Skip to main content
Erschienen in: European Radiology 3/2024

02.09.2023 | Neuro

U-fiber diffusion kurtosis and susceptibility characteristics in relapsing–remitting multiple sclerosis may be related to cognitive deficits and neurodegeneration

verfasst von: Dan Luo, Yuling Peng, Qiyuan Zhu, Qiao Zheng, Qi Luo, Yongliang Han, Xiaoya Chen, Yongmei Li

Erschienen in: European Radiology | Ausgabe 3/2024

Einloggen, um Zugang zu erhalten

Abstract

Objectives

To evaluate the diffusion kurtosis and susceptibility change in the U-fiber region of patients with relapsing–remitting multiple sclerosis (pwRRMS) and their correlations with cognitive status and degeneration.

Materials and methods

Mean kurtosis (MK), axial kurtosis (AK), radial kurtosis (RK), kurtosis fractional anisotropy (KFA), and the mean relative quantitative susceptibility mapping (mrQSM) values in the U-fiber region were compared between 49 pwRRMS and 48 healthy controls (HCs). The U-fiber were divided into upper and deeper groups based on the location. The whole brain volume, gray and white matter volume, and cortical thickness were obtained. The correlations between the mrQSM values, DKI-derived metrics in the U-fiber region and clinical scale scores, brain morphologic parameters were further investigated.

Results

The decreased MK, AK, RK, KFA, and increased mrQSM values in U-fiber lesions (p < 0.001, FDR corrected), decreased RK, KFA, and increased mrQSM values in U-fiber non-lesions (p = 0.034, p < 0.001, p < 0.001, FDR corrected) were found in pwRRMS. There were differences in DKI-derived metrics and susceptibility values between the upper U-fiber region and the deeper one for U-fiber non-lesion areas of pwRRMS and HCs (p < 0.05), but not for U-fiber lesions in DKI-derived metrics. The DKI-derived metrics and susceptibility values were widely related with cognitive tests and brain atrophy.

Conclusion

RRMS patients show abnormal diffusion kurtosis and susceptibility characteristics in the U-fiber region, and these underlying tissue abnormalities are correlated with cognitive deficits and degeneration.

Clinical relevance statement

The macroscopic and microscopic tissue damages of U-fiber help to identify cognitive impairment and brain atrophy in multiple sclerosis and provide underlying pathophysiological mechanism.

