Prospective analysis of circulating metabolites and breast cancer in EPIC

Mathilde His; Vivian Viallon; Laure Dossus; Audrey Gicquiau; David Achaintre; Augustin Scalbert; Pietro Ferrari; Isabelle Romieu; N Charlotte Onland-Moret; Elisabete Weiderpass; Christina C Dahm; Kim Overvad; Anja Olsen; Anne Tjønneland; Agnès Fournier; Joseph A Rothwell; Gianluca Severi; Tilman Kühn; Renée T Fortner; Heiner Boeing; Antonia Trichopoulou; Anna Karakatsani; Georgia Martimianaki; Giovanna Masala; Sabina Sieri; Rosario Tumino; Paolo Vineis; Salvatore Panico; Carla H van Gils; Therese H Nøst; Torkjel M Sandanger; Guri Skeie; J Ramón Quirós; Antonio Agudo; Maria-Jose Sánchez; Pilar Amiano; José María Huerta; Eva Ardanaz; Julie A Schmidt; Ruth C Travis; Elio Riboli; Konstantinos K Tsilidis; Sofia Christakoudi; Marc J Gunter; Sabina Rinaldi

doi:10.1186/s12916-019-1408-4

Prospective analysis of circulating metabolites and breast cancer in EPIC

Mathilde His, Vivian Viallon, Laure Dossus, Audrey Gicquiau, David Achaintre, Augustin Scalbert, Pietro Ferrari, Isabelle Romieu, N Charlotte Onland-Moret, Elisabete Weiderpass, Christina C Dahm, Kim Overvad, Anja Olsen, Anne Tjønneland, Agnès Fournier, Joseph A Rothwell, Gianluca Severi, Tilman Kühn, Renée T Fortner, Heiner BoeingAntonia Trichopoulou, Anna Karakatsani, Georgia Martimianaki, Giovanna Masala, Sabina Sieri, Rosario Tumino, Paolo Vineis, Salvatore Panico, Carla H van Gils, Therese H Nøst, Torkjel M Sandanger, Guri Skeie, J Ramón Quirós, Antonio Agudo, Maria-Jose Sánchez, Pilar Amiano, José María Huerta, Eva Ardanaz, Julie A Schmidt, Ruth C Travis, Elio Riboli, Konstantinos K Tsilidis, Sofia Christakoudi, Marc J Gunter, Sabina Rinaldi

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Abstract

BACKGROUND: Metabolomics is a promising molecular tool to identify novel etiologic pathways leading to cancer. Using a targeted approach, we prospectively investigated the associations between metabolite concentrations in plasma and breast cancer risk.

METHODS: A nested case-control study was established within the European Prospective Investigation into Cancer cohort, which included 1624 first primary incident invasive breast cancer cases (with known estrogen and progesterone receptor and HER2 status) and 1624 matched controls. Metabolites (n = 127, acylcarnitines, amino acids, biogenic amines, glycerophospholipids, hexose, sphingolipids) were measured by mass spectrometry in pre-diagnostic plasma samples and tested for associations with breast cancer incidence using multivariable conditional logistic regression.

RESULTS: Among women not using hormones at baseline (n = 2248), and after control for multiple tests, concentrations of arginine (odds ratio [OR] per SD = 0.79, 95% confidence interval [CI] = 0.70-0.90), asparagine (OR = 0.83 (0.74-0.92)), and phosphatidylcholines (PCs) ae C36:3 (OR = 0.83 (0.76-0.90)), aa C36:3 (OR = 0.84 (0.77-0.93)), ae C34:2 (OR = 0.85 (0.78-0.94)), ae C36:2 (OR = 0.85 (0.78-0.88)), and ae C38:2 (OR = 0.84 (0.76-0.93)) were inversely associated with breast cancer risk, while the acylcarnitine C2 (OR = 1.23 (1.11-1.35)) was positively associated with disease risk. In the overall population, C2 (OR = 1.15 (1.06-1.24)) and PC ae C36:3 (OR = 0.88 (0.82-0.95)) were associated with risk of breast cancer, and these relationships did not differ by breast cancer subtype, age at diagnosis, fasting status, menopausal status, or adiposity.

