Progression of regional grey matter atrophy in multiple sclerosis
See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article. Grey matter atrophy in multiple sclerosis affects certain areas preferentially. Eshaghi et al. use a data-driven computational model to predict the order in which regions atrophy, and use this sequence t...
Uloženo v:
| Vydáno v: | Brain (London, England : 1878) Ročník 141; číslo 6; s. 1665 - 1677 |
|---|---|
| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
England
Oxford University Press
01.06.2018
|
| Témata: | |
| ISSN: | 0006-8950, 1460-2156, 1460-2156 |
| On-line přístup: | Získat plný text |
| Tagy: |
Přidat tag
Žádné tagy, Buďte první, kdo vytvoří štítek k tomuto záznamu!
|
| Abstract | See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.
Grey matter atrophy in multiple sclerosis affects certain areas preferentially. Eshaghi et al. use a data-driven computational model to predict the order in which regions atrophy, and use this sequence to stage patients. Atrophy begins in deep grey matter nuclei and posterior cortical regions, before spreading to other cortical areas.
Abstract
See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.
Grey matter atrophy is present from the earliest stages of multiple sclerosis, but its temporal ordering is poorly understood. We aimed to determine the sequence in which grey matter regions become atrophic in multiple sclerosis and its association with disability accumulation. In this longitudinal study, we included 1417 subjects: 253 with clinically isolated syndrome, 708 with relapsing-remitting multiple sclerosis, 128 with secondary-progressive multiple sclerosis, 125 with primary-progressive multiple sclerosis, and 203 healthy control subjects from seven European centres. Subjects underwent repeated MRI (total number of scans 3604); the mean follow-up for patients was 2.41 years (standard deviation = 1.97). Disability was scored using the Expanded Disability Status Scale. We calculated the volume of brain grey matter regions and brainstem using an unbiased within-subject template and used an established data-driven event-based model to determine the sequence of occurrence of atrophy and its uncertainty. We assigned each subject to a specific event-based model stage, based on the number of their atrophic regions. Linear mixed-effects models were used to explore associations between the rate of increase in event-based model stages, and T2 lesion load, disease-modifying treatments, comorbidity, disease duration and disability accumulation. The first regions to become atrophic in patients with clinically isolated syndrome and relapse-onset multiple sclerosis were the posterior cingulate cortex and precuneus, followed by the middle cingulate cortex, brainstem and thalamus. A similar sequence of atrophy was detected in primary-progressive multiple sclerosis with the involvement of the thalamus, cuneus, precuneus, and pallidum, followed by the brainstem and posterior cingulate cortex. The cerebellum, caudate and putamen showed early atrophy in relapse-onset multiple sclerosis and late atrophy in primary-progressive multiple sclerosis. Patients with secondary-progressive multiple sclerosis showed the highest event-based model stage (the highest number of atrophic regions, P < 0.001) at the study entry. All multiple sclerosis phenotypes, but clinically isolated syndrome, showed a faster rate of increase in the event-based model stage than healthy controls. T2 lesion load and disease duration in all patients were associated with increased event-based model stage, but no effects of disease-modifying treatments and comorbidity on event-based model stage were observed. The annualized rate of event-based model stage was associated with the disability accumulation in relapsing-remitting multiple sclerosis, independent of disease duration (P < 0.0001). The data-driven staging of atrophy progression in a large multiple sclerosis sample demonstrates that grey matter atrophy spreads to involve more regions over time. The sequence in which regions become atrophic is reasonably consistent across multiple sclerosis phenotypes. The spread of atrophy was associated with disease duration and with disability accumulation over time in relapsing-remitting multiple sclerosis. |
|---|---|
| AbstractList | See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.Grey matter atrophy is present from the earliest stages of multiple sclerosis, but its temporal ordering is poorly understood. We aimed to determine the sequence in which grey matter regions become atrophic in multiple sclerosis and its association with disability accumulation. In this longitudinal study, we included 1417 subjects: 253 with clinically isolated syndrome, 708 with relapsing-remitting multiple sclerosis, 128 with secondary-progressive multiple sclerosis, 125 with primary-progressive multiple sclerosis, and 203 healthy control subjects from seven European centres. Subjects underwent repeated MRI (total number of scans 3604); the mean follow-up for patients was 2.41 years (standard deviation = 1.97). Disability was scored using