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Published in: European Radiology 1/2018

01-01-2018 | Magnetic Resonance

Different patterns of longitudinal brain and spinal cord changes and their associations with disability progression in NMO and MS

Authors: Yaou Liu, Yunyun Duan, Jing Huang, Zhuoqiong Ren, Zheng Liu, Huiqing Dong, Florian Weiler, Horst K. Hahn, Fu-Dong Shi, Helmut Butzkueven, Frederik Barkhof, Kuncheng Li

Published in: European Radiology | Issue 1/2018

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Abstract

Objective

To investigate the longitudinal spinal cord and brain changes in neuromyelitis optica (NMO) and multiple sclerosis (MS) and their associations with disability progression.

Patients and methods

We recruited 28 NMO, 22 MS, and 20 healthy controls (HC), who underwent both spinal cord and brain MRI at baseline. Twenty-five NMO and 20 MS completed 1-year follow-up. Baseline spinal cord and brain lesion loads, mean upper cervical cord area (MUCCA), brain, and thalamus volume and their changes during a 1-year follow-up were measured and compared between groups. All the measurements were also compared between progressive and non-progressive groups in NMO and MS.

Results

MUCCA decreased significantly during the 1-year follow-up in NMO not in MS. Percentage brain volume changes (PBVC) and thalamus volume changes in MS were significantly higher than NMO. MUCCA changes were significantly different between progressive and non-progressive groups in NMO, while baseline brain lesion volume and PBVC were associated with disability progression in MS. MUCCA changes during 1-year follow-up showed association with clinical disability in NMO.

Conclusion

Spinal cord atrophy changes were associated with disability progression in NMO, while baseline brain lesion load and whole brain atrophy changes were related to disability progression in MS.

