Skip to main content
Erschienen in: Acta Neuropathologica 4/2008

01.04.2008 | Original Paper

Reduced striatal tyrosine hydroxylase in incidental Lewy body disease

verfasst von: Thomas Gerald Beach, Charles H. Adler, Lucia I. Sue, Jeffrey B. Peirce, Jyothi Bachalakuri, Jessica E. Dalsing-Hernandez, Lih Fen Lue, John N. Caviness, Donald J. Connor, Marwan N. Sabbagh, Douglas G. Walker

Erschienen in: Acta Neuropathologica | Ausgabe 4/2008

Einloggen, um Zugang zu erhalten

Abstract

Incidental Lewy body disease (ILBD) is the term used when Lewy bodies are found in the nervous system of subjects without clinically documented parkinsonism or dementia. The prevalence of ILBD in the elderly population has been estimated at between 3.8 and 30%, depending on subject age and anatomical site of sampling. It has been speculated that ILBD represents the preclinical stage of Parkinson’s disease (PD) and/or dementia with Lewy bodies (DLB). Studies of ILBD could potentially identify early diagnostic signs of these disorders. At present, however, it is impossible to know whether ILBD is a precursor to PD or DLB or is just a benign finding of normal aging. We hypothesized that, if ILBD represents an early stage of PD or DLB, it should be associated with depletion of striatal dopaminergic markers. Eleven subjects with ILBD and 27 control subjects were studied. The ILBD subjects ranged in age from 74 to 96 years (mean 86.5) while the control subjects’ age ranged from 75 to 102 years (mean 86.7). Controls and subjects did not differ in terms of age, postmortem interval, gender distribution, medical history conditions, brain weight, neuritic plaque density or Braak neurofibrillary stage. Quantitative ELISA measurement of striatal tyrosine hydroxylase (TH), the principal enzyme for dopamine synthesis, showed a 49.8% (P = 0.01) reduction in ILBD cases, as compared with control cases. The finding suggests that ILBD is not a benign condition but is likely a precursor to PD and/or DLB.
Literatur
1.
Zurück zum Zitat Consensus recommendations for the postmortem diagnosis of Alzheimer’s disease (1997) The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer’s Disease. Neurobiol Aging 18:S1–S2 Consensus recommendations for the postmortem diagnosis of Alzheimer’s disease (1997) The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer’s Disease. Neurobiol Aging 18:S1–S2
2.
Zurück zum Zitat Abbott RD, Petrovitch H, White LR, Masaki KH, Tanner CM, Curb JD, Grandinetti A, Blanchette PL, Popper JS, Ross GW (2001) Frequency of bowel movements and the future risk of Parkinson’s disease. Neurology 57:456–462PubMed Abbott RD, Petrovitch H, White LR, Masaki KH, Tanner CM, Curb JD, Grandinetti A, Blanchette PL, Popper JS, Ross GW (2001) Frequency of bowel movements and the future risk of Parkinson’s disease. Neurology 57:456–462PubMed
3.
Zurück zum Zitat Adler CH (2005) Nonmotor complications in Parkinson’s disease. Mov Disord 20(Suppl 11):S23–S29PubMedCrossRef Adler CH (2005) Nonmotor complications in Parkinson’s disease. Mov Disord 20(Suppl 11):S23–S29PubMedCrossRef
4.
Zurück zum Zitat Amino T, Orimo S, Itoh Y, Takahashi A, Uchihara T, Mizusawa H (2005) Profound cardiac sympathetic denervation occurs in Parkinson disease. Brain Pathol 15:29–34PubMedCrossRef Amino T, Orimo S, Itoh Y, Takahashi A, Uchihara T, Mizusawa H (2005) Profound cardiac sympathetic denervation occurs in Parkinson disease. Brain Pathol 15:29–34PubMedCrossRef
5.
Zurück zum Zitat Beach TG, Tago H, Nagai T, Kimura H, McGeer PL, McGeer EG (1987) Perfusion-fixation of the human brain for immunohistochemistry: comparison with immersion-fixation. J Neurosci Methods 19:183–192PubMedCrossRef Beach TG, Tago H, Nagai T, Kimura H, McGeer PL, McGeer EG (1987) Perfusion-fixation of the human brain for immunohistochemistry: comparison with immersion-fixation. J Neurosci Methods 19:183–192PubMedCrossRef
6.
Zurück zum Zitat Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 20: 415–455PubMedCrossRef Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 20: 415–455PubMedCrossRef