the Expanded Disability Status Scale. We calculated the volume of brain grey matter regions and brainstem using an unbiased within-subject template and used an established data-driven event-based model to determine the sequence of occurrence of atrophy and its uncertainty. We assigned each subject to a specific event-based model stage, based on the number of their atrophic regions. Linear mixed-effects models were used to explore associations between the rate of increase in event-based model stages, and T2 lesion load, disease-modifying treatments, comorbidity, disease duration and disability accumulation. The first regions to become atrophic in patients with clinically isolated syndrome and relapse-onset multiple sclerosis were the posterior cingulate cortex and precuneus, followed by the middle cingulate cortex, brainstem and thalamus. A similar sequence of atrophy was detected in primary-progressive multiple sclerosis with the involvement of the thalamus, cuneus, precuneus, and pallidum, followed by the brainstem and posterior cingulate cortex. The cerebellum, caudate and putamen showed early atrophy in relapse-onset multiple sclerosis and late atrophy in primary-progressive multiple sclerosis. Patients with secondary-progressive multiple sclerosis showed the highest event-based model stage (the highest number of atrophic regions, P < 0.001) at the study entry. All multiple sclerosis phenotypes, but clinically isolated syndrome, showed a faster rate of increase in the event-based model stage than healthy controls. T2 lesion load and disease duration in all patients were associated with increased event-based model stage, but no effects of disease-modifying treatments and comorbidity on event-based model stage were observed. The annualized rate of event-based model stage was associated with the disability accumulation in relapsing-remitting multiple sclerosis, independent of disease duration (P < 0.0001). The data-driven staging of atrophy progression in a large multiple sclerosis sample demonstrates that grey matter atrophy spreads to involve more regions over time. The sequence in which regions become atrophic is reasonably consistent across multiple sclerosis phenotypes. The spread of atrophy was associated with disease duration and with disability accumulation over time in relapsing-remitting multiple sclerosis.See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.Grey matter atrophy is present from the earliest stages of multiple sclerosis, but its temporal ordering is poorly understood. We aimed to determine the sequence in which grey matter regions become atrophic in multiple sclerosis and its association with disability accumulation. In this longitudinal study, we included 1417 subjects: 253 with clinically isolated syndrome, 708 with relapsing-remitting multiple sclerosis, 128 with secondary-progressive multiple sclerosis, 125 with primary-progressive multiple sclerosis, and 203 healthy control subjects from seven European centres. Subjects underwent repeated MRI (total number of scans 3604); the mean follow-up for patients was 2.41 years (standard deviation = 1.97). Disability was scored using the Expanded Disability Status Scale. We calculated the volume of brain grey matter regions and brainstem using an unbiased within-subject template and used an established data-driven event-based model to determine the sequence of occurrence of atrophy and its uncertainty. We assigned each subject to a specific event-based model stage, based on the number of their atrophic regions. Linear mixed-effects models were used to explore associations between the rate of increase in event-based model stages, and T2 lesion load, disease-modifying treatments, comorbidity, disease duration and disability accumulation. The first regions to become atrophic in patients with clinically isolated syndrome and relapse-onset multiple sclerosis were the posterior cingulate cortex and precuneus, followed by the middle cingulate cortex, brainstem and thalamus. A similar sequence of atrophy was detected in primary-progressive multiple sclerosis with the involvement of the thalamus, cuneus, precuneus, and pallidum, followed by the brainstem and posterior cingulate cortex. The cerebellum, caudate and putamen showed early atrophy in relapse-onset multiple sclerosis and late atrophy in primary-progressive multiple sclerosis. Patients with secondary-progressive multiple sclerosis showed the highest event-based model stage (the highest number of atrophic regions, P < 0.001) at the study entry. All multiple sclerosis phenotypes, but clinically isolated syndrome, showed a faster rate of increase in the event-based model stage than healthy controls. T2 lesion load and disease duration in all patients were associated with increased event-based model stage, but no effects of disease-modifying treatments and comorbidity on event-based model stage were observed. The annualized rate of event-based model stage was associated with the disability accumulation in relapsing-remitting multiple sclerosis, independent of disease duration (P < 0.0001). The data-driven staging of atrophy