Cortical Lewy bodies and Aβ burden are associated with prevalence and timing of dementia in Lewy body diseases

Neuropathology and Applied Neurobiology

Volumn 42, Issue 5, 2016, Pages 436-450

  Ruffmann, C ^a,b   Calboli, F C F ^a   Bravi, I ^a   Gveric, D ^a   Curry, L K ^a   de Smith, A ^a,c   Pavlou, S ^a,d   Buxton, J L ^a   Blakemore, A I F ^a   Takousis, P ^a   Molloy, S ^a   Piccini, P ^a   Dexter, D T ^a   Roncaroli, F ^e   Gentleman, S M ^a   Middleton, L T ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b PARKINSON INSTITUTE   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

alpha synuclein; A ; dementia; Lewy bodies; neuropathology; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E4;

AGED; AMYLOID PLAQUE; ARTICLE; DEMENTIA; DIFFUSE LEWY BODY DISEASE; FEMALE; GENOTYPE; HAPLOTYPE; HETEROZYGOTE; HUMAN; MAJOR CLINICAL STUDY; MALE; NEOCORTEX; NEUROPATHOLOGY; NEUROPIL THREAD; ONSET AGE; PARIETAL CORTEX; PARKINSON DISEASE; PREVALENCE; PRIORITY JOURNAL; TEMPORAL LOBE;

EID: 84978829327     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12294     Document Type: Article

References (67)

1. McKeith IG, Galasko D, Kosaka K, Perry IK, Dickson DW, Hansen LA, Salmon DP, Lowe J, Mirra SS, Byrne EJ, Lennox G, Quinn NP, Edwardson JA, Ince PG, Bergeron C, Burns A, Miller BL, Lovestone S, Collerton D, Jansen ENH, Ballard C, de VR, Wilcock GK, Jellinger KA, Perry RH; for the Consortium on Dementia with Lewy Bodies. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy Bodies (DLB): report of the consortium on DLB international workshop. Neurology 1996; 47: 1113–24
2. Zaccai J, McCracken C, Brayne C. A systematic review of prevalence and incidence studies of dementia with Lewy bodies. Age Ageing 2005; 34: 561–6
3. Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, Broe GA, Cummings J, Dickson DW, Gauthier S, Goldman J, Goetz C, Korczyn A, Lees A, Levy R, Litvan I, McKeith I, Olanow W, Poewe W, Quinn N, Sampaio C, Tolosa E, Dubois B. Clinical diagnostic criteria for dementia associated with Parkinson's disease. Mov Disord 2007; 22: 1689–707
4. Aarsland D, Andersen K, Larsen JP, Lolk A, Nielsen H, Kragh-Sorensen P. Risk of dementia in Parkinson's disease: a community-based, prospective study. Neurology 2001; 56: 730–6
5. Aarsland D, Andersen K, Larsen JP, Lolk A, Nielsen H, Kragh-Sorensen P. Prevalence and characteristics of dementia in Parkinson disease: an 8-year prospective study. Arch Neurol 2003; 60: 387–92
6. 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 ST, Bubois 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 VMY, 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; for the Consortium on DLB. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005; 65: 1863–72
7. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997; 388: 839–40
8. Baba M, Nakajo S, Tu PH, Tomita T, Nakaya K, Lee VM, Trojanowski JQ, Iwatsubo T. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 1998; 152: 879–84
9. Gibb WRG, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry 1988; 51: 745–52
10. Goedert M, Spillantini MG, Del Tredici K, Braak H. 100 years of Lewy pathology. Nat Rev Neurol 2013; 9: 13–24
