Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment

<b>Background/Objectives</b>: The management of early breast cancer (BC) includes surgery, followed by adjuvant radiotherapy, chemotherapy, hormone therapy, or immunotherapy. However, the influence of these interventions in metabolic reprogramming remains unknown. This study explored alt...

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Main Authors: Andrea Jiménez-Franco, Juan Manuel Jiménez-Aguilar, Marta Canela-Capdevila, Raquel García-Pablo, Helena Castañé, Cristian Martínez-Navidad, Pablo Araguas, Bárbara Malavé, Rocío Benavides-Villarreal, Johana C. Acosta, Alina Iuliana Onoiu, Navita Somaiah, Jordi Camps, Jorge Joven, Meritxell Arenas
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语言:English
出版: MDPI AG 2024-09-01
丛编:Biomedicines
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在线阅读:https://www.mdpi.com/2227-9059/12/10/2196
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author Andrea Jiménez-Franco
Juan Manuel Jiménez-Aguilar
Marta Canela-Capdevila
Raquel García-Pablo
Helena Castañé
Cristian Martínez-Navidad
Pablo Araguas
Bárbara Malavé
Rocío Benavides-Villarreal
Johana C. Acosta
Alina Iuliana Onoiu
Navita Somaiah
Jordi Camps
Jorge Joven
Meritxell Arenas
author_facet Andrea Jiménez-Franco
Juan Manuel Jiménez-Aguilar
Marta Canela-Capdevila
Raquel García-Pablo
Helena Castañé
Cristian Martínez-Navidad
Pablo Araguas
Bárbara Malavé
Rocío Benavides-Villarreal
Johana C. Acosta
Alina Iuliana Onoiu
Navita Somaiah
Jordi Camps
Jorge Joven
Meritxell Arenas
author_sort Andrea Jiménez-Franco
collection DOAJ
description <b>Background/Objectives</b>: The management of early breast cancer (BC) includes surgery, followed by adjuvant radiotherapy, chemotherapy, hormone therapy, or immunotherapy. However, the influence of these interventions in metabolic reprogramming remains unknown. This study explored alterations in the plasma metabolome of BC patients following distinct treatments to deepen our understanding of BC pathophysiology, outcomes, and the identification of potential biomarkers. <b>Methods</b>: We included 52 women diagnosed with BC and candidates for surgery as primary oncological treatment. Blood samples were collected at diagnosis, two weeks post-surgery, and one month post-radiotherapy. Plasma samples from 49 healthy women served as controls. Targeted metabolomics assessed 74 metabolites spanning carbohydrates, amino acids, lipids, nucleotide pathways, energy metabolism, and xenobiotic biodegradation. <b>Results</b>: Before treatment, the BC patients exhibited notable changes in carbohydrate, nucleotide, lipid, and amino acid metabolism. We noticed a gradual restoration of specific metabolite levels (hypoxanthine, 3-phosphoglyceric acid, xylonic acid, and maltose) throughout different treatments, suggesting a normalization of the nucleotide and carbohydrate metabolic pathways. Moreover, we observed increased dodecanoic acid concentrations, a metabolite associated with cancer protection. These variations distinguished patients from controls with high specificity and sensitivity. <b>Conclusions</b>: Our preliminary study suggests that oncological treatments modify the metabolism of patients towards a favorable profile with a decrease in the pathways that favor cell proliferation and an increase in the levels of anticancer molecules. These findings emphasize the pivotal role of metabolomics in recognizing the biological pathways influenced by each cancer treatment and the resulting metabolic consequences. Furthermore, it aids in identifying potential biomarkers for disease onset and progression.