progression in a large multiple sclerosis sample demonstrates that grey matter atrophy spreads to involve more regions over time. The sequence in which regions become atrophic is reasonably consistent across multiple sclerosis phenotypes. The spread of atrophy was associated with disease duration and with disability accumulation over time in relapsing-remitting multiple sclerosis. See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.Grey matter atrophy is present from the earliest stages of multiple sclerosis, but its temporal ordering is poorly understood. We aimed to determine the sequence in which grey matter regions become atrophic in multiple sclerosis and its association with disability accumulation. In this longitudinal study, we included 1417 subjects: 253 with clinically isolated syndrome, 708 with relapsing-remitting multiple sclerosis, 128 with secondary-progressive multiple sclerosis, 125 with primary-progressive multiple sclerosis, and 203 healthy control subjects from seven European centres. Subjects underwent repeated MRI (total number of scans 3604); the mean follow-up for patients was 2.41 years (standard deviation = 1.97). Disability was scored using the Expanded Disability Status Scale. We calculated the volume of brain grey matter regions and brainstem using an unbiased within-subject template and used an established data-driven event-based model to determine the sequence of occurrence of atrophy and its uncertainty. We assigned each subject to a specific event-based model stage, based on the number of their atrophic regions. Linear mixed-effects models were used to explore associations between the rate of increase in event-based model stages, and T2 lesion load, disease-modifying treatments, comorbidity, disease duration and disability accumulation. The first regions to become atrophic in patients with clinically isolated syndrome and relapse-onset multiple sclerosis were the posterior cingulate cortex and precuneus, followed by the middle cingulate cortex, brainstem and thalamus. A similar sequence of atrophy was detected in primary-progressive multiple sclerosis with the involvement of the thalamus, cuneus, precuneus, and pallidum, followed by the brainstem and posterior cingulate cortex. The cerebellum, caudate and putamen showed early atrophy in relapse-onset multiple sclerosis and late atrophy in primary-progressive multiple sclerosis. Patients with secondary-progressive multiple sclerosis showed the highest event-based model stage (the highest number of atrophic regions, P < 0.001) at the study entry. All multiple sclerosis phenotypes, but clinically isolated syndrome, showed a faster rate of increase in the event-based model stage than healthy controls. T2 lesion load and disease duration in all patients were associated with increased event-based model stage, but no effects of disease-modifying treatments and comorbidity on event-based model stage were observed. The annualized rate of event-based model stage was associated with the disability accumulation in relapsing-remitting multiple sclerosis, independent of disease duration (P < 0.0001). The data-driven staging of atrophy progression in a large multiple sclerosis sample demonstrates that grey matter atrophy spreads to involve more regions over time. The sequence in which regions become atrophic is reasonably consistent across multiple sclerosis phenotypes. The spread of atrophy was associated with disease duration and with disability accumulation over time in relapsing-remitting multiple sclerosis. See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article. Grey matter atrophy in multiple sclerosis affects certain areas preferentially. Eshaghi et al. use a data-driven computational model to predict the order in which regions atrophy, and use this sequence to stage patients. Atrophy begins in deep grey matter nuclei and posterior cortical regions, before spreading to other cortical areas. Abstract See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article. Grey matter atrophy is present from the earliest stages of multiple sclerosis, but its temporal ordering is poorly understood. We aimed to determine the sequence in which grey matter regions become atrophic in multiple sclerosis and its association with disability accumulation. In this longitudinal study, we included 1417 subjects: 253 with clinically isolated syndrome, 708 with relapsing-remitting multiple sclerosis, 128 with secondary-progressive multiple sclerosis, 125 with primary-progressive multiple sclerosis, and 203 healthy control subjects from seven European centres. Subjects underwent repeated MRI (total number of scans 3604); the mean follow-up for patients was 2.41 years (standard deviation = 1.97). Disability was scored using the Expanded Disability Status Scale. We calculated the volume of brain grey matter regions and brainstem using an unbiased within-subject template and used an established data-driven event-based model to determine the sequence of occurrence of atrophy and its uncertainty. We assigned each subject to a specific event-based model stage, based on the number of their