CONCLUSIONS: These findings point to potentially novel pathways and biomarkers of breast cancer development. Results warrant replication in other epidemiological studies.

Original language	English
Article number	178
Journal	BMC Medicine
Volume	17
Issue number	1
DOIs	https://doi.org/10.1186/s12916-019-1408-4
Publication status	Published - 24 Sept 2019
Externally published	Yes

Keywords

Adult
Aged
Biomarkers/analysis
Breast Neoplasms/blood
Case-Control Studies
Cohort Studies
Female
Humans
Incidence
Mass Spectrometry
Metabolomics/methods
Middle Aged
Prospective Studies
Risk Factors

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1186/s12916-019-1408-4Licence: Other

Prospective analysis of circulating metabolites and breast cancer in EPIC
© 2019 The Authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
Final published version, 0.99 MBLicence: Other

Cite this

His, M., Viallon, V., Dossus, L., Gicquiau, A., Achaintre, D., Scalbert, A., Ferrari, P., Romieu, I., Onland-Moret, N. C., Weiderpass, E., Dahm, C. C., Overvad, K., Olsen, A., Tjønneland, A., Fournier, A., Rothwell, J. A., Severi, G., Kühn, T., Fortner, R. T., ... Rinaldi, S. (2019). Prospective analysis of circulating metabolites and breast cancer in EPIC. BMC Medicine, 17(1), Article 178. https://doi.org/10.1186/s12916-019-1408-4

@article{8fdbb488f5a14261a148acbc47747ec1,

title = "Prospective analysis of circulating metabolites and breast cancer in EPIC",

abstract = "BACKGROUND: Metabolomics is a promising molecular tool to identify novel etiologic pathways leading to cancer. Using a targeted approach, we prospectively investigated the associations between metabolite concentrations in plasma and breast cancer risk.METHODS: A nested case-control study was established within the European Prospective Investigation into Cancer cohort, which included 1624 first primary incident invasive breast cancer cases (with known estrogen and progesterone receptor and HER2 status) and 1624 matched controls. Metabolites (n = 127, acylcarnitines, amino acids, biogenic amines, glycerophospholipids, hexose, sphingolipids) were measured by mass spectrometry in pre-diagnostic plasma samples and tested for associations with breast cancer incidence using multivariable conditional logistic regression.RESULTS: Among women not using hormones at baseline (n = 2248), and after control for multiple tests, concentrations of arginine (odds ratio [OR] per SD = 0.79, 95% confidence interval [CI] = 0.70-0.90), asparagine (OR = 0.83 (0.74-0.92)), and phosphatidylcholines (PCs) ae C36:3 (OR = 0.83 (0.76-0.90)), aa C36:3 (OR = 0.84 (0.77-0.93)), ae C34:2 (OR = 0.85 (0.78-0.94)), ae C36:2 (OR = 0.85 (0.78-0.88)), and ae C38:2 (OR = 0.84 (0.76-0.93)) were inversely associated with breast cancer risk, while the acylcarnitine C2 (OR = 1.23 (1.11-1.35)) was positively associated with disease risk. In the overall population, C2 (OR = 1.15 (1.06-1.24)) and PC ae C36:3 (OR = 0.88 (0.82-0.95)) were associated with risk of breast cancer, and these relationships did not differ by breast cancer subtype, age at diagnosis, fasting status, menopausal status, or adiposity.CONCLUSIONS: These findings point to potentially novel pathways and biomarkers of breast cancer development. Results warrant replication in other epidemiological studies.",

keywords = "Adult, Aged, Biomarkers/analysis, Breast Neoplasms/blood, Case-Control Studies, Cohort Studies, Female, Humans, Incidence, Mass Spectrometry, Metabolomics/methods, Middle Aged, Prospective Studies, Risk Factors",

