Advertisement

Peripheral Lewy body pathology in Parkinson's disease and incidental Lewy body disease: Four cases

  • Kelly Del Tredici
    Correspondence
    Corresponding author at: Clinical Neuroanatomy, Center for Clinical Research (Dept. of Neurology), Helmholtzstrasse 8/1, 89081 Ulm, Germany. Tel.: +49 731 500 63114; fax: +49 731 500 61333.
    Affiliations
    Clinical Neuroanatomy (Center for Clinical Research, Department of Neurology), University of Ulm, 89081 Ulm, Germany
    Search for articles by this author
  • John E. Duda
    Affiliations
    Parkinson's Disease Research, Education & Clinical Center, Philadelphia VA Medical Center & Department of Neurology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
    Search for articles by this author

      Abstract

      The accumulation of Lewy pathology (LP) within autonomic nervous system tissues has received increased attention recently as a possible induction site for Lewy neurodegeneration and a possible source of biopsy material for biomarkers of early Parkinson's disease (PD). Here, we describe LP accumulation within various tissues involving peripheral autonomic nervous system neurons in three PD cases and one case of incidental Lewy body disease. Findings highlight the value of examining pathology within functional neuroanatomical systems and particularly the importance of Lewy neurites (LNs) in the pathophysiology of PD.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Neurological Sciences
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Lewy F.H.
        Paralysis agitans. Part I: Pathologische anatomie.
        in: Lewandowsky M. Handbuch der Neurologie, III, spez. Neurol. II. Springer, Berlin1912: 920-933
        • Tretiakoff C.
        Contribution a l'etude de l'anatomie pathologique du locus niger de Soemmering avec quelques deductions relatives a la pathogenie des troubles du tonus musculaire et de la maladie de Parkinson.
        1919 (Paris)
        • Del Tredici K.
        • Rüb U.
        • de Vos R.A.
        • Bohl J.R.
        • Braak H.
        Where does Parkinson disease pathology begin in the brain?.
        J Neuropathol Exp Neurol. 2002; 61: 413-426
        • Braak H.
        • Del Tredici K.
        • Rüb U.
        • de Vos R.A.
        • Jansen Steur E.N.
        • Braak E.
        Staging of brain pathology related to sporadic Parkinson's disease.
        Neurobiol Aging. 2003; 24: 197-211
        • Braak H.
        • Rüb U.
        • Gai W.P.
        • Del Tredici K.
        Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen.
        J Neural Transm. 2003; 110: 517-536
        • Braak H.
        • Del Tredici K.
        Neuroanatomy and pathology of sporadic Parkinson's disease.
        Adv Anat Embryol Cell Biol. 2009; 201: 1-119
        • Dickson D.W.
        • Fujishiro H.
        • DelleDonne A.
        • Menke J.
        • Ahmed Z.
        • Klos K.J.
        • et al.
        Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease.
        Acta Neuropathol. 2008; 115: 437-444
        • Fujishiro H.
        • Frigerio R.
        • Burnett M.
        • Klos K.J.
        • Josephs K.A.
        • DelleDonne A.
        • et al.
        Cardiac sympathetic denervation correlates with clinical and pathologic stages of Parkinson's disease.
        Mov Disord. 2008; 23: 1085-1092
        • Takeda S.
        • Yamazaki K.
        • Miyakawa T.
        • Arai H.
        Parkinson's disease with involvement of the parasympathetic ganglia.
        Acta Neuropathol. 1993; 86: 397-398
        • Wakabayashi K.
        • Takahashi H.
        • Takeda S.
        • Ohama E.
        • Ikuta F.
        Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses.
        Acta Neuropathol. 1988; 76: 217-221
        • Martinez-Martin P.
        • Schapira A.H.
        • Stocchi F.
        • Sethi K.
        • Odin P.
        • MacPhee G.
        • et al.
        Prevalence of nonmotor symptoms in Parkinson's disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients.
        Mov Disord. 2007; 22: 1623-1629
        • Barone P.
        • Antonini A.
        • Colosimo C.
        • Marconi R.
        • Morgante L.
        • Avarello T.P.
        • et al.
        The PRIAMO study: a multicenter assessment of non motor symptoms and their impact on quality of life in Parkinson's disease.
        Mov Disord. 2009; 24: 1641-1649
        • Verbaan D.