11. Aarsland D, Perry R, Brown A, Larsen JP, Ballard C. Neuropathology of dementia in Parkinson's disease: a prospective, community-based study. Ann Neurol 2005; 58: 773–6
12. Apaydin H, Ahlskog JE, Parisi JE, Boeve BF, Dickson DW. Parkinson disease neuropathology: later-developing dementia and loss of the levodopa response. Arch Neurol 2002; 59: 102–12
13. Hurtig HI, Trojanowski JQ, Galvin J, Ewbank D, Schmidt ML, Lee VM, Clark CM, Glosser G, Stern MB, Gollomp SM, Arnold SE. Alpha-synuclein cortical Lewy bodies correlate with dementia in Parkinson's disease. Neurology 2000; 54: 1916–21
14. Irwin DJ, White MT, Toledo JB, Xie SX, Robinson JL, VanDeerlin V, Lee VMY, Leverenz JB, Montine TJ, Duda JE, Hurtig HI, Trojanowski JQ. Neuropathologic substrates of Parkinson disease dementia. Ann Neurol 2012; 72: 587–98
15. Schneider JA, Arvanitakis Z, Yu L, Boyle PA, Leurgans SE, Bennett DA. Cognitive impairment, decline and fluctuations in older community-dwelling subjects with Lewy bodies. Brain 2012; 135: 3005–14
16. Colosimo C, Hughes AJ, Kilford L, Lees AJ. Lewy body cortical involvement may not always predict dementia in Parkinson's disease. J Neurol Neurosurg Psychiatry 2003; 74: 852–6
17. Parkinnen L, Kauppinen T, Pirttilä T, Autere JM, Alafuzoff I. Alpha-synuclein pathology does not predict extrapyramidal symptoms or dementia. Ann Neurol 2005; 57: 82–91
18. Bennett DA, Wilson RS, Boyle PA, Buchman AS, Schneider JA. Relation of neuropathology to cognition in persons without cognitive impairment. Ann Neurol 2012; 72: 599–609
19. Dickson DW, Fujishiro H, DelleDonne A, Menke J, Ahmed Z, Klos KJ, Josephs KA, Frigerio R, Burnett M, Parisi JE, Ahlskog JE. Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol 2008; 115: 437–44
20. Compta Y, Parkkinen L, O'Sullivan SS, Vandrovcova J, Holton JL, Collins C, Lashley T, Kallis C, Williams DR, de Silva R, Lees AJ, Revesz T. Lewy- and Alzheimer-type pathologies in Parkinson's disease dementia: which is more important? Brain 2011; 34: 1493–505
21. Jellinger KA, Attems J. Prevalence and impact of vascular and Alzheimer pathologies in Lewy body disease. Acta Neuropathol 2008; 115: 427–36
22. Horvath J, Herrmann FR, Burkhard PR, Bouras C, Kovari E. Neuropathology of dementia in a large cohort of patients with Parkinson's disease. Parkinsonism Relat Disord 2013; 19: 864–8
23. Sabbagh MN, Adler CH, Lahti TJ, Connor DJ, Vedders L, Peterson LK, Caviness JN, Shill HA, Sue LI, Ziabreva I, Perry E, Ballard CG, Aarsland D, Walker DH, Beach TG. Parkinson disease with dementia: comparing patients with and without Alzheimer pathology. Alzheimer Dis Assoc Disord 2009; 23: 295–7
24. Ballard C, Ziabreva I, Perry R, Larsen JP, O'Brien J, McKeith I, Perry E, Aarsland D. Differences in neuropathologic characteristics across the Lewy body dementia spectrum. Neurology 2006; 67: 1931–4
25. Fushijiro H, Iseki E, Higashi S, Kasanuki K, Murayama N, Togo T, Katsuse O, Uchikado H, Aoki N, Kosaka K, Arai H, Sato K. Distribution of cerebral amyloid deposition and its relevance to clinical phenotype in Lewy body dementia. Neurosci Lett 2010; 486: 19–23
26. Tsuboi Y, Hirotake U, Dickson DW. Neuropathology of Parkinson's disease dementia and dementia with Lewy bodies with reference to striatal pathology. Parkinsonism Relat Disord 2007;00:S221–4
