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Erschienen in: Acta Neuropathologica 6/2010

01.06.2010 | Original Paper

Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson’s disease

verfasst von: Kelly Del Tredici, Christopher H. Hawkes, Estifanos Ghebremedhin, Heiko Braak

Erschienen in: Acta Neuropathologica | Ausgabe 6/2010

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Abstract

A retrospective autopsy-based study of the human submandibular gland, one of the three major salivary glands, together with anatomically related peripheral structures (cervical superior ganglion, cervical sympathetic trunk, vagal nerve at the level of the carotid bifurcation), was conducted on a cohort consisting of 33 individuals, including 9 patients with neuropathologically confirmed Parkinson’s disease (PD), three individuals with incidental Lewy body disease (iLBD), 2 individuals with neuropathologically confirmed multiple system atrophy (MSA), and 19 controls, using α-synuclein immunohistochemistry in 100 μm polyethylene glycol-embedded tissue sections. Lewy pathology (LP) was present in the submandibular glands and cervical superior ganglia in PD (9/9 cases) and iLBD (2/3 cases) but not in MSA or controls. The cervical sympathetic trunk (7/9 PD cases, 2/3 iLBD cases) and peripheral vagal nerves (9/9 PD cases, 2/3 iLBD cases) also displayed LP. The results are discussed within the context of hyposmia as well as autonomic dysfunction in PD (sialorrhea, sialopenia, dysphagia). Potential disease-related changes in salivary volume, contents, and viscosity might make it possible, in combination with other tests, to employ human saliva as a biomarker.
Literatur
1.
Zurück zum Zitat Bagheri H, Damase-Michel C, Lapeyre-Mestre M et al (1999) A study of salivary secretion in Parkinson’s disease. Clin Neuropharmacol 22:213–215PubMed Bagheri H, Damase-Michel C, Lapeyre-Mestre M et al (1999) A study of salivary secretion in Parkinson’s disease. Clin Neuropharmacol 22:213–215PubMed
2.
Zurück zum Zitat Baltadzhieva R, Gurevich T, Korczyn AD (2005) Autonomic impairment in amyotrophic lateral sclerosis. Curr Opin Neurol 18:487–493CrossRefPubMed Baltadzhieva R, Gurevich T, Korczyn AD (2005) Autonomic impairment in amyotrophic lateral sclerosis. Curr Opin Neurol 18:487–493CrossRefPubMed
3.
Zurück zum Zitat Bassotti G, Germani U, Pagliaricci S et al (1998) Esophageal manometric abnormalities in Parkinson’s disease. Dysphagia 13:28–41CrossRefPubMed Bassotti G, Germani U, Pagliaricci S et al (1998) Esophageal manometric abnormalities in Parkinson’s disease. Dysphagia 13:28–41CrossRefPubMed
4.
Zurück zum Zitat Bateson MC, Gibberd FB, Wilson RSE (1973) Salivary symptoms in Parkinson’s disease. Arch Neurol 29:274–275PubMed Bateson MC, Gibberd FB, Wilson RSE (1973) Salivary symptoms in Parkinson’s disease. Arch Neurol 29:274–275PubMed
5.
Zurück zum Zitat Blessing WW (2004) Lower brain stem regulation of visceral, cardiovascular, and respiratory function. In: Paxinos G, Mai JK (eds) The human nervous system, 2nd edn. Elsevier, London, pp 464–478 Blessing WW (2004) Lower brain stem regulation of visceral, cardiovascular, and respiratory function. In: Paxinos G, Mai JK (eds) The human nervous system, 2nd edn. Elsevier, London, pp 464–478
6.
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. Neurobiol Appl Neurol 32:284–295CrossRef 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. Neurobiol Appl Neurol 32:284–295CrossRef
7.
