Skip to main content

Advertisement

SpringerLink
Log in

Cardiac sympathetic function in the patients with amyotrophic lateral sclerosis: analysis using cardiac [123I] MIBG scintigraphy

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

Abstract

Amyotrophic lateral sclerosis (ALS), which is the most serious form of degenerative motor neuron disease in adults, is characterized by upper and lower motor neuron degeneration, skeletal muscle atrophy, paralysis, and death. Some patients with respiratory-dependent ALS die of sudden cardiac arrest or anoxic encephalopathy following circulatory collapse, which may be associated with sympathetic hyperactivity. Cardiac [123I] MIBG scintigraphy is a diagnostic method of cardiac sympathetic function. However, few reports have addressed cardiac sympathetic function in ALS patients using this technique. We investigated cardiac sympathetic function in 63 ALS patients and 10 healthy volunteers using cardiac [123I] metaiodobenzylguanidine (MIBG) scintigraphy [heart/mediastinum ratio (H/M ratio) in the early phase and washout ratio (WR)] at the time of diagnosis. The WR of cardiac [123I] MIBG scintigraphy, which indicates cardiac sympathetic activity, was significantly increased in ALS patients compared with controls. ALS patients with an increased WR exhibited a significantly higher progression rate compared with those with normal WR. Moreover, the survival of ALS patients with increased WR was significantly decreased compared with those with normal WR. These results suggested that some patients with ALS have sympathetic hyperactivity at the time of diagnosis. ALS patients may suffer from chronic cardiac sympathetic hyperactivity, which is associated with sudden cardiac death and stress induced cardiomyopathy. Increased WR in cardiac [123I] MIBG scintigraphy may be a predictive factor in ALS patients.

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

Similar content being viewed by others

References

  1. Shimizu T, Hayashi H, Kato S, Hayashi M, Tanabe H, Oda M (1994) Circulatory collapse and sudden death in respirator-dependent amyotrophic lateral sclerosis. J Neurol Sci 124:45–55

    Article  PubMed  CAS  Google Scholar 

  2. Hayashi H, Kato S (1989) Total manifestations of amyotrophic lateral sclerosis. J Neurol Sci 93:19–35

    Article  PubMed  CAS  Google Scholar 

  3. Hayashi H, Kato S, Kawada A (1991) Amyotrophic lateral sclerosis patients living beyond respiratory failure. J Neurol Sci 105:73–78

    Article  PubMed  CAS  Google Scholar 

  4. Hayashi H (1994) Long-term in-hospital ventilatory care for patients with ALS. In: Mitsumoto H, Norris FH (eds) Amyotrophic lateral sclerosis: a comprehensive guide to management. Demos publications, New York, pp 127–138

    Google Scholar 

  5. Ohno T, Shimizu T, Kato S, Hayashi H, Hirai S (2001) Effect of tamsulosin hydrochloride on sympathetic hyperactivity in amyotrophic lateral sclerosis. Auton Neurosci 88:94–98

    Article  PubMed  CAS  Google Scholar 

  6. Baltadzhieva R, Gurevich T, Korczyn AD (2005) Autonomic impairment in amyotrophic lateral sclerosis. Curr Opin Neurol 18:487–493

    Article  PubMed  Google Scholar 

  7. Asai H, Hirano M, Udaka F, Shimada K, Oda M, Kubori T, Nishinaka K, Tsujimura T, Izumi Y, Konishi N, Matsumoto S, Kameyama M, Ueno S (2007) Sympathetic disturbance increase risk of sudden cardiac arrest in sporadic ALS. J Neurol Sci 254:78–83

    Article  PubMed  Google Scholar 

  8. Wieland DM, Brown LE, Rogers WL, Worthington KC, Wu JL, Clinthorne NH, Otto CA, Swanson DP, Beierwaltes WH (1981) Myocardial imaging with a radioiodinated norepinephrine storage analog. J Nucl Med 22:22–31

