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Published in: European Radiology 11/2016

01-11-2016 | Neuro

Zebra sign of precentral gyri in amyotrophic lateral sclerosis: A novel finding using phase difference enhanced (PADRE) imaging-initial results

Authors: Shingo Kakeda, Tetsuya Yoneda, Satoru Ide, Mari Miyata, Tomoyo Hashimoto, Koichiro Futatsuya, Keita Watanabe, Atsushi Ogasawara, Junji Moriya, Toru Sato, Kazumasa Okada, Takenori Uozumi, Hiroaki Adachi, Yukunori Korogi

Published in: European Radiology | Issue 11/2016

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Abstract

Objective

We compared the precentral gyri (PG) on the PADRE of patients with amyotrophic lateral sclerosis (ALS) and healthy subjects (HSs) in order to determine whether it is possible to discriminate between ALS patients and HSs on an individual basis.

Methods

First, two radiologists reviewed the appearance of the normal PG and that of ALS patients on PADRE in a non-blinded manner, and deviations from the appearance of the normal PG were recorded. Next, based on the presence of PG abnormalities on PADRE, we performed an observer performance study using 16 ALS patients and 16 HSs.

Results

The radiologists were able to consensually define the PG as abnormal on PADRE when a low-signal-intensity layer was observed in the gray matter of the PG; a three- or four-layer organization (zebra sign) was characterized by the low-signal-intensity layer. The observer performance study demonstrated that the sensitivity, specificity, and accuracy of PG abnormalities on PADRE for discriminating ALS patients from HSs were 94 %, 94 %, and 94 %, respectively, for reviewers 1 and 2.

Conclusions

It was possible to discriminate between ALS patients and HSs based on the presence of PG abnormalities on PADRE, which may reflect upper motor neuron impairment in ALS.