Zurück zum Zitat Boyce HW, Bakheet MR (2005) Sialorrhea: a review of a vexing, often unrecognized sign of oropharyngeal and esophageal disease. J Clin Gastroenterol 39:89–97PubMed Boyce HW, Bakheet MR (2005) Sialorrhea: a review of a vexing, often unrecognized sign of oropharyngeal and esophageal disease. J Clin Gastroenterol 39:89–97PubMed
8.
Zurück zum Zitat Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82:239–259CrossRefPubMed Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82:239–259CrossRefPubMed
9.
Zurück zum Zitat Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211CrossRefPubMed Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211CrossRefPubMed
10.
Zurück zum Zitat Braak H, de Vos RAI, Bohl J, Del Tredici K (2006) Gastric α-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci Lett 39:67–72CrossRef Braak H, de Vos RAI, Bohl J, Del Tredici K (2006) Gastric α-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci Lett 39:67–72CrossRef
11.
Zurück zum Zitat Braak H, Sastre M, Bohl JRE, de Vos RAI, Del Tredici K (2007) Parkinson’s disease: lesions in dorsal horn layer I, involvement of parasympathetic and sympathetic pre- and postganglionic neurons. Acta Neuropathol 113:421–429CrossRefPubMed Braak H, Sastre M, Bohl JRE, de Vos RAI, Del Tredici K (2007) Parkinson’s disease: lesions in dorsal horn layer I, involvement of parasympathetic and sympathetic pre- and postganglionic neurons. Acta Neuropathol 113:421–429CrossRefPubMed
12.
Zurück zum Zitat Bradley RM, Fukami H, Suwabe T (2005) Neurobiology of the gustatory–salivary reflex. Chem Senses 30:i70–i71CrossRefPubMed Bradley RM, Fukami H, Suwabe T (2005) Neurobiology of the gustatory–salivary reflex. Chem Senses 30:i70–i71CrossRefPubMed
13.
Zurück zum Zitat Byrne KG, Pfeiffer RM, Quigley EMM (1994) Gastrointestinal dysfunction in Parkinson’s disease: a report of clinical experience at a single center. J Clin Gastroenterol 19:11–16CrossRefPubMed Byrne KG, Pfeiffer RM, Quigley EMM (1994) Gastrointestinal dysfunction in Parkinson’s disease: a report of clinical experience at a single center. J Clin Gastroenterol 19:11–16CrossRefPubMed
14.
Zurück zum Zitat Cersósimo MG, Benarroch EE (2008) Neural control of the gastrointestinal tract: implications for Parkinson disease. Mov Disord 23:1065–1073CrossRefPubMed Cersósimo MG, Benarroch EE (2008) Neural control of the gastrointestinal tract: implications for Parkinson disease. Mov Disord 23:1065–1073CrossRefPubMed
15.
Zurück zum Zitat Chatoo AH, Lee VM, Linden RA (1953) Evidence for synergism between the masticatory and gustatory parotid salivary reflexes in humans. J Physiol 459:34 Chatoo AH, Lee VM, Linden RA (1953) Evidence for synergism between the masticatory and gustatory parotid salivary reflexes in humans. J Physiol 459:34
16.
Zurück zum Zitat Chou KL, Evatt M, Hinson V, Kompoliti K (2007) Sialorrhea in Parkinson’s disease: a review. Mov Disord 22:2306–2313CrossRefPubMed Chou KL, Evatt M, Hinson V, Kompoliti K (2007) Sialorrhea in Parkinson’s disease: a review. Mov Disord 22:2306–2313CrossRefPubMed
17.
Zurück zum Zitat Cook DI, van Lennep EW, Roberts ML, Young JA (1994) Secretion by the major salivary glands. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 3rd edn. Raven, New York, pp 1061–1117 Cook DI, van Lennep EW, Roberts ML, Young JA (1994) Secretion by the major salivary glands. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 3rd edn. Raven, New York, pp 1061–1117
18.
Zurück zum Zitat Crawford JM (1997) The oral cavity and gastrointestinal tract. In: Kumar V, Cotran RS, Robbins SL (eds) Basic pathology. W.B. Saunders, Philadelphia, pp 470–515 Crawford JM (1997) The oral cavity and gastrointestinal tract. In: Kumar V, Cotran RS, Robbins SL (eds) Basic pathology. W.B. Saunders, Philadelphia, pp 470–515
19.
