Hippocampal sclerosis in advanced age: Clinical and pathological features

Brain

Volumn 134, Issue 5, 2011, Pages 1506-1518

  Nelson, Peter T ^a,b   Schmitt, Frederick A ^b,c   Lin, Yushun ^a   Abner, Erin L ^b   Jicha, Gregory A ^b,c   Patel, Ela ^b   Thomason, Paula C ^b   Neltner, Janna H ^a   Smith, Charles D ^b,c   Santacruz, Karen S ^d   Sonnen, Joshua A ^e   Poon, Leonard W ^f   Gearing, Marla ^g   Green, Robert C ^h   Woodard, John L ⁱ   Van Eldik, Linda J ^b,c   Kryscio, Richard J ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d University of Georgia ^*  (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f UNIVERSITY OF GEORGIA   (United States)

^g EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

biomarkers; cerebrovascular; epilepsy; FTLD; PGRN; stroke

Indexed keywords

APOLIPOPROTEIN E; EOSIN; HEMATOXYLIN; TAR DNA BINDING PROTEIN;

AGED; AGING; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; COGNITION; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; EDUCATIONAL STATUS; FEMALE; FRONTOTEMPORAL DEMENTIA; GENOTYPE; HIPPOCAMPAL SCLEROSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NEUROPATHOLOGY; PREVALENCE; PRIORITY JOURNAL; TISSUE SECTION;

AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; COHORT STUDIES; DNA-BINDING PROTEINS; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MENTAL STATUS SCHEDULE; NEUROPSYCHOLOGICAL TESTS; SCLEROSIS;

EID: 79957469955     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr053     Document Type: Article

References (71)

