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Erschienen in: Clinical Neuroradiology 1/2019

03.01.2018 | Original Article

Cortical and Subcortical Morphometric and Iron Changes in Relapsing-Remitting Multiple Sclerosis and Their Association with White Matter T2 Lesion Load

A 3-Tesla Magnetic Resonance Imaging Study

Erschienen in: Clinical Neuroradiology | Ausgabe 1/2019

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Abstract

Introduction

This study was carried out to investigate the global and regional morphometric and iron changes in grey matter (GM) of multiple sclerosis (MS) patients and link them to the white matter (WM) lesions in a multimodal magnetic resonance imaging approach.

Material and Methods

The study involved 30 relapsing-remitting MS (RRMS) patients along with 30 age-matched healthy controls (HC) who were scanned on a 3T Siemens Trio system. The scanning protocol included a 3D, high resolution T1, T2, and T2*-weighted sequences. The T1-w images were used in FreeSurfer for cortical reconstruction and volumetric segmentation, while T2-w images were used to extract the WM T2 lesions; however, iron and magnetic susceptibility were calculated from the phase data of the T2*-w sequence. Surface-based analyses were performed in FreeSurfer to investigate the regional cortical morphometric changes and their correlations with the expanded disability status scale (EDSS), WM T2 lesions load, cortical iron deposition and magnetic susceptibility.

Results

Significant differences were detected between the RRMS patients and HC for all cortical and subcortical morphometric changes. The EDSS and T2 lesion load showed weak to moderate correlation with the reduced cortical morphometric measurements, increased cortical magnetic susceptibility and iron concentration. All deep grey matter (dGM) volumes showed a significant strong positive correlation with the cortical surface area and volume in RRMS patients and HC.

