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01-06-2005 | Regular Paper

Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease

Authors: Satoshi Orimo, Takeshi Amino, Yoshinori Itoh, Atsushi Takahashi, Tohru Kojo, Toshiki Uchihara, Kuniaki Tsuchiya, Fumiaki Mori, Koichi Wakabayashi, Hitoshi Takahashi

Published in: Acta Neuropathologica | Issue 6/2005

Abstract

Decreased cardiac uptake of meta-iodobenzylguanidine (MIBG) on [¹²³I]MIBG myocardial scintigraphy has been reported in Parkinson’s disease (PD) and dementia with Lewy bodies (DLB). We hypothesized that cardiac sympathetic denervation might account for the pathomechanism. To elucidate the extent, frequency and pattern of cardiac sympathetic nerve involvement in Lewy body disease and related neurodegenerative disorders, we immunohistochemically examined heart tissues from patients with PD (n=11), DLB (n=7), DLB with Alzheimer’s disease (DLB/AD; n=4), multiple system atrophy (MSA; n=8), progressive supranuclear palsy (PSP; n=5), pure AD (n=10) and control subjects (n=5) together with sympathetic ganglia from patients with PD (n=5) and control subjects (n=4), using an antibody against tyrosine hydroxylase (TH). TH-immunoreactive nerve fibers in the hearts had almost entirely disappeared in nearly all the patients with PD, DLB and DLB/AD, whereas they were well preserved in all the patients with PSP and pure AD as well as in all except for one patient with MSA. In PD, neurons in the sympathetic ganglia were preserved in all except for one patient. Decreased cardiac uptake of MIBG in Lewy body disease reflects actual cardiac sympathetic denervation, which precedes the neuronal loss in the sympathetic ganglia.

Algotsson A, Viitanen M, Winblad B, Solders G (1995) Autonomic dysfunction in Alzheimer’s disease. Acta Neurol Scand 91:14–18PubMed

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

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

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 53:1020–1025PubMed

Druschky A, Hilz MJ, Platsch G, Radespiel-Tröger M Drushky K, Kuwert T, Neundörfer B (2000) Differentiation of Parkinson’s disease and multiple system atrophy in early disease stages by means of I-123-MIBG-SPECT. J Neurol Sci 175:3–12CrossRefPubMed

Giubilei F, Strano S, Imbimbo BP, Tisei P, Calcagnini G, Lino S, Frontoni M, Santini M, Fieschi C (1998) Cardiac autonomic dysfunction in patients with Alzheimer disease: possible pathogenetic mechanisms. Alzheimer Dis Assoc Disord 12:356–361PubMed

Goldstein DS, Holmes C, Li S-T, Bruce S, Metman LV, Cannon RO III (2000) Cardiac sympathetic denervation in Parkinson disease. Ann Intern Med 133:338–347PubMed

Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, McKee A, Tabaton M, Litvan I (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44:2015–2019PubMed

Horimoto Y, Matsumoto M, Akatsu H, Ikari H, Kojima K, Yamamoto T, Otsuka Y, Ojika K, Ueda R, Kosaka K (2003) Autonomic dysfunctions in dementia with Lewy bodies. J Neurol 250:530–533CrossRefPubMed

10.

Iwanaga K, Wakabayashi K, Yoshimoto M, Tomita I, Satoh H, Takashima H, Satoh A, Seto M, Tsujihata M, Takahashi H (1999) Lewy body-type degeneration in cardiac plexus in Parkinson’s and incidental Lewy body diseases. Neurology 52:1269–1271PubMed

11.

Kawano H, Okada R, Yano K (2003) Histological study on the distribution of autonomic nerves in the human heart. Heart Vessels 18:32–39CrossRefPubMed

12.

Kimber J, Mathias CJ, Lees AJ, Bleasdale-Barr K, Chang HS, Churchyard A, Watson L (2000) Physiological, pharmacological and neurohormonal assessment of autonomic function in progressive supranuclear palsy. Brain 123:1422–1430CrossRefPubMed

13.