atrophic regions. Linear mixed-effects models were used to explore associations between the rate of increase in event-based model stages, and T2 lesion load, disease-modifying treatments, comorbidity, disease duration and disability accumulation. The first regions to become atrophic in patients with clinically isolated syndrome and relapse-onset multiple sclerosis were the posterior cingulate cortex and precuneus, followed by the middle cingulate cortex, brainstem and thalamus. A similar sequence of atrophy was detected in primary-progressive multiple sclerosis with the involvement of the thalamus, cuneus, precuneus, and pallidum, followed by the brainstem and posterior cingulate cortex. The cerebellum, caudate and putamen showed early atrophy in relapse-onset multiple sclerosis and late atrophy in primary-progressive multiple sclerosis. Patients with secondary-progressive multiple sclerosis showed the highest event-based model stage (the highest number of atrophic regions, P < 0.001) at the study entry. All multiple sclerosis phenotypes, but clinically isolated syndrome, showed a faster rate of increase in the event-based model stage than healthy controls. T2 lesion load and disease duration in all patients were associated with increased event-based model stage, but no effects of disease-modifying treatments and comorbidity on event-based model stage were observed. The annualized rate of event-based model stage was associated with the disability accumulation in relapsing-remitting multiple sclerosis, independent of disease duration (P < 0.0001). The data-driven staging of atrophy progression in a large multiple sclerosis sample demonstrates that grey matter atrophy spreads to involve more regions over time. The sequence in which regions become atrophic is reasonably consistent across multiple sclerosis phenotypes. The spread of atrophy was associated with disease duration and with disability accumulation over time in relapsing-remitting multiple sclerosis. |
| Author | Young, Alexandra L Uitdehaag, Bernard Ciccarelli, Olga Rovira, Alex Thompson, Alan J Rocca, Maria A Battaglini, Marco Ourselin, Sebastien Jorge Cardoso, M Ruggieri, Serena Filippi, Massimo Enzinger, Christian Chard, Declan Gandini Wheeler-Kingshott, Claudia A Cawley, Niamh Barkhof, Frederik Marinescu, Razvan V Firth, Nicholas C Brownlee, Wallace J Gasperini, Claudio Pirpamer, Lukas Sastre-Garriga, Jaume Wottschel, Viktor Eshaghi, Arman Tur, Carmen Leurs, Cyra E Alexander, Daniel C Laura Stromillo, M Vrenken, Hugo De Stefano, Nicola De Angelis, Floriana Prados, Ferran Geurts, Jeroen J G |
| Author_xml | – sequence: 1 givenname: Arman orcidid: 0000-0002-6652-3512 surname: Eshaghi fullname: Eshaghi, Arman email: arman.eshaghi.14@ucl.ac.uk organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 2 givenname: Razvan V surname: Marinescu fullname: Marinescu, Razvan V organization: Centre for Medical Image Computing (CMIC), Department of Computer Science, University College London, UK – sequence: 3 givenname: Alexandra L surname: Young fullname: Young, Alexandra L organization: Centre for Medical Image Computing (CMIC), Department of Computer Science, University College London, UK – sequence: 4 givenname: Nicholas C surname: Firth fullname: Firth, Nicholas C organization: Centre for Medical Image Computing (CMIC), Department of Computer Science, University College London, UK – sequence: 5 givenname: Ferran orcidid: 0000-0002-7872-0142 surname: Prados fullname: Prados, Ferran organization: Translational Imaging Group, Centre for Medical Image Computing (CMIC), Department of Medical Physics and Bioengineering, University College London, London, UK – sequence: 6 givenname: M surname: Jorge Cardoso fullname: Jorge Cardoso, M organization: Translational Imaging Group, Centre for Medical Image Computing (CMIC), Department of Medical Physics and Bioengineering, University College London, London, UK – sequence: 7 givenname: Carmen surname: Tur fullname: Tur, Carmen organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 8 givenname: Floriana surname: De Angelis fullname: De Angelis, Floriana organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 9 givenname: Niamh surname: Cawley fullname: Cawley, Niamh organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 10 givenname: Wallace J surname: Brownlee fullname: Brownlee, Wallace J organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 11 givenname: Nicola surname: De Stefano fullname: De Stefano, Nicola organization: Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy – sequence: 12 givenname: M surname: Laura Stromillo fullname: Laura Stromillo, M organization: Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy – sequence: 13 givenname: Marco surname: Battaglini fullname: Battaglini, Marco organization: Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy – sequence: 14 givenname: Serena surname: Ruggieri fullname: Ruggieri, Serena organization: Department of Neurosciences, S Camillo Forlanini Hospital, Rome, Italy – sequence: 15 givenname: Claudio surname: Gasperini fullname: Gasperini, Claudio organization: Department of