Key Points

PADRE reveals low-signal-intensity layer in the PG of ALS
By PADRE findings on PG, we can discriminate ALS from HSs
PADRE may be a useful method for detecting UMN impairment in ALS
Literature
1.
go back to reference Urban PP, Wicht S, Hopf H (2001) Sensitivity of transcranial magnetic stimulation of cortico-bulbar vs. cortico-spinal tract involvement in Amyotrophic Lateral Sclerosis (ALS). J Neurol 248:850–855CrossRefPubMed Urban PP, Wicht S, Hopf H (2001) Sensitivity of transcranial magnetic stimulation of cortico-bulbar vs. cortico-spinal tract involvement in Amyotrophic Lateral Sclerosis (ALS). J Neurol 248:850–855CrossRefPubMed
2.
go back to reference Zinman L, Cudkowicz M (2011) Emerging targets and treatments in amyotrophic lateral sclerosis. Lancet Neurol 10:481–490CrossRefPubMed Zinman L, Cudkowicz M (2011) Emerging targets and treatments in amyotrophic lateral sclerosis. Lancet Neurol 10:481–490CrossRefPubMed
3.
go back to reference Zhang L, Uluǧ AM, Zimmerman RD, Lin MT, Rubin M, Beal MF (2003) The diagnostic utility of FLAIR imaging in clinically verified amyotrophic lateral sclerosis. J Magn Reson Imaging 17:521–527CrossRefPubMed Zhang L, Uluǧ AM, Zimmerman RD, Lin MT, Rubin M, Beal MF (2003) The diagnostic utility of FLAIR imaging in clinically verified amyotrophic lateral sclerosis. J Magn Reson Imaging 17:521–527CrossRefPubMed
4.
go back to reference Kamada K, Kakeda S, Ohnari N, Moriya J, Sato T, Korogi Y (2008) Signal intensity of motor and sensory cortices on T2-weighted and FLAIR images: intraindividual comparison of 1.5 T and 3T MRI. Eur Radiol 18:2949–2955CrossRefPubMed Kamada K, Kakeda S, Ohnari N, Moriya J, Sato T, Korogi Y (2008) Signal intensity of motor and sensory cortices on T2-weighted and FLAIR images: intraindividual comparison of 1.5 T and 3T MRI. Eur Radiol 18:2949–2955CrossRefPubMed
5.
go back to reference Bowen BC, Pattany PM, Bradley WG et al (2000) MR imaging and localized proton spectroscopy of the precentral gyrus in amyotrophic lateral sclerosis. Am J Neuroradiol 21:647–658PubMed Bowen BC, Pattany PM, Bradley WG et al (2000) MR imaging and localized proton spectroscopy of the precentral gyrus in amyotrophic lateral sclerosis. Am J Neuroradiol 21:647–658PubMed
6.
go back to reference Graham J, Papadakis N, Evans J et al (2004) Diffusion tensor imaging for the assessment of upper motor neuron integrity in ALS. Neurology 63:2111–2119CrossRefPubMed Graham J, Papadakis N, Evans J et al (2004) Diffusion tensor imaging for the assessment of upper motor neuron integrity in ALS. Neurology 63:2111–2119CrossRefPubMed
7.
go back to reference Sach M, Winkler G, Glauche V et al (2004) Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 127:340–350CrossRefPubMed Sach M, Winkler G, Glauche V et al (2004) Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 127:340–350CrossRefPubMed
8.
go back to reference Weisstanner C, Gratz PP, Schroth G et al (2014) Thrombus imaging in acute stroke: correlation of thrombus length on susceptibility-weighted imaging with endovascular reperfusion success. Eur Radiol 24:1735–1741CrossRefPubMedPubMedCentral Weisstanner C, Gratz PP, Schroth G et al (2014) Thrombus imaging in acute stroke: correlation of thrombus length on susceptibility-weighted imaging with endovascular reperfusion success. Eur Radiol 24:1735–1741CrossRefPubMedPubMedCentral
9.
go back to reference Fu J-H, Chuang T-C, Chung H-W et al (2015) Discriminating pyogenic brain abscesses, necrotic glioblastomas, and necrotic metastatic brain tumors by means of susceptibility-weighted imaging. Eur Radiol 25:1413–1420CrossRefPubMed Fu J-H, Chuang T-C, Chung H-W et al (2015) Discriminating pyogenic brain abscesses, necrotic glioblastomas, and necrotic metastatic brain tumors by means of susceptibility-weighted imaging. Eur Radiol 25:1413–1420CrossRefPubMed
10.
go back to reference Ogasawara A, Kakeda S, Watanabe K et al (2015) Quantitative susceptibility mapping in patients with systemic lupus erythematosus: detection of abnormalities in normal-appearing basal ganglia. Eur Radiol :1–8 Ogasawara A, Kakeda S, Watanabe K et al (2015) Quantitative susceptibility mapping in patients with systemic lupus erythematosus: detection of abnormalities in normal-appearing basal ganglia. Eur Radiol :1–8
11.
go back to reference Ide S, Kakeda S, Ueda I et al (2015) Internal structures of the globus pallidus in patients with Parkinson’s disease: evaluation with quantitative susceptibility mapping (QSM). Eur Radiol 25:710–718CrossRefPubMed Ide S, Kakeda S, Ueda I et al (2015) Internal structures of the globus pallidus in patients with Parkinson’s disease: evaluation with quantitative susceptibility mapping (QSM). Eur Radiol 25:710–718CrossRefPubMed
12.
go back to reference 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 26:256–264CrossRefPubMed 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 26:256–264CrossRefPubMed
13.
go back to reference Haacke EM, Cheng NY, House MJ et al (2005) Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging 23:1–25CrossRefPubMed Haacke EM, Cheng NY, House MJ et al (2005) Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging 23:1–25CrossRefPubMed
14.
go back to reference Haacke EM, Xu Y, Cheng YCN, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52:612–618CrossRefPubMed Haacke EM, Xu Y, Cheng YCN, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52:612–618CrossRefPubMed
15.
go back to reference Kakeda S, Korogi Y, Yoneda T et al (2011) A novel tract imaging technique of the brainstem using phase difference enhanced imaging: normal anatomy and initial experience in multiple system atrophy. Eur Radiol 21:2202–2210CrossRefPubMed Kakeda S, Korogi Y, Yoneda T et al (2011) A novel tract imaging technique of the brainstem using phase difference enhanced imaging: normal anatomy and initial experience in multiple system atrophy. Eur Radiol 21:2202–2210CrossRefPubMed
16.
go back to reference Ide S, Kakeda S, Korogi Y et al (2012) Delineation of optic radiation and stria of gennari on high-resolution phase difference enhanced imaging. Acad Radiol 19:1283–1289CrossRefPubMed Ide S, Kakeda S, Korogi Y et al (2012) Delineation of optic radiation and stria of gennari on high-resolution phase difference enhanced imaging. Acad Radiol 19:1283–1289CrossRefPubMed
