Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma

Abstract Glioblastoma (GBM) is the most aggressive primary brain tumor in adults, with a universally lethal prognosis despite maximal standard therapies. Here, we present a consensus treatment protocol based on the metabolic requirements of GBM cells for the two major fermentable fuels: glucose and...

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Main Authors: Tomás Duraj, Miriam Kalamian, Giulio Zuccoli, Joseph C. Maroon, Dominic P. D’Agostino, Adrienne C. Scheck, Angela Poff, Sebastian F. Winter, Jethro Hu, Rainer J. Klement, Alicia Hickson, Derek C. Lee, Isabella Cooper, Barbara Kofler, Kenneth A. Schwartz, Matthew C. L. Phillips, Colin E. Champ, Beth Zupec-Kania, Jocelyn Tan-Shalaby, Fabiano M. Serfaty, Egiroh Omene, Gabriel Arismendi-Morillo, Michael Kiebish, Richard Cheng, Ahmed M. El-Sakka, Axel Pflueger, Edward H. Mathews, Donese Worden, Hanping Shi, Raffaele Ivan Cincione, Jean Pierre Spinosa, Abdul Kadir Slocum, Mehmet Salih Iyikesici, Atsuo Yanagisawa, Geoffrey J. Pilkington, Anthony Chaffee, Wafaa Abdel-Hadi, Amr K. Elsamman, Pavel Klein, Keisuke Hagihara, Zsófia Clemens, George W. Yu, Athanasios E. Evangeliou, Janak K. Nathan, Kris Smith, David Fortin, Jorg Dietrich, Purna Mukherjee, Thomas N. Seyfried
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Language:English
Published: BMC 2024-12-01
Series:BMC Medicine
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Online Access:https://doi.org/10.1186/s12916-024-03775-4
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author Tomás Duraj
Miriam Kalamian
Giulio Zuccoli
Joseph C. Maroon
Dominic P. D’Agostino
Adrienne C. Scheck
Angela Poff
Sebastian F. Winter
Jethro Hu
Rainer J. Klement
Alicia Hickson
Derek C. Lee
Isabella Cooper
Barbara Kofler
Kenneth A. Schwartz
Matthew C. L. Phillips
Colin E. Champ
Beth Zupec-Kania
Jocelyn Tan-Shalaby
Fabiano M. Serfaty
Egiroh Omene
Gabriel Arismendi-Morillo
Michael Kiebish
Richard Cheng
Ahmed M. El-Sakka
Axel Pflueger
Edward H. Mathews
Donese Worden
Hanping Shi
Raffaele Ivan Cincione
Jean Pierre Spinosa
Abdul Kadir Slocum
Mehmet Salih Iyikesici
Atsuo Yanagisawa
Geoffrey J. Pilkington
Anthony Chaffee
Wafaa Abdel-Hadi
Amr K. Elsamman
Pavel Klein
Keisuke Hagihara
Zsófia Clemens
George W. Yu
Athanasios E. Evangeliou
Janak K. Nathan
Kris Smith
David Fortin
Jorg Dietrich
Purna Mukherjee
Thomas N. Seyfried
author_facet Tomás Duraj
Miriam Kalamian
Giulio Zuccoli
Joseph C. Maroon
Dominic P. D’Agostino
Adrienne C. Scheck
Angela Poff
Sebastian F. Winter
Jethro Hu
Rainer J. Klement
Alicia Hickson
Derek C. Lee
Isabella Cooper
Barbara Kofler
Kenneth A. Schwartz
Matthew C. L. Phillips
Colin E. Champ
Beth Zupec-Kania
Jocelyn Tan-Shalaby
Fabiano M. Serfaty
Egiroh Omene
Gabriel Arismendi-Morillo
Michael Kiebish
Richard Cheng
Ahmed M. El-Sakka
Axel Pflueger
Edward H. Mathews
Donese Worden
Hanping Shi
Raffaele Ivan Cincione
Jean Pierre Spinosa
Abdul Kadir Slocum
Mehmet Salih Iyikesici
Atsuo Yanagisawa
Geoffrey J. Pilkington
Anthony Chaffee
Wafaa Abdel-Hadi
Amr K. Elsamman
Pavel Klein
Keisuke Hagihara
Zsófia Clemens
George W. Yu
Athanasios E. Evangeliou
Janak K. Nathan
Kris Smith
David Fortin
Jorg Dietrich
Purna Mukherjee
Thomas N. Seyfried
author_sort Tomás Duraj
collection DOAJ
description Abstract Glioblastoma (GBM) is the most aggressive primary brain tumor in adults, with a universally lethal prognosis despite maximal standard therapies. Here, we present a consensus treatment protocol based on the metabolic requirements of GBM cells for the two major fermentable fuels: glucose and glutamine. Glucose is a source of carbon and ATP synthesis for tumor growth through glycolysis, while glutamine provides nitrogen, carbon, and ATP synthesis through glutaminolysis. As no tumor can grow without anabolic substrates or energy, the simultaneous targeting of glycolysis and glutaminolysis is expected to reduce the proliferation of most if not all GBM cells. Ketogenic metabolic therapy (KMT) leverages diet-drug combinations that inhibit glycolysis, glutaminolysis, and growth signaling while shifting energy metabolism to therapeutic ketosis. The glucose-ketone index (GKI) is a standardized biomarker for assessing biological compliance, ideally via real-time monitoring. KMT aims to increase substrate competition and normalize the tumor microenvironment through GKI-adjusted ketogenic diets, calorie restriction, and fasting, while also targeting glycolytic and glutaminolytic flux using specific metabolic inhibitors. Non-fermentable fuels, such as ketone bodies, fatty acids, or lactate, are comparatively less efficient in supporting the long-term bioenergetic and biosynthetic demands of cancer cell proliferation. The proposed strategy may be implemented as a synergistic metabolic priming baseline in GBM as well as other tumors driven by glycolysis and glutaminolysis, regardless of their residual mitochondrial function. Suggested best practices are provided to guide future KMT research in metabolic oncology, offering a shared, evidence-driven framework for observational and interventional studies.