Conclusions

Grey matter is very much involved in the RRMS and cortical morphometric changes occur in a non-uniform pattern and are very likely to be associated with cortical iron deposition and magnetic susceptibility, dGM atrophy, WM T2 lesion load, and disability.
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Literatur
2.
Zurück zum Zitat Neema M, Stankiewicz J, Arora A, Dandamudi VS, Batt CE, Guss ZD, Al-Sabbagh A, Bakshi R. T1- and T2-based MRI measures of diffuse gray matter and white matter damage in patients with multiple sclerosis. J Neuroimaging. 2007;17:16S–21S.CrossRefPubMed Neema M, Stankiewicz J, Arora A, Dandamudi VS, Batt CE, Guss ZD, Al-Sabbagh A, Bakshi R. T1- and T2-based MRI measures of diffuse gray matter and white matter damage in patients with multiple sclerosis. J Neuroimaging. 2007;17:16S–21S.CrossRefPubMed
3.
Zurück zum Zitat Rovaris M, Rocca MA, Filippi M. Magnetic resonance-based techniques for the study and management of multiple sclerosis. Br Med Bull. 2003;65:133–44.CrossRefPubMed Rovaris M, Rocca MA, Filippi M. Magnetic resonance-based techniques for the study and management of multiple sclerosis. Br Med Bull. 2003;65:133–44.CrossRefPubMed
4.
Zurück zum Zitat Bö L, Geurts JJ, van der Valk P, Polman C, Barkhof F. Lack of correlation between cortical demyelination and white matter pathologic changes in multiple sclerosis. Arch Neurol. 2007;64:76–80.CrossRefPubMed Bö L, Geurts JJ, van der Valk P, Polman C, Barkhof F. Lack of correlation between cortical demyelination and white matter pathologic changes in multiple sclerosis. Arch Neurol. 2007;64:76–80.CrossRefPubMed
6.
Zurück zum Zitat Schutzer SE, Angel TE, Liu T, Schepmoes AA, Xie F, Bergquist J, Vécsei L, Zadori D, Camp DG 2nd, Holland BK, Smith RD, Coyle PK. Gray matter is targeted in first-attack multiple sclerosis. PLoS ONE. 2013;8:e66117.CrossRefPubMedPubMedCentral Schutzer SE, Angel TE, Liu T, Schepmoes AA, Xie F, Bergquist J, Vécsei L, Zadori D, Camp DG 2nd, Holland BK, Smith RD, Coyle PK. Gray matter is targeted in first-attack multiple sclerosis. PLoS ONE. 2013;8:e66117.CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Pirko I, Lucchinetti CF, Sriram S, Bakshi R. Gray matter involvement in multiple sclerosis. Neurology. 2007;68:634–42.CrossRefPubMed Pirko I, Lucchinetti CF, Sriram S, Bakshi R. Gray matter involvement in multiple sclerosis. Neurology. 2007;68:634–42.CrossRefPubMed
8.
Zurück zum Zitat Dawson JW. The histology of multiple sclerosis. Philos Trans R Soc. 1916;50:517–740. Dawson JW. The histology of multiple sclerosis. Philos Trans R Soc. 1916;50:517–740.
9.
Zurück zum Zitat Kutzelnigg A1, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, Bergmann M, Schmidbauer M, Parisi JE, Lassmann H. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain. 2005;128:2705–12.CrossRefPubMed Kutzelnigg A1, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, Bergmann M, Schmidbauer M, Parisi JE, Lassmann H. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain. 2005;128:2705–12.CrossRefPubMed
10.
Zurück zum Zitat Geurts JJ, Bö L, Pouwels PJ, Castelijns JA, Polman CH, Barkhof F. Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology. AJNR Am J Neuroradiol. 2005;26(3):572–7.PubMed Geurts JJ, Bö L, Pouwels PJ, Castelijns JA, Polman CH, Barkhof F. Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology. AJNR Am J Neuroradiol. 2005;26(3):572–7.PubMed
11.
Zurück zum Zitat Kidd D, Barkhof F, McConnell R, Algra PR, Allen IV, Revesz T. Cortical lesions in multiple sclerosis. Brain. 1999;122:17–26.CrossRefPubMed Kidd D, Barkhof F, McConnell R, Algra PR, Allen IV, Revesz T. Cortical lesions in multiple sclerosis. Brain. 1999;122:17–26.CrossRefPubMed