Key Points

• Spinal cord atrophy progression was observed in NMO.
• Spinal cord atrophy changes were associated with disability progression in NMO.
• Brain lesion and atrophy were related to disability progression in MS.
Literature
1.
go back to reference Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG (2007) The spectrum of neuromyelitis optica. Lancet Neurol 6:805–815CrossRefPubMed Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG (2007) The spectrum of neuromyelitis optica. Lancet Neurol 6:805–815CrossRefPubMed
2.
go back to reference Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66:1485–1489CrossRefPubMed Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66:1485–1489CrossRefPubMed
3.
go back to reference Tackley G, Kuker W, Palace J (2014) Magnetic resonance imaging in neuromyelitis optica. Mult Scler Tackley G, Kuker W, Palace J (2014) Magnetic resonance imaging in neuromyelitis optica. Mult Scler
4.
go back to reference Fujihara K (2011) Neuromyelitis optica and astrocytic damage in its pathogenesis. J Neurol Sci 306:183–187CrossRefPubMed Fujihara K (2011) Neuromyelitis optica and astrocytic damage in its pathogenesis. J Neurol Sci 306:183–187CrossRefPubMed
5.
go back to reference Lucchinetti CF, Guo Y, Popescu BF, Fujihara K, Itoyama Y, Misu T (2014) The pathology of an autoimmune astrocytopathy: lessons learned from neuromyelitis optica. Brain Pathol 24:83–97CrossRefPubMedPubMedCentral Lucchinetti CF, Guo Y, Popescu BF, Fujihara K, Itoyama Y, Misu T (2014) The pathology of an autoimmune astrocytopathy: lessons learned from neuromyelitis optica. Brain Pathol 24:83–97CrossRefPubMedPubMedCentral
6.
go back to reference Lennon VA, Wingerchuk DM, Kryzer TJ et al (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364:2106–2112CrossRefPubMed Lennon VA, Wingerchuk DM, Kryzer TJ et al (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364:2106–2112CrossRefPubMed
7.
go back to reference Palace J, Leite MI, Nairne A, Vincent A (2010) Interferon Beta treatment in neuromyelitis optica: increase in relapses and aquaporin 4 antibody titers. Arch Neurol 67:1016–1017CrossRefPubMed Palace J, Leite MI, Nairne A, Vincent A (2010) Interferon Beta treatment in neuromyelitis optica: increase in relapses and aquaporin 4 antibody titers. Arch Neurol 67:1016–1017CrossRefPubMed
8.
go back to reference Shimizu J, Hatanaka Y, Hasegawa M et al (2010) IFNbeta-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 75:1423–1427CrossRefPubMed Shimizu J, Hatanaka Y, Hasegawa M et al (2010) IFNbeta-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 75:1423–1427CrossRefPubMed
9.
go back to reference Min JH, Kim BJ, Lee KH (2011) Development of extensive brain lesions following fingolimod (FTY720) treatment in a patient with neuromyelitis optica spectrum disorder. Mult Scler 18:113–115CrossRefPubMed Min JH, Kim BJ, Lee KH (2011) Development of extensive brain lesions following fingolimod (FTY720) treatment in a patient with neuromyelitis optica spectrum disorder. Mult Scler 18:113–115CrossRefPubMed
10.
go back to reference Duan Y, Liu Y, Liang P et al (2012) Comparison of grey matter atrophy between patients with neuromyelitis optica and multiple sclerosis: a voxel-based morphometry study. Eur J Radiol 81:e110–e114CrossRefPubMed Duan Y, Liu Y, Liang P et al (2012) Comparison of grey matter atrophy between patients with neuromyelitis optica and multiple sclerosis: a voxel-based morphometry study. Eur J Radiol 81:e110–e114CrossRefPubMed
11.
go back to reference Calabrese M, Oh MS, Favaretto A et al (2012) No MRI evidence of cortical lesions in neuromyelitis optica. Neurology 79:1671–1676CrossRefPubMed Calabrese M, Oh MS, Favaretto A et al (2012) No MRI evidence of cortical lesions in neuromyelitis optica. Neurology 79:1671–1676CrossRefPubMed
12.
go back to reference Blanc F, Noblet V, Jung B et al (2013) White matter atrophy and cognitive dysfunctions in neuromyelitis optica. PLoS One 7:e33878CrossRef Blanc F, Noblet V, Jung B et al (2013) White matter atrophy and cognitive dysfunctions in neuromyelitis optica. PLoS One 7:e33878CrossRef
13.
go back to reference Liu Y, Wang J, Daams M et al (2015) Differential patterns of spinal cord and brain atrophy in NMO and MS. Neurology 84:1465–1472CrossRefPubMed Liu Y, Wang J, Daams M et al (2015) Differential patterns of spinal cord and brain atrophy in NMO and MS. Neurology 84:1465–1472CrossRefPubMed