17.
go back to reference Kakeda S, Korogi Y, Yoneda T et al (2013) Parkinson’s disease: diagnostic potential of high-resolution phase difference enhanced MR imaging at 3 T. Eur Radiol 23:1102–1111CrossRefPubMed Kakeda S, Korogi Y, Yoneda T et al (2013) Parkinson’s disease: diagnostic potential of high-resolution phase difference enhanced MR imaging at 3 T. Eur Radiol 23:1102–1111CrossRefPubMed
18.
go back to reference Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler 1:293–299 Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler 1:293–299
19.
go back to reference de Carvalho M, Dengler R, Eisen A et al (2008) Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol 119:497–503CrossRefPubMed de Carvalho M, Dengler R, Eisen A et al (2008) Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol 119:497–503CrossRefPubMed
20.
go back to reference Gordon P, Cheng B, Katz I et al (2006) The natural history of primary lateral sclerosis. Neurology 66:647–653CrossRefPubMed Gordon P, Cheng B, Katz I et al (2006) The natural history of primary lateral sclerosis. Neurology 66:647–653CrossRefPubMed
21.
go back to reference Balendra R, Jones A, Jivraj N et al (2014) Use of clinical staging in amyotrophic lateral sclerosis for phase 3 clinical trials. J Neurol Neurosurg Psychiatry :jnnp-2013-306865 Balendra R, Jones A, Jivraj N et al (2014) Use of clinical staging in amyotrophic lateral sclerosis for phase 3 clinical trials. J Neurol Neurosurg Psychiatry :jnnp-2013-306865
23.
go back to reference Yousry T, Schmid U, Alkadhi H et al (1997) Localization of the motor hand area to a knob on the precentral gyrus. Brain 120:141–157CrossRefPubMed Yousry T, Schmid U, Alkadhi H et al (1997) Localization of the motor hand area to a knob on the precentral gyrus. Brain 120:141–157CrossRefPubMed
24.
go back to reference Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMed Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMed
25.
go back to reference Lambert E, Mulder D (1957) Electromyographic studies in amyotrophic lateral sclerosis. Proceedings of the staff meetings Mayo Clinic, pp 441 Lambert E, Mulder D (1957) Electromyographic studies in amyotrophic lateral sclerosis. Proceedings of the staff meetings Mayo Clinic, pp 441
26.
go back to reference Kakeda S, Korogi Y, Kamada K et al (2008) Signal intensity of the motor cortex on phase-weighted imaging at 3T. Am J Neuroradiol 29:1171–1175CrossRefPubMed Kakeda S, Korogi Y, Kamada K et al (2008) Signal intensity of the motor cortex on phase-weighted imaging at 3T. Am J Neuroradiol 29:1171–1175CrossRefPubMed
27.
go back to reference Tong KA, Ashwal S, Holshouser BA et al (2003) Hemorrhagic shearing lesions in children and adolescents with posttraumatic diffuse axonal injury: improved detection and initial results 1. Radiology 227:332–339CrossRefPubMed Tong KA, Ashwal S, Holshouser BA et al (2003) Hemorrhagic shearing lesions in children and adolescents with posttraumatic diffuse axonal injury: improved detection and initial results 1. Radiology 227:332–339CrossRefPubMed
28.
go back to reference Kakeda S, Yoneda T, Ide S, Watanabe K, Hiai Y, Korogi Y (2015) Signal intensity of superficial white matter on phase difference enhanced imaging as a landmark of the perirolandic cortex. Acta Radiol :0284185115585162 Kakeda S, Yoneda T, Ide S, Watanabe K, Hiai Y, Korogi Y (2015) Signal intensity of superficial white matter on phase difference enhanced imaging as a landmark of the perirolandic cortex. Acta Radiol :0284185115585162
29.
go back to reference Jones E, Coulter J, Wise S (1979) Commissural columns in the sensory motor cortex of monkeys. J Comp Neurol 188:113–135CrossRefPubMed Jones E, Coulter J, Wise S (1979) Commissural columns in the sensory motor cortex of monkeys. J Comp Neurol 188:113–135CrossRefPubMed
30.
go back to reference Udaka F, Kameyama M, Tomonaga M (1986) Degeneration of Betz cells in motor neuron disease. A Golgi study. Acta Neuropathol 70:289–295CrossRefPubMed Udaka F, Kameyama M, Tomonaga M (1986) Degeneration of Betz cells in motor neuron disease. A Golgi study. Acta Neuropathol 70:289–295CrossRefPubMed
31.
go back to reference Kwan JY, Jeong SY, Van Gelderen P et al (2012) Iron accumulation in deep cortical layers accounts for MRI signal abnormalities in ALS: correlating 7 Tesla MRI and pathology. PLoS One 7, e35241CrossRefPubMedPubMedCentral Kwan JY, Jeong SY, Van Gelderen P et al (2012) Iron accumulation in deep cortical layers accounts for MRI signal abnormalities in ALS: correlating 7 Tesla MRI and pathology. PLoS One 7, e35241CrossRefPubMedPubMedCentral
32.
go back to reference Yu J, Qi F, Wang N et al (2014) Increased iron level in motor cortex of amyotrophic lateral sclerosis patients: an in vivo MR study. Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration :1–5 Yu J, Qi F, Wang N et al (2014) Increased iron level in motor cortex of amyotrophic lateral sclerosis patients: an in vivo MR study. Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration :1–5
33.
go back to reference Schweitzer AD, Liu T, Gupta A et al (2015) Quantitative susceptibility mapping of the motor cortex in amyotrophic lateral sclerosis and primary lateral sclerosis. Am J Roentgenol 204:1086–1092CrossRef Schweitzer AD, Liu T, Gupta A et al (2015) Quantitative susceptibility mapping of the motor cortex in amyotrophic lateral sclerosis and primary lateral sclerosis. Am J Roentgenol 204:1086–1092CrossRef
Metadata
Title
Zebra sign of precentral gyri in amyotrophic lateral sclerosis: A novel finding using phase difference enhanced (PADRE) imaging-initial results
Authors
Shingo Kakeda
Tetsuya Yoneda
Satoru Ide
Mari Miyata
Tomoyo Hashimoto
Koichiro Futatsuya
Keita Watanabe
Atsushi Ogasawara
Junji Moriya
Toru Sato
Kazumasa Okada
Takenori Uozumi
Hiroaki Adachi
Yukunori Korogi
Publication date
01-11-2016
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 11/2016
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-016-4219-4

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