Key Points

• Diffusion kurtosis and susceptibility changes are present in the U-fiber region of multiple sclerosis.
• There are gradients in diffusion kurtosis and susceptibility characteristics in the U-fiber region.
• Tissue damages in the U-fiber region are correlated with cognitive impairment and brain atrophy.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Alotaibi A, Podlasek A, AlTokhis A, Aldhebaib A, Dineen RA, Constantinescu CS (2021) Investigating microstructural changes in white matter in multiple sclerosis: a systematic review and meta-analysis of neurite orientation dispersion and density imaging. Brain Sci 11:1151PubMedPubMedCentral Alotaibi A, Podlasek A, AlTokhis A, Aldhebaib A, Dineen RA, Constantinescu CS (2021) Investigating microstructural changes in white matter in multiple sclerosis: a systematic review and meta-analysis of neurite orientation dispersion and density imaging. Brain Sci 11:1151PubMedPubMedCentral
2.
Zurück zum Zitat Phillips OR, Nuechterlein KH, Asarnow RF et al (2011) Mapping corticocortical structural integrity in schizophrenia and effects of genetic liability. Biol Psychiatry 70:680–689PubMed Phillips OR, Nuechterlein KH, Asarnow RF et al (2011) Mapping corticocortical structural integrity in schizophrenia and effects of genetic liability. Biol Psychiatry 70:680–689PubMed
3.
Zurück zum Zitat Nazeri A, Chakravarty MM, Felsky D et al (2013) Alterations of superficial white matter in schizophrenia and relationship to cognitive performance. Neuropsychopharmacology 38:1954–1962PubMedPubMedCentral Nazeri A, Chakravarty MM, Felsky D et al (2013) Alterations of superficial white matter in schizophrenia and relationship to cognitive performance. Neuropsychopharmacology 38:1954–1962PubMedPubMedCentral
4.
Zurück zum Zitat Guevara M, Guevara P, Román C, Mangin JF (2020) Superficial white matter: a review on the dMRI analysis methods and applications. Neuroimage 212:116673PubMed Guevara M, Guevara P, Román C, Mangin JF (2020) Superficial white matter: a review on the dMRI analysis methods and applications. Neuroimage 212:116673PubMed
5.
Zurück zum Zitat Movahedian Attar F, Kirilina E, Haenelt D et al (2020) Mapping Short Association Fibers in the Early Cortical Visual Processing Stream Using In Vivo Diffusion Tractography. Cereb Cortex 30:4496–4514PubMedPubMedCentral Movahedian Attar F, Kirilina E, Haenelt D et al (2020) Mapping Short Association Fibers in the Early Cortical Visual Processing Stream Using In Vivo Diffusion Tractography. Cereb Cortex 30:4496–4514PubMedPubMedCentral
6.
Zurück zum Zitat Medrano Martorell S, Cuadrado Blázquez M, García Figueredo D, González Ortiz S, Capellades Font J (2012) Imágenes puntiformes hiperintensas en la sustancia blanca: una aproximación diagnóstica [Hyperintense punctiform images in the white matter: a diagnostic approach]. Radiologia 54:321–335PubMed Medrano Martorell S, Cuadrado Blázquez M, García Figueredo D, González Ortiz S, Capellades Font J (2012) Imágenes puntiformes hiperintensas en la sustancia blanca: una aproximación diagnóstica [Hyperintense punctiform images in the white matter: a diagnostic approach]. Radiologia 54:321–335PubMed
7.
Zurück zum Zitat Shukla DK, Keehn B, Smylie DM, Müller RA (2011) Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder. Neuropsychologia 49:1378–1382PubMedPubMedCentral Shukla DK, Keehn B, Smylie DM, Müller RA (2011) Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder. Neuropsychologia 49:1378–1382PubMedPubMedCentral
8.
