Skip to main content
Top
Published in: BMC Neurology 1/2017

Open Access 01-12-2017 | Research article

Automated segmentation of cerebral deep gray matter from MRI scans: effect of field strength on sensitivity and reliability

Authors: Renxin Chu, Shelley Hurwitz, Shahamat Tauhid, Rohit Bakshi

Published in: BMC Neurology | Issue 1/2017

Login to get access

Abstract

Background

The cerebral subcortical deep gray matter nuclei (DGM) are a common, early, and clinically-relevant site of atrophy in multiple sclerosis (MS). Robust and reliable DGM segmentation could prove useful to evaluate putative neuroprotective MS therapies. The objective of the study was to compare the sensitivity and reliability of DGM volumes obtained from 1.5T vs. 3T MRI.

Methods

Fourteen patients with MS [age (mean, range) 50.2 (32.0–60.8) years, disease duration 18.4 (8.2–35.5) years, Expanded Disability Status Scale score 3.1 (0–6), median 3.0] and 15 normal controls (NC) underwent brain 3D T1-weighted paired scan-rescans at 1.5T and 3T. DGM (caudate, thalamus, globus pallidus, and putamen) segmentation was obtained by the fully automated FSL-FIRST pipeline. Both raw and normalized volumes were derived.

Results

DGM volumes were generally higher at 3T vs. 1.5T in both groups. For raw volumes, 3T showed slightly better sensitivity (thalamus: p = 0.02; caudate: p = 0.10; putamen: p = 0.02; globus pallidus: p = 0.0004; total DGM: p = 0.01) than 1.5T (thalamus: p = 0.05; caudate: p = 0.09; putamen: p = 0.03; globus pallidus: p = 0.0006; total DGM: p = 0.02) for detecting DGM atrophy in MS vs. NC. For normalized volumes, 3T but not 1.5T detected atrophy in the globus pallidus in the MS group. Across all subjects, scan-rescan reliability was generally very high for both platforms, showing slightly higher reliability for some DGM volumes at 3T. Raw volumes showed higher reliability than normalized volumes. Raw DGM volume showed higher reliability than the individual structures.