1. Ala TA, Beh GO, Frey WH 2nd. Pure hippocampal sclerosis: A rare cause of dementia mimicking Alzheimer's disease. Neurology 2000; 54: 843-8. (Pubitemid 30111340)
2. Amador-Ortiz C, Ahmed Z, Zehr C, Dickson DW. Hippocampal sclerosis dementia differs from hippocampal sclerosis in frontal lobe degeneration. Acta Neuropathol 2007a; 113: 245-52. (Pubitemid 46443560)
3. Amador-Ortiz C, Lin WL, Ahmed Z, Personett D, Davies P, Duara R, et al. TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer's disease. Ann. Neurol 2007b; 61: 435-45. (Pubitemid 46878771)
4. Armstrong RA, Ellis W, Hamilton RL, Mackenzie IR, Hedreen J, Gearing M, et al. Neuropathological heterogeneity in frontotemporal lobar degeneration with TDP-43 proteinopathy: A quantitative study of 94 cases using principal components analysis. J Neural Transm 2010; 117: 227-39.
5. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992; 42 (3 Pt 1): 631-9.
6. Attems J, Jellinger KA. Hippocampal sclerosis in Alzheimer disease and other dementias. Neurology 2006; 66: 775. (Pubitemid 43739848)
7. Baborie A, Griffiths TD, Jaros E, McKeith IG, Burn DJ, Richardson A, et al. Pathological correlates of frontotemporal lobar degeneration in the elderly. Acta Neuropathol 2010.
8. Barker WW, Luis CA, Kashuba A, Luis M, Harwood DG, Loewenstein D, et al. Relative frequencies of Alzheimer disease, Lewy body, vascular and frontotemporal dementia, and hippocampal sclerosis in the State of Florida Brain Bank. Alzheimer Disease and Associated Disorders 2002; 16: 203-12. (Pubitemid 35434796)
9. Beach TG, Sue L, Scott S, Layne K, Newell A, Walker D, et al. Hippocampal sclerosis dementia with tauopathy. Brain Pathol 2003; 13: 263-78. (Pubitemid 36975818)
10. Blass DM, Hatanpaa KJ, Brandt J, Rao V, Steinberg M, Troncoso JC, et al. Dementia in hippocampal sclerosis resembles frontotemporal dementia more than Alzheimer disease. Neurology 2004; 63: 492-7. (Pubitemid 39031379)
11. Cairns NJ, Bigio EH, Mackenzie IR, Neumann M, Lee VM, Hatanpaa KJ, et al. Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: Consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007; 114: 5-22. (Pubitemid 47029055)
12. Chui HC, Zarow C, Mack WJ, Ellis WG, Zheng L, Jagust WJ, et al. Cognitive impact of subcortical vascular and Alzheimer's disease pathology. Ann Neurol 2006; 60: 677-87. (Pubitemid 46048485)
13. Clark AW, White CL 3rd, Manz HJ, Parhad IM, Curry B, Whitehouse PJ, et al. Primary degenerative dementia without Alzheimer pathology. Can J Neurol Sci 1986; 13 (Suppl 4): 462-70. (Pubitemid 17212703)
14. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Ageing, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol Age 1997; 18 (Suppl 4): S1-2.
15. Corey-Bloom J, Sabbagh MN, Bondi MW, Hansen L, Alford MF, Masliah E, et al. Hippocampal sclerosis contributes to dementia in the elderly. Neurology 1997; 48: 154-60. (Pubitemid 27039534)
16. Crystal HA, Dickson D, Davies P, Masur D, Grober E, Lipton RB. The relative frequency of "dementia of unknown etiology" increases with age and is nearly 50% in nonagenarians. Arch Neurol 2000; 57: 713-9. (Pubitemid 30252807)
17. Davis DG, Schmitt FA, Wekstein DR, Markesbery WR. Alzheimer neuropathologic alterations in aged cognitively normal subjects. J Neuropathol Exp Neurol 1999; 58: 376-88. (Pubitemid 29187900)
18. Davidson Y, Kelley T, Mackenzie IR, Pickering-Brown S, Du Plessis D, Neary D, et al. Ubiquitinated pathological lesions in frontotemporal lobar degeneration contain the TAR DNA-binding protein, TDP-43. Acta Neuropathol 2007; 113: 521-33. (Pubitemid 46672598)
19. Dickson DW, Davies P, Bevona C, Van Hoeven KH, Factor SM, Grober E, et al. Hippocampal sclerosis: A common pathological feature of dementia in very old (4 or = 80 years of age) humans. Acta Neuropathol 1994; 88: 212-21. (Pubitemid 24265424)
20. Dolan D, Troncoso J, Resnick SM, Crain BJ, Zonderman AB, O'Brien RJ. Age, Alzheimer's disease and dementia in the Baltimore longitudinal study of ageing. Brain 2010; 133 (Pt 8): 2225-31.
21. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12: 189-98.