Zurück zum Zitat Miki Y, Grossman RI, Jk U et al (1998) Isolated U-fiber involvement in MS: preliminary observations. Neurology 50:1301–1306PubMed Miki Y, Grossman RI, Jk U et al (1998) Isolated U-fiber involvement in MS: preliminary observations. Neurology 50:1301–1306PubMed
9.
Zurück zum Zitat Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597–613PubMed Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597–613PubMed
10.
Zurück zum Zitat Wu M, Kumar A, Yang S (2016) Development and aging of superficial white matter myelin from young adulthood to old age: mapping by vertex-based surface statistics (VBSS). Hum Brain Mapp 37:1759–1769PubMedPubMedCentral Wu M, Kumar A, Yang S (2016) Development and aging of superficial white matter myelin from young adulthood to old age: mapping by vertex-based surface statistics (VBSS). Hum Brain Mapp 37:1759–1769PubMedPubMedCentral
11.
Zurück zum Zitat Liewald D, Miller R, Logothetis N, Wagner HJ, Schüz A (2014) Distribution of axon diameters in cortical white matter: an electron-microscopic study on three human brains and a macaque. Biol Cybern 108:541–557PubMedPubMedCentral Liewald D, Miller R, Logothetis N, Wagner HJ, Schüz A (2014) Distribution of axon diameters in cortical white matter: an electron-microscopic study on three human brains and a macaque. Biol Cybern 108:541–557PubMedPubMedCentral
12.
Zurück zum Zitat Phillips OR, Clark KA, Luders E et al (2013) Superficial white matter: effects of age, sex, and hemisphere. Brain Connect 3:146–159PubMedPubMedCentral Phillips OR, Clark KA, Luders E et al (2013) Superficial white matter: effects of age, sex, and hemisphere. Brain Connect 3:146–159PubMedPubMedCentral
13.
Zurück zum Zitat Butt AM, Berry M (2000) Oligodendrocytes and the control of myelination in vivo: new insights from the rat anterior medullary velum. J Neurosci Res 59:477–488PubMed Butt AM, Berry M (2000) Oligodendrocytes and the control of myelination in vivo: new insights from the rat anterior medullary velum. J Neurosci Res 59:477–488PubMed
14.
Zurück zum Zitat Haroutunian V, Katsel P, Roussos P, Davis KL, Altshuler LL, Bartzokis G (2014) Myelination, oligodendrocytes, and serious mental illness. Glia 62:1856–1877PubMed Haroutunian V, Katsel P, Roussos P, Davis KL, Altshuler LL, Bartzokis G (2014) Myelination, oligodendrocytes, and serious mental illness. Glia 62:1856–1877PubMed
15.
Zurück zum Zitat Buyukturkoglu K, Vergara C, Fuentealba V et al (2022) Machine learning to investigate superficial white matter integrity in early multiple sclerosis. J Neuroimaging 32:36–47PubMed Buyukturkoglu K, Vergara C, Fuentealba V et al (2022) Machine learning to investigate superficial white matter integrity in early multiple sclerosis. J Neuroimaging 32:36–47PubMed
16.
Zurück zum Zitat Oishi K, Zilles K, Amunts K et al (2008) Human brain white matter atlas: identification and assignment of common anatomical structures in superficial white matter. Neuroimage 43:447–457PubMed Oishi K, Zilles K, Amunts K et al (2008) Human brain white matter atlas: identification and assignment of common anatomical structures in superficial white matter. Neuroimage 43:447–457PubMed
17.
Zurück zum Zitat Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505PubMed Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505PubMed
18.
Zurück zum Zitat Kirilina E, Helbling S, Morawski M et al (2020) Superficial white matter imaging: Contrast mechanisms and whole-brain in vivo mapping. Sci Adv 6:eaaz9281PubMedPubMedCentralADS Kirilina E, Helbling S, Morawski M et al (2020) Superficial white matter imaging: Contrast mechanisms and whole-brain in vivo mapping. Sci Adv 6:eaaz9281PubMedPubMedCentralADS
19.