Conclusions

These results suggest somewhat higher sensitivity and reliability of DGM volumes obtained from 3T vs. 1.5T MRI. Further studies should assess the role of this 3T pipeline in tracking potential MS neurotherapeutic effects.
Literature
1.
go back to reference Houtchens MK, Benedict RH, Killiany R, Sharma J, Jaisani Z, Singh B, et al. Thalamic atrophy and cognition in multiple sclerosis. Neurology. 2007;69:1213–23.CrossRefPubMed Houtchens MK, Benedict RH, Killiany R, Sharma J, Jaisani Z, Singh B, et al. Thalamic atrophy and cognition in multiple sclerosis. Neurology. 2007;69:1213–23.CrossRefPubMed
2.
go back to reference Bergsland N, Horakova D, Dwyer MG, Dolezal O, Seidl ZK, Vaneckova M, et al. Subcortical and cortical gray matter atrophy in a large sample of patients with clinically isolated syndrome and early relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol. 2012;33:1573–8.CrossRefPubMed Bergsland N, Horakova D, Dwyer MG, Dolezal O, Seidl ZK, Vaneckova M, et al. Subcortical and cortical gray matter atrophy in a large sample of patients with clinically isolated syndrome and early relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol. 2012;33:1573–8.CrossRefPubMed
3.
go back to reference 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;15:30S–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;15:30S–45S.CrossRefPubMed
4.
go back to reference Nourbakhsh B, Azevedo C, Maghzi AH, Spain R, Pelletier D, Waubant E. Subcortical grey matter volumes predict subsequent walking function in early multiple sclerosis. J Neurol Sci. 2016;366:229–33.CrossRefPubMed Nourbakhsh B, Azevedo C, Maghzi AH, Spain R, Pelletier D, Waubant E. Subcortical grey matter volumes predict subsequent walking function in early multiple sclerosis. J Neurol Sci. 2016;366:229–33.CrossRefPubMed
5.
go back to reference Dupuy SL, Tauhid S, Hurwitz S, Chu R, Yousuf F, Bakshi R. The effect of dimethyl fumarate on cerebral gray matter atrophy in multiple sclerosis. Neurol Ther. 2016;5:215–29.CrossRefPubMedPubMedCentral Dupuy SL, Tauhid S, Hurwitz S, Chu R, Yousuf F, Bakshi R. The effect of dimethyl fumarate on cerebral gray matter atrophy in multiple sclerosis. Neurol Ther. 2016;5:215–29.CrossRefPubMedPubMedCentral
6.
go back to reference Kim G, Chu R, Yousuf F, Tauhid S, Stazzone L, Houtchens MK, et al. Sample size requirements for 1 year treatment effects using deep gray matter volume from 3T MRI in progressive forms of multiple sclerosis. Int J Neurosci. [Epub ahead of print]. doi:10.1080/00207454.2017.1283313. Kim G, Chu R, Yousuf F, Tauhid S, Stazzone L, Houtchens MK, et al. Sample size requirements for 1 year treatment effects using deep gray matter volume from 3T MRI in progressive forms of multiple sclerosis. Int J Neurosci. [Epub ahead of print]. doi:10.​1080/​00207454.​2017.​1283313.
7.
go back to reference Ontaneda D, Fox RJ, Chataway J. Clinical trials in progressive multiple sclerosis: lessons learned and future perspectives. Lancet Neurol. 2015;14:208–23.CrossRefPubMedPubMedCentral Ontaneda D, Fox RJ, Chataway J. Clinical trials in progressive multiple sclerosis: lessons learned and future perspectives. Lancet Neurol. 2015;14:208–23.CrossRefPubMedPubMedCentral
8.
go back to reference Filippi M, Rocca MA, Arnold DL, Bakshi R, Barkhof F, De Sefano N, et al. EFNS guideline on the use of neuroimaging in the management of multiple sclerosis. Eur J Neurol. 2006;13:313–25.CrossRefPubMed Filippi M, Rocca MA, Arnold DL, Bakshi R, Barkhof F, De Sefano N, et al. EFNS guideline on the use of neuroimaging in the management of multiple sclerosis. Eur J Neurol. 2006;13:313–25.CrossRefPubMed
9.
go back to reference Filippi M, Wolinsky JS, Comi G. CORAL Study Group. Effects of oral glatiramer acetate on clinical and MRI-monitored disease activity in patients with relapsing multiple sclerosis: a multicentre, double-blind, randomised, placebo-controlled study. Lancet Neurol. 2006;5:213–20.CrossRefPubMed Filippi M, Wolinsky JS, Comi G. CORAL Study Group. Effects of oral glatiramer acetate on clinical and MRI-monitored disease activity in patients with relapsing multiple sclerosis: a multicentre, double-blind, randomised, placebo-controlled study. Lancet Neurol. 2006;5:213–20.CrossRefPubMed