7.
Zurück zum Zitat Bezard E, Dovero S, Prunier C, Ravenscroft P, Chalon S, Guilloteau D, Crossman AR, Bioulac B, Brotchie JM, Gross CE (2001) Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson’s disease. J Neurosci 21:6853–6861PubMed Bezard E, Dovero S, Prunier C, Ravenscroft P, Chalon S, Guilloteau D, Crossman AR, Bioulac B, Brotchie JM, Gross CE (2001) Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson’s disease. J Neurosci 21:6853–6861PubMed
8.
Zurück zum Zitat Bloch A, Probst A, Bissig H, Adams H, Tolnay M (2006) Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurobiol 32:284–295PubMedCrossRef Bloch A, Probst A, Bissig H, Adams H, Tolnay M (2006) Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurobiol 32:284–295PubMedCrossRef
9.
Zurück zum Zitat Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 82:239–259CrossRef Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 82:239–259CrossRef
10.
Zurück zum Zitat Braak H, Del Tredici K, Bratzke H, Hamm-Clement J, Sandmann-Keil D, Rub U (2002) Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson’s disease (preclinical and clinical stages). J Neurol 249(Suppl 3):III/1–III/5 Braak H, Del Tredici K, Bratzke H, Hamm-Clement J, Sandmann-Keil D, Rub U (2002) Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson’s disease (preclinical and clinical stages). J Neurol 249(Suppl 3):III/1–III/5
11.
Zurück zum Zitat Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedCrossRef Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedCrossRef
12.
Zurück zum Zitat Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134PubMedCrossRef Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134PubMedCrossRef
13.
Zurück zum Zitat Carlsson A, Winblad B (1976) Influence of age and time interval between death and autopsy on dopamine and 3-methoxytyramine levels in human basal ganglia. J Neural Transm 38:271–276PubMedCrossRef Carlsson A, Winblad B (1976) Influence of age and time interval between death and autopsy on dopamine and 3-methoxytyramine levels in human basal ganglia. J Neural Transm 38:271–276PubMedCrossRef
14.
Zurück zum Zitat Daniel SE, Hawkes CH (1992) Preliminary diagnosis of Parkinson’s disease by olfactory bulb pathology. Lancet 340:186PubMedCrossRef Daniel SE, Hawkes CH (1992) Preliminary diagnosis of Parkinson’s disease by olfactory bulb pathology. Lancet 340:186PubMedCrossRef
15.
Zurück zum Zitat den Hartog Jager WA, Bethlem J (1960) The distribution of Lewy bodies in the central and autonomic nervous systems in idiopathic paralysis agitans. J Neurol Neurosurg Psychiatry 23:283–290CrossRef den Hartog Jager WA, Bethlem J (1960) The distribution of Lewy bodies in the central and autonomic nervous systems in idiopathic paralysis agitans. J Neurol Neurosurg Psychiatry 23:283–290CrossRef
16.
Zurück zum Zitat Dexter DT, Sian J, Rose S, Hindmarsh JG, Mann VM, Cooper JM, Wells FR, Daniel SE, Lees AJ, Schapira AH (1994) Indices of oxidative stress and mitochondrial function in individuals with incidental Lewy body disease. Ann Neurol 35:38–44PubMedCrossRef Dexter DT, Sian J, Rose S, Hindmarsh JG, Mann VM, Cooper JM, Wells FR, Daniel SE, Lees AJ, Schapira AH (1994) Indices of oxidative stress and mitochondrial function in individuals with incidental Lewy body disease. Ann Neurol 35:38–44PubMedCrossRef
17.
Zurück zum Zitat Fearnley JM, Lees AJ (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301PubMedCrossRef Fearnley JM, Lees AJ (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301PubMedCrossRef
18.
Zurück zum Zitat Forno LS, Norville RL (1976) Ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol (Berl) 34:183–197CrossRef Forno LS, Norville RL (1976) Ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol (Berl) 34:183–197CrossRef
19.