Zurück zum Zitat Stojanovski S, Nazeri A, Lepage C, Ameis S, Voineskos AN, Wheeler AL (2019) Microstructural abnormalities in deep and superficial white matter in youths with mild traumatic brain injury. Neuroimage Clin 24:102102PubMedPubMedCentral Stojanovski S, Nazeri A, Lepage C, Ameis S, Voineskos AN, Wheeler AL (2019) Microstructural abnormalities in deep and superficial white matter in youths with mild traumatic brain injury. Neuroimage Clin 24:102102PubMedPubMedCentral
20.
Zurück zum Zitat Bigham B, Zamanpour SA, Zemorshidi F, Boroumand F, Zare H (2020) Identification of superficial white matter abnormalities in Alzheimer’s disease and mild cognitive impairment using diffusion tensor imaging. J Alzheimers Dis Rep 4:49–59PubMedPubMedCentral Bigham B, Zamanpour SA, Zemorshidi F, Boroumand F, Zare H (2020) Identification of superficial white matter abnormalities in Alzheimer’s disease and mild cognitive impairment using diffusion tensor imaging. J Alzheimers Dis Rep 4:49–59PubMedPubMedCentral
21.
Zurück zum Zitat Rocca MA, Amato MP, De Stefano N et al (2015) Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol 14:302–317PubMed Rocca MA, Amato MP, De Stefano N et al (2015) Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol 14:302–317PubMed
22.
Zurück zum Zitat Benedict RHB, Amato MP, DeLuca J, Geurts JJG (2020) Cognitive impairment in multiple sclerosis: clinical management, MRI, and therapeutic avenues. Lancet Neurol 19:860–871PubMedPubMedCentral Benedict RHB, Amato MP, DeLuca J, Geurts JJG (2020) Cognitive impairment in multiple sclerosis: clinical management, MRI, and therapeutic avenues. Lancet Neurol 19:860–871PubMedPubMedCentral
23.
Zurück zum Zitat Jandric D, Lipp I, Paling D et al (2021) Mechanisms of network changes in cognitive impairment in multiple sclerosis. Neurology 97:e1886–e1897PubMedPubMedCentral Jandric D, Lipp I, Paling D et al (2021) Mechanisms of network changes in cognitive impairment in multiple sclerosis. Neurology 97:e1886–e1897PubMedPubMedCentral
24.
Zurück zum Zitat Li HQ, Yin B, Quan C et al (2018) Evaluation of patients with relapsing-remitting multiple sclerosis using tract-based spatial statistics analysis: diffusion kurtosis imaging. BMC Neurol 18:108PubMedPubMedCentral Li HQ, Yin B, Quan C et al (2018) Evaluation of patients with relapsing-remitting multiple sclerosis using tract-based spatial statistics analysis: diffusion kurtosis imaging. BMC Neurol 18:108PubMedPubMedCentral
25.
Zurück zum Zitat van der Weijden CW, van der Hoorn A, Potze JH et al (2022) Diffusion-derived parameters in lesions, peri-lesion, and normal-appearing white matter in multiple sclerosis using tensor, kurtosis, and fixel-based analysis. J Cereb Blood Flow Metab 42:2095–2106PubMedPubMedCentral van der Weijden CW, van der Hoorn A, Potze JH et al (2022) Diffusion-derived parameters in lesions, peri-lesion, and normal-appearing white matter in multiple sclerosis using tensor, kurtosis, and fixel-based analysis. J Cereb Blood Flow Metab 42:2095–2106PubMedPubMedCentral
26.
Zurück zum Zitat Rahmanzadeh R, Galbusera R, Lu PJ et al (2022) A new advanced mri biomarker for remyelinated lesions in multiple sclerosis. Ann Neurol 92:486–502PubMedPubMedCentral Rahmanzadeh R, Galbusera R, Lu PJ et al (2022) A new advanced mri biomarker for remyelinated lesions in multiple sclerosis. Ann Neurol 92:486–502PubMedPubMedCentral
27.
Zurück zum Zitat Schweser F, Hagemeier J, Dwyer MG et al (2021) Decreasing brain iron in multiple sclerosis: the difference between concentration and content in iron MRI. Hum Brain Mapp 42:1463–1474PubMed Schweser F, Hagemeier J, Dwyer MG et al (2021) Decreasing brain iron in multiple sclerosis: the difference between concentration and content in iron MRI. Hum Brain Mapp 42:1463–1474PubMed