12.
Zurück zum Zitat Peterson JW, Bö L, Mörk S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol. 2001;50:389–400.CrossRefPubMed Peterson JW, Bö L, Mörk S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol. 2001;50:389–400.CrossRefPubMed
13.
Zurück zum Zitat Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology. 2006;67:960–7.CrossRefPubMed Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology. 2006;67:960–7.CrossRefPubMed
14.
Zurück zum Zitat Dutta R, Chang A, Doud MK, Kidd GJ, Ribaudo MV, Young EA, Fox RJ, Staugaitis SM, Trapp BD. Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients. Ann Neurol. 2011;69:445–54.CrossRefPubMedPubMedCentral Dutta R, Chang A, Doud MK, Kidd GJ, Ribaudo MV, Young EA, Fox RJ, Staugaitis SM, Trapp BD. Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients. Ann Neurol. 2011;69:445–54.CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Bakshi R, Dandamudi VSR, Neema M, De C, Bermel RA. Measurement of brain and spinal cord atrophy by magnetic resonance imaging as a tool to monitor multiple sclerosis. J Neuroimaging. 2005;15(4 Suppl):30S-45S.CrossRefPubMed Bakshi R, Dandamudi VSR, Neema M, De C, Bermel RA. Measurement of brain and spinal cord atrophy by magnetic resonance imaging as a tool to monitor multiple sclerosis. J Neuroimaging. 2005;15(4 Suppl):30S-45S.CrossRefPubMed
16.
Zurück zum Zitat Fisher E, Lee JC, Nakamura K, Rudick RA. Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol. 2008;64:255–65.CrossRefPubMed Fisher E, Lee JC, Nakamura K, Rudick RA. Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol. 2008;64:255–65.CrossRefPubMed
17.
Zurück zum Zitat Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR. Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci. 2004;5:863–73.CrossRefPubMed Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR. Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci. 2004;5:863–73.CrossRefPubMed
18.
Zurück zum Zitat Sadrzadeh SM, Saffari Y. Iron and brain disorders. Am J Clin Pathol. 2004;121 Suppl:S64–70.CrossRef Sadrzadeh SM, Saffari Y. Iron and brain disorders. Am J Clin Pathol. 2004;121 Suppl:S64–70.CrossRef
19.
Zurück zum Zitat LeVine SM. Iron deposits in multiple sclerosis and Alzheimer’s disease brains. Brain Res. 1997;760:298–303.CrossRefPubMed LeVine SM. Iron deposits in multiple sclerosis and Alzheimer’s disease brains. Brain Res. 1997;760:298–303.CrossRefPubMed
20.
Zurück zum Zitat Al-Radaideh AM, Wharton SJ, Lim SY, Tench CR, Morgan PS, Bowtell RW, Constantinescu CS, Gowland PA. Increased iron accumulation occurs in the earliest stages of demyelinating disease: an ultra-high field susceptibility mapping study in Clinically Isolated Syndrome. Mult Scler. 2013;19:896–903.CrossRefPubMed Al-Radaideh AM, Wharton SJ, Lim SY, Tench CR, Morgan PS, Bowtell RW, Constantinescu CS, Gowland PA. Increased iron accumulation occurs in the earliest stages of demyelinating disease: an ultra-high field susceptibility mapping study in Clinically Isolated Syndrome. Mult Scler. 2013;19:896–903.CrossRefPubMed
21.
Zurück zum Zitat Hallgren B, Sourander P. The effect of age on the non-haemin iron in the human brain. J Neurochem. 1958;3:41–51.CrossRefPubMed Hallgren B, Sourander P. The effect of age on the non-haemin iron in the human brain. J Neurochem. 1958;3:41–51.CrossRefPubMed
22.
Zurück zum Zitat Hebbrecht G, Maenhaut W, De Reuck J. Brain trace elements and aging. Nucl Instrum Methods Phys Res B. 1999;150:208–13.CrossRef Hebbrecht G, Maenhaut W, De Reuck J. Brain trace elements and aging. Nucl Instrum Methods Phys Res B. 1999;150:208–13.CrossRef