Neurosciences, S Camillo Forlanini Hospital, Rome, Italy – sequence: 16 givenname: Massimo surname: Filippi fullname: Filippi, Massimo organization: Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy – sequence: 17 givenname: Maria A surname: Rocca fullname: Rocca, Maria A organization: Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy – sequence: 18 givenname: Alex surname: Rovira fullname: Rovira, Alex organization: MR Unit and Section of Neuroradiology, Department of Radiology, Hospital Universitari Vall d'Hebron, Universitat Autònoma de Barcelona, Barcelona, Spain – sequence: 19 givenname: Jaume surname: Sastre-Garriga fullname: Sastre-Garriga, Jaume organization: Department of Neurology/Neuroimmunology, Multiple Sclerosis Centre of Catalonia (CEMCAT), Hospital Universitari Vall d'Hebron, Universitat Autònoma de Barcelona, Barcelona, Spain – sequence: 20 givenname: Jeroen J G surname: Geurts fullname: Geurts, Jeroen J G organization: Department of Anatomy and Neurosciences, VUmc MS Center, Neuroscience Amsterdam, VU University Medical Center, Amsterdam, The Netherlands – sequence: 21 givenname: Hugo surname: Vrenken fullname: Vrenken, Hugo organization: Department of Radiology and Nuclear Medicine, MS Center Amsterdam, Amsterdam, The Netherlands – sequence: 22 givenname: Viktor surname: Wottschel fullname: Wottschel, Viktor organization: Department of Radiology and Nuclear Medicine, MS Center Amsterdam, Amsterdam, The Netherlands – sequence: 23 givenname: Cyra E surname: Leurs fullname: Leurs, Cyra E organization: Department of Neurology, MS Center Amsterdam, VU University Medical Center, Amsterdam, The Netherlands – sequence: 24 givenname: Bernard surname: Uitdehaag fullname: Uitdehaag, Bernard organization: Department of Neurology, MS Center Amsterdam, VU University Medical Center, Amsterdam, The Netherlands – sequence: 25 givenname: Lukas surname: Pirpamer fullname: Pirpamer, Lukas organization: Department of Neurology, Medical University of Graz, Graz, Austria – sequence: 26 givenname: Christian surname: Enzinger fullname: Enzinger, Christian organization: Department of Neurology, Medical University of Graz, Graz, Austria – sequence: 27 givenname: Sebastien surname: Ourselin fullname: Ourselin, Sebastien organization: Translational Imaging Group, Centre for Medical Image Computing (CMIC), Department of Medical Physics and Bioengineering, University College London, London, UK – sequence: 28 givenname: Claudia A surname: Gandini Wheeler-Kingshott fullname: Gandini Wheeler-Kingshott, Claudia A organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 29 givenname: Declan surname: Chard fullname: Chard, Declan organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 30 givenname: Alan J surname: Thompson fullname: Thompson, Alan J organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 31 givenname: Frederik surname: Barkhof fullname: Barkhof, Frederik organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK – sequence: 32 givenname: Daniel C surname: Alexander fullname: Alexander, Daniel C organization: Centre for Medical Image Computing (CMIC), Department of Computer Science, University College London, UK – sequence: 33 givenname: Olga surname: Ciccarelli fullname: Ciccarelli, Olga organization: Queen Square Multiple Sclerosis Centre, UCL Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29741648$$D View this record in MEDLINE/PubMed |
| BookMark | eNo9kD1PwzAQhi1URD9gY0beYAk9O7aTjFXFl1QJhu6R7TjFyImDnQjl3xNoYbrTvY_udM8SzVrfGoSuCdwTKNK1CtK2a_k1Qp6foQVhAhJKuJihBQCIJC84zNEyxg8AwlIqLtCcFhkjguULtHkL_hBMjNa32Nc4mMPUSYen4Ygb2fcmYNkH372P2La4GVxvO2dw1M4EH228ROe1dNFcneoK7R8f9tvnZPf69LLd7BI9neoTWjEutJaKK8F4rnhhMq0Lxeuq1hUhKZfUiKwGVWQVFwyokjARrKg4T-t0he6Oa7vgPwcT-7KxURvnZGv8EEsKqcjyHAhM6M0JHVRjqrILtpFhLP--noDbI-CH7j8lUP74LH99lkef6TeLdGoT |
| CitedBy_id | crossref_primary_10_1016_j_msard_2024_105424 crossref_primary_10_1016_j_msard_2023_104853 crossref_primary_10_1016_j_acra_2024_07_031 crossref_primary_10_1016_j_msard_2021_102794 crossref_primary_10_3892_mmr_2021_12211 crossref_primary_10_1016_j_msard_2021_103407 crossref_primary_10_1162_netn_a_00162 crossref_primary_10_1002_ana_26290 crossref_primary_10_1038_s41582_020_00421_4 crossref_primary_10_1007_s00415_024_12514_x crossref_primary_10_1136_jnnp_2022_329854 crossref_primary_10_1097_WNF_0000000000000598 crossref_primary_10_1111_ene_15827 crossref_primary_10_3389_fneur_2020_546744 crossref_primary_10_3389_fninf_2023_1060511 crossref_primary_10_1002_jmri_27862 crossref_primary_10_1177_13524585221099169 crossref_primary_10_1016_j_neubiorev_2024_105716 crossref_primary_10_1177_13524585211059766 crossref_primary_10_1111_jon_12688 crossref_primary_10_1002_brb3_3327 crossref_primary_10_1177_0271678X221121849 crossref_primary_10_1177_1352458520958356 crossref_primary_10_1007_s00330_020_07199_5 crossref_primary_10_1111_cns_70225 crossref_primary_10_1177_1352458518817987 crossref_primary_10_1177_15459683211046257 crossref_primary_10_1212_NXI_0000000000200399 crossref_primary_10_12688_wellcomeopenres_17731_1 crossref_primary_10_1038_s41746_019_0127_8 crossref_primary_10_1007_s00415_021_10777_2 