28.
Zurück zum Zitat Thompson AJ, Banwell BL, Barkhof F et al (2018) Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol 17:162–173PubMed Thompson AJ, Banwell BL, Barkhof F et al (2018) Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol 17:162–173PubMed
29.
Zurück zum Zitat Chan KS, Marques JP (2021) SEPIA-Susceptibility mapping pipeline tool for phase images. Neuroimage 227:117611PubMed Chan KS, Marques JP (2021) SEPIA-Susceptibility mapping pipeline tool for phase images. Neuroimage 227:117611PubMed
30.
Zurück zum Zitat Haacke EM, Ayaz M, Khan A et al (2007) Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain. J Magn Reson Imaging 26:256–264PubMed Haacke EM, Ayaz M, Khan A et al (2007) Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain. J Magn Reson Imaging 26:256–264PubMed
31.
Zurück zum Zitat Chen W, Zhang Y, Mu K et al (2017) Quantifying the susceptibility variation of normal-appearing white matter in multiple sclerosis by quantitative susceptibility mapping. AJR Am J Roentgenol 209:889–894PubMed Chen W, Zhang Y, Mu K et al (2017) Quantifying the susceptibility variation of normal-appearing white matter in multiple sclerosis by quantitative susceptibility mapping. AJR Am J Roentgenol 209:889–894PubMed
32.
Zurück zum Zitat Lu P, Yuan T, Liu X, Tian G, Zhang J, Sha Y (2020) Role of diffusional kurtosis imaging in differentiating neuromyelitis optica-related and multiple sclerosis-related acute optic neuritis: comparison with diffusion-weighted imaging. J Comput Assist Tomogr 44:47–52PubMed Lu P, Yuan T, Liu X, Tian G, Zhang J, Sha Y (2020) Role of diffusional kurtosis imaging in differentiating neuromyelitis optica-related and multiple sclerosis-related acute optic neuritis: comparison with diffusion-weighted imaging. J Comput Assist Tomogr 44:47–52PubMed
33.
Zurück zum Zitat Coutu JP, Chen JJ, Rosas HD, Salat DH (2014) Non-Gaussian water diffusion in aging white matter. Neurobiol Aging 35:1412–1421PubMed Coutu JP, Chen JJ, Rosas HD, Salat DH (2014) Non-Gaussian water diffusion in aging white matter. Neurobiol Aging 35:1412–1421PubMed
34.
Zurück zum Zitat Bian W, Tranvinh E, Tourdias T et al (2016) In vivo 7T MR quantitative susceptibility mapping reveals opposite susceptibility contrast between cortical and white matter lesions in multiple sclerosis. AJNR Am J Neuroradiol 37:1808–1815PubMedPubMedCentral Bian W, Tranvinh E, Tourdias T et al (2016) In vivo 7T MR quantitative susceptibility mapping reveals opposite susceptibility contrast between cortical and white matter lesions in multiple sclerosis. AJNR Am J Neuroradiol 37:1808–1815PubMedPubMedCentral
35.
Zurück zum Zitat Wisnieff C, Ramanan S, Olesik J, Gauthier S, Wang Y, Pitt D (2015) Quantitative susceptibility mapping (QSM) of white matter multiple sclerosis lesions: Interpreting positive susceptibility and the presence of iron. Magn Reson Med 74:564–570PubMed Wisnieff C, Ramanan S, Olesik J, Gauthier S, Wang Y, Pitt D (2015) Quantitative susceptibility mapping (QSM) of white matter multiple sclerosis lesions: Interpreting positive susceptibility and the presence of iron. Magn Reson Med 74:564–570PubMed
36.
Zurück zum Zitat Sheng H, Zhao B, Ge Y (2019) Blood perfusion and cellular microstructural changes associated with iron deposition in multiple sclerosis lesions. Front Neurol 10:747PubMedPubMedCentral Sheng H, Zhao B, Ge Y (2019) Blood perfusion and cellular microstructural changes associated with iron deposition in multiple sclerosis lesions. Front Neurol 10:747PubMedPubMedCentral