10.
go back to reference Zivadinov R, Bakshi R. Role of MRI in multiple sclerosis I: inflammation and lesions. Front Biosci. 2004;9:665–83.CrossRefPubMed Zivadinov R, Bakshi R. Role of MRI in multiple sclerosis I: inflammation and lesions. Front Biosci. 2004;9:665–83.CrossRefPubMed
11.
go back to reference Li DK, Held U, Petkau J, Daumer M, Barkhof F, Fazekas F, et al. MRI T2 lesion burden in multiple sclerosis: a plateauing relationship with clinical disability. Neurology. 2006;66:1384–9.CrossRefPubMed Li DK, Held U, Petkau J, Daumer M, Barkhof F, Fazekas F, et al. MRI T2 lesion burden in multiple sclerosis: a plateauing relationship with clinical disability. Neurology. 2006;66:1384–9.CrossRefPubMed
12.
go back to reference Zurawski J, Lassmann H, Bakshi R. Use of magnetic resonance imaging to visualize leptomeningeal inflammation in patients with multiple sclerosis: A review. JAMA Neurol. 2017;74:100–9.CrossRefPubMed Zurawski J, Lassmann H, Bakshi R. Use of magnetic resonance imaging to visualize leptomeningeal inflammation in patients with multiple sclerosis: A review. JAMA Neurol. 2017;74:100–9.CrossRefPubMed
13.
go back to reference Sicotte NL, Voskuhl RR, Bouvier S, Klutch R, Cohen MS, Mazziotta JC. Comparison of multiple sclerosis lesions at 1.5 and 3.0 Tesla. Investig Radiol. 2003;38:423–7. Sicotte NL, Voskuhl RR, Bouvier S, Klutch R, Cohen MS, Mazziotta JC. Comparison of multiple sclerosis lesions at 1.5 and 3.0 Tesla. Investig Radiol. 2003;38:423–7.
14.
go back to reference Stankiewicz JM, Glanz BI, Healy BC, Arora A, Neema M, Benedict RH, et al. Brain MRI lesion load at 1.5T and 3T versus clinical status in multiple sclerosis. J Neuroimaging. 2011;21:e50–6.CrossRefPubMedPubMedCentral Stankiewicz JM, Glanz BI, Healy BC, Arora A, Neema M, Benedict RH, et al. Brain MRI lesion load at 1.5T and 3T versus clinical status in multiple sclerosis. J Neuroimaging. 2011;21:e50–6.CrossRefPubMedPubMedCentral
15.
go back to reference Chu R, Tauhid S, Glanz BI, Healy BC, Kim G, Oommen VV, et al. whole brain volume measured from 1.5T versus 3T MRI in healthy subjects and patients with multiple sclerosis. J Neuroimaging. 2016;26:62–7.CrossRefPubMed Chu R, Tauhid S, Glanz BI, Healy BC, Kim G, Oommen VV, et al. whole brain volume measured from 1.5T versus 3T MRI in healthy subjects and patients with multiple sclerosis. J Neuroimaging. 2016;26:62–7.CrossRefPubMed
16.
go back to reference Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol. 2005;58:840–6.CrossRefPubMed Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol. 2005;58:840–6.CrossRefPubMed
17.
go back to reference Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33:1444–52.CrossRefPubMed Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33:1444–52.CrossRefPubMed
18.
go back to reference Fischer JS, Rudick RA, Cutter GR, Reingold SC. The multiple sclerosis functional composite measure (MSFC): an integrated approach to MS clinical outcome assessment. National MS Society Clinical Outcomes Assessment Task Force. Mult Scler. 1999;5:244–50.CrossRefPubMed Fischer JS, Rudick RA, Cutter GR, Reingold SC. The multiple sclerosis functional composite measure (MSFC): an integrated approach to MS clinical outcome assessment. National MS Society Clinical Outcomes Assessment Task Force. Mult Scler. 1999;5:244–50.CrossRefPubMed
19.
go back to reference Kalavathi P, Prasath VB. Methods on skull stripping of MRI head scan images–a review. J Digit Imaging. 2016;29:365–79.CrossRefPubMed Kalavathi P, Prasath VB. Methods on skull stripping of MRI head scan images–a review. J Digit Imaging. 2016;29:365–79.CrossRefPubMed
20.
go back to reference Meng X, Rosenthal R, Rubin DB. Comparing correlated correlation coefficients. Psychol Bull. 1992;111:172–5.CrossRef Meng X, Rosenthal R, Rubin DB. Comparing correlated correlation coefficients. Psychol Bull. 1992;111:172–5.CrossRef
21.
go back to reference Winer BJ, Dr B, Michels KM. Statistical Principles in Experimental Design. 2nd ed. New York: McGraw-Hill; 1971. Winer BJ, Dr B, Michels KM. Statistical Principles in Experimental Design. 2nd ed. New York: McGraw-Hill; 1971.
22.