crossref_primary_10_1093_brain_awab132 crossref_primary_10_3390_ijms24021639 crossref_primary_10_1007_s00415_022_11387_2 crossref_primary_10_1177_1352458520938999 crossref_primary_10_1177_13524585211031786 crossref_primary_10_1007_s00415_020_10023_1 crossref_primary_10_1007_s00401_020_02168_0 crossref_primary_10_1016_j_msard_2023_104714 crossref_primary_10_1080_14737175_2024_2398484 crossref_primary_10_3390_jcm11102841 crossref_primary_10_1177_1756286419859722 crossref_primary_10_1007_s00234_023_03189_8 crossref_primary_10_3389_fdata_2021_661110 crossref_primary_10_1098_rsos_241052 crossref_primary_10_1038_s41419_023_05783_3 crossref_primary_10_1093_braincomms_fcaf254 crossref_primary_10_1136_jnnp_2020_324826 crossref_primary_10_1016_j_nicl_2022_102959 crossref_primary_10_1016_j_msard_2021_103430 crossref_primary_10_1177_13524585211011390 crossref_primary_10_1111_ene_15289 crossref_primary_10_1007_s00415_024_12656_y crossref_primary_10_1162_netn_a_00258 crossref_primary_10_1126_scitranslmed_abc2888 crossref_primary_10_1093_arclin_acad070 crossref_primary_10_1016_j_jns_2023_120847 crossref_primary_10_1016_j_msard_2024_105550 crossref_primary_10_3389_frobt_2022_926255 crossref_primary_10_1007_s00330_025_11892_8 crossref_primary_10_1007_s00415_020_10376_7 crossref_primary_10_1007_s00415_022_11386_3 crossref_primary_10_1038_s41398_024_03073_w crossref_primary_10_3390_ijms26178656 crossref_primary_10_1212_WNL_0000000000210080 crossref_primary_10_1038_s41582_020_00439_8 crossref_primary_10_1016_j_nbd_2023_106084 crossref_primary_10_1212_NXI_0000000000200222 crossref_primary_10_1177_1756286419877081 crossref_primary_10_3233_JAD_221007 crossref_primary_10_1177_1352458520966292 crossref_primary_10_1007_s00234_024_03354_7 crossref_primary_10_1002_acn3_52085 crossref_primary_10_1016_j_ynirp_2022_100086 crossref_primary_10_1038_s41380_022_01625_4 crossref_primary_10_1016_j_msard_2019_101899 crossref_primary_10_1111_epi_17316 crossref_primary_10_1016_j_clinph_2025_2110942 crossref_primary_10_1080_14737175_2025_2450788 crossref_primary_10_1002_hbm_26151 crossref_primary_10_1016_S1474_4422_18_30455_1 crossref_primary_10_1177_1352458519881760 crossref_primary_10_1111_cns_14050 crossref_primary_10_1002_jmri_29046 crossref_primary_10_1007_s00415_023_12102_5 crossref_primary_10_1016_j_msard_2020_102343 crossref_primary_10_1172_JCI177692 crossref_primary_10_1371_journal_pone_0288967 crossref_primary_10_1136_jnnp_2021_327803 crossref_primary_10_1007_s00401_024_02796_w crossref_primary_10_1016_j_msard_2023_104510 crossref_primary_10_1177_13524585211020296 crossref_primary_10_1111_bpa_12813 crossref_primary_10_1016_j_msard_2022_104116 crossref_primary_10_1038_s41577_022_00718_z crossref_primary_10_1186_s12967_024_04892_7 crossref_primary_10_1016_j_msard_2023_104516 crossref_primary_10_1136_jnnp_2025_335925 crossref_primary_10_1177_1756286420975223 crossref_primary_10_1007_s00415_022_11494_0 crossref_primary_10_3390_ijms26083579 crossref_primary_10_1016_j_nicl_2022_103065 crossref_primary_10_1111_jon_12625 crossref_primary_10_1136_jnnp_2020_325421 crossref_primary_10_1002_brb3_2573 crossref_primary_10_3390_ijms26178523 crossref_primary_10_1007_s00415_023_11870_4 crossref_primary_10_1177_1352458521999274 crossref_primary_10_1007_s11055_022_01310_7 crossref_primary_10_1016_j_msard_2023_104528 crossref_primary_10_1111_ejn_16543 crossref_primary_10_3390_biom14101210 crossref_primary_10_1016_j_nicl_2023_103354 crossref_primary_10_1007_s00415_022_11021_1 crossref_primary_10_1186_s40001_025_03026_z crossref_primary_10_1109_JBHI_2022_3208517 crossref_primary_10_1002_alz_12083 crossref_primary_10_1016_j_neurot_2024_e00432 crossref_primary_10_3389_frai_2021_613261 crossref_primary_10_1093_brain_awab033 crossref_primary_10_1186_s12883_020_01736_x crossref_primary_10_3389_fneur_2019_01173 crossref_primary_10_1212_WNL_0000000000007254 crossref_primary_10_1515_revneuro_2020_0140 crossref_primary_10_1016_j_neuroimage_2025_121162 crossref_primary_10_1002_acn3_52311 crossref_primary_10_1016_j_nicl_2020_102550 crossref_primary_10_1177_13524585211066598 crossref_primary_10_1002_hbm_26117 crossref_primary_10_1016_j_cobeha_2024_101436 crossref_primary_10_1016_j_brain_2024_100097 crossref_primary_10_1177_1352458519851247 crossref_primary_10_1093_brain_awad288 crossref_primary_10_1093_brain_awae251 crossref_primary_10_3390_biomedicines10020231 crossref_primary_10_1002_hbm_25389 crossref_primary_10_1007_s00330_024_11157_w crossref_primary_10_3389_fneur_2021_632749 crossref_primary_10_1148_radiol_221512 crossref_primary_10_1038_s41582_019_0183_3 crossref_primary_10_1111_ene_14214 crossref_primary_10_1038_s41598_022_08477_6 crossref_primary_10_1177_13524585211046739 crossref_primary_10_1002_nbm_4964 crossref_primary_10_1038_s41467_021_22265_2 crossref_primary_10_1002_hbm_26106 crossref_primary_10_1016_S1474_4422_24_00027_9 crossref_primary_10_1007_s40263_022_00927_z crossref_primary_10_1162_imag_a_00010 crossref_primary_10_1007_s00415_022_11405_3 crossref_primary_10_1080_14728222_2020_1842358 crossref_primary_10_7554_eLife_49298 crossref_primary_10_1016_j_neuri_2022_100071 crossref_primary_10_1007_s00330_022_08610_z