37.
Zurück zum Zitat Zhang Y, Gauthier SA, Gupta A et al (2016) Quantitative susceptibility mapping and R2* measured changes during white matter lesion development in multiple sclerosis: myelin breakdown, myelin debris degradation and removal, and iron accumulation. AJNR Am J Neuroradiol 37:1629–1635PubMedPubMedCentral Zhang Y, Gauthier SA, Gupta A et al (2016) Quantitative susceptibility mapping and R2* measured changes during white matter lesion development in multiple sclerosis: myelin breakdown, myelin debris degradation and removal, and iron accumulation. AJNR Am J Neuroradiol 37:1629–1635PubMedPubMedCentral
38.
Zurück zum Zitat Aljishi RH, Almatrafi RJ, Alzayer ZA, Alkhamis BA, Yaseen EE, Alkhotani AM (2021) Prevalence of anxiety and depression in patients with multiple sclerosis in Saudi Arabia: a cross-sectional study. Cureus 13:e20792PubMedPubMedCentral Aljishi RH, Almatrafi RJ, Alzayer ZA, Alkhamis BA, Yaseen EE, Alkhotani AM (2021) Prevalence of anxiety and depression in patients with multiple sclerosis in Saudi Arabia: a cross-sectional study. Cureus 13:e20792PubMedPubMedCentral
39.
Zurück zum Zitat Broch L, Flemmen HØ, Simonsen CS et al (2022) Fatigue in multiple sclerosis is associated with socioeconomic factors. Mult Scler Relat Disord 64:103955PubMed Broch L, Flemmen HØ, Simonsen CS et al (2022) Fatigue in multiple sclerosis is associated with socioeconomic factors. Mult Scler Relat Disord 64:103955PubMed
40.
Zurück zum Zitat Moore H, Nair KPS, Baster K, Middleton R, Paling D, Sharrack B (2022) Fatigue in multiple sclerosis: a UK MS-register based study. Mult Scler Relat Disord 64:103954PubMed Moore H, Nair KPS, Baster K, Middleton R, Paling D, Sharrack B (2022) Fatigue in multiple sclerosis: a UK MS-register based study. Mult Scler Relat Disord 64:103954PubMed
41.
Zurück zum Zitat Phillips OR, Joshi SH, Narr KL et al (2018) Superficial white matter damage in anti-NMDA receptor encephalitis. J Neurol Neurosurg Psychiatry 89:518–525PubMed Phillips OR, Joshi SH, Narr KL et al (2018) Superficial white matter damage in anti-NMDA receptor encephalitis. J Neurol Neurosurg Psychiatry 89:518–525PubMed
42.
Zurück zum Zitat Migliore S, Ghazaryan A, Simonelli I et al (2017) Cognitive impairment in relapsing-remitting multiple sclerosis patients with very mild clinical disability. Behav Neurol 2017:7404289PubMedPubMedCentral Migliore S, Ghazaryan A, Simonelli I et al (2017) Cognitive impairment in relapsing-remitting multiple sclerosis patients with very mild clinical disability. Behav Neurol 2017:7404289PubMedPubMedCentral
43.
Zurück zum Zitat Haider L, Prados F, Chung K et al (2021) Cortical involvement determines impairment 30 years after a clinically isolated syndrome. Brain 144:1384–1395PubMedPubMedCentral Haider L, Prados F, Chung K et al (2021) Cortical involvement determines impairment 30 years after a clinically isolated syndrome. Brain 144:1384–1395PubMedPubMedCentral
44.
Zurück zum Zitat Fujimori J, Fujihara K, Wattjes M, Nakashima I (2021) Patterns of cortical grey matter thickness reduction in multiple sclerosis. Brain Behav 11:e02050PubMedPubMedCentral Fujimori J, Fujihara K, Wattjes M, Nakashima I (2021) Patterns of cortical grey matter thickness reduction in multiple sclerosis. Brain Behav 11:e02050PubMedPubMedCentral
45.
Zurück zum Zitat Narayana PA, Govindarajan KA, Goel P et al (2012) Regional cortical thickness in relapsing remitting multiple sclerosis: a multi-center study. Neuroimage Clin 2:120–131PubMedPubMedCentral Narayana PA, Govindarajan KA, Goel P et al (2012) Regional cortical thickness in relapsing remitting multiple sclerosis: a multi-center study. Neuroimage Clin 2:120–131PubMedPubMedCentral