23.
Zurück zum Zitat Ramos P, Santos A, Pinto NR, Mendes R, Magalhães T, Almeida A. Iron levels in the human brain: a post-mortem study of anatomical region differences and age-related changes. J Trace Elem Med Biol. 2014;28:13–7.CrossRefPubMed Ramos P, Santos A, Pinto NR, Mendes R, Magalhães T, Almeida A. Iron levels in the human brain: a post-mortem study of anatomical region differences and age-related changes. J Trace Elem Med Biol. 2014;28:13–7.CrossRefPubMed
24.
Zurück zum Zitat Yao B, Hametner S, van Gelderen P, Merkle H, Chen C, Lassmann H, Duyn JH, Bagnato F. 7 Tesla magnetic resonance imaging to detect cortical pathology in multiple sclerosis. PLoS ONE. 2014;9:e108863.CrossRefPubMedPubMedCentral Yao B, Hametner S, van Gelderen P, Merkle H, Chen C, Lassmann H, Duyn JH, Bagnato F. 7 Tesla magnetic resonance imaging to detect cortical pathology in multiple sclerosis. PLoS ONE. 2014;9:e108863.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Buijs M, Doan NT, van Rooden S, Versluis MJ, van Lew B, Milles J, van der Grond J, van Buchem MA. In vivo assessment of iron content of the cerebral cortex in healthy aging using 7‑Tesla T2*-weighted phase imaging. Neurobiol Aging. 2017;53:20–6.CrossRefPubMed Buijs M, Doan NT, van Rooden S, Versluis MJ, van Lew B, Milles J, van der Grond J, van Buchem MA. In vivo assessment of iron content of the cerebral cortex in healthy aging using 7‑Tesla T2*-weighted phase imaging. Neurobiol Aging. 2017;53:20–6.CrossRefPubMed
26.
Zurück zum Zitat Moodie J, Healy BC, Buckle GJ, Gauthier SA, Glanz BI, Arora A, Ceccarelli A, Tauhid S, Han XM, Venkataraman A, Chitnis T, Khoury SJ, Guttmann CR, Weiner HL, Neema M, Bakshi R. Magnetic resonance disease severity scale (MRDSS) for patients with multiple sclerosis: a longitudinal study. J Neurol Sci. 2012;315:49–54.CrossRefPubMed Moodie J, Healy BC, Buckle GJ, Gauthier SA, Glanz BI, Arora A, Ceccarelli A, Tauhid S, Han XM, Venkataraman A, Chitnis T, Khoury SJ, Guttmann CR, Weiner HL, Neema M, Bakshi R. Magnetic resonance disease severity scale (MRDSS) for patients with multiple sclerosis: a longitudinal study. J Neurol Sci. 2012;315:49–54.CrossRefPubMed
27.
Zurück zum Zitat Raz E, Branson B, Jensen JH, Bester M, Babb JS, Herbert J, Grossman RI, Inglese M. Relationship between iron accumulation and white matter injury in multiple sclerosis: a case-control study. J Neurol. 2015;262:402–9.CrossRefPubMed Raz E, Branson B, Jensen JH, Bester M, Babb JS, Herbert J, Grossman RI, Inglese M. Relationship between iron accumulation and white matter injury in multiple sclerosis: a case-control study. J Neurol. 2015;262:402–9.CrossRefPubMed
28.
Zurück zum Zitat Wharton S, Schäfer A, Bowtell R. Susceptibility mapping in the human brain using threshold-based k‑space division. Magn Reson Med. 2010;63:1292–304.CrossRefPubMed Wharton S, Schäfer A, Bowtell R. Susceptibility mapping in the human brain using threshold-based k‑space division. Magn Reson Med. 2010;63:1292–304.CrossRefPubMed
29.
Zurück zum Zitat Haacke EM, Ayaz M, Khan A, Manova ES, Krishnamurthy B, Gollapalli L, Ciulla C, Kim I, Petersen F, Kirsch W. Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain. J Magn Reson Imaging. 2007;26:256–64.CrossRefPubMed Haacke EM, Ayaz M, Khan A, Manova ES, Krishnamurthy B, Gollapalli L, Ciulla C, Kim I, Petersen F, Kirsch W. Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain. J Magn Reson Imaging. 2007;26:256–64.CrossRefPubMed
30.