15.
go back to reference Brownlee WJ, Altmann DR, Alves Da Mota P et al. (2016) Association of asymptomatic spinal cord lesions and atrophy with disability 5 years after a clinically isolated syndrome. Mult Scler Brownlee WJ, Altmann DR, Alves Da Mota P et al. (2016) Association of asymptomatic spinal cord lesions and atrophy with disability 5 years after a clinically isolated syndrome. Mult Scler
16.
go back to reference Lukas C, Knol DL, Sombekke MH et al (2015) Cervical spinal cord volume loss is related to clinical disability progression in multiple sclerosis. J Neurol Neurosurg Psychiatry 86:410–418CrossRefPubMed Lukas C, Knol DL, Sombekke MH et al (2015) Cervical spinal cord volume loss is related to clinical disability progression in multiple sclerosis. J Neurol Neurosurg Psychiatry 86:410–418CrossRefPubMed
17.
go back to reference Schoonheim MM, Hulst HE, Brandt RB et al (2015) Thalamus structure and function determine severity of cognitive impairment in multiple sclerosis. Neurology 84:776–783CrossRefPubMed Schoonheim MM, Hulst HE, Brandt RB et al (2015) Thalamus structure and function determine severity of cognitive impairment in multiple sclerosis. Neurology 84:776–783CrossRefPubMed
18.
go back to reference Daams M, Weiler F, Steenwijk MD et al. (2014) Mean upper cervical cord area (MUCCA) measurement in long-standing multiple sclerosis: Relation to brain findings and clinical disability. Mult Scler Daams M, Weiler F, Steenwijk MD et al. (2014) Mean upper cervical cord area (MUCCA) measurement in long-standing multiple sclerosis: Relation to brain findings and clinical disability. Mult Scler
19.
go back to reference Polman CH, Reingold SC, Edan G et al (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol 58:840–846CrossRefPubMed Polman CH, Reingold SC, Edan G et al (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol 58:840–846CrossRefPubMed
20.
go back to reference Takahashi T, Fujihara K, Nakashima I et al (2006) Establishment of a new sensitive assay for anti-human aquaporin-4 antibody in neuromyelitis optica. Tohoku J Exp Med 210:307–313CrossRefPubMed Takahashi T, Fujihara K, Nakashima I et al (2006) Establishment of a new sensitive assay for anti-human aquaporin-4 antibody in neuromyelitis optica. Tohoku J Exp Med 210:307–313CrossRefPubMed
21.
go back to reference Agosta F, Absinta M, Sormani MP et al (2007) In vivo assessment of cervical cord damage in MS patients: a longitudinal diffusion tensor MRI study. Brain 130:2211–2219CrossRefPubMed Agosta F, Absinta M, Sormani MP et al (2007) In vivo assessment of cervical cord damage in MS patients: a longitudinal diffusion tensor MRI study. Brain 130:2211–2219CrossRefPubMed
22.
go back to reference Miller DH, Barkhof F, Berry I, Kappos L, Scotti G, Thompson AJ (1991) Magnetic resonance imaging in monitoring the treatment of multiple sclerosis: concerted action guidelines. J Neurol Neurosurg Psychiatry 54:683–688CrossRefPubMedPubMedCentral Miller DH, Barkhof F, Berry I, Kappos L, Scotti G, Thompson AJ (1991) Magnetic resonance imaging in monitoring the treatment of multiple sclerosis: concerted action guidelines. J Neurol Neurosurg Psychiatry 54:683–688CrossRefPubMedPubMedCentral
23.
go back to reference Smith SM, Zhang Y, Jenkinson M et al (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17:479–489CrossRefPubMed Smith SM, Zhang Y, Jenkinson M et al (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17:479–489CrossRefPubMed
24.
go back to reference Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56:907–922CrossRefPubMedPubMedCentral Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56:907–922CrossRefPubMedPubMedCentral
25.
go back to reference Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219CrossRefPubMed Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219CrossRefPubMed
26.
go back to reference Vrenken H, Vos EK, van der Flier WM et al (2014) Validation of the automated method VIENA: an accurate, precise, and robust measure of ventricular enlargement. Hum Brain Mapp 35:1101–1110CrossRefPubMed Vrenken H, Vos EK, van der Flier WM et al (2014) Validation of the automated method VIENA: an accurate, precise, and robust measure of ventricular enlargement. Hum Brain Mapp 35:1101–1110CrossRefPubMed