author = "Mathilde His and Vivian Viallon and Laure Dossus and Audrey Gicquiau and David Achaintre and Augustin Scalbert and Pietro Ferrari and Isabelle Romieu and Onland-Moret, {N Charlotte} and Elisabete Weiderpass and Dahm, {Christina C} and Kim Overvad and Anja Olsen and Anne Tj{\o}nneland and Agn{\`e}s Fournier and Rothwell, {Joseph A} and Gianluca Severi and Tilman K{\"u}hn and Fortner, {Ren{\'e}e T} and Heiner Boeing and Antonia Trichopoulou and Anna Karakatsani and Georgia Martimianaki and Giovanna Masala and Sabina Sieri and Rosario Tumino and Paolo Vineis and Salvatore Panico and {van Gils}, {Carla H} and N{\o}st, {Therese H} and Sandanger, {Torkjel M} and Guri Skeie and Quir{\'o}s, {J Ram{\'o}n} and Antonio Agudo and Maria-Jose S{\'a}nchez and Pilar Amiano and Huerta, {Jos{\'e} Mar{\'i}a} and Eva Ardanaz and Schmidt, {Julie A} and Travis, {Ruth C} and Elio Riboli and Tsilidis, {Konstantinos K} and Sofia Christakoudi and Gunter, {Marc J} and Sabina Rinaldi",

year = "2019",

month = sep,

day = "24",

doi = "10.1186/s12916-019-1408-4",

language = "English",

volume = "17",

journal = "BMC Medicine",

issn = "1741-7015",

publisher = "BioMed Central Ltd",

number = "1",

}

His, M, Viallon, V, Dossus, L, Gicquiau, A, Achaintre, D, Scalbert, A, Ferrari, P, Romieu, I, Onland-Moret, NC, Weiderpass, E, Dahm, CC, Overvad, K, Olsen, A, Tjønneland, A, Fournier, A, Rothwell, JA, Severi, G, Kühn, T, Fortner, RT, Boeing, H, Trichopoulou, A, Karakatsani, A, Martimianaki, G, Masala, G, Sieri, S, Tumino, R, Vineis, P, Panico, S, van Gils, CH, Nøst, TH, Sandanger, TM, Skeie, G, Quirós, JR, Agudo, A, Sánchez, M-J, Amiano, P, Huerta, JM, Ardanaz, E, Schmidt, JA, Travis, RC, Riboli, E, Tsilidis, KK, Christakoudi, S, Gunter, MJ & Rinaldi, S 2019, 'Prospective analysis of circulating metabolites and breast cancer in EPIC', BMC Medicine, vol. 17, no. 1, 178. https://doi.org/10.1186/s12916-019-1408-4