Zurück zum Zitat Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, Goldberg MS, Shen J, Takio K, Iwatsubo T (2002) Alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4:160–164PubMedCrossRef Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, Goldberg MS, Shen J, Takio K, Iwatsubo T (2002) Alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4:160–164PubMedCrossRef
20.
Zurück zum Zitat Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752PubMed Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752PubMed
21.
Zurück zum Zitat Goldstein DS, Holmes C, Li ST, Bruce S, Metman LV, Cannon RO III (2000) Cardiac sympathetic denervation in Parkinson disease. Ann Intern Med 133:338–347PubMed Goldstein DS, Holmes C, Li ST, Bruce S, Metman LV, Cannon RO III (2000) Cardiac sympathetic denervation in Parkinson disease. Ann Intern Med 133:338–347PubMed
22.
Zurück zum Zitat Hawkes C (2006) Olfaction in neurodegenerative disorder. Adv Otorhinolaryngol 63:133–151PubMed Hawkes C (2006) Olfaction in neurodegenerative disorder. Adv Otorhinolaryngol 63:133–151PubMed
23.
Zurück zum Zitat Hornykiewicz O (1993) Parkinson’s disease and the adaptive capacity of the nigrostriatal dopamine system: possible neurochemical mechanisms. Adv Neurol 60:140–147PubMed Hornykiewicz O (1993) Parkinson’s disease and the adaptive capacity of the nigrostriatal dopamine system: possible neurochemical mechanisms. Adv Neurol 60:140–147PubMed
24.
Zurück zum Zitat Ishihara L, Brayne C (2006) A systematic review of depression and mental illness preceding Parkinson’s disease. Acta Neurol Scand 113:211–220PubMedCrossRef Ishihara L, Brayne C (2006) A systematic review of depression and mental illness preceding Parkinson’s disease. Acta Neurol Scand 113:211–220PubMedCrossRef
25.
Zurück zum Zitat 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 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
26.
Zurück zum Zitat Jellinger KA (2004) Lewy body-related alpha-synucleinopathy in the aged human brain. J Neural Transm 111:1219–1235PubMedCrossRef Jellinger KA (2004) Lewy body-related alpha-synucleinopathy in the aged human brain. J Neural Transm 111:1219–1235PubMedCrossRef
27.
Zurück zum Zitat Jellinger KA, Attems J (2006) Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies? Acta Neuropathol (Berl) 112:253–260CrossRef Jellinger KA, Attems J (2006) Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies? Acta Neuropathol (Berl) 112:253–260CrossRef
28.
Zurück zum Zitat Johnston BT, Li Q, Castell JA, Castell DO (1995) Swallowing and esophageal function in Parkinson’s disease. Am J Gastroenterol 90:1741–1746PubMed Johnston BT, Li Q, Castell JA, Castell DO (1995) Swallowing and esophageal function in Parkinson’s disease. Am J Gastroenterol 90:1741–1746PubMed
29.
Zurück zum Zitat Katzenschlager R, Lees AJ (2004) Olfaction and Parkinson’s syndromes: its role in differential diagnosis. Curr Opin Neurol 17:417–423PubMedCrossRef Katzenschlager R, Lees AJ (2004) Olfaction and Parkinson’s syndromes: its role in differential diagnosis. Curr Opin Neurol 17:417–423PubMedCrossRef
30.
Zurück zum Zitat Kovari E, Burkhardt K, Lobrinus JA, Bouras C (2007) Lewy body dysphagia. Acta Neuropathol (Berl) 114:295–298CrossRef Kovari E, Burkhardt K, Lobrinus JA, Bouras C (2007) Lewy body dysphagia. Acta Neuropathol (Berl) 114:295–298CrossRef
31.
Zurück zum Zitat Lemke MR, Fuchs G, Gemende I, Herting B, Oehlwein C, Reichmann H, Rieke J, Volkmann J (2004) Depression and Parkinson’s disease. J Neurol 251(Suppl 6):VI/24–VI/27 Lemke MR, Fuchs G, Gemende I, Herting B, Oehlwein C, Reichmann H, Rieke J, Volkmann J (2004) Depression and Parkinson’s disease. J Neurol 251(Suppl 6):VI/24–VI/27
32.
Zurück zum Zitat Li ST, Dendi R, Holmes C, Goldstein DS (2002) Progressive loss of cardiac sympathetic innervation in Parkinson’s disease. Ann Neurol 52:220–223PubMedCrossRef Li ST, Dendi R, Holmes C, Goldstein DS (2002) Progressive loss of cardiac sympathetic innervation in Parkinson’s disease. Ann Neurol 52:220–223PubMedCrossRef
33.
