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August 31, 2021; 97 (9) Research Article

Feasibility and Biological Activity of a Ketogenic/Intermittent-Fasting Diet in Patients With Glioma

View ORCID ProfileKarisa C. Schreck, Fang-Chi Hsu, View ORCID ProfileAdam Berrington, View ORCID ProfileBobbie Henry-Barron, Diane Vizthum, Lindsay Blair, View ORCID ProfileEric H. Kossoff, Linda Easter, View ORCID ProfileChristopher T. Whitlow, Peter B. Barker, View ORCID ProfileMackenzie C. Cervenka, View ORCID ProfileJaishri O. Blakeley, View ORCID ProfileRoy E. Strowd
First published July 7, 2021, DOI: https://doi.org/10.1212/WNL.0000000000012386
Karisa C. Schreck
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Fang-Chi Hsu
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Adam Berrington
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Bobbie Henry-Barron
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Diane Vizthum
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Lindsay Blair
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Eric H. Kossoff
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Linda Easter
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Christopher T. Whitlow
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Peter B. Barker
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Mackenzie C. Cervenka
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Jaishri O. Blakeley
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
MD
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Roy E. Strowd
From the Departments of Neurology (K.C.S., J.O.B., L.B., E.H.K., M.C.C., R.E.S.), Oncology (K.C.S., J.O.B.), Neurosurgery (K.C.S., J.O.B.), and Radiology (A.B., P.B.B.) and Institute for Clinical and Translational Research (B.H.-B., D.V.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Biostatistics and Data Science (F.-C.H., C.T.W.), Clinical Research Unit (L.E.), Department of Radiology (C.T.W.), Department of Biomedical Engineering (C.T.W.), Clinical and Translational Science Institute (C.T.W.), Department of Neurology (R.E.S.), and Department of Oncology (R.E.S.), Wake Forest School of Medicine, Winston-Salem, NC; and Sir Peter Mansfield Imaging Centre (A.B.), School of Physics and Astronomy, University of Nottingham, UK.
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Citation
Feasibility and Biological Activity of a Ketogenic/Intermittent-Fasting Diet in Patients With Glioma
Karisa C. Schreck, Fang-Chi Hsu, Adam Berrington, Bobbie Henry-Barron, Diane Vizthum, Lindsay Blair, Eric H. Kossoff, Linda Easter, Christopher T. Whitlow, Peter B. Barker, Mackenzie C. Cervenka, Jaishri O. Blakeley, Roy E. Strowd
Neurology Aug 2021, 97 (9) e953-e963; DOI: 10.1212/WNL.0000000000012386

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Abstract

Objective To examine the feasibility, safety, systemic biological activity, and cerebral activity of a ketogenic dietary intervention in patients with glioma.

Methods Twenty-five patients with biopsy-confirmed World Health Organization grade 2 to 4 astrocytoma with stable disease after adjuvant chemotherapy were enrolled in an 8-week Glioma Atkins-Based Diet (GLAD). GLAD consisted of 2 fasting days (calories <20% calculated estimated needs) interleaved between 5 modified Atkins diet days (net carbohydrates ≤20 g/d) each week. The primary outcome was dietary adherence by food records. Markers of systemic and cerebral activity included weekly urine ketones, serum insulin, glucose, hemoglobin A1c, insulin-like growth factor-1, and magnetic resonance spectroscopy at baseline and week 8.

Results Twenty-one patients (84%) completed the study. Eighty percent of patients reached ≥40 mg/dL urine acetoacetate during the study. Forty-eight percent of patients were adherent by food record. The diet was well tolerated, with two grade 3 adverse events (neutropenia, seizure). Measures of systemic activity, including hemoglobin A1c, insulin, and fat body mass, decreased significantly, while lean body mass increased. Magnetic resonance spectroscopy demonstrated increased ketone concentrations (β-hydroxybutyrate [bHB] and acetone) in both lesional and contralateral brain compared to baseline. Average ketonuria correlated with cerebral ketones in lesional (tumor) and contralateral brain (bHB Rs = 0.52, p = 0.05). Subgroup analysis of isocitrate dehydrogenase–mutant glioma showed no differences in cerebral metabolites after controlling for ketonuria.

Conclusion The GLAD dietary intervention, while demanding, produced meaningful ketonuria and significant systemic and cerebral metabolic changes in participants. Ketonuria in participants correlated with cerebral ketone concentration and appears to be a better indicator of systemic activity than patient-reported food records.

Trial Registration Information ClinicalTrials.gov Identifier: NCT02286167.

Glossary

AcAc=
acetoacetate;
Ace=
acetone;
bHB=
β-hydroxybutyrate;
BIA=
bioelectric impedance analysis;
BMI=
body mass index;
Cho=
phosphocholine;
CTCAE=
Common Terminology Criteria for Adverse Events;
GLAD=
Glioma Modified Atkins Diet;
Gln=
glutamine;
Glu=
glutamate;
Glx=
combination of Gln and Glu;
IDH=
isocitrate dehydrogenase;
IGF-1=
insulin-like growth factor-1;
KDT=
ketogenic diet therapy;
MAD=
modified Atkins diet;
MG=
malignant glioma;
MRS=
magnetic resonance spectroscopy;
RD=
registered dietitian;
2-HG=
2-hydroxyglutarate;
WBC=
white blood cell count;
WT=
wild-type

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • CME Course: NPub.org/cmelist

  • Received November 13, 2020.
  • Accepted in final form May 28, 2021.
  • © 2021 American Academy of Neurology
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