Skip to main content

Advertisement

SpringerLink
Log in

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

  • Neuro
  • Published:
European Radiology Aims and scope Submit manuscript

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

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

PADRE:

Phase difference enhanced imaging

SWI:

Susceptibility-weighted imaging

ALS:

Amyotrophic lateral sclerosis

PLS:

Primary lateral sclerosis

GM:

Gray matter

WM:

White matter

LSIL:

Low-signal-intensity layer

UMN:

Upper motor neuron

LMN:

Lower motor neuron

References

  1. 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 248:850–855

    Article  CAS  PubMed  Google Scholar 

  2. Zinman L, Cudkowicz M (2011) Emerging targets and treatments in amyotrophic lateral sclerosis. Lancet Neurol 10:481–490

    Article  CAS  PubMed  Google Scholar 

  3. 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 17:521–527

    Article  PubMed  Google Scholar 

  4. 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 18:2949–2955

    Article  PubMed  Google Scholar 

  5. 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 21:647–658

    CAS  PubMed  Google Scholar 

  6. Graham J, Papadakis N, Evans J et al (2004) Diffusion tensor imaging for the assessment of upper motor neuron integrity in ALS. Neurology 63:2111–2119

    Article  CAS  PubMed  Google Scholar 

  7. Sach M, Winkler G, Glauche V et al (2004) Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 127:340–350

    Article  PubMed  Google Scholar 

  8. 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 24:1735–1741

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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 25:1413–1420

    Article  PubMed  Google Scholar 

  10. 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. 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 25:710–718

    Article  PubMed  Google Scholar 

  12. 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 26:256–264

    Article  PubMed  Google Scholar 

  13. Haacke EM, Cheng NY, House MJ et al (2005) Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging 23:1–25

    Article  CAS  PubMed  Google Scholar 

  14. Haacke EM, Xu Y, Cheng YCN, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52:612–618

    Article  PubMed  Google Scholar 

  15. 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 21:2202–2210

    Article  PubMed  Google Scholar 

  16. 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 19:1283–1289

    Article  PubMed  Google Scholar 

  17. 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 23:1102–1111

    Article  PubMed  Google Scholar 

  18. 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

    CAS  Google Scholar 

  19. de Carvalho M, Dengler R, Eisen A et al (2008) Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol 119:497–503

    Article  PubMed  Google Scholar 

  20. Gordon P, Cheng B, Katz I et al (2006) The natural history of primary lateral sclerosis. Neurology 66:647–653

    Article  CAS  PubMed  Google Scholar 

  21. 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

  22. Roche JC, Rojas-Garcia R, Scott KM et al (2012) A proposed staging system for amyotrophic lateral sclerosis. Brain 135:847–852

    Article  PubMed  PubMed Central  Google Scholar 

  23. Yousry T, Schmid U, Alkadhi H et al (1997) Localization of the motor hand area to a knob on the precentral gyrus. Brain 120:141–157

    Article  PubMed  Google Scholar 

  24. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  25. Lambert E, Mulder D (1957) Electromyographic studies in amyotrophic lateral sclerosis. Proceedings of the staff meetings Mayo Clinic, pp 441

  26. Kakeda S, Korogi Y, Kamada K et al (2008) Signal intensity of the motor cortex on phase-weighted imaging at 3T. Am J Neuroradiol 29:1171–1175

    Article  CAS  PubMed  Google Scholar 

  27. 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 227:332–339

    Article  PubMed  Google Scholar 

  28. 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. Jones E, Coulter J, Wise S (1979) Commissural columns in the sensory motor cortex of monkeys. J Comp Neurol 188:113–135

    Article  CAS  PubMed  Google Scholar 

  30. Udaka F, Kameyama M, Tomonaga M (1986) Degeneration of Betz cells in motor neuron disease. A Golgi study. Acta Neuropathol 70:289–295

    Article  CAS  PubMed  Google Scholar 

  31. 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, e35241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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. 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 204:1086–1092

    Article  Google Scholar 

Download references

Acknowledgements

The scientific guarantor of this publication is Yukunori Korogi, M.D. The authors of this manuscript declare no relationships with any companies. The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. Methodology: retrospective case-control study performed at one institution.

Author information

Authors and Affiliations

  1. Department of Radiology, University of Occupational and Environmental Health, School of Medicine, 1-1 Iseigaoka, Yahatanishi-ku, Kitakyushu, 807-8555, Japan

    Shingo Kakeda, Satoru Ide, Mari Miyata, Koichiro Futatsuya, Keita Watanabe, Atsushi Ogasawara, Junji Moriya, Toru Sato & Yukunori Korogi

  2. Department of Medical Physics in Advanced Biomedical Sciences, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan

    Tetsuya Yoneda

  3. Department of Neurology, University of Occupational and Environmental Health, School of Medicine, Kitakyushu, Japan

    Tomoyo Hashimoto, Kazumasa Okada & Hiroaki Adachi

  4. Department of Neurology, Wakamatsu Hospital of the University of Occupational and Environmental Health, School of Medicine, Kitakyushu, Japan

    Takenori Uozumi

Authors
  1. Shingo Kakeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tetsuya Yoneda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Satoru Ide
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mari Miyata
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tomoyo Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Koichiro Futatsuya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Keita Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Atsushi Ogasawara
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Junji Moriya
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Toru Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kazumasa Okada
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Takenori Uozumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Hiroaki Adachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yukunori Korogi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shingo Kakeda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kakeda, S., Yoneda, T., Ide, S. et al. Zebra sign of precentral gyri in amyotrophic lateral sclerosis: A novel finding using phase difference enhanced (PADRE) imaging-initial results. Eur Radiol 26, 4173–4183 (2016). https://doi.org/10.1007/s00330-016-4219-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-016-4219-4

Keywords

Search

Navigation