27. Jellinger KA, Attems J. Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies? Acta Neuropathol 2006; 112: 253–60
28. Kalaitzakis ME, Graeber MB, Gentleman SM, Pearce RKB. Striatal beta-amyloid deposition in Parkinson disease with dementia. J Neuropathol Exp Neurol 2008; 67: 155–61
29. Kalaitzakis ME, Walls AJ, Pearce RKB, Gentleman SM. Striatal Aβ peptide deposition mirrors dementia and differentiates DLB and PDD from other parkinsonian syndromes. Neurobiol Dis 2011; 41: 377–84
30. Howlett DR, Whitfield D, Johnson M, Attems J, O'Brien JT, Aarsland D, Lai MKP, Lee JH, Chen C, Ballard C, Hortobagyi T, Francis PT. Regional multiple pathology scores are associated with cognitive decline in Lewy Body Dementias. Brain Pathol 2014; 25(4): 401–408. doi: 10.1111/bpa.12182
31. Nelson PT, Kryscio RJ, Jicha GA, Abner EL, Schmitt FA, Xu LO, Cooper G, Smith CD, Markesbery WR. Relative preservation of MMSE scores in autopsy-proven dementia with Lewy bodies. Neurology 2009; 73: 1127–33
32. Lashley T, Holton JL, Gray E, Kirkham K, O'Sullivan SS, Hilbig A, Wood NW, Lees AJ, Revesz T. Cortical alpha-synuclein load is associated with amyloid-beta plaque burden in a subset of Parkinson's disease patients. Acta Neuropathol 2008; 115: 417–25
33. Mattila PM, Rinne JO, Helenius H, Dickson DW, Roytta M. Alpha-synuclein-immunoreactive cortical Lewy bodies are associated with cognitive impairment in Parkinson's disease. Acta Neuropathol 2000; 100: 285–90
34. Pletnikova O, West N, Lee MK, Rudow GL, Skolasky RL, Dawson TM, Marsh L, Troncoso JC. Abeta deposition is associated with enhanced cortical alpha-synuclein lesions in Lewy body diseases. Neurobiol Aging 2005; 26: 1183–92
35. Colom-Cadena M, Gelpi E, Charif S, Belbin O, Blesa R, Marti MJ, Clarimon J, Lleo A. Confluence of α-synuclein, tau, and β-amyloid pathologies in Dementia with Lewy Bodies. J Neuropathol Exp Neurol 2013; 72: 1203–12
36. Tsuang D, Leverenz JB, Lopez OL, Hamilton RL, Bennett DA, Schneider JA, Buchman AS, Larson EB, Crane PK, Kaye JA, Kramer P, Woltjer R, Trojanowski JQ, Weintraub D, Chen-Plotkin AS, Irwin DJ, Rick J, Schellenberg GD, Watson GS, Kukull W, Nelson PT, Jicha GA, Neltner JH, Galasko D, Masliah E, Quinn JF, Chung KA, Yearout D, Mata IF, Wan JY, Edwards KL, Montine TJ, Zabetian CP. APOE ϵ4 increases risk for dementia in pure synucleinopathies. JAMA Neurol 2013; 70: 223–8
37. Goris A, Williams-Gray CH, Clark GR, Foltynie T, Lewis SJ, Brown J, Ban M, Spillantini MG, Compston A, Burn DJ, Chinnery PF, Barker RA, Sawcer SJ. Tau and alpha-synuclein in susceptibility to, and dementia in, Parkinson's disease. Ann Neurol 2007; 62: 145–53
38. Williams-Gray CH, Evans JR, Goris A, Foltynie T, Ban M, Robbins TW, Brayne C, Kolachana BS, Weinberger DR, Sawcer SJ, Barker RA. The distinct cognitive syndromes of Parkinson's disease: 5 year follow-up of the Campaign cohort. Brain 2009; 132: 2958–69
39. Colom-Cadena M, Gelpi E, Martí MJ, Charif S, Dols-Icardo O, Blesa R, Clarimon J, Lleo A. MAPT H1 haplotype is associated with enhanced α-synuclein deposition in dementia with Lewy bodies. Neurobiol Aging 2013; 34: 936–42