go back to reference Jovicich J, Czanner S, Han X, Salat D, van der Kouwe A, Quinn B, et al. MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. NeuroImage. 2009;46:177–92.CrossRefPubMedPubMedCentral Jovicich J, Czanner S, Han X, Salat D, van der Kouwe A, Quinn B, et al. MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. NeuroImage. 2009;46:177–92.CrossRefPubMedPubMedCentral
23.
go back to reference Chow N, Hwang KS, Hurtz S, Green AE, Somme JH, Thompson PM, et al. Comparing 3T and 1.5T MRI for mapping hippocampal atrophy in the Alzheimer's Disease Neuroimaging Initiative. AJNR Am J Neuroradiol. 2015;36:653–60.CrossRefPubMed Chow N, Hwang KS, Hurtz S, Green AE, Somme JH, Thompson PM, et al. Comparing 3T and 1.5T MRI for mapping hippocampal atrophy in the Alzheimer's Disease Neuroimaging Initiative. AJNR Am J Neuroradiol. 2015;36:653–60.CrossRefPubMed
24.
go back to reference Kollia K, Maderwald S, Putzki N, Schlamann M, Theysohn JM, Kraff O, et al. First clinical study on ultra-high-field MR imaging in patients with multiple sclerosis: comparison of 1.5T and 7T. AJNR Am J Neuroradiol. 2009;30:699–702.CrossRefPubMed Kollia K, Maderwald S, Putzki N, Schlamann M, Theysohn JM, Kraff O, et al. First clinical study on ultra-high-field MR imaging in patients with multiple sclerosis: comparison of 1.5T and 7T. AJNR Am J Neuroradiol. 2009;30:699–702.CrossRefPubMed
25.
go back to reference Neema M, Arora A, Healy BC, Guss ZD, Brass SD, Duan Y, et al. Deep gray matter involvement on brain MRI scans is associated with clinical progression in multiple sclerosis. J Neuroimaging. 2009;19:3–8.CrossRefPubMedPubMedCentral Neema M, Arora A, Healy BC, Guss ZD, Brass SD, Duan Y, et al. Deep gray matter involvement on brain MRI scans is associated with clinical progression in multiple sclerosis. J Neuroimaging. 2009;19:3–8.CrossRefPubMedPubMedCentral
26.
go back to reference Lassmann H, van Horssen J, Mahad D. Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol. 2012;8:647–56.CrossRefPubMed Lassmann H, van Horssen J, Mahad D. Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol. 2012;8:647–56.CrossRefPubMed
27.
go back to reference Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, et al. The relation between inflammation and neurodegeneration in multiple sclerosis. Brain. 2009;132:1175–89.CrossRefPubMedPubMedCentral Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, et al. The relation between inflammation and neurodegeneration in multiple sclerosis. Brain. 2009;132:1175–89.CrossRefPubMedPubMedCentral
28.
go back to reference Harrison DM, Oh J, Roy S, Wood ET, Whetstone A, Seigo MA, et al. Thalamic lesions in multiple sclerosis by 7T MRI: Clinical implications and relationship to cortical pathology. Mult Scler. 2015;21:1139–50.CrossRefPubMedPubMedCentral Harrison DM, Oh J, Roy S, Wood ET, Whetstone A, Seigo MA, et al. Thalamic lesions in multiple sclerosis by 7T MRI: Clinical implications and relationship to cortical pathology. Mult Scler. 2015;21:1139–50.CrossRefPubMedPubMedCentral
29.
go back to reference Klawiter EC, Ceccarelli A, Arora A, Jackson JS, Bakshi S, Kim G, et al. Corpus callosum atrophy correlates with gray matter atrophy in patients with multiple sclerosis. J Neuroimaging. 2015;25:62–7.CrossRefPubMed Klawiter EC, Ceccarelli A, Arora A, Jackson JS, Bakshi S, Kim G, et al. Corpus callosum atrophy correlates with gray matter atrophy in patients with multiple sclerosis. J Neuroimaging. 2015;25:62–7.CrossRefPubMed
30.
go back to reference Yang C-Y, Liu HM, Chen SK, Chen YF, Lee CW, Yeh LR. Reproducibility of brain morphometry from short-term repeat clinical MRI examinations: a retrospective study. PLoS One. 2016;11:e0146913.CrossRefPubMedPubMedCentral Yang C-Y, Liu HM, Chen SK, Chen YF, Lee CW, Yeh LR. Reproducibility of brain morphometry from short-term repeat clinical MRI examinations: a retrospective study. PLoS One. 2016;11:e0146913.CrossRefPubMedPubMedCentral
31.
go back to reference Shinohara RT, Oh J, Nair G, Calabresi PA, Davatzikos C, Doshi J, et al. Volumetric analysis from a harmonized multisite brain MRI study of a single subject with multiple sclerosis. AJNR Am J Neuroradiol. [Epub ahead of print]. 10.3174/ajnr.A5254. Shinohara RT, Oh J, Nair G, Calabresi PA, Davatzikos C, Doshi J, et al. Volumetric analysis from a harmonized multisite brain MRI study of a single subject with multiple sclerosis. AJNR Am J Neuroradiol. [Epub ahead of print]. 10.​3174/​ajnr.​A5254.