    PubMed  CAS  Google Scholar 

  9. Sisson JC, Shapiro B, Meyers L, Mallete S, Mangner TJ, Wieland DM, Glowniak JV, Sherman P, Beierwaltes WH (1987) Metaiodobenzyl-guanidine to map scintigraphically the adrenergic nervous system in man. J Nucl Med 28:1625–1636

    PubMed  CAS  Google Scholar 

  10. Sisson JC, Bolgos G, Johnson J (1991) Measuring acute changes in adrenergic nerve activity of the heart in the living animal. Am Heart J 121:1119–1123

    Article  PubMed  CAS  Google Scholar 

  11. Yoshita M (1998) Differentiation of idiopathic Parkinson’s disease from striatonigral degeneration and progressive supranuclear palsy using iodine-123 meta-iodobenzylguanidine myocardial scintigraphy. J Neurol Sci 155:60–67

    Article  PubMed  CAS  Google Scholar 

  12. Braune S, Reinhardt M, Schnitzer R, Riedel A, Lücking CH (1999) Cardiac uptake of [123I] MIBG separates Parkinson’s disease from multiple system atrophy. Neurology 53:1020–1025

    Article  PubMed  CAS  Google Scholar 

  13. Brooks BR (1994) El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on motor neuron diseases/amyotrophic lateral sclerosis of the world federation of neurology research group on neuromuscular diseases and the El Escorial “clinical limits of amyotrophic lateral sclerosis” workshop contributors. J Neurol Sci 124(Suppl):96–107

    Article  PubMed  Google Scholar 

  14. Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, Nakanishi A (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS study group (Phase III). J Neurol Sci 169:13–21

    Article  PubMed  CAS  Google Scholar 

  15. Kimura F, Fujimura C, Ishida S, Nakajima H, Furutama D, Uehara H, Shinoda K, Sugino M, Hanafusa T (2006) Progression rate of ALDFRS-R at time of diagnosis predicts survival time in ALS. Neurology 66:265–267

    Article  PubMed  CAS  Google Scholar 

  16. Ziegler MG, Lake CR, Wood JH (1980) Relationship between cerebrospinal fluid norepinephrine and blood pressure in neurogenic patients. Clin Exp Hypretens 2:995–1008

    Article  CAS  Google Scholar 

  17. Sachs C, Conradi S, Kajiser L (1985) Autonomic function in amyotrophic lateral sclerosis: a study of cardiovascular responses. Acta Neurol Scand 71:373–378

    Article  PubMed  CAS  Google Scholar 

  18. Litchy WJ, Low PA, Daube JR, Windebank AJ (1987) Autonomic abnormalities in amyotrophic lateral sclerosis. Neurology 37(Suppl I):162

    Google Scholar 

  19. Chida K, Sakamaki S, Takasu T (1989) Alteration in autonomic function and cardiovascular regulation in amyotrophic lateral sclerosis. J Neurol 236:127–130

    Article  PubMed  CAS  Google Scholar 

  20. Nogùes MA, Stalberg EV (1989) Autonomic analysis of heart rate variation: II. Findings in patients attending an EMG laboratory. Muscle Nerve 12:1001–1008

    Article  PubMed  Google Scholar 

  21. Tamura N, Shimazu K, Yamamoto T, Watanabe S, Onoda A, Itokawa K, Hamaguchi K (1991) A supplementary study of sympathetic nervous hypertension in motor neuron disease. Auton Nerv Syst 28:357–363 (in Japanese, abstract in English)

    Google Scholar 

  22. Shindo K, Tsunoda S, Shiozawa Z (1995) Increased sympathetic outflow to muscles in patients with amyotrophic lateral sclerosis: a comparison with other neuromuscular patients. J Neurol Sci 134:57–60

    Article  PubMed  CAS  Google Scholar 

  23. Low PA, McLeod JG (1993) The autonomic neuropathies. In: Low PA (ed) Clinical autonomic disorders: evaluation and management. Little Brown, Boston, pp 395–421

    Google Scholar 

  24. Brownell B, Oppenheimer DR, Hughes JT (1970) The central nervous system in motor neurone disease. J Neurol Neurosurg Psychiatry 33:338–357

