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

Authors :
Marie Breeur
Pietro Ferrari
Laure Dossus
Mazda Jenab
Mattias Johansson
Sabina Rinaldi
Ruth C. Travis
Mathilde His
Tim J. Key
Julie A. Schmidt
Kim Overvad
Anne Tjønneland
Cecilie Kyrø
Joseph A. Rothwell
Nasser Laouali
Gianluca Severi
Rudolf Kaaks
Verena Katzke
Matthias B. Schulze
Fabian Eichelmann
Domenico Palli
Sara Grioni
Salvatore Panico
Rosario Tumino
Carlotta Sacerdote
Bas Bueno-de-Mesquita
Karina Standahl Olsen
Torkjel Manning Sandanger
Therese Haugdahl Nøst
J. Ramón Quirós
Catalina Bonet
Miguel Rodríguez Barranco
María-Dolores Chirlaque
Eva Ardanaz
Malte Sandsveden
Jonas Manjer
Linda Vidman
Matilda Rentoft
David Muller
Kostas Tsilidis
Alicia K. Heath
Hector Keun
Jerzy Adamski
Pekka Keski-Rahkonen
Augustin Scalbert
Marc J. Gunter
Vivian Viallon
Cancer Research UK
Centre International de Recherche contre le Cancer - International Agency for Research on Cancer (CIRC - IARC)
Organisation Mondiale de la Santé / World Health Organization Office (OMS / WHO)
Centre de recherche en épidémiologie et santé des populations (CESP)
Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Hôpital Paul Brousse-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Saclay
Kræftens Bekæmpelse, DCS
Deutsches Krebsforschungszentrum, DKFZ
Centre International de Recherche sur le Cancer, CIRC: 2014/1183, C8221/A19170
Seventh Framework Programme, FP7: 2014/1193, 313010, C19335/A21351
National Research Council, NRC
World Cancer Research Fund International, WCRF
University of Maryland School of Public Health, SPH
Medical Research Council, MRC: MR/M012190/1
Cancer Research UK, CRUK: C8221/A29017
World Cancer Research Fund, WCRF
Imperial College London
European Commission, EC
Institut National de la Santé et de la Recherche Médicale, Inserm
Bundesministerium für Bildung und Forschung, BMBF
Cancerfonden
Generalitat de Catalunya
Ministerie van Volksgezondheid, Welzijn en Sport, VWS
Fondation ARC pour la Recherche sur le Cancer, ARC
Ligue Contre le Cancer
Vetenskapsrådet, VR
Instituto de Salud Carlos III, ISCIII
Associazione Italiana per la Ricerca sul Cancro, AIRC
Deutsche Krebshilfe
Institut National Du Cancer, INCa: 2009-139, 2013/1002, 2014-1-RT-02-CIRC-1, 2015-166
Institut Gustave-Roussy
Mutuelle Générale de l'Education Nationale, MGEN
Consejería de Salud y Familias, Junta de Andalucía
NIHR Imperial Biomedical Research Centre, BRC
The coordination of EPIC is financially supported by International Agency for Research on Cancer (IARC) and by the Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, which has additional infrastructure support provided by the NIHR Imperial Biomedical Research Centre (BRC).
This paper is dedicated to the memory our of colleague Dr. Bas Bueno-de-Mesquita. Where authors are identified as personnel of the International Agency for Research on Cancer/World Health Organization, the authors alone are responsible for the views expressed in this article and they do not necessarily represent the decisions, policy, or views of the International Agency for Research on Cancer/World Health Organization.
The national cohorts are supported by Danish Cancer Society (Denmark)
Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l’Education Nationale, Institut National de la Santé et de la Recherche Médicale (INSERM) (France)
German Cancer Aid, German Cancer Research Center (DKFZ), German Institute of Human Nutrition Potsdam-Rehbruecke (DIfE), Federal Ministry of Education and Research (BMBF) (Germany)
Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy, Compagnia di SanPaolo and National Research Council (Italy)
Dutch Ministry of Public Health, Welfare and Sports (VWS), Netherlands Cancer Registry (NKR), LK Research Funds, Dutch Prevention Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF), Statistics Netherlands (The Netherlands)
Health Research Fund (FIS) - Instituto de Salud Carlos III (ISCIII), Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, and the Catalan Institute of Oncology - ICO (Spain)
Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Västerbotten (Sweden)
Cancer Research UK (14136 to EPIC-Norfolk
C8221/A29017 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk
MR/M012190/1 to EPIC-Oxford) (UK). IDIBELL acknowledges support from the Generalitat de Catalunya through the CERCA Program. The breast cancer study was funded by the French National Cancer Institute (grant number 2015-166). The colorectal cancer studies were funded by World Cancer Research Fund (reference: 2013/1002
reference: 313010
reference: 2014/1193
INCa
grant numbers 2009-139 and 2014-1-RT-02-CIRC-1) and by internal funds of the IARC. For the participants in the prostate cancer study, sample retrieval and preparation, and assays of metabolites were supported by Cancer Research UK (C8221/A19170), and funding for grant 2014/1183 was obtained from the World Cancer Research Fund (WCRF UK), as part of the World Cancer Research Fund International grant programme. Mathilde His’ work reported here was undertaken during the tenure of a postdoctoral fellowship awarded by the International Agency for Research on Cancer, financed by the Fondation ARC. The funders were not involved in designing the study
collecting, analysing, and interpreting results
or writing and submitting the manuscript for publication.
HAL UVSQ, Équipe
Source :
BMC Med. 20:351 (2022), Breeur, M, Ferrari, P, Dossus, L, Jenab, M, Johansson, M, Rinaldi, S, Travis, R C, His, M, Key, T J, Schmidt, J A, Overvad, K, Tjønneland, A, Kyrø, C, Rothwell, J A, Laouali, N, Severi, G, Kaaks, R, Katzke, V, Schulze, M B, Eichelmann, F, Palli, D, Grioni, S, Panico, S, Tumino, R, Sacerdote, C, Bueno-de-Mesquita, B, Olsen, K S, Sandanger, T M, Nøst, T H, Quirós, J R, Bonet, C, Barranco, M R, Chirlaque, M-D, Ardanaz, E, Sandsveden, M, Manjer, J, Vidman, L, Rentoft, M, Muller, D, Tsilidis, K, Heath, A K, Keun, H, Adamski, J, Keski-Rahkonen, P, Scalbert, A, Gunter, M J & Viallon, V 2022, ' Pan-cancer analysis of pre-diagnostic blood metabolite concentrations in the European Prospective Investigation into Cancer and Nutrition ', BMC Medicine, vol. 20, no. 1, 351 . https://doi.org/10.1186/s12916-022-02553-4, BMC Medicine, BMC Medicine, 2022, 20 (1), pp.351. ⟨10.1186/s12916-022-02553-4⟩
Publication Year :
2022
Publisher :
Umeå universitet, Onkologi, 2022.

