Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer

IntroductionThe progression of solid cancers is manifested at the systemic level as molecular changes in the metabolome of body fluids, an emerging source of cancer biomarkers.MethodsWe analyzed quantitatively the serum metabolite profile using high-resolution mass spectrometry. Metabolic profiles w...

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Main Authors: Katarzyna Mrowiec, Julia Debik, Karol Jelonek, Agata Kurczyk, Lucyna Ponge, Agata Wilk, Marcela Krzempek, Guro F. Giskeødegård, Tone F. Bathen, Piotr Widłak
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-04-01
Series:Frontiers in Oncology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2024.1377373/full
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author Katarzyna Mrowiec
Julia Debik
Julia Debik
Karol Jelonek
Agata Kurczyk
Lucyna Ponge
Agata Wilk
Agata Wilk
Marcela Krzempek
Guro F. Giskeødegård
Tone F. Bathen
Tone F. Bathen
Piotr Widłak
author_facet Katarzyna Mrowiec
Julia Debik
Julia Debik
Karol Jelonek
Agata Kurczyk
Lucyna Ponge
Agata Wilk
Agata Wilk
Marcela Krzempek
Guro F. Giskeødegård
Tone F. Bathen
Tone F. Bathen
Piotr Widłak
author_sort Katarzyna Mrowiec
collection DOAJ
description IntroductionThe progression of solid cancers is manifested at the systemic level as molecular changes in the metabolome of body fluids, an emerging source of cancer biomarkers.MethodsWe analyzed quantitatively the serum metabolite profile using high-resolution mass spectrometry. Metabolic profiles were compared between breast cancer patients (n=112) and two groups of healthy women (from Poland and Norway; n=95 and n=112, respectively) with similar age distributions.ResultsDespite differences between both cohorts of controls, a set of 43 metabolites and lipids uniformly discriminated against breast cancer patients and healthy women. Moreover, smaller groups of female patients with other types of solid cancers (colorectal, head and neck, and lung cancers) were analyzed, which revealed a set of 42 metabolites and lipids that uniformly differentiated all three cancer types from both cohorts of healthy women. A common part of both sets, which could be called a multi-cancer signature, contained 23 compounds, which included reduced levels of a few amino acids (alanine, aspartate, glutamine, histidine, phenylalanine, and leucine/isoleucine), lysophosphatidylcholines (exemplified by LPC(18:0)), and diglycerides. Interestingly, a reduced concentration of the most abundant cholesteryl ester (CE(18:2)) typical for other cancers was the least significant in the serum of breast cancer patients. Components present in a multi-cancer signature enabled the establishment of a well-performing breast cancer classifier, which predicted cancer with a very high precision in independent groups of women (AUC>0.95).DiscussionIn conclusion, metabolites critical for discriminating breast cancer patients from controls included components of hypothetical multi-cancer signature, which indicated wider potential applicability of a general serum metabolome cancer biomarker.
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spelling doaj.art-6ffcb6adce7948709ed3aa30fe4cc7122024-04-04T05:04:51ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2024-04-011410.3389/fonc.2024.13773731377373Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancerKatarzyna Mrowiec0Julia Debik1Julia Debik2Karol Jelonek3Agata Kurczyk4Lucyna Ponge5Agata Wilk6Agata Wilk7Marcela Krzempek8Guro F. Giskeødegård9Tone F. Bathen10Tone F. Bathen11Piotr Widłak12Center for Translational Research and Molecular Biology of Cancer, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice, PolandDepartment of Circulation and Medical Imaging, The Norwegian University of Science and Technology, Trondheim, NorwayDepartment of Public Health and Nursing, The Norwegian University of Science and Technology, Trondheim, NorwayCenter for Translational Research and Molecular Biology of Cancer, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice, PolandDepartment of Biostatistics and Bioinformatics, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice, PolandCenter for Translational Research and Molecular Biology of Cancer, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice, PolandDepartment of Biostatistics and Bioinformatics, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice, PolandDepartment of Systems Biology and Engineering, Silesian University of Technology, Gliwice, PolandDepartment of Biostatistics and Bioinformatics, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice, PolandDepartment of Circulation and Medical Imaging, The Norwegian University of Science and Technology, Trondheim, NorwayDepartment of Circulation and Medical Imaging, The Norwegian University of Science and Technology, Trondheim, NorwayClinic of Radiology and Nuclear Medicine, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway2nd Department of Radiology, Medical University of Gdansk, Gdansk, PolandIntroductionThe progression of solid cancers is manifested at the systemic level as molecular changes in the metabolome of body fluids, an emerging source of cancer biomarkers.MethodsWe analyzed quantitatively the serum metabolite profile using high-resolution mass spectrometry. Metabolic profiles were compared between breast cancer patients (n=112) and two groups of healthy women (from Poland and Norway; n=95 and n=112, respectively) with similar age distributions.ResultsDespite differences between both cohorts of controls, a set of 43 metabolites and lipids uniformly discriminated against breast cancer patients and healthy women. Moreover, smaller groups of female patients with other types of solid cancers (colorectal, head and neck, and lung cancers) were analyzed, which revealed a set of 42 metabolites and lipids that uniformly differentiated all three cancer types from both cohorts of healthy women. A common part of both sets, which could be called a multi-cancer signature, contained 23 compounds, which included reduced levels of a few amino acids (alanine, aspartate, glutamine, histidine, phenylalanine, and leucine/isoleucine), lysophosphatidylcholines (exemplified by LPC(18:0)), and diglycerides. Interestingly, a reduced concentration of the most abundant cholesteryl ester (CE(18:2)) typical for other cancers was the least significant in the serum of breast cancer patients. Components present in a multi-cancer signature enabled the establishment of a well-performing breast cancer classifier, which predicted cancer with a very high precision in independent groups of women (AUC>0.95).DiscussionIn conclusion, metabolites critical for discriminating breast cancer patients from controls included components of hypothetical multi-cancer signature, which indicated wider potential applicability of a general serum metabolome cancer biomarker.https://www.frontiersin.org/articles/10.3389/fonc.2024.1377373/fullbiomarkerbreast cancerhigh-resolution mass spectrometrymetabolomicsmulticancer signatureserum metabolome
spellingShingle Katarzyna Mrowiec
Julia Debik
Julia Debik
Karol Jelonek
Agata Kurczyk
Lucyna Ponge
Agata Wilk
Agata Wilk
Marcela Krzempek
Guro F. Giskeødegård
Tone F. Bathen
Tone F. Bathen
Piotr Widłak
Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer
Frontiers in Oncology
biomarker
breast cancer
high-resolution mass spectrometry
metabolomics
multicancer signature
serum metabolome
title Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer
title_full Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer
title_fullStr Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer
title_full_unstemmed Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer
title_short Profiling of serum metabolome of breast cancer: multi-cancer features discriminate between healthy women and patients with breast cancer
title_sort profiling of serum metabolome of breast cancer multi cancer features discriminate between healthy women and patients with breast cancer
topic biomarker
breast cancer
high-resolution mass spectrometry
metabolomics
multicancer signature
serum metabolome
url https://www.frontiersin.org/articles/10.3389/fonc.2024.1377373/full
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