Zurück zum Zitat Del Tredici K, Rüb U, de Vos RAI, Bohl JRE, Braak H (2002) Where does Parkinson pathology begin in the brain? J Neuropathol Exp Neurol 61:413–426PubMed Del Tredici K, Rüb U, de Vos RAI, Bohl JRE, Braak H (2002) Where does Parkinson pathology begin in the brain? J Neuropathol Exp Neurol 61:413–426PubMed
20.
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
21.
Zurück zum Zitat Dickson DW, Fujishiro H, DelleDonne A et al (2008) Evidence that incidental Lewy body disease is pre-symptomatic Parkinson’s disease. Acta Neuropathol 115:437–444CrossRefPubMed Dickson DW, Fujishiro H, DelleDonne A et al (2008) Evidence that incidental Lewy body disease is pre-symptomatic Parkinson’s disease. Acta Neuropathol 115:437–444CrossRefPubMed
22.
Zurück zum Zitat Dickson DW, Braak H, Duda JE et al (2009) Diagnostic criteria for the neuropathological assessment of Parkinson disease. Lancet Neurol 8:1150–1157CrossRefPubMed Dickson DW, Braak H, Duda JE et al (2009) Diagnostic criteria for the neuropathological assessment of Parkinson disease. Lancet Neurol 8:1150–1157CrossRefPubMed
23.
Zurück zum Zitat Doty RL, Deems D, Stellar S (1988) Olfactory dysfunction in Parkinson’s disease: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 38:1237–1244PubMed Doty RL, Deems D, Stellar S (1988) Olfactory dysfunction in Parkinson’s disease: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 38:1237–1244PubMed
24.
Zurück zum Zitat Doty RL, Stern MB, Pfeiffer C, Gollomp SM, Hurtig HI (1992) Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 55:138–142CrossRefPubMed Doty RL, Stern MB, Pfeiffer C, Gollomp SM, Hurtig HI (1992) Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 55:138–142CrossRefPubMed
25.
Zurück zum Zitat Edwards LL, Pfeiffer RF, Quigley EMM, Hofman R, Balluff M (1991) Gastrointestinal symptoms in Parkinson’s disease. Mov Disord 6:151–156CrossRefPubMed Edwards LL, Pfeiffer RF, Quigley EMM, Hofman R, Balluff M (1991) Gastrointestinal symptoms in Parkinson’s disease. Mov Disord 6:151–156CrossRefPubMed
26.
Zurück zum Zitat Edwards LL, Quigley EM, Harned RK, Hofmann R, Pfeiffer RF (1994) Characterization of swallowing and defecation in Parkinson’s disease. Am J Gastroenterol 1:15–25 Edwards LL, Quigley EM, Harned RK, Hofmann R, Pfeiffer RF (1994) Characterization of swallowing and defecation in Parkinson’s disease. Am J Gastroenterol 1:15–25
27.
Zurück zum Zitat Emmelin N (1987) Nerve interactions in salivary glands. J Dent Res 66:509–517PubMed Emmelin N (1987) Nerve interactions in salivary glands. J Dent Res 66:509–517PubMed
28.
Zurück zum Zitat Evatt ML, Chaudhuri KR, Chou KL et al (2009) Dysautonomia rating scales in Parkinson’s disease: sialorrhea, dysphagia, and constipation—critique and recommendations by Movement Disorders Task Force on Rating Scales for Parkinson’s disease. Mov Disord 24:635–646CrossRefPubMed Evatt ML, Chaudhuri KR, Chou KL et al (2009) Dysautonomia rating scales in Parkinson’s disease: sialorrhea, dysphagia, and constipation—critique and recommendations by Movement Disorders Task Force on Rating Scales for Parkinson’s disease. Mov Disord 24:635–646CrossRefPubMed
29.
