Reduced cerebral gray matter and altered white matter in boys with Duchenne muscular dystrophy
Objective Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full‐length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associate...
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| Published in | Annals of neurology Vol. 76; no. 3; pp. 403 - 411 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.09.2014
Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0364-5134 1531-8249 1531-8249 |
| DOI | 10.1002/ana.24222 |
Cover
| Abstract | Objective
Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full‐length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD.
Methods
T1‐weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age‐matched controls (age = 8–18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140+ and DMD_Dp140−).
Results
DMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140− subjects contributed most to the gray matter volume differences and performed worse on information processing.
Interpretation
Both gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140− subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development. Ann Neurol 2014;76:403–411 |
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| AbstractList | Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD.OBJECTIVEDuchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD.T1-weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age-matched controls (age = 8-18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140(+) and DMD_Dp140(-) ).METHODST1-weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age-matched controls (age = 8-18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140(+) and DMD_Dp140(-) ).DMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140(-) subjects contributed most to the gray matter volume differences and performed worse on information processing.RESULTSDMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140(-) subjects contributed most to the gray matter volume differences and performed worse on information processing.Both gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140(-) subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development.INTERPRETATIONBoth gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140(-) subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development. Objective Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD. Methods T1-weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age-matched controls (age=8-18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140 super(+) and DMD_Dp140 super(-)). Results DMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140 super(-) subjects contributed most to the gray matter volume differences and performed worse on information processing. Interpretation Both gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140 super(-) subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development. Ann Neurol 2014; 76:403-411 Objective Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full‐length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD. Methods T1‐weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age‐matched controls (age = 8–18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140+ and DMD_Dp140−). Results DMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140− subjects contributed most to the gray matter volume differences and performed worse on information processing. Interpretation Both gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140− subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development. Ann Neurol 2014;76:403–411 Objective Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD. Methods T1-weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age-matched controls (age=8-18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140+ and DMD_Dp140-). Results DMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140- subjects contributed most to the gray matter volume differences and performed worse on information processing. Interpretation Both gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140- subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development. Ann Neurol 2014;76:403-411 [PUBLICATION ABSTRACT] Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length dystrophin protein in muscle. Multiple dystrophin isoforms are expressed in brain, but little is known about their function. DMD is associated with specific learning and behavioral disabilities that are more prominent in patients with mutations in the distal part of the DMD gene, predicted to affect expression of shorter protein isoforms. We used quantitative magnetic resonance (MR) imaging to study brain microstructure in DMD. T1-weighted and diffusion tensor images were obtained on a 3T MR scanner from 30 patients and 22 age-matched controls (age = 8-18 years). All subjects underwent neuropsychological examination. Group comparisons on tissue volume and diffusion tensor imaging parameters were made between DMD patients and controls, and between 2 DMD subgroups that were classified according to predicted Dp140 isoform expression (DMD_Dp140(+) and DMD_Dp140(-) ). DMD patients had smaller total brain volume, smaller gray matter volume, lower white matter fractional anisotropy, and higher white matter mean and radial diffusivity than healthy controls. DMD patients also performed worse on neuropsychological examination. Subgroup analyses showed that DMD_Dp140(-) subjects contributed most to the gray matter volume differences and performed worse on information processing. Both gray and white matter is affected in boys with DMD at a whole brain level. Differences between the DMD_Dp140(-) subgroup and controls indicate an important role for the Dp140 dystrophin isoform in cerebral development. |
