Skip to main content
SpringerLink
Log in

Hirayama disease is a pure spinal motor neuron disorder—a combined DTI and transcranial magnetic stimulation study

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Hirayama disease (HirD) is a juvenile spinal muscular atrophy predominantly affecting young men with an initially progressive course followed by a stable plateau within several years. It is a matter of debate whether HirD is a widespread motor neuron or more focal cervical cord disease. Whether the supraspinal pathways of the corticospinal tract (CST) are also affected has not been studied systematically. We analyzed CST integrity in seven HirD patients and 11 controls of similar age and gender using diffusion tensor imaging at a 1.5-T scanner and central motor conduction time (CMCT) using transcranial magnetic stimulation. The apparent diffusion coefficient, fractional anisotropy, and axial and radial diffusivity coefficients were determined bilaterally at four representative CST levels and along the whole CST using a probabilistic fiber tracking approach. There were no differences between the initially affected and the contralateral side in HirD patients and no difference between HirD patients and controls for both the ROI-based and the whole CST analyses. Radial diffusivity of the CST was positively correlated with years of disease progression in HirD patients. CMCT was normal in HirD patients. Combined anatomical and functional measurements established normal integrity of the supraspinal CST in HirD patients lending support to the notion that HirD is a pure spinal motor neuron disorder.

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

Similar content being viewed by others

References

  1. Hirayama K, Tsubaki T, Toyokura Y, Okinaka S (1963) Juvenile muscular atrophy of unilateral upper extremity. Neurology 13:373–380

    Article  PubMed  CAS  Google Scholar 

  2. Hirayama K (2000) Juvenile muscular atrophy of distal upper extremity (Hirayama disease). Intern Med 39:283–290

    Article  PubMed  CAS  Google Scholar 

  3. Tashiro K, Kikuchi S, Itoyama Y, Tokumaru Y, Sobue G, Mukai E, Akiguchi I, Nakashima K, Kira JI, Hirayama K (2006) Nationwide survey of juvenile muscular atrophy of distal upper extremity (Hirayama disease) in Japan. Amyotroph Lateral Scler 7:38–45

    Article  PubMed  Google Scholar 

  4. Gourie-Devi M, Suresh TG, Shankar SK (1984) Monomelic amyotrophy. Arch Neurol 41:388–394

    Article  PubMed  CAS  Google Scholar 

  5. Hashimoto O, Asada M, Ohta M, Kuroiwa Y (1976) Clinical observations of juvenile nonprogressive muscular atrophy localized in hand and forearm. J Neurol 211:105–110

    Article  PubMed  CAS  Google Scholar 

  6. Sakai K, Ono K, Okamoto Y, Murakami H, Yamada M (2011) Cervical flexion myelopathy in a patient showing apparent long tract signs: a severe form of Hirayama disease. Joint Bone Spine 78:316–318

    Article  PubMed  Google Scholar 

  7. Sonwalkar HA, Shah RS, Khan FK, Gupta AK, Bodhey NK, Vottath S, Purkayastha S (2008) Imaging features in Hirayama disease. Neurol India 56:22–26

    Article  PubMed  Google Scholar 

  8. Iwasaki Y, Tashiro K, Kikuchi S, Kitagawa M, Isu T, Abe H (1987) Cervical flexion myelopathy: a “tight dural canal mechanism”. Case report. J Neurosurg 66:935–937

    Article  PubMed  CAS  Google Scholar 

  9. Konno S, Goto S, Murakami M, Mochizuki M, Motegi H, Moriya H (1997) Juvenile amyotrophy of the distal upper extremity: pathologic findings of the dura mater and surgical management. Spine 22:486–492

    Article  PubMed  CAS  Google Scholar 

  10. Chen CJ, Chen CM, Wu CL, Ro LS, Chen ST, Lee TH (1998) Hirayama disease: MR diagnosis. AJNR Am J Neuroradiol 19:365–368

    PubMed  CAS  Google Scholar 

  11. Chen CJ, Hsu HL, Tseng YC, Lyu RK, Chen CM, Huang YC, Wang LJ, Wong YC, See LC (2004) Hirayama flexion myelopathy: neutral-position MR imaging findings—importance of loss of attachment. Radiology 231:39–44