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spelling doaj.art-6aaf45b5ff4f4750a32b51aa16b5e47c2024-10-25T13:49:27ZengMDPI AGBiomedicines2227-90592024-09-011210219610.3390/biomedicines12102196Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant TreatmentAndrea Jiménez-Franco0Juan Manuel Jiménez-Aguilar1Marta Canela-Capdevila2Raquel García-Pablo3Helena Castañé4Cristian Martínez-Navidad5Pablo Araguas6Bárbara Malavé7Rocío Benavides-Villarreal8Johana C. Acosta9Alina Iuliana Onoiu10Navita Somaiah11Jordi Camps12Jorge Joven13Meritxell Arenas14Unitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainDepartment of Radiation Oncology, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainDepartment of Radiation Oncology, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainThe Royal Marsden NHS Foundation Trust and Division of Radiotherapy and Imaging, Institute of Cancer Research, 131-139 Dovehouse St, London SW3 6JZ, UKUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, SpainUnitat de Recerca Biomèdica, Hospital Universitari Sant Joan de Reus, Institut d’Investigació Sanitària Pere Virgili, Universitat Rovira i Virgili, Av. Dr. Josep Laporte 2, 43204 Reus, Spain<b>Background/Objectives</b>: The management of early breast cancer (BC) includes surgery, followed by adjuvant radiotherapy, chemotherapy, hormone therapy, or immunotherapy. However, the influence of these interventions in metabolic reprogramming remains unknown. This study explored alterations in the plasma metabolome of BC patients following distinct treatments to deepen our understanding of BC pathophysiology, outcomes, and the identification of potential biomarkers. <b>Methods</b>: We included 52 women diagnosed with BC and candidates for surgery as primary oncological treatment. Blood samples were collected at diagnosis, two weeks post-surgery, and one month post-radiotherapy. Plasma samples from 49 healthy women served as controls. Targeted metabolomics assessed 74 metabolites spanning carbohydrates, amino acids, lipids, nucleotide pathways, energy metabolism, and xenobiotic biodegradation. <b>Results</b>: Before treatment, the BC patients exhibited notable changes in carbohydrate, nucleotide, lipid, and amino acid metabolism. We noticed a gradual restoration of specific metabolite levels (hypoxanthine, 3-phosphoglyceric acid, xylonic acid, and maltose) throughout different treatments, suggesting a normalization of the nucleotide and carbohydrate metabolic pathways. Moreover, we observed increased dodecanoic acid concentrations, a metabolite associated with cancer protection. These variations distinguished patients from controls with high specificity and sensitivity. <b>Conclusions</b>: Our preliminary study suggests that oncological treatments modify the metabolism of patients towards a favorable profile with a decrease in the pathways that favor cell proliferation and an increase in the levels of anticancer molecules. These findings emphasize the pivotal role of metabolomics in recognizing the biological pathways influenced by each cancer treatment and the resulting metabolic consequences. Furthermore, it aids in identifying potential biomarkers for disease onset and progression.https://www.mdpi.com/2227-9059/12/10/2196breast cancerchemotherapymetabolismmetabolomicsradiotherapy
spellingShingle Andrea Jiménez-Franco
Juan Manuel Jiménez-Aguilar
Marta Canela-Capdevila
Raquel García-Pablo
Helena Castañé
Cristian Martínez-Navidad
Pablo Araguas
Bárbara Malavé
Rocío Benavides-Villarreal
Johana C. Acosta
Alina Iuliana Onoiu
Navita Somaiah
Jordi Camps
Jorge Joven
Meritxell Arenas
Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment
Biomedicines
breast cancer
chemotherapy
metabolism
metabolomics
radiotherapy
title Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment
title_full Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment
title_fullStr Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment
title_full_unstemmed Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment
title_short Preliminary Metabolomics Study Suggests Favorable Metabolic Changes in the Plasma of Breast Cancer Patients after Surgery and Adjuvant Treatment
title_sort preliminary metabolomics study suggests favorable metabolic changes in the plasma of breast cancer patients after surgery and adjuvant treatment
topic breast cancer
chemotherapy
metabolism
metabolomics
radiotherapy
url https://www.mdpi.com/2227-9059/12/10/2196
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