        • Marinus J.
        • Visser M.
        • van Rooden S.M.
        • Stiggelbout A.M.
        • van Hilten J.J.
        Patient-reported autonomic symptoms in Parkinson disease.
        Neurology. 2007; 69: 333-341
        • Gallagher D.A.
        • Lees A.J.
        • Schrag A.
        What are the most important nonmotor symptoms in patients with Parkinson's disease and are we missing them?.
        Mov Disord. 2010; 25: 2493-2500
        • Martinez-Martin P.
        • Rodriguez-Blazquez C.
        • Kurtis M.M.
        • Chaudhuri K.R.
        The impact of non-motor symptoms on health-related quality of life of patients with Parkinson's disease.
        Mov Disord. 2011; 26: 399-406
        • Iwanaga K.
        • Wakabayashi K.
        • Yoshimoto M.
        • Tomita I.
        • Satoh H.
        • Takashima H.
        • et al.
        Lewy body-type degeneration in cardiac plexus in Parkinson's and incidental Lewy body diseases.
        Neurology. 1999; 52: 1269-1271
        • Bloch A.
        • Probst A.
        • Bissig H.
        • Adams H.
        • Tolnay M.
        Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects.
        Neuropathol Appl Neurobiol. 2006; 32: 284-295
        • Abbott R.D.
        • Ross G.W.
        • Petrovitch H.
        • Tanner C.M.
        • Davis D.G.
        • Masaki K.H.
        • et al.
        Bowel movement frequency in late-life and incidental Lewy bodies.
        Mov Disord. 2007; 22: 1581-1586
        • Minguez-Castellanos A.
        • Chamorro C.E.
        • Escamilla-Sevilla F.
        • Ortega-Moreno A.
        • Rebollo A.C.
        • Gomez-Rio M.
        • et al.
        Do alpha-synuclein aggregates in autonomic plexuses predate Lewy body disorders?: a cohort study.
        Neurology. 2007; 68: 2012-2018
        • Frigerio R.
        • Fujishiro H.
        • Maraganore D.M.
        • Klos K.J.
        • DelleDonne A.
        • Heckman M.G.
        • et al.
        Comparison of risk factor profiles in incidental Lewy body disease and Parkinson disease.
        Arch Neurol. 2009; 66: 1114-1119
        • Adler C.H.
        • Connor D.J.
        • Hentz J.G.
        • Sabbagh M.N.
        • Caviness J.N.
        • Shill H.A.
        • et al.
        Incidental Lewy body disease: clinical comparison to a control cohort.
        Mov Disord. 2010; 25: 642-646
        • Dickson D.W.
        • Braak H.
        • Duda J.E.
        • Duyckaerts C.
        • Gasser T.
        • Halliday G.M.
        • et al.
        Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria.
        Lancet Neurol. 2009; 8: 1150-1157
        • Del Tredici K.
        • Hawkes C.H.
        • Ghebremedhin E.
        • Braak H.
        Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson's disease.
        Acta Neuropathol. 2010; 119: 703-713
        • Braak H.
        • Sastre M.
        • Bohl J.R.
        • de Vos R.A.I.
        • Del Tredici K.
        Parkinson's disease: lesions in dorsal horn layer I, involvement of parasympathetic and sympathetic pre- and postganglionic neurons.
        Acta Neuropathol. 2007; 113: 421-429
        • Braak H.
        • Braak E.
        Neuropathological stageing of Alzheimer-related changes.
        Acta Neuropathol. 1991; 82: 239-259
        • Braak H.
        • Alafuzoff I.
        • Arzberger T.
        • Kretzschmar H.
        • Del Tredici K.
        Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry.
        Acta Neuropathol. 2006; 112: 389-404
        • Thal D.R.
        • Rüb U.
        • Orantes M.
        • Braak H.
        Phases of Abeta-deposition in the human brain and its relevance for the development of AD.
        Neurology. 2002; 58: 1791-1800
        • Braak H.
        • Del Tredici K.
        The pathological process underlying Alzheimer's disease in individuals under thirty.
        Acta Neuropathol. 2011; 121: 171-181
        • Braak H.
        • de Vos R.A.
        • Bohl J.
        • Del Tredici K.
        Gastric alpha-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology.
        Neurosci Lett. 2006; 396: 67-72
        • Chou K.L.
        • Evatt M.