    Article  PubMed  Google Scholar 

  12. Ammendola A, Gallo A, Iannaccone T, Tedeschi G (2008) Hirayama disease: three cases assessed by F wave, somatosensory and motor evoked potentials and magnetic resonance imaging not supporting flexion myelopathy. Neurol Sci 29:303–311

    Article  PubMed  Google Scholar 

  13. Willeit J, Kiechl S, Kiechl-Kohlendorfer U, Golaszewski S, Peer S, Poewe W (2001) Juvenile asymmetric segmental spinal muscular atrophy (Hirayama’s disease): three cases without evidence of “flexion myelopathy”. Acta Neurol Scand 104:320–322

    Article  PubMed  CAS  Google Scholar 

  14. Robberecht W, Aguirre T, Van den Bosch L, Theys P, Nees H, Cassiman JJ, Matthijs G (1997) Familial juvenile focal amyotrophy of the upper extremity (Hirayama disease). Superoxide dismutase 1 genotype and activity. Arch Neurol 54:46–50

    Article  PubMed  CAS  Google Scholar 

  15. Schroder R, Keller E, Flacke S, Schmidt S, Pohl C, Klockgether T, Schlegel U (1999) MRI findings in Hirayama’s disease: flexion-induced cervical myelopathy or intrinsic motor neuron disease? J Neurol 246:1069–1074

    Article  PubMed  CAS  Google Scholar 

  16. Misra UK, Kalita J, Mishra VN, Phadke RV, Hadique A (2006) Effect of neck flexion on F wave, somatosensory evoked potentials, and magnetic resonance imaging in Hirayama disease. J Neurol Neurosurg Psychiatry 77:695–698

    Article  PubMed  CAS  Google Scholar 

  17. Schlegel U, Jerusalem F, Tackmann W, Cordt A, Tsuda Y (1987) Benign juvenile focal muscular atrophy of upper extremities—a familial case. J Neurol Sci 80:351–353

    Article  PubMed  CAS  Google Scholar 

  18. Hirayama K (1991) Non-progressive juvenile spinal muscular atrophy of the distal upper limb (Hirayama disease). In: Jong JD (ed) Handbook of clinical neurology. Elsevier, Amsterdam, pp 107–120

    Google Scholar 

  19. Bodammer N, Kaufmann J, Kanowski M, Tempelmann C (2004) Eddy current correction in diffusion-weighted imaging using pairs of images acquired with opposite diffusion gradient polarity. Magn Reson Med 51:188–193

    Article  PubMed  Google Scholar 

  20. Papadakis NG, Xing D, Huang CL, Hall LD, Carpenter TA (1999) A comparative study of acquisition schemes for diffusion tensor imaging using MRI. J Magn Reson 137:67–82

    Article  PubMed  CAS  Google Scholar 

  21. Woods RP, Grafton ST, Holmes CJ, Cherry SR, Mazziotta JC (1998) Automated image registration: I general methods and intrasubject, intramodality validation. J Comput Assist Tomogr 22:139–152

    Article  PubMed  CAS  Google Scholar 

  22. Pajevic S, Pierpaoli C (1999) Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med 42:526–540

    Article  PubMed  CAS  Google Scholar 

  23. Bodammer NC, Kaufmann J, Kanowski M, Tempelmann C (2009) Monte Carlo-based diffusion tensor tractography with a geometrically corrected voxel-centre connecting method. Phys Med Biol 54:1009–1033

    Article  PubMed  CAS  Google Scholar 

  24. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546

    Article  PubMed  Google Scholar 

  25. Mori S, Oishi K, Faria AV (2009) White matter atlases based on diffusion tensor imaging. Curr Opin Neurol 22:362–369

    Article  PubMed  Google Scholar 

  26. Glenn OA, Ludeman NA, Berman JI, Wu YW, Lu Y, Bartha AI, Vigneron DB, Chung SW, Ferriero DM, Barkovich AJ, Henry RG (2007) Diffusion tensor MR imaging tractography of the pyramidal tracts correlates with clinical motor function in children with congenital hemiparesis. AJNR Am J Neuroradiol 28:1796–1802

    Article  PubMed  CAS  Google Scholar 

  27. Pradhan S (2009) Bilaterally symmetric form of Hirayama disease. Neurology 72:2083–2089

    Article  PubMed  Google Scholar 

  28. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436

    Article  PubMed  Google Scholar 

  29. Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, Song SK, Cross AH, Benzinger TL (2011) Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. Neuroimage 55:1454–1460

