Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients

Abstract Mitochondrial myopathy (MM) with progressive external ophthalmoplegia (PEO) is a common manifestation of mitochondrial disease in adulthood, for which there is no curative therapy. In mice with MM, ketogenic diet significantly delayed progression of the disease. We asked in this pilot study...

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Main Authors: Sofia Ahola, Mari Auranen, Pirjo Isohanni, Satu Niemisalo, Niina Urho, Jana Buzkova, Vidya Velagapudi, Nina Lundbom, Antti Hakkarainen, Tiina Muurinen, Päivi Piirilä, Kirsi H Pietiläinen, Anu Suomalainen
Format: Article
Language:English
Published: Springer Nature 2016-09-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201606592
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author Sofia Ahola
Mari Auranen
Pirjo Isohanni
Satu Niemisalo
Niina Urho
Jana Buzkova
Vidya Velagapudi
Nina Lundbom
Antti Hakkarainen
Tiina Muurinen
Päivi Piirilä
Kirsi H Pietiläinen
Anu Suomalainen
author_facet Sofia Ahola
Mari Auranen
Pirjo Isohanni
Satu Niemisalo
Niina Urho
Jana Buzkova
Vidya Velagapudi
Nina Lundbom
Antti Hakkarainen
Tiina Muurinen
Päivi Piirilä
Kirsi H Pietiläinen
Anu Suomalainen
author_sort Sofia Ahola
collection DOAJ
description Abstract Mitochondrial myopathy (MM) with progressive external ophthalmoplegia (PEO) is a common manifestation of mitochondrial disease in adulthood, for which there is no curative therapy. In mice with MM, ketogenic diet significantly delayed progression of the disease. We asked in this pilot study what effects high‐fat, low‐carbohydrate “modified Atkins” diet (mAD) had for PEO/MM patients and control subjects and followed up the effects by clinical, morphological, transcriptomic, and metabolomic analyses. All of our five patients, irrespective of genotype, showed a subacute response after 1.5–2 weeks of diet, with progressive muscle pain and leakage of muscle enzymes, leading to premature discontinuation of the diet. Analysis of muscle ultrastructure revealed selective fiber damage, especially in the ragged‐red‐fibers (RRFs), a MM hallmark. Two years of follow‐up showed improvement of muscle strength, suggesting activation of muscle regeneration. Our results indicate that (i) nutrition can modify mitochondrial disease progression, (ii) dietary counseling should be part of MM care, (iii) short mAD is a tool to induce targeted RRF lysis, and (iv) mAD, a common weight‐loss method, may induce muscle damage in a population subgroup.
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spelling doaj-art-a0ecd12a5c6544f69d9acb19eea6a1d62025-08-20T03:05:55ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842016-09-018111234124710.15252/emmm.201606592Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patientsSofia Ahola0Mari Auranen1Pirjo Isohanni2Satu Niemisalo3Niina Urho4Jana Buzkova5Vidya Velagapudi6Nina Lundbom7Antti Hakkarainen8Tiina Muurinen9Päivi Piirilä10Kirsi H Pietiläinen11Anu Suomalainen12Research Program of Molecular Neurology, Biomedicum Helsinki, University of HelsinkiResearch Program of Molecular Neurology, Biomedicum Helsinki, University of HelsinkiResearch Program of Molecular Neurology, Biomedicum Helsinki, University of HelsinkiObesity Research Unit, Research Programs Unit, Diabetes and Obesity, University of HelsinkiClinical Neurosciences, Neurology, University of Helsinki and Helsinki University HospitalResearch Program of Molecular Neurology, Biomedicum Helsinki, University of HelsinkiMetabolomics Unit, Institute for Molecular Medicine Finland FIMM, University of HelsinkiDepartment of Radiology, University of Helsinki and HUS Radiology, Helsinki Medical Imaging CenterDepartment of Radiology, University of Helsinki and HUS Radiology, Helsinki Medical Imaging CenterDepartment of Clinical Physiology and Nuclear Medicine, Laboratory of Clinical Physiology, Helsinki University HospitalsDepartment of Clinical Physiology and Nuclear Medicine, Laboratory of Clinical Physiology, Helsinki University HospitalsClinical Neurosciences, Neurology, University of Helsinki and Helsinki University HospitalResearch Program of Molecular Neurology, Biomedicum Helsinki, University of HelsinkiAbstract Mitochondrial myopathy (MM) with progressive external ophthalmoplegia (PEO) is a common manifestation of mitochondrial disease in adulthood, for which there is no curative therapy. In mice with MM, ketogenic diet significantly delayed progression of the disease. We asked in this pilot study what effects high‐fat, low‐carbohydrate “modified Atkins” diet (mAD) had for PEO/MM patients and control subjects and followed up the effects by clinical, morphological, transcriptomic, and metabolomic analyses. All of our five patients, irrespective of genotype, showed a subacute response after 1.5–2 weeks of diet, with progressive muscle pain and leakage of muscle enzymes, leading to premature discontinuation of the diet. Analysis of muscle ultrastructure revealed selective fiber damage, especially in the ragged‐red‐fibers (RRFs), a MM hallmark. Two years of follow‐up showed improvement of muscle strength, suggesting activation of muscle regeneration. Our results indicate that (i) nutrition can modify mitochondrial disease progression, (ii) dietary counseling should be part of MM care, (iii) short mAD is a tool to induce targeted RRF lysis, and (iv) mAD, a common weight‐loss method, may induce muscle damage in a population subgroup.https://doi.org/10.15252/emmm.201606592mitochondrial myopathymodified Atkins dietPEOragged‐red‐fibers
spellingShingle Sofia Ahola
Mari Auranen
Pirjo Isohanni
Satu Niemisalo
Niina Urho
Jana Buzkova
Vidya Velagapudi
Nina Lundbom
Antti Hakkarainen
Tiina Muurinen
Päivi Piirilä
Kirsi H Pietiläinen
Anu Suomalainen
Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients
EMBO Molecular Medicine
mitochondrial myopathy
modified Atkins diet
PEO
ragged‐red‐fibers
title Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients
title_full Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients
title_fullStr Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients
title_full_unstemmed Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients
title_short Modified Atkins diet induces subacute selective ragged‐red‐fiber lysis in mitochondrial myopathy patients
title_sort modified atkins diet induces subacute selective ragged red fiber lysis in mitochondrial myopathy patients
topic mitochondrial myopathy
modified Atkins diet
PEO
ragged‐red‐fibers
url https://doi.org/10.15252/emmm.201606592
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