    Article  PubMed  CAS  Google Scholar 

  25. Kennedy PG, Duchen LW (1985) A quantitative study of intermediolateral column cells in motor neuron disease and the Shy-Drager syndrome. J Neurol Neurosurg Psychiatry 48:1103–1106

    Article  PubMed  CAS  Google Scholar 

  26. Konno H, Yamamoto T, Iwasaki Y, Iizuka H (1986) Shy-Drager syndrome and amyotrophic lateral sclerosis. Cytoarchitectonic and morphometric studies of sacral autonomic neurons. J Neurol Sci 73:193–204

    Article  PubMed  CAS  Google Scholar 

  27. Takahashi H, Oyanagi K, Ikuta F (1993) The intermediolateral nucleus in sporadic amyotrophic lateral sclerosis. Acta Neuropathol (Berl) 86:190–192

    Article  CAS  Google Scholar 

  28. Benarroch EE (1993) The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin Proc 68:988–1001

    Article  PubMed  CAS  Google Scholar 

  29. Cechetto DF, Wilson JX, Smith KE, Wolski D, Silver MD, Hachinski VC (1989) Autonomic and myocardial changes in middle cerebral artery occlusion: stroke models in the rat. Brain Res 502:296–305

    Article  PubMed  CAS  Google Scholar 

  30. Akashi YJ, Nakazawa K, Sakakibara M, Miyake F, Musha H, Sasaka K (2004) 123I-MIBG myocardial scintigraphy in patients with “takotsubo” cardiomyopathy. J Nucl Med 45:1121–1127

    PubMed  Google Scholar 

  31. Nagamachi S, Jinnouchi S, Kurose T, Ohnishi T, Flores LG 2nd, Nakahara H, Futami S, Tamura S, Matsukura S (1998) 123I-MIBG myocardial scintigraphy in diabetic patients: relationship with 201Tl uptake and cardiac autonomic function. Ann Nucl Med 12:323–331

    Article  PubMed  CAS  Google Scholar 

  32. Morimoto S, Terada K, Keira N, Satoda M, Inoue K, Tatsukawa H, Katoh S, Ida K, Sugihara H, Takeda K, Nakagawa M (1996) Investigation of the relationship between regression of hypertensive cardiac hypertrophy and improvement of cardiac sympathetic nervous dysfunction using iodine-123 metaiodobenzylguanidine myocardial imaging. Eur J Nucl Med 23:756–761

    Article  PubMed  CAS  Google Scholar 

  33. Yoshita M, Hayashi M, Hirai S (1998) Decreased myocardial accumulation of 123I-meta-iodobenzyl guanidine in Parkinson’s disease. Nucl Med Commun 19:137–142

    Article  PubMed  CAS  Google Scholar 

  34. Iwasa K, Nakajima K, Yoshikawa H, Tada A, Taki J, Takamori M (1998) Decreased myocardial 123I-MIBG uptake in Parkinson’s disease. Acta Neurol Scand 97:303–306

    Article  PubMed  CAS  Google Scholar 

  35. Braune S, Reinhardt M, Bathmann J, Krause T, Lehmann M, Lucking CH (1998) Impaired cardiac uptake of meta- [123 I] iodobenzylguanidine in Parkinson’s disease with autonomic failure. Acta Neurol Scand 97:307–314

    Article  PubMed  CAS  Google Scholar 

  36. Satoh A, Serita T, Seto M, Tomita I, Satoh H, Iwanaga K, Takahashi H, Tsujihata M (1999) Loss of 123I-MIBG uptake by the heart in Parkinson’s disease: assessment of cardiac sympathetic denervation and diagnostic value. J Nucl Med 40:371–375

    PubMed  CAS  Google Scholar 

  37. Orimo S, Ozawa E, Nakade S, Sugimato T, Mizusawa H (1999) (123)I- metaiodobenzylguanidine myocardial scintigraphy in Parkinson’s disease. J Neurol Neurosurg Psychiatry 67:189–194