46.
Zurück zum Zitat Tsagkas C, Chakravarty MM, Gaetano L et al (2020) Longitudinal patterns of cortical thinning in multiple sclerosis. Hum Brain Mapp 41:2198–2215PubMedPubMedCentral Tsagkas C, Chakravarty MM, Gaetano L et al (2020) Longitudinal patterns of cortical thinning in multiple sclerosis. Hum Brain Mapp 41:2198–2215PubMedPubMedCentral
47.
Zurück zum Zitat Wang C, Barnett MH, Yiannikas C et al (2019) Lesion activity and chronic demyelination are the major determinants of brain atrophy in MS. Neurol Neuroimmunol Neuroinflamm 6:e593PubMedPubMedCentral Wang C, Barnett MH, Yiannikas C et al (2019) Lesion activity and chronic demyelination are the major determinants of brain atrophy in MS. Neurol Neuroimmunol Neuroinflamm 6:e593PubMedPubMedCentral
48.
Zurück zum Zitat Hidalgo de la Cruz M, Valsasina P, Meani A et al (2021) Differential association of cortical, subcortical and spinal cord damage with multiple sclerosis disability milestones: A multiparametric MRI study. Mult Scler 28:406–417PubMed Hidalgo de la Cruz M, Valsasina P, Meani A et al (2021) Differential association of cortical, subcortical and spinal cord damage with multiple sclerosis disability milestones: A multiparametric MRI study. Mult Scler 28:406–417PubMed
49.
Zurück zum Zitat Bergsland N, Horakova D, Dwyer MG et al (2018) Gray matter atrophy patterns in multiple sclerosis: A 10-year source-based morphometry study. Neuroimage Clin 17:444–451PubMed Bergsland N, Horakova D, Dwyer MG et al (2018) Gray matter atrophy patterns in multiple sclerosis: A 10-year source-based morphometry study. Neuroimage Clin 17:444–451PubMed
50.
Zurück zum Zitat Tarasiuk J, Kapica-Topczewska K, Czarnowska A, Chorąży M, Kochanowicz J, Kułakowska A (2021) Co-occurrence of fatigue and depression in people with multiple sclerosis: a mini-review. Front Neurol 12:817256PubMed Tarasiuk J, Kapica-Topczewska K, Czarnowska A, Chorąży M, Kochanowicz J, Kułakowska A (2021) Co-occurrence of fatigue and depression in people with multiple sclerosis: a mini-review. Front Neurol 12:817256PubMed
Metadaten
Titel
U-fiber diffusion kurtosis and susceptibility characteristics in relapsing–remitting multiple sclerosis may be related to cognitive deficits and neurodegeneration
verfasst von
Dan Luo
Yuling Peng
Qiyuan Zhu
Qiao Zheng
Qi Luo
Yongliang Han
Xiaoya Chen
Yongmei Li
Publikationsdatum
02.09.2023
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 3/2024
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-023-10114-3

Weitere Artikel der Ausgabe 3/2024

European Radiology 3/2024 Zur Ausgabe

Mammakarzinom: Brustdichte beeinflusst rezidivfreies Überleben

26.05.2024 Mammakarzinom Nachrichten

Frauen, die zum Zeitpunkt der Brustkrebsdiagnose eine hohe mammografische Brustdichte aufweisen, haben ein erhöhtes Risiko für ein baldiges Rezidiv, legen neue Daten nahe.

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

17.05.2024 Klinik aktuell Nachrichten

Sie sei „ethisch geboten“, meint Gesundheitsminister Karl Lauterbach: mehr Transparenz über die Qualität von Klinikbehandlungen. Um sie abzubilden, lässt er gegen den Widerstand vieler Länder einen virtuellen Klinik-Atlas freischalten.

Klinikreform soll zehntausende Menschenleben retten

15.05.2024 Klinik aktuell Nachrichten

Gesundheitsminister Lauterbach hat die vom Bundeskabinett beschlossene Klinikreform verteidigt. Kritik an den Plänen kommt vom Marburger Bund. Und in den Ländern wird über den Gang zum Vermittlungsausschuss spekuliert.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.