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 73:193–204CrossRefPubMed

14.

Kosaka K (1990) Diffuse Lewy body disease in Japan. J Neurol 237:197–204CrossRefPubMed

15.

Matthews MR (1992) Autonomic ganglia in multiple system atrophy and pure autonomic failure. In: Bannister R, Mathias CJ (eds) Autonomic failure: a textbook of clinical disorders of the autonomic nervous system. Oxford University Press, New York, pp 593–621

16.

Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The Consortium to Establish a Registry for Alzheimer’s disease (CERAD). Part ll. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41:479–486PubMed

17.

Nishie M, Mori F, Fujiwara H, Hasegawa M, Yoshimoto M, Iwatsubo T, Takahashi H, Wakabayashi K (2004) Accumulation of phosphorylated α-synuclein in the brain and peripheral ganglia of patients with multiple system atrophy. Acta Neuropathol 107:292–298CrossRefPubMed

18.

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

19.

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 57:1140–1141PubMed

20.

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 73:776–777CrossRefPubMed

21.

Orimo S, Ozawa E, Nakade S, Hattori H, Tsuchiya K, Taki K, Takahashi A (2003) [¹²³I]MIBG myocardial scintigraphy differentiates corticobasal degeneration from Parkinson’s disease. Intern Med 42:127–128PubMed

22.

Polinsky RJ, Kopin IJ, Ebert MH, Weise V (1981) Pharmacologic distinction of different orthostatic hypotension syndromes. Neurology 31:1–7

23.

Saito Y, Kawashima A, Ruberu NN, Fujiwara H, Koyama S, Sawabe M, Arai T, Nagura H, Yamanouchi H, Hasegawa M, Iwatsubo T, Murayama S (2003) Accumulation of phosphorylated alpha-synuclein in aging human brain. J Neuropathol Exp Neurol 62:644–654PubMed

24.

Satoh A, Serita T, Seto M, Tomita I, Satoh H, Iwanaga K, Takashima H, Tsujihata M (1999) Loss of¹²³I-MIBG uptake by the heart in Parkinson’s disease: assessment of cardiac sympathetic denervation and diagnostic value. J Nucl Med 40:371–375PubMed

25.

Schatz IJ, Bannister SR, Freeman RL (1996) Consensus statement on the definition of orthostatic hypotension, pure autonomic failure, and multiple system atrophy. Neurology 46:1470PubMed

26.

Taki J, Nakajima K, Hwang E-H, 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

27.

Wakabayashi K, Takahashi H, Ohama E, Takeda S, Ikuta F (1993) Lewy bodies in the visceral autonomic nervous system in Parkinson’s disease. In: Narabayashi H, Nagatsu N, Yanagisawa N, Mizuno Y (eds) Advances in Neurology. Lippincott-Raven, New York, pp 609–612

28.

Watanabe H, Ieda T, Katayama T, Takeda A, Akiba I, Doyu M, Hirayama M, Sobue G (2001) Cardiac¹²³I-meta-iodobenzylguanidine (MIBG) uptake in dementia with Lewy bodies: comparison with Alzheimer’s disease. J Neurol Neurosurg Psychiatry 70:781–783CrossRefPubMed

29.

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 155:60–67CrossRefPubMed

30.

Yoshita M, Taki J, Yamada M (2001) A clinical role for [¹²³I]MIBG myocardial scintigraphy in the distinction between dementia of the Alzheimer’s-type and dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 71:583–588CrossRefPubMed

Title: Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease
Authors: Satoshi Orimo
Takeshi Amino
Yoshinori Itoh
Atsushi Takahashi
Tohru Kojo
Toshiki Uchihara
Kuniaki Tsuchiya
Fumiaki Mori
Koichi Wakabayashi
Hitoshi Takahashi
Publication date: 01-06-2005
Publisher: Springer-Verlag
Published in: Acta Neuropathologica / Issue 6/2005
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-005-0995-7

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Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease

Abstract

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Abstract

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