Zurück zum Zitat Forno LS, Norville RL (1976) Ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol 34:183–197CrossRefPubMed Forno LS, Norville RL (1976) Ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol 34:183–197CrossRefPubMed
31.
Zurück zum Zitat Fujishiro H, Frigerio R, Burnett M et al (2008) Cardiac sympathetic denervation correlates with clinical and pathologic stages of Parkinson’s disease. Mov Disord 23:1085–1092CrossRefPubMed Fujishiro H, Frigerio R, Burnett M et al (2008) Cardiac sympathetic denervation correlates with clinical and pathologic stages of Parkinson’s disease. Mov Disord 23:1085–1092CrossRefPubMed
32.
Zurück zum Zitat Fumimura Y, Ikemura M, Saito Y et al (2007) Analysis of the adrenal gland is useful for evaluating pathology of the peripheral autonomic nervous system in Lewy body disease. J Neuropathol Exp Neurol 66:354–362CrossRefPubMed Fumimura Y, Ikemura M, Saito Y et al (2007) Analysis of the adrenal gland is useful for evaluating pathology of the peripheral autonomic nervous system in Lewy body disease. J Neuropathol Exp Neurol 66:354–362CrossRefPubMed
33.
Zurück zum Zitat Garrett JR (1967) The innervation of normal human submandibular and parotid salivary glands. Arch Oral Biol 12:1417CrossRefPubMed Garrett JR (1967) The innervation of normal human submandibular and parotid salivary glands. Arch Oral Biol 12:1417CrossRefPubMed
34.
Zurück zum Zitat Garrett JR (1987) The proper role of nerves in salivatory secretion—a review. J Dent Res 66:387–397PubMed Garrett JR (1987) The proper role of nerves in salivatory secretion—a review. J Dent Res 66:387–397PubMed
35.
Zurück zum Zitat Gerling G, Garrett JR, Paterson KL et al (2008) Innervation and secretory function of transplanted human submandibular salivary glands. Transplantation 85:135–140CrossRef Gerling G, Garrett JR, Paterson KL et al (2008) Innervation and secretory function of transplanted human submandibular salivary glands. Transplantation 85:135–140CrossRef
36.
Zurück zum Zitat Ghebremedhin E, Del Tredici K, Langston JW, Braak H (2009) Diminished tyrosine hydroxylase immunoreactivity in the cardiac conduction system and myocardium in Parkinson’s disease: an anatomical study. Acta Neuropathol 118:777–784CrossRefPubMed Ghebremedhin E, Del Tredici K, Langston JW, Braak H (2009) Diminished tyrosine hydroxylase immunoreactivity in the cardiac conduction system and myocardium in Parkinson’s disease: an anatomical study. Acta Neuropathol 118:777–784CrossRefPubMed
37.
Zurück zum Zitat Giess R, Werner E, Beck M et al (2002) Impaired salivary gland function reveals autonomic dysfunction in amyotrophic lateral sclerosis. J Neurol 249:1246–1249CrossRefPubMed Giess R, Werner E, Beck M et al (2002) Impaired salivary gland function reveals autonomic dysfunction in amyotrophic lateral sclerosis. J Neurol 249:1246–1249CrossRefPubMed
38.
Zurück zum Zitat Gilman S, Wenning GK, Low PA et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676CrossRefPubMed Gilman S, Wenning GK, Low PA et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676CrossRefPubMed
39.
Zurück zum Zitat Goetz CG, Power W, Rascol O et al (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028CrossRefPubMed Goetz CG, Power W, Rascol O et al (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028CrossRefPubMed
40.
Zurück zum Zitat Goldstein DS, Holmes CS, Dendi R, Bruce SR, Li ST (2002) Orthostatic hypotension from sympathetic denervation in Parkinson’s disease. Neurology 58:1247–1255PubMed Goldstein DS, Holmes CS, Dendi R, Bruce SR, Li ST (2002) Orthostatic hypotension from sympathetic denervation in Parkinson’s disease. Neurology 58:1247–1255PubMed
41.