    Article  PubMed  Google Scholar 

  30. Gallo A, Rocca MA, Tortorella P, Ammendola A, Tedeschi G, Filippi M (2006) A multiparametric brain and cord MR imaging study of a patient with Hirayama disease. AJNR Am J Neuroradiol 27:2115–2117

    PubMed  CAS  Google Scholar 

  31. Misra UK, Kalita J (1995) Central motor conduction in Hirayama disease. Electroencephalogr Clin Neurophysiol 97:73–76

    Article  PubMed  CAS  Google Scholar 

  32. Rigamonti A, Usai S, Curone M, D’Amico D, Bussone G (2004) Hirayama disease: description of an Italian case. Neurol Sci 25:102–103

    Article  PubMed  CAS  Google Scholar 

  33. Polo A, Curro’ Dossi M, Fiaschi A, Zanette GP, Rizzuto N (2003) Peripheral and segmental spinal abnormalities of median and ulnar somatosensory evoked potentials in Hirayama’s disease. J Neurol Neurosurg Psychiatry 74:627–632

    Article  PubMed  CAS  Google Scholar 

  34. Chiba S, Yonekura K, Nonaka M, Imai T, Matumoto H, Wada T (2004) Advanced Hirayama disease with successful improvement of activities of daily living by operative reconstruction. Intern Med 43:79–81

    Article  PubMed  Google Scholar 

  35. Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, Buchel C, Weiller C (2004) Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 127:340–350

    Article  PubMed  Google Scholar 

  36. Cosottini M, Giannelli M, Siciliano G, Lazzarotti G, Michelassi MC, Del Corona A, Bartolozzi C, Murri L (2005) Diffusion-tensor MR imaging of corticospinal tract in amyotrophic lateral sclerosis and progressive muscular atrophy. Radiology 237:258–264

    Article  PubMed  Google Scholar 

  37. Hirayama K, Tomonaga M, Kitano K, Yamada T, Kojima S, Arai K (1987) Focal cervical poliopathy causing juvenile muscular atrophy of distal upper extremity: a pathological study. J Neurol Neurosurg Psychiatry 50:285–290

    Article  PubMed  CAS  Google Scholar 

  38. Desai JA, Melanson M (2011) Teaching neuroimages: anterior horn cell hyperintensity in Hirayama disease. Neurology 77:e73

    Article  PubMed  Google Scholar 

  39. Routal RV, Pal GP (1999) A study of motoneuron groups and motor columns of the human spinal cord. J Anat 195:211–224

    Article  PubMed  Google Scholar 

  40. Romanes GJ (1964) The motor pools of the spinal cord. Prog Brain Res 11:93–119

    Article  PubMed  CAS  Google Scholar 

  41. Sharrard WJ (1955) The distribution of the permanent paralysis in the lower limb in poliomyelitis; a clinical and pathological study. J Bone Joint Surg Br 37:540–558

    PubMed  Google Scholar 

  42. Munchau A, Rosenkranz T (2000) Benign monomelic amyotrophy of the lower limb—case report and brief review of the literature. Eur Neurol 43:238–240

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

All authors declare no conflicts of interest in respect to the content of this article.

Ethical standards

All human studies must state that they have been approved by the appropriate ethics committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

Author information

Authors and Affiliations

  1. Department of Psychiatry, Memory Clinic, University Hospital Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany

    Kai Boelmans

  2. Department of Neurology, Otto-von-Guericke-University, Magdeburg, Germany

    Kai Boelmans, Jörn Kaufmann & Stefan Vielhaber

  3. Department of Neurology, University Hospital Hamburg-Eppendorf, Hamburg, Germany

    Alexander Münchau

  4. Department of Neurology, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany

    Sophie Schmelzer, Malte Kornhuber, Stephan Zierz & Charly Gaul

Authors
  1. Kai Boelmans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jörn Kaufmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sophie Schmelzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Vielhaber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Malte Kornhuber
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexander Münchau
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stephan Zierz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Charly Gaul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kai Boelmans.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boelmans, K., Kaufmann, J., Schmelzer, S. et al. Hirayama disease is a pure spinal motor neuron disorder—a combined DTI and transcranial magnetic stimulation study. J Neurol 260, 540–548 (2013). https://doi.org/10.1007/s00415-012-6674-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-012-6674-4

Keywords

Search

Navigation