22. Gosche KM, Mortimer JA, Smith CD, Markesbery WR, Snowdon DA. Hippocampal volume as an index of Alzheimer neuropathology: Findings from the Nun Study. Neurology 2002; 58 (10): 1476-82. (Pubitemid 34552952)
23. Hatanpaa KJ, Blass DM, Pletnikova O, Crain BJ, Bigio EH, Hedreen JC, et al. Most cases of dementia with hippocampal sclerosis may represent frontotemporal dementia. Neurology 2004; 63: 538-42.
24. Hensley B, Martin P, MacDonald M, Poon L, Jazwinski SM, Green RC, et al. Family history and adaptation among centenarians and octogenarians. Gerontology 2010; 56: 83-7.
25. Horn M, Schlote W. Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol 1992; 85: 79-87.
26. Jellinger K. Pure hippocampal sclerosis: A rare cause of dementia mimicking Alzheimer's disease. Neurology 2000; 55: 739-40.
27. Jellinger KA. Hippocampal sclerosis: A common pathological feature of dementia in very old humans. Acta Neuropathol 1994; 88: 599. (Pubitemid 24364711)
28. Jellinger KA, Attems J. Neuropathological evaluation of mixed dementia. J Neurol Sci 2007; 257: 80-7. (Pubitemid 46856518)
29. Josephs KA, Ahmed Z, Katsuse O, Parisi JF, Boeve BF, Knopman DS, et al. Neuropathologic features of frontotemporal lobar degeneration with ubiquitin-positive inclusions with progranulin gene (PGRN) mutations. J Neuropathol Exp Neurol 2007; 66: 142-51. (Pubitemid 46208735)
30. Josephs KA, Stroh A, Dugger B, Dickson DW. Evaluation of subcortical pathology and clinical correlations in FTLD-U subtypes. Acta Neuropathol 2009; 118: 349-58.
31. Josephs KA, Whitwell JL, Knopman DS, Hu WT, Stroh DA, Baker M, et al. Abnormal TDP-43 immunoreactivity in AD modifies clinicopathologic and radiologic phenotype. Neurology 2008; 70: 1850-57. (Pubitemid 351653955)
32. King A, Sweeney F, Bodi I, Troakes C, Maekawa S, Al-Sarraj S. Abnormal TDP-43 expression is identified in the neocortex in cases of dementia pugilistica, but is mainly confined to the limbic system when identified in high and moderate stages of Alzheimer's disease. Neuropathology 2010; 30: 408-19.
33. Kotapka MJ, Graham DI, Adams JH, Gennarelli TA. Hippocampal pathology in fatal non-missile human head injury. Acta Neuropathol 1992; 83: 530-4.
34. Kril JJ, Patel S, Harding AJ, Halliday GM. Patients with vascular dementia due to microvascular pathology have significant hippocampal neuronal loss. J Neurol Neurosurg Psychiatry 2002; 72: 747-51. (Pubitemid 34557018)
35. Lee EB, Lee VM, Trojanowski JQ, Neumann M. TDP-43 immunoreactivity in anoxic, ischemic and neoplastic lesions of the central nervous system. Acta Neuropathol 2008; 115: 305-11.
36. Leverenz JB, Agustin CM, Tsuang D, Peskind ER, Edland SD, Nochlin D, et al. Clinical and neuropathological characteristics of hippocampal sclerosis: A community-based study. Arch Neurol 2002; 59 (7): 1099-106. (Pubitemid 34755822)
37. Lippa CF, Dickson DW. Hippocampal sclerosis dementia: Expanding the phenotypes of frontotemporal dementias? Neurology 2004; 63: 414-5. (Pubitemid 39031368)
38. Mackenzie IR, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, et al. Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: Classification and relation to clinical phenotype. Acta Neuropathol 2006; 112: 539-49. (Pubitemid 44550678)
39. McKee AC, Gavett BE, Stern RA, Nowinski CJ, Cantu RC, Kowall NW, et al. TDP-43 proteinopathy and motor neuron disease in chronic traumatic encephalopathy. J Neuropathol Exp Neurol 2010; 69: 918-29.
40. Martins CA, Oulhaj A, de Jager CA, Williams JH. APOE alleles predict the rate of cognitive decline in Alzheimer disease: A nonlinear model. Neurology 2005; 65: 1888-93. (Pubitemid 43970105)
41. Miki Y, Mori F, Hori E, Kaimori M, Wakabayashi K. Hippocampal sclerosis with four-repeat tau-positive round inclusions in the dentate gyrus: A new type of four-repeat tauopathy. Acta Neuropathol 2009; 117: 713-8.
42. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991; 41: 479-86.
43. Morris JC, Heyman A, Mohs RC, Hughes JP, van Belle G, Fillenbaum G, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 1989; 39: 1159-65. (Pubitemid 19239715)