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spelling doaj-art-f493bd6a9af94b99a15a8ff738e02f2b2024-12-08T12:33:07ZengBMCBMC Medicine1741-70152024-12-0122114910.1186/s12916-024-03775-4Clinical research framework proposal for ketogenic metabolic therapy in glioblastomaTomás Duraj0Miriam Kalamian1Giulio Zuccoli2Joseph C. Maroon3Dominic P. D’Agostino4Adrienne C. Scheck5Angela Poff6Sebastian F. Winter7Jethro Hu8Rainer J. Klement9Alicia Hickson10Derek C. Lee11Isabella Cooper12Barbara Kofler13Kenneth A. Schwartz14Matthew C. L. Phillips15Colin E. Champ16Beth Zupec-Kania17Jocelyn Tan-Shalaby18Fabiano M. Serfaty19Egiroh Omene20Gabriel Arismendi-Morillo21Michael Kiebish22Richard Cheng23Ahmed M. El-Sakka24Axel Pflueger25Edward H. Mathews26Donese Worden27Hanping Shi28Raffaele Ivan Cincione29Jean Pierre Spinosa30Abdul Kadir Slocum31Mehmet Salih Iyikesici32Atsuo Yanagisawa33Geoffrey J. Pilkington34Anthony Chaffee35Wafaa Abdel-Hadi36Amr K. Elsamman37Pavel Klein38Keisuke Hagihara39Zsófia Clemens40George W. Yu41Athanasios E. Evangeliou42Janak K. Nathan43Kris Smith44David Fortin45Jorg Dietrich46Purna MukherjeeThomas N. Seyfried47Biology Department, Boston CollegeDietary Therapies LLCNeuroradiology, Private PracticeDepartment of Neurological Surgery, University of Pittsburgh Medical CenterDepartment of Molecular Pharmacology and Physiology, University of South Florida Morsani College of MedicineDepartment of Child Health, University of Arizona College of MedicineDepartment of Molecular Pharmacology and Physiology, University of South Florida Morsani College of MedicineDepartment of Neurology, Division of Neuro-Oncology, Massachusetts General Hospital Cancer Center, Harvard Medical SchoolCedars-Sinai Cancer, Cedars-Sinai Medical CenterDepartment of Radiotherapy and Radiation Oncology, Leopoldina Hospital SchweinfurtRayma HealthBiology Department, Boston CollegeAgeing Biology and Age-Related Diseases Group, School of Life Sciences, University of WestminsterResearch Program for Receptor Biochemistry and Tumor Metabolism, Department of Pediatrics, University Hospital of the Paracelsus Medical UniversityDepartment of Medicine, Michigan State UniversityDepartment of Neurology, Waikato HospitalExercise Oncology & Resiliency Center and Department of Radiation Oncology, Allegheny Health NetworkKetogenic Therapies LLCSchool of Medicine, University of Pittsburgh, Veteran Affairs Pittsburgh Healthcare SystemDepartment of Clinical Medicine, State University of Rio de Janeiro (UERJ)Department of Oncology, Cross Cancer InstituteDepartment of Medicine, Faculty of Health Sciences, University of DeustoBPGbio IncCheng Integrative Health CenterMetabolic Terrain Institute of HealthPflueger Medical Nephrologyand , Internal Medicine Services P.L.L.CDepartment of Physiology, Faculty of Health Sciences, University of PretoriaArizona State UniversityDepartment of Gastrointestinal Surgery and Department of Clinical Nutrition, Beijing Shijitan Hospital, Capital Medical UniversityDepartment of Clinical and Experimental Medicine, University of FoggiaIntegrative Oncology, Breast and Gynecologic Oncology SurgeryMedical Oncology, ChemoThermia Oncology CenterDepartment of Medical Oncology, Altınbaş University Bahçelievler Medical Park HospitalThe Japanese College of Intravenous TherapyUniversity of PortsmouthDepartment of Neurosurgery, Sir Charles Gairdner HospitalClinical Oncology Department, Cairo UniversityNeurosurgery Department, Cairo UniversityMid-Atlantic Epilepsy and Sleep CenterDepartment of Advanced Hybrid Medicine, Graduate School of Medicine, Osaka UniversityInternational Center for Medical Nutritional InterventionGeorge W, Yu Foundation For Nutrition & Health and Aegis Medical & Research AssociatesDepartment of Pediatrics, Medical School, Aristotle University of Thessaloniki, Papageorgiou