crossref_primary_10_1177_1352458519887346 crossref_primary_10_1212_NXI_0000000000001083 crossref_primary_10_3390_cells11030440 crossref_primary_10_7717_peerj_15299 crossref_primary_10_1080_17470919_2020_1766562 crossref_primary_10_1016_j_msard_2019_02_021 crossref_primary_10_3389_fimmu_2025_1543649 crossref_primary_10_1002_ana_25808 crossref_primary_10_1016_j_bbr_2025_115457 crossref_primary_10_1136_jnnp_2022_330343 crossref_primary_10_1177_13524585241303491 crossref_primary_10_1007_s00415_023_11736_9 crossref_primary_10_1016_j_clineuro_2021_106805 crossref_primary_10_1016_j_jneuroim_2024_578445 crossref_primary_10_1016_j_msard_2021_103031 crossref_primary_10_1186_s12974_020_01936_9 crossref_primary_10_1136_svn_2023_002791 crossref_primary_10_1016_j_msard_2023_104568 crossref_primary_10_1007_s00115_021_01103_2 crossref_primary_10_21518_ms2025_222 crossref_primary_10_1016_j_msard_2021_103036 crossref_primary_10_1177_1352458519900972 crossref_primary_10_1002_nbm_5235 crossref_primary_10_1111_ene_14471 crossref_primary_10_1002_jmri_27806 crossref_primary_10_1186_s12974_022_02618_4 crossref_primary_10_3389_fnins_2023_1268860 crossref_primary_10_1038_s41380_024_02452_5 crossref_primary_10_1016_j_nicl_2024_103606 crossref_primary_10_3390_ijms231810651 crossref_primary_10_1038_s41582_021_00581_x crossref_primary_10_1177_13524585231188096 crossref_primary_10_1016_j_msard_2023_104560 crossref_primary_10_1002_hbm_70284 crossref_primary_10_1002_hbm_24989 crossref_primary_10_1136_jnnp_2020_325610 crossref_primary_10_1177_1352458519845287 crossref_primary_10_1177_13524585211022174 crossref_primary_10_1016_j_msard_2025_106435 crossref_primary_10_3389_fneur_2023_1268411 crossref_primary_10_1002_ana_26529 crossref_primary_10_1007_s00062_022_01144_3 crossref_primary_10_1016_j_csbj_2025_05_003 crossref_primary_10_1016_j_biopsych_2023_11_010 crossref_primary_10_1126_scitranslmed_adi0295 crossref_primary_10_1038_s41583_023_00779_6 crossref_primary_10_1007_s00415_023_11778_z crossref_primary_10_1148_radiol_2020200430 crossref_primary_10_1177_13524585211033184 crossref_primary_10_1007_s00415_021_10576_9 crossref_primary_10_1126_scitranslmed_aat7108 crossref_primary_10_1177_13524585221139575 crossref_primary_10_1002_eji_202250228 crossref_primary_10_1080_1744666X_2021_1986005 crossref_primary_10_3389_fneur_2023_1165267 crossref_primary_10_3390_medicina59061082 crossref_primary_10_1016_j_neurol_2019_09_004 crossref_primary_10_1016_j_neuron_2019_01_056 crossref_primary_10_3389_fnins_2019_00594 crossref_primary_10_1007_s12021_025_09740_7 crossref_primary_10_1177_13524585241259648 crossref_primary_10_1016_j_jneuroim_2023_578280 crossref_primary_10_1111_ene_15742 crossref_primary_10_1177_02841851241305738 crossref_primary_10_1016_j_nicl_2021_102632 crossref_primary_10_1016_j_immuni_2019_12_004 crossref_primary_10_1093_brain_awy114 crossref_primary_10_1016_j_cortex_2021_08_011 crossref_primary_10_1002_hbm_70141 crossref_primary_10_1016_j_msard_2022_104083 crossref_primary_10_1002_hbm_25375 crossref_primary_10_1002_hbm_26464 crossref_primary_10_1016_j_msard_2022_104077 crossref_primary_10_12688_f1000research_20906_1 crossref_primary_10_3389_fneur_2020_575611 crossref_primary_10_1016_j_nicl_2021_102606 crossref_primary_10_1016_j_neurad_2023_11_007 crossref_primary_10_1177_17562864211066751 crossref_primary_10_3390_medicina58030377 crossref_primary_10_1038_s41598_021_96132_x crossref_primary_10_1111_ejn_15854 crossref_primary_10_3390_app14135626 crossref_primary_10_3389_frai_2022_660581 crossref_primary_10_1002_acn3_50872 crossref_primary_10_3390_neurolint14020042 crossref_primary_10_1212_WNL_0000000000210228 crossref_primary_10_1212_WNL_0000000000011494 crossref_primary_10_1016_j_msard_2019_101462 crossref_primary_10_1007_s00415_024_12516_9 crossref_primary_10_3389_fnmol_2023_1087745 crossref_primary_10_1016_j_clineuro_2023_107739 crossref_primary_10_3390_jpm13101488 crossref_primary_10_1038_s41380_023_01943_1 crossref_primary_10_3389_fneur_2020_00606 crossref_primary_10_1073_pnas_2421806122 crossref_primary_10_1212_WNL_0000000000008198 crossref_primary_10_1212_NXI_0000000000000900 crossref_primary_10_1016_j_nicl_2019_102003 crossref_primary_10_1016_j_nicl_2019_101954 crossref_primary_10_1186_s40035_023_00389_3 crossref_primary_10_1093_brain_awaa461 crossref_primary_10_1016_j_msard_2022_104183 |
| ContentType | Journal Article |
| Copyright | The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. 2018 |
| Copyright_xml | – notice: The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. 2018 |
| DBID | TOX NPM 7X8 |
| DOI | 10.1093/brain/awy088 |
| DatabaseName | Oxford Open Journals PubMed MEDLINE - Academic |
| DatabaseTitle | PubMed MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic PubMed |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: TOX name: Oxford Journals Open Access Collection url: https://academic.oup.com/journals/ sourceTypes: Publisher – sequence: 3 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Medicine |
| EISSN | 1460-2156 |
| EndPage | 1677 |
| ExternalDocumentID | 29741648 10.1093/brain/awy088 |