Zurück zum Zitat Susceptibility weighted imaging in MRI: basic concepts and clinical applications. Eds. EM Haacke, JR Reichenbach, John Wiley & Sons, 2014 Susceptibility weighted imaging in MRI: basic concepts and clinical applications. Eds. EM Haacke, JR Reichenbach, John Wiley & Sons, 2014
31.
Zurück zum Zitat Udupa JK, Samarasekera S. Fuzzy connectedness and object definition: theory, algorithms, and applications in image segmentation. Graph Models Image Process. 1996;58:246–61.CrossRef Udupa JK, Samarasekera S. Fuzzy connectedness and object definition: theory, algorithms, and applications in image segmentation. Graph Models Image Process. 1996;58:246–61.CrossRef
32.
Zurück zum Zitat Liu M, Habib C, Miao Y, Haacke EM. Measuring iron content with phase. Susceptibility weighted imaging in MRI: basic concepts and clinical applications. Eds. EM Haacke, JR Reichenbach, pp. 369–401, John Wiley & Sons 2011.CrossRef Liu M, Habib C, Miao Y, Haacke EM. Measuring iron content with phase. Susceptibility weighted imaging in MRI: basic concepts and clinical applications. Eds. EM Haacke, JR Reichenbach, pp. 369–401, John Wiley & Sons 2011.CrossRef
33.
Zurück zum Zitat Battaglini M, Jenkinson M, De Stefano N. Evaluating and reducing the impact of white matter lesions on brain volume measurements. Hum Brain Mapp. 2012;33:2062–71.CrossRefPubMed Battaglini M, Jenkinson M, De Stefano N. Evaluating and reducing the impact of white matter lesions on brain volume measurements. Hum Brain Mapp. 2012;33:2062–71.CrossRefPubMed
34.
Zurück zum Zitat Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–55.CrossRefPubMed Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–55.CrossRefPubMed
35.
Zurück zum Zitat Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9:195–207.CrossRefPubMed Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9:195–207.CrossRefPubMed
36.
Zurück zum Zitat Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9:179–94.CrossRefPubMed Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9:179–94.CrossRefPubMed
37.
Zurück zum Zitat Sailer M, Fischl B, Salat D, Tempelmann C, Schönfeld MA, Busa E, Bodammer N, Heinze HJ, Dale A. Focal thinning of the cerebral cortex in multiple sclerosis. Brain. 2003;126:1734–44.CrossRefPubMed Sailer M, Fischl B, Salat D, Tempelmann C, Schönfeld MA, Busa E, Bodammer N, Heinze HJ, Dale A. Focal thinning of the cerebral cortex in multiple sclerosis. Brain. 2003;126:1734–44.CrossRefPubMed
38.
Zurück zum Zitat Narayana PA, Govindarajan KA, Goel P, Datta S, Lincoln JA, Cofield SS, Cutter GR, Lublin FD, Wolinsky JS; MRI Analysis Center at Houston; The CombiRx Investigators Group. Regional cortical thickness in relapsing remitting multiple sclerosis: a multi-center study. Neuroimage Clin. 2013;2:120–31.CrossRef Narayana PA, Govindarajan KA, Goel P, Datta S, Lincoln JA, Cofield SS, Cutter GR, Lublin FD, Wolinsky JS; MRI Analysis Center at Houston; The CombiRx Investigators Group. Regional cortical thickness in relapsing remitting multiple sclerosis: a multi-center study. Neuroimage Clin. 2013;2:120–31.CrossRef
39.
Zurück zum Zitat Geisseler O, Pflugshaupt T, Bezzola L, Reuter K, Weller D, Schuknecht B, Brugger P, Linnebank M. Cortical thinning in the anterior cingulate cortex predicts multiple sclerosis patients’ fluency performance in a lateralised manner. Neuroimage Clin. 2016;10:89–95.CrossRefPubMed Geisseler O, Pflugshaupt T, Bezzola L, Reuter K, Weller D, Schuknecht B, Brugger P, Linnebank M. Cortical thinning in the anterior cingulate cortex predicts multiple sclerosis patients’ fluency performance in a lateralised manner. Neuroimage Clin. 2016;10:89–95.CrossRefPubMed