40. Schmechel DE, Saunders AM, Strittmatter WJ, Crain BJ, Hulette CM, Joo SH, Pericak-Vance MA, Goldgaber D, Roses AD. Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late onset Alzheimer disease. Proc Natl Acad Sci U S A 1993; 90: 9649–53
41. Kobayashi S, Tateno M, Park TW, Utsumi K, Sohma H, Ito YM, Kokai Y, Saito T. Apolipoprotein E4 frequencies in a Japanese population with Alzheimer's disease and dementia with Lewy bodies. PLoS ONE 2011; 6: e18569
42. Lane R, He Y, Morris C, Leverenz JB, Emre M, Ballard C. BuChE-K and APOE e4 allele frequencies in Lewy body dementias, and influence of genotype and hyperhomocysteinemia on cognitive decline. Mov Disord 2009; 24: 392–400
43. Polvikosky T, Sulkava R, Haltia M, Kainulainen K, Vuorio A, Verkkoniemi A, Niinisto L, Halonen P, Kontula K. Apoliprotein E, dementia, and cortical deposition of β-Amyloid protein. N Engl J Med 1995; 333: 1242–7
44. Bras J, Guerreiro R, Darwent L, Parkkinen L, Ansorge A, Escott-Price V, Hernandez DG, Nalls MA, Clark LN, Honig LS, Marder K, Van Der Flier WM, Lemstra A, Scheltens P, Rogaeva E, St George-Hyslop P, Londos E, Zetterberg H, Ortega-Cubero S, Pastor P, Ferman TJ, Graff-Radford NR, Ross OA, Barber I, Braae A, Brown K, Morgan K, Maetzler W, Berg D, Troakes C, Al-Sarraj S, Lashley T, Compta Y, Revesz T, Lees A, Cairns N, Halliday GM, Mann D, Pickering-Brown S, Dickson DW, Singleton A, Hardy J. Genetic analysis implicates APOE, SNCA and suggests lysosomal dysfunction in the etiology of dementia with Lewy bodies. Hum Mol Genet 2014; 23: 6139–46
45. Huang X, Chen P, Kaufer DI, Troster AI, Poole C. Apolipoprotein E and dementia in Parkinson disease: a meta-analysis. Arch Neurol 2006; 63: 189–93
46. Pankratz N, Byder L, Halter C, Rudolph A, Shults CW, Conneally PM, Foroud T, Nichols WC. Presence of an APOE4 allele results in significantly earlier onset of Parkinson's disease and a higher risk with dementia. Mov Disord 2006; 21: 45–9
47. Jasinska-Myga B, Opala G, Goetz CG, Tustanowski J, Ochudio S, Gorzkowska A, Tyrpa J. Apolipoprotein E gene polymorphism, total plasma cholesterol level, and Parkinson disease dementia. Arch Neurol 2007; 64: 261–5
48. Williams-Gray CH, Goris A, Saiki M, Foltynie T, Compston DA, Sawcer SJ, Barker RA. Apoliprotein E genotype as a risk factor for susceptibility to and dementia in Parkinson's disease. J Neurol 2009; 256: 493–8
49. Wakabayashi K, Kakita A, Hayashi S, Okuizumi K, Onodera O, Tanaka H, Ishikawa A, Tsuji S, Takahashi H. Apolipoprotein E epsilon4 allele and progression of cortical Lewy body pathology in Parkinson's disease. Acta Neuropathol 1998; 95: 450–4
50. Diagnostic and Statistical Manual of Mental Disorders 4th edn. Washington, DC: American Psychiatric Association, 2000
51. Alafuzoff I, Ince PG, Arzberger T, Al-Sarraj S, Bell J, Bodi I, Bogdanovic N, Bugiani O, Ferrer I, Gelpi E, Gentleman S, Giaccone G, Ironside JW, Kavantzas N, King A, Korkolopoulou P, Kovacs GG, Meyronet D, Monoranu C, Parchi P, Parkkinen L, Patsouris E, Roggendorf W, Rozemuller A, Stadelmann N, Streichenberger N, Thal DR, Kretzschmar H. Staging/typing of Lewy body related α-synuclein pathology: a study of the BrainNet Europe Consortium. Acta Neuropathol 2009; 117: 635–52