| Author | Doorenweerd, Nathalie Webb, Andrew Verschuuren, Jan J. Hendriksen, Jos G. Ginjaar, Ieke B. Wokke, Beatrijs H. Schrans, Debby G. Straathof, Chiara S. Niks, Erik H. van den Bergen, Janneke C. Dumas, Eve M. van Zwet, Erik W. Kan, Hermien E. Spitali, Pietro van Buchem, Mark A. |
| Author_xml | – sequence: 1 givenname: Nathalie surname: Doorenweerd fullname: Doorenweerd, Nathalie email: N.Doorenweerd@lumc.nl organization: Department of Radiology, C. J. Gorter Center for High Field MRI, Leiden University Medical Center, Leiden – sequence: 2 givenname: Chiara S. surname: Straathof fullname: Straathof, Chiara S. organization: Department of Neurology, Leiden University Medical Center, Leiden – sequence: 3 givenname: Eve M. surname: Dumas fullname: Dumas, Eve M. organization: Department of Neurology, Leiden University Medical Center, Leiden – sequence: 4 givenname: Pietro surname: Spitali fullname: Spitali, Pietro organization: Department of Human Genetics, Leiden University Medical Center, Leiden – sequence: 5 givenname: Ieke B. surname: Ginjaar fullname: Ginjaar, Ieke B. organization: Department of Clinical Genetics, Leiden University Medical Center, Leiden – sequence: 6 givenname: Beatrijs H. surname: Wokke fullname: Wokke, Beatrijs H. organization: Department of Neurology, Leiden University Medical Center, Leiden – sequence: 7 givenname: Debby G. surname: Schrans fullname: Schrans, Debby G. organization: Department of Neurological Learning Disabilities, Kempenhaeghe Epilepsy Center, Heeze – sequence: 8 givenname: Janneke C. surname: van den Bergen fullname: van den Bergen, Janneke C. organization: Department of Neurology, Leiden University Medical Center, Leiden – sequence: 9 givenname: Erik W. surname: van Zwet fullname: van Zwet, Erik W. organization: Department of Medical Statistics, Leiden University Medical Center, Leiden – sequence: 10 givenname: Andrew surname: Webb fullname: Webb, Andrew organization: Department of Radiology, C. J. Gorter Center for High Field MRI, Leiden University Medical Center, Leiden – sequence: 11 givenname: Mark A. surname: van Buchem fullname: van Buchem, Mark A. organization: Department of Radiology, C. J. Gorter Center for High Field MRI, Leiden University Medical Center, Leiden – sequence: 12 givenname: Jan J. surname: Verschuuren fullname: Verschuuren, Jan J. organization: Department of Neurology, Leiden University Medical Center, Leiden – sequence: 13 givenname: Jos G. surname: Hendriksen fullname: Hendriksen, Jos G. organization: Department of Neurological Learning Disabilities, Kempenhaeghe Epilepsy Center, Heeze – sequence: 14 givenname: Erik H. surname: Niks fullname: Niks, Erik H. organization: Department of Neurology, Leiden University Medical Center, Leiden – sequence: 15 givenname: Hermien E. surname: Kan fullname: Kan, Hermien E. organization: Department of Radiology, C. J. Gorter Center for High Field MRI, Leiden University Medical Center, Leiden |
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article-title: Decreased gray matter concentration and local synchronization of spontaneous activity in the motor, cortex in Duchenne muscular dystrophy publication-title: AJNR Am J Neuroradiol |
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Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full‐length... Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length dystrophin... Objective Duchenne muscular dystrophy (DMD) is characterized by progressive muscle weakness caused by DMD gene mutations leading to absence of the full-length... |
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| SubjectTerms | Adolescent Cerebral Cortex - pathology Child Diffusion Tensor Imaging - instrumentation Diffusion Tensor Imaging - methods Dystrophin - genetics Gray Matter - pathology Humans Magnetic Resonance Imaging - instrumentation Magnetic Resonance Imaging - methods Male Medical research Muscular dystrophy Muscular Dystrophy, Duchenne - genetics Muscular Dystrophy, Duchenne - pathology Muscular Dystrophy, Duchenne - physiopathology Mutation Mutation - genetics Nerve Fibers, Myelinated - pathology Protein Isoforms - genetics White Matter - pathology |
| Title | Reduced cerebral gray matter and altered white matter in boys with Duchenne muscular dystrophy |
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