TY - JOUR

T1 - Prospective analysis of circulating metabolites and breast cancer in EPIC

AU - His, Mathilde

AU - Viallon, Vivian

AU - Dossus, Laure

AU - Gicquiau, Audrey

AU - Achaintre, David

AU - Scalbert, Augustin

AU - Ferrari, Pietro

AU - Romieu, Isabelle

AU - Onland-Moret, N Charlotte

AU - Weiderpass, Elisabete

AU - Dahm, Christina C

AU - Overvad, Kim

AU - Olsen, Anja

AU - Tjønneland, Anne

AU - Fournier, Agnès

AU - Rothwell, Joseph A

AU - Severi, Gianluca

AU - Kühn, Tilman

AU - Fortner, Renée T

AU - Boeing, Heiner

AU - Trichopoulou, Antonia

AU - Karakatsani, Anna

AU - Martimianaki, Georgia

AU - Masala, Giovanna

AU - Sieri, Sabina

AU - Tumino, Rosario

AU - Vineis, Paolo

AU - Panico, Salvatore

AU - van Gils, Carla H

AU - Nøst, Therese H

AU - Sandanger, Torkjel M

AU - Skeie, Guri

AU - Quirós, J Ramón

AU - Agudo, Antonio

AU - Sánchez, Maria-Jose

AU - Amiano, Pilar

AU - Huerta, José María

AU - Ardanaz, Eva

AU - Schmidt, Julie A

AU - Travis, Ruth C

AU - Riboli, Elio

AU - Tsilidis, Konstantinos K

AU - Christakoudi, Sofia

AU - Gunter, Marc J

AU - Rinaldi, Sabina

PY - 2019/9/24

Y1 - 2019/9/24

N2 - BACKGROUND: Metabolomics is a promising molecular tool to identify novel etiologic pathways leading to cancer. Using a targeted approach, we prospectively investigated the associations between metabolite concentrations in plasma and breast cancer risk.METHODS: A nested case-control study was established within the European Prospective Investigation into Cancer cohort, which included 1624 first primary incident invasive breast cancer cases (with known estrogen and progesterone receptor and HER2 status) and 1624 matched controls. Metabolites (n = 127, acylcarnitines, amino acids, biogenic amines, glycerophospholipids, hexose, sphingolipids) were measured by mass spectrometry in pre-diagnostic plasma samples and tested for associations with breast cancer incidence using multivariable conditional logistic regression.RESULTS: Among women not using hormones at baseline (n = 2248), and after control for multiple tests, concentrations of arginine (odds ratio [OR] per SD = 0.79, 95% confidence interval [CI] = 0.70-0.90), asparagine (OR = 0.83 (0.74-0.92)), and phosphatidylcholines (PCs) ae C36:3 (OR = 0.83 (0.76-0.90)), aa C36:3 (OR = 0.84 (0.77-0.93)), ae C34:2 (OR = 0.85 (0.78-0.94)), ae C36:2 (OR = 0.85 (0.78-0.88)), and ae C38:2 (OR = 0.84 (0.76-0.93)) were inversely associated with breast cancer risk, while the acylcarnitine C2 (OR = 1.23 (1.11-1.35)) was positively associated with disease risk. In the overall population, C2 (OR = 1.15 (1.06-1.24)) and PC ae C36:3 (OR = 0.88 (0.82-0.95)) were associated with risk of breast cancer, and these relationships did not differ by breast cancer subtype, age at diagnosis, fasting status, menopausal status, or adiposity.CONCLUSIONS: These findings point to potentially novel pathways and biomarkers of breast cancer development. Results warrant replication in other epidemiological studies.

AB - BACKGROUND: Metabolomics is a promising molecular tool to identify novel etiologic pathways leading to cancer. Using a targeted approach, we prospectively investigated the associations between metabolite concentrations in plasma and breast cancer risk.METHODS: A nested case-control study was established within the European Prospective Investigation into Cancer cohort, which included 1624 first primary incident invasive breast cancer cases (with known estrogen and progesterone receptor and HER2 status) and 1624 matched controls. Metabolites (n = 127, acylcarnitines, amino acids, biogenic amines, glycerophospholipids, hexose, sphingolipids) were measured by mass spectrometry in pre-diagnostic plasma samples and tested for associations with breast cancer incidence using multivariable conditional logistic regression.RESULTS: Among women not using hormones at baseline (n = 2248), and after control for multiple tests, concentrations of arginine (odds ratio [OR] per SD = 0.79, 95% confidence interval [CI] = 0.70-0.90), asparagine (OR = 0.83 (0.74-0.92)), and phosphatidylcholines (PCs) ae C36:3 (OR = 0.83 (0.76-0.90)), aa C36:3 (OR = 0.84 (0.77-0.93)), ae C34:2 (OR = 0.85 (0.78-0.94)), ae C36:2 (OR = 0.85 (0.78-0.88)), and ae C38:2 (OR = 0.84 (0.76-0.93)) were inversely associated with breast cancer risk, while the acylcarnitine C2 (OR = 1.23 (1.11-1.35)) was positively associated with disease risk. In the overall population, C2 (OR = 1.15 (1.06-1.24)) and PC ae C36:3 (OR = 0.88 (0.82-0.95)) were associated with risk of breast cancer, and these relationships did not differ by breast cancer subtype, age at diagnosis, fasting status, menopausal status, or adiposity.CONCLUSIONS: These findings point to potentially novel pathways and biomarkers of breast cancer development. Results warrant replication in other epidemiological studies.

KW - Adult

KW - Aged

KW - Biomarkers/analysis

KW - Breast Neoplasms/blood

KW - Case-Control Studies

KW - Cohort Studies

KW - Female

KW - Humans

KW - Incidence

KW - Mass Spectrometry

KW - Metabolomics/methods

KW - Middle Aged

KW - Prospective Studies

KW - Risk Factors

U2 - 10.1186/s12916-019-1408-4

DO - 10.1186/s12916-019-1408-4

M3 - Article

C2 - 31547832

SN - 1741-7015

VL - 17

JO - BMC Medicine

JF - BMC Medicine

IS - 1

M1 - 178

ER -

Prospective analysis of circulating metabolites and breast cancer in EPIC

Abstract

Keywords

UN SDGs

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