Zurück zum Zitat Hawkes CH, Shephard BC, Daniel SE (1997) Olfactory dysfunction in Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:436–444CrossRefPubMed Hawkes CH, Shephard BC, Daniel SE (1997) Olfactory dysfunction in Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:436–444CrossRefPubMed
42.
Zurück zum Zitat Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG (2008) The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord 23:837–844CrossRefPubMed Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG (2008) The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord 23:837–844CrossRefPubMed
43.
Zurück zum Zitat Hornby PJ, Abrahams TP (2000) Central control of lower esophageal sphincter relaxation. Am J Med 108(Suppl 4):90S–98SCrossRefPubMed Hornby PJ, Abrahams TP (2000) Central control of lower esophageal sphincter relaxation. Am J Med 108(Suppl 4):90S–98SCrossRefPubMed
44.
Zurück zum Zitat Iwanaga K, Wakabayashi K, Yoshimoto M et al (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 et al (1999) Lewy body type degeneration in cardiac plexus in Parkinson’s and incidental Lewy body diseases. Neurology 52:1269–1271PubMed
45.
Zurück zum Zitat Kaplan MD, Baum BJ (1993) The function of saliva. Dysphagia 9:225–229CrossRef Kaplan MD, Baum BJ (1993) The function of saliva. Dysphagia 9:225–229CrossRef
46.
Zurück zum Zitat Klosen P, Maessen X, de Aguilar P (1993) PEG embedding for immunocytochemistry: application to the analysis of immunoreactivity loss during histological processing. J Histochem Cytochem 41:455–463PubMed Klosen P, Maessen X, de Aguilar P (1993) PEG embedding for immunocytochemistry: application to the analysis of immunoreactivity loss during histological processing. J Histochem Cytochem 41:455–463PubMed
47.
Zurück zum Zitat Kuusisto E, Parkkinen L, Alafuzoff I (2003) Morphogenesis of Lewy bodies: dissimilar incorporation of α-synuclein, ubiquitin, and p62. J Neuropathol Exp Neurol 62:1241–1253PubMed Kuusisto E, Parkkinen L, Alafuzoff I (2003) Morphogenesis of Lewy bodies: dissimilar incorporation of α-synuclein, ubiquitin, and p62. J Neuropathol Exp Neurol 62:1241–1253PubMed
48.
Zurück zum Zitat Kyriacou K, Garrett JR (1988) Morphological changes in the rabbit submandibular gland after parasympathetic or sympathetic denervation. Arch Oral Biol 33:281–290CrossRefPubMed Kyriacou K, Garrett JR (1988) Morphological changes in the rabbit submandibular gland after parasympathetic or sympathetic denervation. Arch Oral Biol 33:281–290CrossRefPubMed
49.
Zurück zum Zitat Leopold NA, Kagel MC (1995) Prepharyngeal dysphagia in Parkinson’s disease. Dysphagia 11:14–22CrossRef Leopold NA, Kagel MC (1995) Prepharyngeal dysphagia in Parkinson’s disease. Dysphagia 11:14–22CrossRef
50.
Zurück zum Zitat Leopold NA, Kagel MC (1997) Pharyngo-esophageal dysphagia in Parkinson’s disease. Dysphagia 12:11–18CrossRefPubMed Leopold NA, Kagel MC (1997) Pharyngo-esophageal dysphagia in Parkinson’s disease. Dysphagia 12:11–18CrossRefPubMed
51.
52.
Zurück zum Zitat Markesbery WR, Jicha GA, Liu H, Schmitt FA (2009) Lewy body pathology in normal elderly subjects. J Neuropathol Exp Neurol 68:816–822CrossRefPubMed Markesbery WR, Jicha GA, Liu H, Schmitt FA (2009) Lewy body pathology in normal elderly subjects. J Neuropathol Exp Neurol 68:816–822CrossRefPubMed
53.