27.
go back to reference Lukas C, Hahn HK, Bellenberg B et al (2004) Sensitivity and reproducibility of a new fast 3D segmentation technique for clinical MR-based brain volumetry in multiple sclerosis. Neuroradiology 46:906–915CrossRefPubMed Lukas C, Hahn HK, Bellenberg B et al (2004) Sensitivity and reproducibility of a new fast 3D segmentation technique for clinical MR-based brain volumetry in multiple sclerosis. Neuroradiology 46:906–915CrossRefPubMed
28.
go back to reference Lukas C, Sombekke MH, Bellenberg B et al (2013) Relevance of spinal cord abnormalities to clinical disability in multiple sclerosis: MR imaging findings in a large cohort of patients. Radiology 269:542–552CrossRefPubMed Lukas C, Sombekke MH, Bellenberg B et al (2013) Relevance of spinal cord abnormalities to clinical disability in multiple sclerosis: MR imaging findings in a large cohort of patients. Radiology 269:542–552CrossRefPubMed
29.
go back to reference Matthews L, Kolind S, Brazier A et al (2015) Imaging surrogates of disease activity in neuromyelitis optica allow distinction from multiple sclerosis. PLoS One 10:e0137715CrossRefPubMedPubMedCentral Matthews L, Kolind S, Brazier A et al (2015) Imaging surrogates of disease activity in neuromyelitis optica allow distinction from multiple sclerosis. PLoS One 10:e0137715CrossRefPubMedPubMedCentral
30.
go back to reference Saji E, Arakawa M, Yanagawa K et al (2013) Cognitive impairment and cortical degeneration in neuromyelitis optica. Ann Neurol 73:65–76CrossRefPubMed Saji E, Arakawa M, Yanagawa K et al (2013) Cognitive impairment and cortical degeneration in neuromyelitis optica. Ann Neurol 73:65–76CrossRefPubMed
31.
go back to reference Rocca MA, Mesaros S, Pagani E, Sormani MP, Comi G, Filippi M (2010) Thalamic damage and long-term progression of disability in multiple sclerosis. Radiology 257:463–469CrossRefPubMed Rocca MA, Mesaros S, Pagani E, Sormani MP, Comi G, Filippi M (2010) Thalamic damage and long-term progression of disability in multiple sclerosis. Radiology 257:463–469CrossRefPubMed
32.
go back to reference Ishikawa M, Matsumoto M, Fujimura Y, Chiba K, Toyama Y (2003) Changes of cervical spinal cord and cervical spinal canal with age in asymptomatic subjects. Spinal Cord 41:159–163CrossRefPubMed Ishikawa M, Matsumoto M, Fujimura Y, Chiba K, Toyama Y (2003) Changes of cervical spinal cord and cervical spinal canal with age in asymptomatic subjects. Spinal Cord 41:159–163CrossRefPubMed
33.
go back to reference Ciccarelli O, Wheeler-Kingshott CA, McLean MA et al (2007) Spinal cord spectroscopy and diffusion-based tractography to assess acute disability in multiple sclerosis. Brain 130:2220–2231CrossRefPubMed Ciccarelli O, Wheeler-Kingshott CA, McLean MA et al (2007) Spinal cord spectroscopy and diffusion-based tractography to assess acute disability in multiple sclerosis. Brain 130:2220–2231CrossRefPubMed
34.
go back to reference Valsasina P, Rocca MA, Absinta M et al (2012) Cervical cord FMRI abnormalities differ between the progressive forms of multiple sclerosis. Hum Brain Mapp 33:2072–2080CrossRefPubMed Valsasina P, Rocca MA, Absinta M et al (2012) Cervical cord FMRI abnormalities differ between the progressive forms of multiple sclerosis. Hum Brain Mapp 33:2072–2080CrossRefPubMed
35.
go back to reference Naismith RT, Xu J, Tutlam NT et al (2012) Diffusion tensor imaging in acute optic neuropathies: predictor of clinical outcomes. Arch Neurol 69:65–71CrossRefPubMed Naismith RT, Xu J, Tutlam NT et al (2012) Diffusion tensor imaging in acute optic neuropathies: predictor of clinical outcomes. Arch Neurol 69:65–71CrossRefPubMed
Metadata
Title
Different patterns of longitudinal brain and spinal cord changes and their associations with disability progression in NMO and MS
Authors
Yaou Liu
Yunyun Duan
Jing Huang
Zhuoqiong Ren
Zheng Liu
Huiqing Dong
Florian Weiler
Horst K. Hahn
Fu-Dong Shi
Helmut Butzkueven
Frederik Barkhof
Kuncheng Li
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 1/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-4921-x

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