        • Hinson V.
        • Kompoliti K.
        Sialorrhea in Parkinson's disease: a review.
        Mov Disord. 2007; 22: 2306-2313
        • Evatt M.L.
        • Chaudhuri K.R.
        • Chou K.L.
        • Cubo E.
        • Hinson V.
        • Kompoliti K.
        • et al.
        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. 2009; 24: 635-646
        • Leopold N.A.
        • Kagel M.C.
        Pharyngo-esophageal dysphagia in Parkinson's disease.
        Dysphagia. 1997; 12: 11-18
        • den Hartog Jager W.A.
        • Bethlem J.
        The distribution of Lewy bodies in the central and autonomic nervous systems in idiopathic paralysis agitans.
        J Neurol Neurosurg Psychiatry. 1960; 23: 283-290
        • Qualman S.J.
        • Haupt H.M.
        • Yang P.
        • Hamilton S.R.
        Esophageal Lewy bodies associated with ganglion cell loss in achalasia. Similarity to Parkinson's disease.
        Gastroenterology. 1984; 87: 848-856
        • Fumimura Y.
        • Ikemura M.
        • Saito Y.
        • Sengoku R.
        • Kanemaru K.
        • Sawabe M.
        • et al.
        Analysis of the adrenal gland is useful for evaluating pathology of the peripheral autonomic nervous system in Lewy body disease.
        J Neuropathol Exp Neurol. 2007; 66: 354-362
        • Miki Y.
        • Mori F.
        • Wakabayashi K.
        • Kuroda N.
        • Orimo S.
        Incidental Lewy body disease restricted to the heart and stellate ganglia.
        Mov Disord. 2009; 24: 2299-2301
        • Orimo S.
        • Amino T.
        • Itoh Y.
        • Takahashi A.
        • Kojo T.
        • Uchihara T.
        • et al.
        Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease.
        Acta Neuropathol. 2005; 109: 583-588
        • Orimo S.
        • Uchihara T.
        • Nakamura A.
        • Mori F.
        • Kakita A.
        • Wakabayashi K.
        • et al.
        Axonal alpha-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson's disease.
        Brain. 2008; 131: 642-650
        • Duda J.E.
        Pathology and neurotransmitter abnormalities of dementia with Lewy bodies.
        Dement Geriatr Cogn Disord. 2004; 17: 3-14
        • Duda J.E.
        Olfactory system pathology as a model of Lewy neurodegenerative disease.
        J Neurol Sci. 2010; 289: 49-54
        • Olanow C.W.
        • Perl D.P.
        • Demartino G.N.
        • McNaught K.S.
        Lewy-body formation is an aggresome-related process: a hypothesis.
        Lancet Neurol. 2004; 3: 496-503
        • Giasson B.I.
        • Duda J.E.
        • Quinn S.M.
        • Zhang B.
        • Trojanowski J.Q.
        • Lee V.M.
        Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein.
        Neuron. 2002; 34: 521-533
        • Goldstein L.S.
        Do disorders of movement cause movement disorders and dementia?.
        Neuron. 2003; 40: 415-425
        • Roy S.
        • Zhang B.
        • Lee V.M.
        • Trojanowski J.Q.
        Axonal transport defects: a common theme in neurodegenerative diseases.
        Acta Neuropathol. 2005; 109: 5-13
        • Li W.
        • Hoffman P.N.
        • Stirling W.
        • Price D.L.
        • Lee M.K.
        Axonal transport of human alpha-synuclein slows with aging but is not affected by familial Parkinson's disease-linked mutations.
        J Neurochem. 2004; 88: 401-410
        • Edwards L.L.
        • Quigley E.M.
        • Harned R.K.
        • Hofman R.
        • Pfeiffer R.F.
        Characterization of swallowing and defecation in Parkinson's disease.
        Am J Gastroenterol. 1994; 89: 15-25
        • Proulx M.
        • de Courval F.P.
        • Wiseman M.A.
        • Panisset M.
        Salivary production in Parkinson's disease.
        Mov Disord. 2005; 20: 204-207
        • Tumilasci O.R.
        • Cersosimo M.G.
        • Belforte J.E.
        • Micheli F.E.
        • Benarroch E.E.
        • Pazo J.H.
        Quantitative study of salivary secretion in Parkinson's disease.
        Mov Disord. 2006; 21: 660-667