Zurück zum Zitat Martinez-Madrigal F, Micheau C (1989) Histology of the major salivary glands. Am J Surg Pathol 13:879–899PubMedCrossRef Martinez-Madrigal F, Micheau C (1989) Histology of the major salivary glands. Am J Surg Pathol 13:879–899PubMedCrossRef
54.
Zurück zum Zitat Martinez-Marin P, Schapira AHV, Stocchi F et al (2007) Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting: study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 23:1623–1629CrossRef Martinez-Marin P, Schapira AHV, Stocchi F et al (2007) Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting: study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 23:1623–1629CrossRef
55.
Zurück zum Zitat McKeith IG, Dickson DW, Lowe J et al (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872CrossRefPubMed McKeith IG, Dickson DW, Lowe J et al (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872CrossRefPubMed
56.
Zurück zum Zitat Miki Y, Mori F, Wakabayashi K, Kuroda N, Orimo S (2009) Incidental Lewy body disease restricted to the heart and stellate ganglion. Mov Disord 24:2299–2301CrossRefPubMed Miki Y, Mori F, Wakabayashi K, Kuroda N, Orimo S (2009) Incidental Lewy body disease restricted to the heart and stellate ganglion. Mov Disord 24:2299–2301CrossRefPubMed
57.
Zurück zum Zitat Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F et al (2007) Do α-synuclein aggregates in autonomic plexuses predate Lewy body disorders? A cohort study. Neurology 68:2012–2018CrossRefPubMed Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F et al (2007) Do α-synuclein aggregates in autonomic plexuses predate Lewy body disorders? A cohort study. Neurology 68:2012–2018CrossRefPubMed
58.
Zurück zum Zitat Nishie M, Mori F, Yoshimoto M, Takahashi H, Wakabayashi K (2004) A quantitative investigation of neuronal cytoplasmic and intranuclear inclusions in the pontine and inferior olivary nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 30:546–554CrossRefPubMed Nishie M, Mori F, Yoshimoto M, Takahashi H, Wakabayashi K (2004) A quantitative investigation of neuronal cytoplasmic and intranuclear inclusions in the pontine and inferior olivary nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 30:546–554CrossRefPubMed
59.
Zurück zum Zitat Orimo S, Takahashi A, Uchihara T et al (2007) Degeneration of cardiac sympathetic nerve begins in the early disease process of Parkinson’s disease. Brain Pathol 17:24–30CrossRefPubMed Orimo S, Takahashi A, Uchihara T et al (2007) Degeneration of cardiac sympathetic nerve begins in the early disease process of Parkinson’s disease. Brain Pathol 17:24–30CrossRefPubMed
60.
Zurück zum Zitat Orimo S, Uchihara T, Nakamura A et al (2008) Axonal α-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson’s disease. Brain 131:642–650CrossRefPubMed Orimo S, Uchihara T, Nakamura A et al (2008) Axonal α-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson’s disease. Brain 131:642–650CrossRefPubMed
61.
Zurück zum Zitat Pfeiffer RF (1998) Gastrointestinal dysfunction in Parkinson’s disease. Clin Neurosci 5:136–146PubMed Pfeiffer RF (1998) Gastrointestinal dysfunction in Parkinson’s disease. Clin Neurosci 5:136–146PubMed
62.
Zurück zum Zitat Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson’s disease. Lancet Neurol 2:107–116CrossRefPubMed Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson’s disease. Lancet Neurol 2:107–116CrossRefPubMed
63.
Zurück zum Zitat Probst A, Bloch A, Tolnay M (2008) New insights into the pathology of Parkinson’s disease: does the peripheral autonomic nervous system become central? Eur J Neurol 15(Suppl 1):1–4CrossRefPubMed Probst A, Bloch A, Tolnay M (2008) New insights into the pathology of Parkinson’s disease: does the peripheral autonomic nervous system become central? Eur J Neurol 15(Suppl 1):1–4CrossRefPubMed
64.