    Article  PubMed  CAS  Google Scholar 

  38. Takatsu H, Nishida H, Matsuo H, Watanabe S, Nagashima K, Wada H, Noda T, Nishigaki K, Fujiwara H (2000) Cardiac sympathetic denervation from the early stage of Parkinson’s disease: clinical and experimental studies with radiolabeled MIBG. J Nucl Med 41:71–77

    PubMed  CAS  Google Scholar 

  39. Taki J, Nakajima K, Hwang EH, Matsunari I, Komai K, Yoshita M, Sakajiri K, Tonami N (2000) Peripheral sympathetic dysfunction in patients with Parkinson’s disease without autonomic failure is heart selective and disease specific. Eur J Nucl Med 27:566–573

    Article  PubMed  CAS  Google Scholar 

  40. Hamada K, Hirayama M, Watanabe H, Kobayashi R, Ito H, Ieda T, Koike Y, Sobue G (2003) Onset age and severity of motor impairment are associated with reduction of myocardial 123I-MIBG uptake in Parkinson’s disease. J Neurol Neurosurg Psychiatry 74:423–426

    Article  PubMed  CAS  Google Scholar 

  41. Orimo S, Ozawa E, Oka T, Nakade S, Tsuchiya K, Yoshimoto M, Wakabayashi K, Takahashi H (2001) Different histopathology accounting for a decrease in myocardial MIBG uptake in PD and MSA. Neurology 57:1140–1141

    Article  PubMed  CAS  Google Scholar 

  42. Orimo S, Oka T, Miura H, Tsuchiya K, Mori F, Wakabayashi K, Nagao T, Yokochi M (2002) Sympathetic cardiac denervation in Parkinson’s disease and pure autonomic failure but not in multiple system atrophy. J Neurol Neurosurg Psychiatry 73:776–777

    Article  PubMed  CAS  Google Scholar 

  43. Amino T, Orimo S, Itoh Y, Takahashi A, Uchihara T, Mizusawa H (2005) Profound cardiac sympathetic denervation occurs in Parkinson disease. Brain Pathol 15:29–34

    Article  PubMed  Google Scholar 

  44. Orimo S, Amino T, Itoh Y, Takahashi A, Kojo T, Uchihara T, Tsuchiya K, Mori F, Wakabayashi K, Takahashi H (2005) Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease. Acta Neuropathol 109:583–588

    Article  PubMed  Google Scholar 

  45. Druschky A, Spitzer A, Platsch G, Claus D, Feistel H, Druschky K, Hilz MJ, Neundorfer B (1999) Cardiac sympathetic denervation in early stages of amyotrophic lateral sclerosis demonstrated by 123I-MIBG-SPECT. Acta Neurol Scand 99:308–314

    Article  PubMed  CAS  Google Scholar 

  46. Tanaka Y, Yoshikura N, Harada N, Yamada M, Koumura A, Sakurai T, Hayashi Y, Kimura A, Hozumi I, Inuzuka T (2012) Late-onset patients with sporadic amyotrophic lateral sclerosis in Japan have a higher progression rate of ALSFRS-R at the time of diagnosis. Intern Med 51:579–584

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

The authors state that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Neurology and Geriatrics, Graduate School of Medicine, Gifu University, 1-1 Yanagido, Gifu, Gifu Prefecture, 501-1194, Japan

    Yuji Tanaka, Megumi Yamada, Akihiro Koumura, Takeo Sakurai, Yuichi Hayashi, Akio Kimura, Isao Hozumi & Takashi Inuzuka

Authors
  1. Yuji Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Megumi Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akihiro Koumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takeo Sakurai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuichi Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Akio Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Isao Hozumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Takashi Inuzuka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuji Tanaka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tanaka, Y., Yamada, M., Koumura, A. et al. Cardiac sympathetic function in the patients with amyotrophic lateral sclerosis: analysis using cardiac [123I] MIBG scintigraphy. J Neurol 260, 2380–2386 (2013). https://doi.org/10.1007/s00415-013-7005-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-013-7005-0

Keywords

Search

Navigation