Zurück zum Zitat McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, Del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VM, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872PubMedCrossRef McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, Del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VM, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872PubMedCrossRef
34.
Zurück zum Zitat Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F, Ortega-Moreno A, Rebollo AC, Gomez-Rio M, Concha A, Munoz DG (2007) Do alpha-synuclein aggregates in autonomic plexuses predate Lewy body disorders?: a cohort study. Neurology 68:2012–2018PubMedCrossRef Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F, Ortega-Moreno A, Rebollo AC, Gomez-Rio M, Concha A, Munoz DG (2007) Do alpha-synuclein aggregates in autonomic plexuses predate Lewy body disorders?: a cohort study. Neurology 68:2012–2018PubMedCrossRef
35.
Zurück zum Zitat 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 II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41:479–486PubMed 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 II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41:479–486PubMed
36.
Zurück zum Zitat Nakajima R, Takahashi K, Nakamura H, Otomo E, Kameyama M (1981) A quantitative study on the intermediolateral cells of the thoracic cord in degenerative diseases of the nervous system (author’s transl). Rinsho Shinkeigaku 21:581–586PubMed Nakajima R, Takahashi K, Nakamura H, Otomo E, Kameyama M (1981) A quantitative study on the intermediolateral cells of the thoracic cord in degenerative diseases of the nervous system (author’s transl). Rinsho Shinkeigaku 21:581–586PubMed
37.
Zurück zum Zitat Oyanagi K, Wakabayashi K, Ohama E, Takeda S, Horikawa Y, Morita T, Ikuta F (1990) Lewy bodies in the lower sacral parasympathetic neurons of a patient with Parkinson’s disease. Acta Neuropathol (Berl) 80:558–559CrossRef Oyanagi K, Wakabayashi K, Ohama E, Takeda S, Horikawa Y, Morita T, Ikuta F (1990) Lewy bodies in the lower sacral parasympathetic neurons of a patient with Parkinson’s disease. Acta Neuropathol (Berl) 80:558–559CrossRef
38.
Zurück zum Zitat Paganini-Hill A (2001) Risk factors for Parkinson’s disease: the leisure world cohort study. Neuroepidemiology 20:118–124PubMedCrossRef Paganini-Hill A (2001) Risk factors for Parkinson’s disease: the leisure world cohort study. Neuroepidemiology 20:118–124PubMedCrossRef
39.
Zurück zum Zitat Pearce RK, Hawkes CH, Daniel SE (1995) The anterior olfactory nucleus in Parkinson’s disease. Mov Disord 10:283–287PubMedCrossRef Pearce RK, Hawkes CH, Daniel SE (1995) The anterior olfactory nucleus in Parkinson’s disease. Mov Disord 10:283–287PubMedCrossRef
40.
Zurück zum Zitat Potulska A, Friedman A, Krolicki L, Spychala A (2003) Swallowing disorders in Parkinson’s disease. Parkinsonism Relat Disord 9:349–353PubMedCrossRef Potulska A, Friedman A, Krolicki L, Spychala A (2003) Swallowing disorders in Parkinson’s disease. Parkinsonism Relat Disord 9:349–353PubMedCrossRef
41.
Zurück zum Zitat Ross GW, Abbott RD, Petrovitch H, Tanner CM, Davis DG, Nelson J, Markesbery WR, Hardman J, Masaki K, Launer L, White LR (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21:2062–2067PubMedCrossRef Ross GW, Abbott RD, Petrovitch H, Tanner CM, Davis DG, Nelson J, Markesbery WR, Hardman J, Masaki K, Launer L, White LR (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21:2062–2067PubMedCrossRef
42.
Zurück zum Zitat Saito Y, Ruberu NN, Sawabe M, Arai T, Kazama H, Hosoi T, Yamanouchi H, Murayama S (2004) Lewy body-related alpha-synucleinopathy in aging. J Neuropathol Exp Neurol 63:742–749PubMed Saito Y, Ruberu NN, Sawabe M, Arai T, Kazama H, Hosoi T, Yamanouchi H, Murayama S (2004) Lewy body-related alpha-synucleinopathy in aging. J Neuropathol Exp Neurol 63:742–749PubMed
43.
Zurück zum Zitat Satoh A, Serita T, Seto M, Tomita I, Satoh H, Iwanaga K, Takashima 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 40:371–375PubMed Satoh A, Serita T, Seto M, Tomita I, Satoh H, Iwanaga K, Takashima 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 40:371–375PubMed
