Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic parkinson's disease

Acta Neuropathologica

Volumn 119, Issue 6, 2010, Pages 703-713

  Tredici, Kelly Del ^a   Hawkes, Christopher H ^b   Ghebremedhin, Estifanos ^a,c   Braak, Heiko ^a  

^a UNIVERSITY OF ULM   (Germany)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Alpha synuclein; Autonomic nervous system ganglia; Dysphagia; Esophagus; Lewy body disease; Lewy neuritis; Parkinson's disease; Peripheral nervous system; Sialopenia; Sialorrhea; Submandibular gland; Superior cervical ganglion; Synucleinopathy

Indexed keywords

ALPHA SYNUCLEIN; MACROGOL;

ADULT; AGED; ARTICLE; AUTONOMIC DYSFUNCTION; CAROTID ARTERY BIFURCATION; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; DYSPHAGIA; FEMALE; HUMAN; HYPERSALIVATION; HYPOSMIA; IMMUNOHISTOCHEMISTRY; LEWY BODY; MALE; PARKINSON DISEASE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SHY DRAGER SYNDROME; SIALOPENIA; SUBMANDIBULAR GLAND; SUPERIOR CERVICAL GANGLION; SYMPATHETIC TRUNK; TISSUE SECTION; VAGUS NERVE;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; COHORT STUDIES; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LEWY BODIES; LEWY BODY DISEASE; MALE; MIDDLE AGED; MULTIPLE SYSTEM ATROPHY; PARKINSON DISEASE; RETROSPECTIVE STUDIES; SUBMANDIBULAR GLAND; SUPERIOR CERVICAL GANGLION; VAGUS NERVE;

EID: 77953022918     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-010-0665-2     Document Type: Article

References (83)