Zurück zum Zitat Proctor GB, Carpenter GH (2007) Regulation of salivary gland function by autonomic nerves. Auton Neurosci Basic Clin 133:3–18CrossRef Proctor GB, Carpenter GH (2007) Regulation of salivary gland function by autonomic nerves. Auton Neurosci Basic Clin 133:3–18CrossRef
65.
Zurück zum Zitat Proulx M, de Courval FP, Wiseman MA, Panisset M (2005) Salivary production in Parkinson’s disease. Mov Disord 20:204–207CrossRefPubMed Proulx M, de Courval FP, Wiseman MA, Panisset M (2005) Salivary production in Parkinson’s disease. Mov Disord 20:204–207CrossRefPubMed
66.
Zurück zum Zitat Qualman SJ, Haupt HM, Yang P, Hamilton SR (1984) Esophageal Lewy bodies associated with ganglion cell loss in achalasia. Similarity to Parkinson’s disease. Gastroenterology 87:848–856PubMed Qualman SJ, Haupt HM, Yang P, Hamilton SR (1984) Esophageal Lewy bodies associated with ganglion cell loss in achalasia. Similarity to Parkinson’s disease. Gastroenterology 87:848–856PubMed
67.
Zurück zum Zitat Richards WG, Sugarbaker DJ (1995) Neuronal control of esophageal function. Chest Surg Clin North Am 5:157–171 Richards WG, Sugarbaker DJ (1995) Neuronal control of esophageal function. Chest Surg Clin North Am 5:157–171
68.
Zurück zum Zitat Robbins JA, Logemann JA, Kirshner HS (1986) Swallowing and speech production in Parkinson’s disease. Ann Neurol 19:283–287CrossRefPubMed Robbins JA, Logemann JA, Kirshner HS (1986) Swallowing and speech production in Parkinson’s disease. Ann Neurol 19:283–287CrossRefPubMed
69.
Zurück zum Zitat Ross GW, Petrovitch H, Abbott RD et al (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21:2062–2067CrossRefPubMed Ross GW, Petrovitch H, Abbott RD et al (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21:2062–2067CrossRefPubMed
70.
Zurück zum Zitat Schwab RS, England AS (1958) Parkinson’s disease. J Chronic Dis 8:448–501CrossRef Schwab RS, England AS (1958) Parkinson’s disease. J Chronic Dis 8:448–501CrossRef
71.
Zurück zum Zitat Shannon IL, Suddick RP, Chauncey HH (1969) Effect of atropine-induced flow rate depression on composition of unstimulated human parotid fluid. Arch Oral Biol 14:761–770CrossRefPubMed Shannon IL, Suddick RP, Chauncey HH (1969) Effect of atropine-induced flow rate depression on composition of unstimulated human parotid fluid. Arch Oral Biol 14:761–770CrossRefPubMed
72.
Zurück zum Zitat Siddiqui MF, Rast S, Lynn MJ, Auchus AP, Pfeiffer RF (2002) Autonomic dysfunction in Parkinson’s disease: a comprehensive symptom survey. Parkinsonism Rel Disord 8:277–284CrossRef Siddiqui MF, Rast S, Lynn MJ, Auchus AP, Pfeiffer RF (2002) Autonomic dysfunction in Parkinson’s disease: a comprehensive symptom survey. Parkinsonism Rel Disord 8:277–284CrossRef
74.
Zurück zum Zitat Sone M, Yoshida M, Hashizume Y, Hishikawa N, Sobue G (2005) α-Synuclein-immunoreactive structure formation is enhanced in sympathetic ganglia of patients with multiple system atrophy. Acta Neuropathol 110:19–26CrossRefPubMed Sone M, Yoshida M, Hashizume Y, Hishikawa N, Sobue G (2005) α-Synuclein-immunoreactive structure formation is enhanced in sympathetic ganglia of patients with multiple system atrophy. Acta Neuropathol 110:19–26CrossRefPubMed
75.