40.
Zurück zum Zitat Nygaard GO, Walhovd KB, Sowa P, Chepkoech JL, Bjørnerud A, Due-Tønnessen P, Landrø NI, Damangir S, Spulber G, Storsve AB, Beyer MK, Fjell AM, Celius EG, Harbo HF. Cortical thickness and surface area relate to specific symptoms in early relapsing-remitting multiple sclerosis. Mult Scler. 2015;21:402–14.CrossRefPubMed Nygaard GO, Walhovd KB, Sowa P, Chepkoech JL, Bjørnerud A, Due-Tønnessen P, Landrø NI, Damangir S, Spulber G, Storsve AB, Beyer MK, Fjell AM, Celius EG, Harbo HF. Cortical thickness and surface area relate to specific symptoms in early relapsing-remitting multiple sclerosis. Mult Scler. 2015;21:402–14.CrossRefPubMed
41.
Zurück zum Zitat Hier DB, Wang J. Reduced cortical surface area in multiple sclerosis. Neurol Res. 2007;29:231–2.CrossRefPubMed Hier DB, Wang J. Reduced cortical surface area in multiple sclerosis. Neurol Res. 2007;29:231–2.CrossRefPubMed
42.
Zurück zum Zitat Charil A, Dagher A, Lerch JP, Zijdenbos AP, Worsley KJ, Evans AC. Focal cortical atrophy in multiple sclerosis: relation to lesion load and disability. Neuroimage. 2007;34:509–17.CrossRefPubMed Charil A, Dagher A, Lerch JP, Zijdenbos AP, Worsley KJ, Evans AC. Focal cortical atrophy in multiple sclerosis: relation to lesion load and disability. Neuroimage. 2007;34:509–17.CrossRefPubMed
43.
Zurück zum Zitat Datta S, Staewen TD, Cofield SS, Cutter GR, Lublin FD, Wolinsky JS, Narayana PA; MRI Analysis Center at Houston; CombiRx Investigators Group. Regional gray matter atrophy in relapsing remitting multiple sclerosis: baseline analysis of multi-center data. Mult Scler Relat Disord. 2015;4:124–36.CrossRefPubMedPubMedCentral Datta S, Staewen TD, Cofield SS, Cutter GR, Lublin FD, Wolinsky JS, Narayana PA; MRI Analysis Center at Houston; CombiRx Investigators Group. Regional gray matter atrophy in relapsing remitting multiple sclerosis: baseline analysis of multi-center data. Mult Scler Relat Disord. 2015;4:124–36.CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Filippi M, Rocca MA, Horsfield MA, Hametner S, Geurts JJ, Comi G, Lassmann H. Imaging cortical damage and dysfunction in multiple sclerosis. JAMA Neurol. 2013;70:556-64.CrossRefPubMed Filippi M, Rocca MA, Horsfield MA, Hametner S, Geurts JJ, Comi G, Lassmann H. Imaging cortical damage and dysfunction in multiple sclerosis. JAMA Neurol. 2013;70:556-64.CrossRefPubMed
45.
Zurück zum Zitat Filippi M, Preziosa P, Copetti M, Riccitelli G, Horsfield MA, Martinelli V, Comi G, Rocca MA. Gray matter damage predicts the accumulation of disability 13 years later in MS. Neurology. 2013;81:1759–67.CrossRefPubMed Filippi M, Preziosa P, Copetti M, Riccitelli G, Horsfield MA, Martinelli V, Comi G, Rocca MA. Gray matter damage predicts the accumulation of disability 13 years later in MS. Neurology. 2013;81:1759–67.CrossRefPubMed
46.
Zurück zum Zitat Jacobsen C, Hagemeier J, Myhr KM, Nyland H, Lode K, Bergsland N, Ramasamy DP, Dalaker TO, Larsen JP, Farbu E, Zivadinov R. Brain atrophy and disability progression in multiple sclerosis patients: a 10-year follow-up study. J Neurol Neurosurg Psychiatr. 2014;85:1109–15.CrossRef Jacobsen C, Hagemeier J, Myhr KM, Nyland H, Lode K, Bergsland N, Ramasamy DP, Dalaker TO, Larsen JP, Farbu E, Zivadinov R. Brain atrophy and disability progression in multiple sclerosis patients: a 10-year follow-up study. J Neurol Neurosurg Psychiatr. 2014;85:1109–15.CrossRef
47.
