthetal, Germany.
German Center for Diabetes Research (DZD), 85764, Neuherberg, Germany.

Domenico Palli (D)

Institute of Cancer Research, Prevention and Clinical Network (ISPRO), 50139, Florence, Italy.

Sara Grioni (S)

Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, 20133, Milan, Italy.

Salvatore Panico (S)

Dipartimento di Medicina Clinica e Chirurgia, Federico II University, 80131, Naples, Italy.

Rosario Tumino (R)

Hyblean Association for Epidemiological Research, AIRE-ONLUS, 97100, Ragusa, Italy.

Carlotta Sacerdote (C)

Unit of Cancer Epidemiology Città della Salute e della Scienza University-Hospital, 10126, Turin, Italy.

Bas Bueno-de-Mesquita (B)

Centre for Nutrition, Prevention and Health Services, National Institute for Public Health and the Environment (RIVM), PO Box 1, 3720, BA, Bilthoven, The Netherlands.

Karina Standahl Olsen (KS)

Department of Community Medicine, UiT The Arctic University of Norway, N-9037, Tromsø, Norway.

Torkjel Manning Sandanger (TM)

Department of Community Medicine, UiT The Arctic University of Norway, N-9037, Tromsø, Norway.

Therese Haugdahl Nøst (TH)

Department of Community Medicine, UiT The Arctic University of Norway, N-9037, Tromsø, Norway.

J Ramón Quirós (JR)

Public Health Directorate, 33006, Oviedo, Asturias, Spain.

Catalina Bonet (C)

Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO), Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, 08908, Barcelona, Spain.

Miguel Rodríguez Barranco (MR)

Escuela Andaluza de Salud Pública (EASP), 18011, Granada, Spain.
Instituto de Investigación Biosanitaria ibs. GRANADA, 18012, Granada, Spain.
Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), 28029, Madrid, Spain.

María-Dolores Chirlaque (MD)

Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), 28029, Madrid, Spain.
Department of Epidemiology, Regional Health Council, IMIB-Arrixaca, Murcia University, 30003, Murcia, Spain.

Eva Ardanaz (E)

Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), 28029, Madrid, Spain.
Navarra Public Health Institute, 31003, Pamplona, Spain.
IdiSNA, Navarra Institute for Health Research, 31008, Pamplona, Spain.

Malte Sandsveden (M)

Department of Clinical Sciences Malmö Lund University, SE-214 28, Malmö, Sweden.

Jonas Manjer (J)

Departement of Surgery, Skåne University Hospital Malmö, Lund University, SE-214 28, Malmö, Sweden.

Linda Vidman (L)

Department of Radiation Sciences, Oncology Umeå University, SE-901 87, Umeå, Sweden.

Matilda Rentoft (M)

Department of Radiation Sciences, Oncology Umeå University, SE-901 87, Umeå, Sweden.

David Muller (D)

Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, W2 1PG, UK.

Kostas Tsilidis (K)

Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, W2 1PG, UK.

Alicia K Heath (AK)

Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, W2 1PG, UK.

Hector Keun (H)

Department of Surgery and Cancer, Cancer Metabolism and Systems Toxicology Group, Division of Cancer, Imperial College London, London, SW7 2AZ, UK.

Jerzy Adamski (J)

Institute of Experimental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764, Neuherberg, Germany.
Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117597, Singapore.
Institute of Biochemistry, Faculty of Medicine, University of Ljubljana, 1000, Ljubljana, Slovenia.

Pekka Keski-Rahkonen (P)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Augustin Scalbert (A)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Marc J Gunter (MJ)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France.

Vivian Viallon (V)

Nutrition and Metabolism Branch, International Agency for Research on Cancer, NME Branch, 69372 CEDEX 08, Lyon, France. viallonv@iarc.who.int.

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