44.
Zurück zum Zitat Scigliano G, Musicco M, Soliveri P, Piccolo I, Ronchetti G, Girotti F (2006) Reduced risk factors for vascular disorders in Parkinson disease patients: a case-control study. Stroke 37:1184–1188PubMedCrossRef Scigliano G, Musicco M, Soliveri P, Piccolo I, Ronchetti G, Girotti F (2006) Reduced risk factors for vascular disorders in Parkinson disease patients: a case-control study. Stroke 37:1184–1188PubMedCrossRef
45.
Zurück zum Zitat Sharabi Y, Li ST, Dendi R, Holmes C, Goldstein DS (2003) Neurotransmitter specificity of sympathetic denervation in Parkinson’s disease. Neurology 60:1036–1039PubMed Sharabi Y, Li ST, Dendi R, Holmes C, Goldstein DS (2003) Neurotransmitter specificity of sympathetic denervation in Parkinson’s disease. Neurology 60:1036–1039PubMed
46.
Zurück zum Zitat Takeda S, Yamazaki K, Miyakawa T, Arai H (1993) Parkinson’s disease with involvement of the parasympathetic ganglia. Acta Neuropathol (Berl) 86:397–398CrossRef Takeda S, Yamazaki K, Miyakawa T, Arai H (1993) Parkinson’s disease with involvement of the parasympathetic ganglia. Acta Neuropathol (Berl) 86:397–398CrossRef
47.
Zurück zum Zitat Taki J, Yoshita M, Yamada M, Tonami N (2004) Significance of 123I-MIBG scintigraphy as a pathophysiological indicator in the assessment of Parkinson’s disease and related disorders: it can be a specific marker for Lewy body disease. Ann Nucl Med 18: 453–461PubMed Taki J, Yoshita M, Yamada M, Tonami N (2004) Significance of 123I-MIBG scintigraphy as a pathophysiological indicator in the assessment of Parkinson’s disease and related disorders: it can be a specific marker for Lewy body disease. Ann Nucl Med 18: 453–461PubMed
48.
Zurück zum Zitat Tsuboi Y, Wszolek ZK, Graff-Radford NR, Cookson N, Dickson DW (2003) Tau pathology in the olfactory bulb correlates with Braak stage, Lewy body pathology and apolipoprotein epsilon4. Neuropathol Appl Neurobiol 29: 503–510PubMedCrossRef Tsuboi Y, Wszolek ZK, Graff-Radford NR, Cookson N, Dickson DW (2003) Tau pathology in the olfactory bulb correlates with Braak stage, Lewy body pathology and apolipoprotein epsilon4. Neuropathol Appl Neurobiol 29: 503–510PubMedCrossRef
49.
Zurück zum Zitat Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1988) Parkinson’s disease: the presence of Lewy bodies in Auerbach’s and Meissner’s plexuses. Acta Neuropathol (Berl) 76:217–221CrossRef Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1988) Parkinson’s disease: the presence of Lewy bodies in Auerbach’s and Meissner’s plexuses. Acta Neuropathol (Berl) 76:217–221CrossRef
50.
Zurück zum Zitat Wenning GK, Ebersbach G, Verny M, Chaudhuri KR, Jellinger K, McKee A, Poewe W, Litvan I (1999) Progression of falls in postmortem-confirmed parkinsonian disorders. Mov Disord 14:947–950PubMedCrossRef Wenning GK, Ebersbach G, Verny M, Chaudhuri KR, Jellinger K, McKee A, Poewe W, Litvan I (1999) Progression of falls in postmortem-confirmed parkinsonian disorders. Mov Disord 14:947–950PubMedCrossRef
51.
Zurück zum Zitat Wood BH, Bilclough JA, Bowron A, Walker RW (2002) Incidence and prediction of falls in Parkinson’s disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 72:721–725PubMedCrossRef Wood BH, Bilclough JA, Bowron A, Walker RW (2002) Incidence and prediction of falls in Parkinson’s disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 72:721–725PubMedCrossRef
Metadaten
Titel
Reduced striatal tyrosine hydroxylase in incidental Lewy body disease
verfasst von
Thomas Gerald Beach
Charles H. Adler
Lucia I. Sue
Jeffrey B. Peirce
Jyothi Bachalakuri
Jessica E. Dalsing-Hernandez
Lih Fen Lue
John N. Caviness
Donald J. Connor
Marwan N. Sabbagh
Douglas G. Walker
Publikationsdatum
01.04.2008
Verlag
Springer-Verlag
Erschienen in
Acta Neuropathologica / Ausgabe 4/2008
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-007-0313-7

Weitere Artikel der Ausgabe 4/2008

Acta Neuropathologica 4/2008 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.