| Genre | Research Support, Non-U.S. Gov't Journal Article |
| GrantInformation_xml | – fundername: EPSRC sequence: 0 grantid: M020533, M006093, J020990 funderid: 10.13039/501100000266 |
| GroupedDBID | --- -E4 -~X .2P .I3 .XZ .ZR 0R~ 1TH 23N 2WC 4.4 482 48X 53G 5GY 5RE 5VS 5WA 5WD 6PF 70D AABZA AACZT AAIMJ AAJKP AAJQQ AAMDB AAMVS AAOGV AAPNW AAPQZ AAPXW AARHZ AAUAY AAUQX AAVAP AAVLN AAWTL ABEJV ABEUO ABIVO ABIXL ABJNI ABKDP ABLJU ABMNT ABNHQ ABNKS ABPTD ABQLI ABQNK ABWST ABXVV ABZBJ ACGFS ACIWK ACPRK ACUFI ACUTJ ACUTO ACYHN ADBBV ADEYI ADEZT ADGKP ADGZP ADHKW ADHZD ADIPN ADJQC ADOCK ADQBN ADRIX ADRTK ADVEK ADYVW ADZXQ AEGPL AEJOX AEKSI AELWJ AEMDU AENEX AENZO AEPUE AETBJ AEWNT AFFZL AFGWE AFIYH AFOFC AFXAL AFXEN AGINJ AGKEF AGQXC AGSYK AGUTN AHMBA AHMMS AHXPO AIJHB AJEEA AKWXX ALMA_UNASSIGNED_HOLDINGS ALUQC APIBT APWMN ARIXL ATGXG AXUDD AYOIW BAWUL BAYMD BCRHZ BEYMZ BHONS BQDIO BR6 BSWAC BTRTY BVRKM C45 CDBKE COF CS3 CZ4 DAKXR DIK DILTD DU5 D~K E3Z EBS EE~ EJD EMOBN ENERS F5P F9B FECEO FHSFR FLUFQ FOEOM FOTVD FQBLK GAUVT GJXCC GX1 H13 H5~ HAR HW0 HZ~ IOX J21 J5H JXSIZ KAQDR KBUDW KOP KQ8 KSI KSN L7B M-Z M49 MHKGH ML0 N9A NGC NLBLG NOMLY NOYVH NU- O9- OAUYM OAWHX OBOKY OCZFY ODMLO OHH OJQWA OJZSN OK1 OPAEJ OVD OWPYF P2P PAFKI PEELM PQQKQ Q1. Q5Y R44 RD5 RIG ROL ROX ROZ RUSNO RW1 RXO TCURE TEORI TJX TLC TOX TR2 VVN W8F WH7 WOQ X7H YAYTL YKOAZ YSK YXANX ZKX ~91 ABDFA ABGNP ABVGC NPM 7X8 ABPQP ABUFD ABXZS ADNBA AEMQT AFYAG AJBYB AJNCP ALXQX |
| ID | FETCH-LOGICAL-c416t-2d456ccab5b6458b59e7cc9b5fdfcd1135a2e67f0b97d56402ba07cc49d553f3 |
| IEDL.DBID | TOX |
| ISICitedReferencesCount | 286 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000434113500018&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 0006-8950 1460-2156 |
| IngestDate | Sun Nov 09 12:39:15 EST 2025 Wed Feb 19 02:33:32 EST 2025 Fri Dec 06 10:16:16 EST 2024 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 6 |
| Keywords | atrophy probabilistic modelling grey matter disability accumulation multiple sclerosis |
| Language | English |
| License | This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c416t-2d456ccab5b6458b59e7cc9b5fdfcd1135a2e67f0b97d56402ba07cc49d553f3 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| ORCID | 0000-0002-6652-3512 0000-0002-7872-0142 |
| OpenAccessLink | https://dx.doi.org/10.1093/brain/awy088 |
| PMID | 29741648 |
| PQID | 2036788010 |
| PQPubID | 23479 |
| PageCount | 13 |
| ParticipantIDs | proquest_miscellaneous_2036788010 pubmed_primary_29741648 oup_primary_10_1093_brain_awy088 |
| PublicationCentury | 2000 |
| PublicationDate | 2018-06-01 |
| PublicationDateYYYYMMDD | 2018-06-01 |
| PublicationDate_xml | – month: 06 year: 2018 text: 2018-06-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | England |
| PublicationPlace_xml | – name: England |
| PublicationTitle | Brain (London, England : 1878) |
| PublicationTitleAlternate | Brain |
| PublicationYear | 2018 |
| Publisher | Oxford University Press |
| Publisher_xml | – sequence: 0 name: Oxford University Press |
| References | 29800475 - Brain. 2018 Jun 1;141(6):1580-1583 |
| References_xml | – reference: 29800475 - Brain. 2018 Jun 1;141(6):1580-1583 |
| SSID | ssj0014326 |
| Score | 2.6646502 |
| Snippet | See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.
Grey matter atrophy in multiple sclerosis affects certain... See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.Grey matter atrophy is present from the earliest stages of... |
| SourceID | proquest pubmed oup |
| SourceType | Aggregation Database Index Database Publisher |
| StartPage | 1665 |
| Title | Progression of regional grey matter atrophy in multiple sclerosis |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/29741648 https://www.proquest.com/docview/2036788010 |
| Volume | 141 |
| WOSCitedRecordID | wos000434113500018&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV07T8MwED5BhRAL70d5VEZijRrbcWyPFaJioKVDh2xRHrbUgRQ1Laj_nnMcOhQkWDxEiRN9vtjf-TvfATxQI0uhCxbQjLMgEtwEiklsFOexNYwb0RwUfpHjsUoSPWmTJNW_SPia93NXK6Gffa7xh8C5lgrl7Hn6mmzUgog3ZdXc1BsoLcI2wH374a0zbD-oZLOkDI_-_THHcNiyRjLww3wCO6Y6hf1Rq4ufwWDiwqx8ig0yt8SVW3AUm-DFNXlrcmgSt-uNoJJZRb7DCEmN3eE6OavPYTp8mj4-B21xhKBADrUMWInUB-HPRR5HQuVCG1kUOhe2tEVJKRcZM7G0Ya5xNGJ0E_MsxDsiXQrBLb-ATjWvzBWQDCkMDUse6hC5UWiySEYqNqqwHP1mSrtAELb03We_SL1qzdMGidQj0YX7b0xTNE-nOWSVma_q1Omc6GWj19eFSw_2piemHR2M1PXfL7iBA2Qqysdo3UJnuViZO9grPpazetGDXZkobMeTUa-xjC_UlLQn |
| linkProvider | Oxford University Press |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Progression+of+regional+grey+matter+atrophy+in+multiple+sclerosis&rft.jtitle=Brain+%28London%2C+England+%3A+1878%29&rft.au=Eshaghi%2C+Arman&rft.au=Marinescu%2C+Razvan+V&rft.au=Young%2C+Alexandra+L&rft.au=Firth%2C+Nicholas+C&rft.date=2018-06-01&rft.pub=Oxford+University+Press&rft.issn=0006-8950&rft.eissn=1460-2156&rft.volume=141&rft.issue=6&rft.spage=1665&rft.epage=1677&rft_id=info:doi/10.1093%2Fbrain%2Fawy088&rft.externalDocID=10.1093%2Fbrain%2Fawy088 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0006-8950&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0006-8950&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0006-8950&client=summon |