Zurück zum Zitat Takeda S, Yamazaki K, Miyakawa T, Arai H (1993) Parkinson’s disease with involvement of the parasympathetic ganglia. Acta Neuropathol 86:397–398CrossRefPubMed Takeda S, Yamazaki K, Miyakawa T, Arai H (1993) Parkinson’s disease with involvement of the parasympathetic ganglia. Acta Neuropathol 86:397–398CrossRefPubMed
76.
Zurück zum Zitat Taki J, Nakajima K, Hwang EH et al (2000) Peripheral sympathetic dysfunction in patients with Parkinson’s disease without autonomic failure is heart selective and disease specific. Eur J Nucl Med 27:566–573CrossRefPubMed Taki J, Nakajima K, Hwang EH et al (2000) Peripheral sympathetic dysfunction in patients with Parkinson’s disease without autonomic failure is heart selective and disease specific. Eur J Nucl Med 27:566–573CrossRefPubMed
77.
Zurück zum Zitat Tissingh G, Berendse HW, Bergmanns P et al (2001) Loss of olfaction in de novo and treated Parkinson’s disease: possible implications for early diagnosis. Mov Disord 16:41–46CrossRefPubMed Tissingh G, Berendse HW, Bergmanns P et al (2001) Loss of olfaction in de novo and treated Parkinson’s disease: possible implications for early diagnosis. Mov Disord 16:41–46CrossRefPubMed
78.
Zurück zum Zitat Tumilasci OR, Cersósimo MG, Belforte JE, Micheli FE, Benarroch EE, Pazo JH (2006) Quantitative study of salivary secretion in Parkinson’s disease. Mov Disord 21:660–667CrossRefPubMed Tumilasci OR, Cersósimo MG, Belforte JE, Micheli FE, Benarroch EE, Pazo JH (2006) Quantitative study of salivary secretion in Parkinson’s disease. Mov Disord 21:660–667CrossRefPubMed
79.
Zurück zum Zitat Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, van Hilten JJ (2007) Patient-reported autonomic symptoms in Parkinson’s disease. Neurology 69:333–341CrossRefPubMed Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, van Hilten JJ (2007) Patient-reported autonomic symptoms in Parkinson’s disease. Neurology 69:333–341CrossRefPubMed
80.
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 76:217–221CrossRefPubMed 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 76:217–221CrossRefPubMed
81.
Zurück zum Zitat Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1990) Parkinson’s disease: an immunohistochemical study of Lewy body-containing neurons in the enteric nervous system. Acta Neuropathol 79:581–583CrossRefPubMed Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1990) Parkinson’s disease: an immunohistochemical study of Lewy body-containing neurons in the enteric nervous system. Acta Neuropathol 79:581–583CrossRefPubMed
82.
Zurück zum Zitat Wakabayashi K, Takahashi H, Obata K, Ikuta F (1992) Immunocytochemical localization of synaptic vesicle-specific protein in Lewy body-containing neurons in Parkinson’s disease. Neurosci Lett 138:237–240CrossRefPubMed Wakabayashi K, Takahashi H, Obata K, Ikuta F (1992) Immunocytochemical localization of synaptic vesicle-specific protein in Lewy body-containing neurons in Parkinson’s disease. Neurosci Lett 138:237–240CrossRefPubMed
83.
Zurück zum Zitat Wakabayashi K, Takahashi H, Ohama E, Takeda S, Ikuta F (1993) Lewy bodies in the visceral autonomic nervous system in Parkinson’s disease. Adv Neurol 60:609–612PubMed Wakabayashi K, Takahashi H, Ohama E, Takeda S, Ikuta F (1993) Lewy bodies in the visceral autonomic nervous system in Parkinson’s disease. Adv Neurol 60:609–612PubMed
Metadaten
Titel
Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson’s disease
verfasst von
Kelly Del Tredici
Christopher H. Hawkes
Estifanos Ghebremedhin
Heiko Braak
Publikationsdatum
01.06.2010
Verlag
Springer-Verlag
Erschienen in
Acta Neuropathologica / Ausgabe 6/2010
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-010-0665-2

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