32.
go back to reference Tsivgoulis G, Katsanos AH, Grigoriadis N, Hadjigeorgiou GM, Heliopoulos I, Kilidireas C, et al. The effect of disease modifying therapies on brain atrophy in patients with relapsing-remitting multiple sclerosis: a systematic review and meta-analysis. PLoS One. 2015;10:e0116511.CrossRefPubMedPubMedCentral Tsivgoulis G, Katsanos AH, Grigoriadis N, Hadjigeorgiou GM, Heliopoulos I, Kilidireas C, et al. The effect of disease modifying therapies on brain atrophy in patients with relapsing-remitting multiple sclerosis: a systematic review and meta-analysis. PLoS One. 2015;10:e0116511.CrossRefPubMedPubMedCentral
33.
go back to reference Khoury SJ, Bakshi R. Cerebral pseudoatrophy or real atrophy after therapy in multiple sclerosis. Ann Neurol. 2010;68:778–9.CrossRefPubMed Khoury SJ, Bakshi R. Cerebral pseudoatrophy or real atrophy after therapy in multiple sclerosis. Ann Neurol. 2010;68:778–9.CrossRefPubMed
34.
go back to reference Ceccarelli A, Rocca MA, Pagani E, Colombo B, Martinelli V, Comi G, et al. Voxel-based morphometry study of grey matter loss in MS patients with different clinical phenotypes. NeuroImage. 2008;42:315–22.CrossRefPubMed Ceccarelli A, Rocca MA, Pagani E, Colombo B, Martinelli V, Comi G, et al. Voxel-based morphometry study of grey matter loss in MS patients with different clinical phenotypes. NeuroImage. 2008;42:315–22.CrossRefPubMed
35.
go back to reference Benedict RH, Ramasamy D, Munschauer F, Weinstock-Guttman B, Zivadinov R. Memory impairment in multiple sclerosis: correlation with deep grey matter and mesial temporal atrophy. J Neurol Neurosurg Psychiatry. 2009;80:201–6.CrossRefPubMed Benedict RH, Ramasamy D, Munschauer F, Weinstock-Guttman B, Zivadinov R. Memory impairment in multiple sclerosis: correlation with deep grey matter and mesial temporal atrophy. J Neurol Neurosurg Psychiatry. 2009;80:201–6.CrossRefPubMed
36.
go back to reference Popescu V, Schoonheim MM, Versteeg A, Chaturvedi N, Jonker M, Xavier de Menezes R, et al. Grey matter atrophy in multiple sclerosis: clinical interpretation depends on choice of analysis method. PLoS One. 2016;11:e0143942.CrossRefPubMedPubMedCentral Popescu V, Schoonheim MM, Versteeg A, Chaturvedi N, Jonker M, Xavier de Menezes R, et al. Grey matter atrophy in multiple sclerosis: clinical interpretation depends on choice of analysis method. PLoS One. 2016;11:e0143942.CrossRefPubMedPubMedCentral
37.
go back to reference Jones BC, Nair G, Shea CD, Crainiceanu CM, Cortese IC, Reich DS. Quantification of multiple-sclerosis-related brain atrophy in two heterogeneous MRI datasets using mixed-effects modeling. Neuroimage Clin. 2013;3:171–9.CrossRefPubMedPubMedCentral Jones BC, Nair G, Shea CD, Crainiceanu CM, Cortese IC, Reich DS. Quantification of multiple-sclerosis-related brain atrophy in two heterogeneous MRI datasets using mixed-effects modeling. Neuroimage Clin. 2013;3:171–9.CrossRefPubMedPubMedCentral
38.
go back to reference Chua AS, Egorova S, Anderson MC, Polgar-Turcsanyi M, Chitnis T, Weiner HL, et al. Handling changes in MRI acquisition parameters in modeling whole brain lesion volume and atrophy data in multiple sclerosis subjects: Comparison of linear mixed-effect models. Neuroimage: Clin. 2015;8:606–10.CrossRef Chua AS, Egorova S, Anderson MC, Polgar-Turcsanyi M, Chitnis T, Weiner HL, et al. Handling changes in MRI acquisition parameters in modeling whole brain lesion volume and atrophy data in multiple sclerosis subjects: Comparison of linear mixed-effect models. Neuroimage: Clin. 2015;8:606–10.CrossRef
Metadata
Title
Automated segmentation of cerebral deep gray matter from MRI scans: effect of field strength on sensitivity and reliability
Authors
Renxin Chu
Shelley Hurwitz
Shahamat Tauhid
Rohit Bakshi
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2017
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-017-0949-4

Other articles of this Issue 1/2017

BMC Neurology 1/2017 Go to the issue