1. Bagheri H, Damase-Michel C, Lapeyre-Mestre M et al (1999) A study of salivary secretion in Parkinson's disease. Clin Neuropharmacol 22:213-215.
2. Baltadzhieva R, Gurevich T, Korczyn AD (2005) Autonomic impairment in amyotrophic lateral sclerosis. Curr Opin Neurol 18:487-493.
3. Bassotti G, Germani U, Pagliaricci S et al (1998) Esophageal manometric abnormalities in Parkinson's disease. Dysphagia 13:28-41.
4. Bateson MC, Gibberd FB, Wilson RSE (1973) Salivary symptoms in Parkinson's disease. Arch Neurol 29:274-275.
5. 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. Bloch A, Probst A, Bissig H, Adams H, Tolnay M (2006) Alphasynuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neurobiol Appl Neurol 32:284-295.
7. Boyce HW, Bakheet MR (2005) Sialorrhea: a review of a vexing, often unrecognized sign of oropharyngeal and esophageal disease. J Clin Gastroenterol 39:89-97.
8. Braak H, Braak E (1991) Neuropathological staging of Alzheimer- related changes. Acta Neuropathol 82:239-259.
9. Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24:197-211.
10. Braak H, de Vos RAI, Bohl J, Del Tredici K (2006) Gastric a-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 39:67-72.
11. 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 113:421-429.
12. Bradley RM, Fukami H, Suwabe T (2005) Neurobiology of the gustatory-salivary reflex. Chem Senses 30:i70-i71.
13. 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 19:11-16.
14. Cersósimo MG, Benarroch EE (2008) Neural control of the gastrointestinal tract: implications for Parkinson disease. Mov Disord 23:1065-1073.
15. 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. Chou KL, Evatt M, Hinson V, Kompoliti K (2007) Sialorrhea in Parkinson's disease: a review. Mov Disord 22:2306-2313.
17. 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. 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. 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 61:413-426.
20. 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 23:283-290.
21. Dickson DW, Fujishiro H, DelleDonne A et al (2008) Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol 115:437-444.
22. Dickson DW, Braak H, Duda JE et al (2009) Diagnostic criteria for the neuropathological assessment of Parkinson disease. Lancet Neurol 8:1150-1157.
23. 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 38:1237-1244.
24. 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 55:138-142.
25. Edwards LL, Pfeiffer RF, Quigley EMM, Hofman R, Balluff M (1991) Gastrointestinal symptoms in Parkinson's disease. Mov Disord 6:151-156.
26. 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. Emmelin N (1987) Nerve interactions in salivary glands. J Dent Res 66:509-517.
28. 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 24:635-646.
29. Forno LS, Norville RL (1976) Ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol 34:183-197.
30. Frigerio R, Fujishiro H, Ahn TB et al (2009) Incidental Lewy body disease: do some cases represent a preclinical stage of dementia with Lewy bodies? Neurobiol Aging. doi:10.1016/j.neurobiolaging.2009.05.019.
31. Fujishiro H, Frigerio R, Burnett M et al (2008) Cardiac sympathetic denervation correlates with clinical and pathologic stages of Parkinson's disease. Mov Disord 23:1085-1092.
32. 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 66:354-362.
33. Garrett JR (1967) The innervation of normal human submandibular and parotid salivary glands. Arch Oral Biol 12:1417.
34. Garrett JR (1987) The proper role of nerves in salivatory secretion- a review. J Dent Res 66:387-397.
35. Gerling G, Garrett JR, Paterson KL et al (2008) Innervation and secretory function of transplanted human submandibular salivary glands. Transplantation 85:135-140.
36. 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 118:777-784.
37. Giess R, Werner E, Beck M et al (2002) Impaired salivary gland function reveals autonomic dysfunction in amyotrophic lateral sclerosis. J Neurol 249:1246-1249.
38. Gilman S, Wenning GK, Low PA et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670-676.
39. 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 19:1020-1028.
40. Goldstein DS, Holmes CS, Dendi R, Bruce SR, Li ST (2002) Orthostatic hypotension from sympathetic denervation in Parkinson's disease. Neurology 58:1247-1255. (Pubitemid 34411870)
41. Hawkes CH, Shephard BC, Daniel SE (1997) Olfactory dysfunction in Parkinson's disease. J Neurol Neurosurg Psychiatry 62:436-444.
42. 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 23:837-844.
43. Hornby PJ, Abrahams TP (2000) Central control of lower esophageal sphincter relaxation. Am J Med 108(Suppl 4):90S- 98S.
44. 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 52:1269-1271.
45. Kaplan MD, Baum BJ (1993) The function of saliva. Dysphagia 9:225-229.
46. 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 41:455-463.
47. Kuusisto E, Parkkinen L, Alafuzoff I (2003) Morphogenesis of Lewy bodies: dissimilar incorporation of a-synuclein, ubiquitin, and p62. J Neuropathol Exp Neurol 62:1241-1253.
48. Kyriacou K, Garrett JR (1988) Morphological changes in the rabbit submandibular gland after parasympathetic or sympathetic denervation. Arch Oral Biol 33:281-290.
49. Leopold NA, Kagel MC (1995) Prepharyngeal dysphagia in Parkinson's disease. Dysphagia 11:14-22.
50. Leopold NA, Kagel MC (1997) Pharyngo-esophageal dysphagia in Parkinson's disease. Dysphagia 12:11-18.
51. Loewy AD (1991) Forebrain nuclei involved in autonomic control. Prog Brain Res 87:253-268.
52. Markesbery WR, Jicha GA, Liu H, Schmitt FA (2009) Lewy body pathology in normal elderly subjects. J Neuropathol Exp Neurol 68:816-822.
53. Martinez-Madrigal F, Micheau C (1989) Histology of the major salivary glands. Am J Surg Pathol 13:879-899.
54. 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 23:1623-1629.
55. McKeith IG, Dickson DW, Lowe J et al (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863-1872.
56. Miki Y, Mori F, Wakabayashi K, Kuroda N, Orimo S (2009) Incidental Lewy body disease restricted to the heart and stellate ganglion. Mov Disord 24:2299-2301.
57. 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 68:2012-2018.
58. 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 30:546-554.
59. 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 17:24-30.
60. Orimo S, Uchihara T, Nakamura A et al (2008) Axonal a-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson's disease. Brain 131:642-650.
61. Pfeiffer RF (1998) Gastrointestinal dysfunction in Parkinson's disease. Clin Neurosci 5:136-146.
62. Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson's disease. Lancet Neurol 2:107-116.
63. 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):1-4.
64. Proctor GB, Carpenter GH (2007) Regulation of salivary gland function by autonomic nerves. Auton Neurosci Basic Clin 133:3-18.
65. Proulx M, de Courval FP, Wiseman MA, Panisset M (2005) Salivary production in Parkinson's disease. Mov Disord 20:204-207.
66. 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 87:848-856.
67. Richards WG, Sugarbaker DJ (1995) Neuronal control of esophageal function. Chest Surg Clin North Am 5:157-171.
68. Robbins JA, Logemann JA, Kirshner HS (1986) Swallowing and speech production in Parkinson's disease. Ann Neurol 19:283-287.
69. Ross GW, Petrovitch H, Abbott RD et al (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21:2062-2067.
70. Schwab RS, England AS (1958) Parkinson's disease. J Chronic Dis 8:448-501.
71. Shannon IL, Suddick RP, Chauncey HH (1969) Effect of atropine- induced flow rate depression on composition of unstimulated human parotid fluid. Arch Oral Biol 14:761-770.
72. Siddiqui MF, Rast S, Lynn MJ, Auchus AP, Pfeiffer RF (2002) Autonomic dysfunction in Parkinson's disease: a comprehensive symptom survey. Parkinsonism Rel Disord 8:277-284.
73. Silvers AR, Som PM (1998) Salivary glands. Radiol Clin North Am 36:941-966.
74. Sone M, Yoshida M, Hashizume Y, Hishikawa N, Sobue G (2005) a-Synuclein-immunoreactive structure formation is enhanced in sympathetic ganglia of patients with multiple system atrophy. Acta Neuropathol 110:19-26.
75. Takeda S, Yamazaki K, Miyakawa T, Arai H (1993) Parkinson's disease with involvement of the parasympathetic ganglia. Acta Neuropathol 86:397-398.
76. 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 27:566-573.
77. 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 16:41-46.
78. Tumilasci OR, Cersósimo MG, Belforte JE, Micheli FE, Benarroch EE, Pazo JH (2006) Quantitative study of salivary secretion in Parkinson's disease. Mov Disord 21:660-667.
79. 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:.
80. 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 76:217-221.
81. 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 79:581-583.
82. 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 138:237-240.
83. 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 60:609-612.