Abstract

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.

Details

Language :
English
ISSN :
17417015
Database :
OpenAIRE
Journal :
BMC Med. 20:351 (2022), Breeur, M, Ferrari, P, Dossus, L, Jenab, M, Johansson, M, Rinaldi, S, Travis, R C, His, M, Key, T J, Schmidt, J A, Overvad, K, Tjønneland, A, Kyrø, C, Rothwell, J A, Laouali, N, Severi, G, Kaaks, R, Katzke, V, Schulze, M B, Eichelmann, F, Palli, D, Grioni, S, Panico, S, Tumino, R, Sacerdote, C, Bueno-de-Mesquita, B, Olsen, K S, Sandanger, T M, Nøst, T H, Quirós, J R, Bonet, C, Barranco, M R, Chirlaque, M-D, Ardanaz, E, Sandsveden, M, Manjer, J, Vidman, L, Rentoft, M, Muller, D, Tsilidis, K, Heath, A K, Keun, H, Adamski, J, Keski-Rahkonen, P, Scalbert, A, Gunter, M J & Viallon, V 2022, ' Pan-cancer analysis of pre-diagnostic blood metabolite concentrations in the European Prospective Investigation into Cancer and Nutrition ', BMC Medicine, vol. 20, no. 1, 351 . https://doi.org/10.1186/s12916-022-02553-4, BMC Medicine, BMC Medicine, 2022, 20 (1), pp.351. ⟨10.1186/s12916-022-02553-4⟩
Accession number :
edsair.doi.dedup.....527be4cd7ccff29ea77eab9cd5066ad2