Hospital, EfkarpiaDr. DY Patil Medical College, Hospital and Research CentreBarrow Neurological Institute, Dignity Health St. Joseph’s Hospital and Medical CenterUniversité de SherbrookeDepartment of Neurology, Division of Neuro-Oncology, Massachusetts General Hospital Cancer Center, Harvard Medical SchoolBiology Department, Boston CollegeAbstract Glioblastoma (GBM) is the most aggressive primary brain tumor in adults, with a universally lethal prognosis despite maximal standard therapies. Here, we present a consensus treatment protocol based on the metabolic requirements of GBM cells for the two major fermentable fuels: glucose and glutamine. Glucose is a source of carbon and ATP synthesis for tumor growth through glycolysis, while glutamine provides nitrogen, carbon, and ATP synthesis through glutaminolysis. As no tumor can grow without anabolic substrates or energy, the simultaneous targeting of glycolysis and glutaminolysis is expected to reduce the proliferation of most if not all GBM cells. Ketogenic metabolic therapy (KMT) leverages diet-drug combinations that inhibit glycolysis, glutaminolysis, and growth signaling while shifting energy metabolism to therapeutic ketosis. The glucose-ketone index (GKI) is a standardized biomarker for assessing biological compliance, ideally via real-time monitoring. KMT aims to increase substrate competition and normalize the tumor microenvironment through GKI-adjusted ketogenic diets, calorie restriction, and fasting, while also targeting glycolytic and glutaminolytic flux using specific metabolic inhibitors. Non-fermentable fuels, such as ketone bodies, fatty acids, or lactate, are comparatively less efficient in supporting the long-term bioenergetic and biosynthetic demands of cancer cell proliferation. The proposed strategy may be implemented as a synergistic metabolic priming baseline in GBM as well as other tumors driven by glycolysis and glutaminolysis, regardless of their residual mitochondrial function. Suggested best practices are provided to guide future KMT research in metabolic oncology, offering a shared, evidence-driven framework for observational and interventional studies.https://doi.org/10.1186/s12916-024-03775-4CancerGlioblastomaMetabolismResearch designWarburg EffectGlutaminolysis
spellingShingle Tomás Duraj
Miriam Kalamian
Giulio Zuccoli
Joseph C. Maroon
Dominic P. D’Agostino
Adrienne C. Scheck
Angela Poff
Sebastian F. Winter
Jethro Hu
Rainer J. Klement
Alicia Hickson
Derek C. Lee
Isabella Cooper
Barbara Kofler
Kenneth A. Schwartz
Matthew C. L. Phillips
Colin E. Champ
Beth Zupec-Kania
Jocelyn Tan-Shalaby
Fabiano M. Serfaty
Egiroh Omene
Gabriel Arismendi-Morillo
Michael Kiebish
Richard Cheng
Ahmed M. El-Sakka
Axel Pflueger
Edward H. Mathews
Donese Worden
Hanping Shi
Raffaele Ivan Cincione
Jean Pierre Spinosa
Abdul Kadir Slocum
Mehmet Salih Iyikesici
Atsuo Yanagisawa
Geoffrey J. Pilkington
Anthony Chaffee
Wafaa Abdel-Hadi
Amr K. Elsamman
Pavel Klein
Keisuke Hagihara
Zsófia Clemens
George W. Yu
Athanasios E. Evangeliou
Janak K. Nathan
Kris Smith
David Fortin
Jorg Dietrich
Purna Mukherjee
Thomas N. Seyfried
Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
BMC Medicine
Cancer
Glioblastoma
Metabolism
Research design
Warburg Effect
Glutaminolysis
title Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
title_full Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
title_fullStr Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
title_full_unstemmed Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
title_short Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
title_sort clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
topic Cancer
Glioblastoma
Metabolism
Research design
Warburg Effect
Glutaminolysis
url https://doi.org/10.1186/s12916-024-03775-4
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