52. Alafuzoff I, Arzberger T, Al-Sarraj S, Bodi I, Bogdanovic N, Braak H, Bugiani O, Del-Tredici K, Ferrer I, Gelpi E, Giaccone G, Graeber MB, Ince P, Kamphorst W, King A, Korkolopoulou P, Kovacs GG, Larionov S, Meyronet D, Monoranu C, Parchi P, Patsouris E, Roggendorf W, Seilhean D, Tagliavini F, Stadelmann C, Streichenberger N, Thal DR, Wharton SB, Kretzschmar H. Staging of neurofibrillary pathology in Alzheimer's disease: a study of the Brain-Net Europe Consortium. Brain Pathol 2008; 18: 484–96
53. Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, Nelson PT, Shneider JA, Thal DR, Trojanowski JQ, Vinters HV, Hyman BT. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach. Acta Neuropathol 2012; 123: 1–11
54. The R project for statistical computing. Available at: http://www.r-project.org (last accessed 01-08-2015)
55. Harding AJ, Halliday GM. Cortical Lewy body pathology in the diagnosis of dementia. Acta Neuropathol 2001; 102: 355–63
56. Edison P, Rowe CC, Rinne JO, Ng S, Ahmed I, Kemppainen N, Villemagne VL, O'Keefe G, Nagren K, Chaudhury KR, Masters CL, Brooks DJ. Amyloid load in Parkinson's disease dementia and Lewy body dementia measured with [11C]PIB positron emission tomography. J Neurol Neurosurg Psychiatry 2008; 79: 1331–8
57. Shimada H, Shinotoh H, Hirano S, Miyoshi M, Sato K, Tanaka N, Ota T, Fukushi K, Irie T, Ito H, Higuchi M, Kuwabara S, Suhara T. β-amyloid in Lewy body disease is related to Alzheimer's disease-like atrophy. Mov Disord 2013; 28: 169–75
58. Halliday G, Hely M, Reid W, Morris J. The progression of pathology in longitudinally followed patients with Parkinson's disease. Acta Neuropathol 2008; 115: 409–15
59. Kok E, Haikonen S, Luoto T, Huhtala H, Goebeler S, Haapasalo H, Karhunen PJ. Apolipoprotein E-dependent accumulation of Alzheimer disease-related lesions begins in middle age. Ann Neurol 2009; 65: 650–7
60. Kempster PA, O'Sullivan SS, Holton JL, Revesz T, Lees AJ. Relationships between age and late progression of Parkinson's disease: a clinico-pathological study. Brain 2010; 133: 1755–62
61. Braak H, Del Tredici K, Rüb U, de Vos RAI, Jansen Steur ENH, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003; 24: 197–211
62. Masliah E, Rockenstein E, Veinbergs I, Sagara Y, Mallory M, Hashimoto M, Mucke L. beta-amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci U S A 2001; 98: 12245–50
63. Tsigelny IF, Crews L, Desplats P, Shaked GM, Sharikov Y, Mizuno H, Spencer B, Rockenstein E, Trejo M, Platoshyn O, Yuan JX, Masliah E. Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PLoS ONE 2008; 3: e3135
64. Gearing M, Schneider JA, Rebeck GW, Hyman BT, Mirra SS. Alzheimer's disease with and without coexisting Parkinson's disease changes: apolipoprotein E genotype and neuropathologic correlates. Neurology 1995; 45: 1985–90
65. Lippa CF, Smith TW, Saunders AM, Crook R, Pulaski-Salo D, Davies P, Hardy J, Roses AD, Dickson D. Apolipoprotein E genotype and Lewy body disease. Neurology 1995; 45: 97–103
66. Vernon AC, Ballard C, Modo M. Neuroimaging for Lewy body disease: is the in vivo molecular imaging of α-synuclein neuropathology required and feasible? Brain Res Rev 2010; 65: 28–65
67. Attems J, Neltner JH, Nelson PT. Quantitative neuropathological assessment to investigate cerebral multi-morbidity. Alzheimers Res Ther 2014; 6: 85