Zurück zum Zitat Hammond KE, Metcalf M, Carvajal L, Okuda DT, Srinivasan R, Vigneron D, Nelson SJ, Pelletier D. Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol. 2008;64:707–13.CrossRefPubMed Hammond KE, Metcalf M, Carvajal L, Okuda DT, Srinivasan R, Vigneron D, Nelson SJ, Pelletier D. Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol. 2008;64:707–13.CrossRefPubMed
48.
Zurück zum Zitat Chen X, Zeng C, Luo T, Ouyang Y, Lv F, Rumzan R, Wang Z, Li Q, Wang J, Hou H, Huang F, Li Y. Iron deposition of the deep grey matter in patients with multiple sclerosis and neuromyelitis optica: a control quantitative study by 3D-enhanced susceptibility-weighted angiography (ESWAN). Eur J Radiol. 2012;81:e633–9.CrossRefPubMed Chen X, Zeng C, Luo T, Ouyang Y, Lv F, Rumzan R, Wang Z, Li Q, Wang J, Hou H, Huang F, Li Y. Iron deposition of the deep grey matter in patients with multiple sclerosis and neuromyelitis optica: a control quantitative study by 3D-enhanced susceptibility-weighted angiography (ESWAN). Eur J Radiol. 2012;81:e633–9.CrossRefPubMed
49.
Zurück zum Zitat Du S, Sah SK, Zeng C, Wang J, Liu Y, Xiong H, Li Y. Iron deposition in the gray matter in patients with relapse-remitting multiple sclerosis: a longitudinal study using three-dimensional (3D)-enhanced T2*-weighted angiography (ESWAN). Eur J Radiol. 2015;84:1325–32.CrossRefPubMed Du S, Sah SK, Zeng C, Wang J, Liu Y, Xiong H, Li Y. Iron deposition in the gray matter in patients with relapse-remitting multiple sclerosis: a longitudinal study using three-dimensional (3D)-enhanced T2*-weighted angiography (ESWAN). Eur J Radiol. 2015;84:1325–32.CrossRefPubMed
50.
Zurück zum Zitat Lee J, Shmueli K, Fukunaga M, van Gelderen P, Merkle H, Silva AC, Duyn JH. Sensitivity of MRI resonance frequency to the orientation of brain tissue microstructure. Proc Natl Acad Sci U S A. 2010;107:5130-5.CrossRefPubMedPubMedCentral Lee J, Shmueli K, Fukunaga M, van Gelderen P, Merkle H, Silva AC, Duyn JH. Sensitivity of MRI resonance frequency to the orientation of brain tissue microstructure. Proc Natl Acad Sci U S A. 2010;107:5130-5.CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Prinster A, Quarantelli M, Orefice G, Lanzillo R, Brunetti A, Mollica C, Salvatore E, Morra VB, Coppola G, Vacca G, Alfano B, Salvatore M. Grey matter loss in relapsing–remitting multiple sclerosis: a voxel-based morphometry study. Neuroimage. 2006;29:859–67.CrossRefPubMed Prinster A, Quarantelli M, Orefice G, Lanzillo R, Brunetti A, Mollica C, Salvatore E, Morra VB, Coppola G, Vacca G, Alfano B, Salvatore M. Grey matter loss in relapsing–remitting multiple sclerosis: a voxel-based morphometry study. Neuroimage. 2006;29:859–67.CrossRefPubMed
52.
Zurück zum Zitat Preziosa P, Pagani E, Mesaros S, Riccitelli GC, Dackovic J, Drulovic J, Filippi M, Rocca MA. Progression of regional atrophy in the left hemisphere contributes to clinical and cognitive deterioration in multiple sclerosis: a 5‑year study. Hum Brain Mapp. 2017;38:5648–65.CrossRefPubMed Preziosa P, Pagani E, Mesaros S, Riccitelli GC, Dackovic J, Drulovic J, Filippi M, Rocca MA. Progression of regional atrophy in the left hemisphere contributes to clinical and cognitive deterioration in multiple sclerosis: a 5‑year study. Hum Brain Mapp. 2017;38:5648–65.CrossRefPubMed
Metadaten
Titel
Cortical and Subcortical Morphometric and Iron Changes in Relapsing-Remitting Multiple Sclerosis and Their Association with White Matter T2 Lesion Load
A 3-Tesla Magnetic Resonance Imaging Study
Publikationsdatum
03.01.2018
Erschienen in
Clinical Neuroradiology / Ausgabe 1/2019
Print ISSN: 1869-1439
Elektronische ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-017-0654-0

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