44. Nelson PT, Abner EL, Scheff SW, Schmitt FA, Kryscio RJ, Jicha GA, et al. Alzheimer's-type neuropathology in the precuneus is not increased relative to other areas of neocortex across a range of cognitive impairment. Neuroscience Lett 2009a; 450: 336-9.
45. Nelson PT, Abner EL, Schmitt FA, Kryscio RJ, Jicha GA, Santacruz K, et al. Brains with medial temporal lobe neurofibrillary tangles but no neuritic amyloid plaques are a diagnostic dilemma but may have pathogenetic aspects distinct from Alzheimer disease. J Neuropathol Exp Neurol 2009b; 68: 774-84.
46. Nelson PT, Abner EL, Schmitt FA, Kryscio RJ, Jicha GA, Smith CD, et al. Modeling the association between 43 different clinical and pathological variables and the severity of cognitive impairment in a large autopsy cohort of elderly persons. Brain Pathol 2008; 20: 66-79.
47. Nelson PT, Braak H, Markesbery WR. Neuropathology and cognitive impairment in Alzheimer disease: A complex but coherent relationship. J Neuropathol Exp Neurol 2009c; 68: 1-14.
48. Nelson PT, Jicha GA, Schmitt FA, Liu H, Davis DG, Mendiondo MS, et al. Clinicopathologic correlations in a large Alzheimer disease center autopsy cohort: Neuritic plaques and neurofibrillary tangles "do count" when stageing disease severity. J Neuropathol Exp Neurol 2007; 66: 1136-46. (Pubitemid 350294663)
49. Nelson PT, Kryscio RJ, Abner EL, Schmitt FA, Jicha GA, Mendiondo MS, et al. Acetylcholinesterase inhibitor treatment is associated with relatively slow cognitive decline in patients with Alzheimer's disease and AD + DLB. J Alzheimers Dis 2009d; 16: 29-34.
50. Nelson PT, Kukull WA, Frosch MP. Thinking outside the box: Alzheimer-type neuropathology that does not map directly onto current consensus recommendations. J Neuropathol Exp Neurol 2010; 69: 449-54.
51. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-3. (Pubitemid 44547757)
52. Ng T, Graham DI, Adams JH, Ford I. Changes in the hippocampus and the cerebellum resulting from hypoxic insults: Frequency and distribution. Acta Neuropathol 1989; 78: 438-43. (Pubitemid 19200594)
53. Petrovitch H, Ross GW, Steinhorn SC, Abbott RD, Markesbery W, Davis D, et al. AD lesions and infarcts in demented and non-demented Japanese-American men. Ann Neurol 2005; 57: 98-103. (Pubitemid 40053320)
54. Poon LW, Clayton GM, Martin P, Johnson MA, Courtenay BC, Sweaney AL, et al. The Georgia Centenarian Study. Int J Ageing Hum Dev 1992; 34: 1-17.
55. Poon LW, Jazwinski SM, Green RC, Woodard JL, Martin P, Rodgers WL, et al. Methodological considerations in studying centenarians: Lessons learned from the Georgia centenarian studies. In: Poon LW, Perls TT, editors. Annual review of gerontology and geriatrics: Biopsychosocial approaches to longevity 2007 ed. Vol. 27. New York: Springer; 2007. p. 231-64.
56. Probst A, Taylor KI, Tolnay M. Hippocampal sclerosis dementia: A reappraisal. Acta Neuropathol 2007; 114: 335-45. (Pubitemid 47500345)
57. Riley KP, Snowdon DA, Markesbery WR. Alzheimer's neurofibrillary pathology and the spectrum of cognitive function: Findings from the Nun Study. Ann Neurol 2002; 51: 567-77.
58. Rohrer JD, Geser F, Zhou J, Gennatas ED, Sidhu M, Trojanowski JQ, et al. TDP-43 subtypes are associated with distinct atrophy patterns in frontotemporal dementia. Neurology 2010; 75: 2204-11.
59. Saito Y, Murayama S. Neuropathology of mild cognitive impairment. Neuropathology 2007; 27: 578-84. (Pubitemid 350045670)
60. Sampathu DM, Neumann M, Kwong LK, Chou TT, Micsenyi M, Truax A, et al. Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol 2006; 169: 1343-52. (Pubitemid 351194368)
61. Schneider JA, Aggarwal NT, Barnes L, Boyle P, Bennett DA. The neuropathology of older persons with and without dementia from community versus clinic cohorts. J Alzheimers Dis 2009a; 18: 691-701.
62. Schneider JA, Arvanitakis Z, Bang W, Bennett DA. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology 2007; 69: 2197-204. (Pubitemid 350294674)
63. Schneider JA, Arvanitakis Z, Leurgans SE, Bennett DA. The neuropathology of probable Alzheimer disease and mild cognitive impairment. Ann Neurol 2009b; 66: 200-8.
64. Schmitt FA, Davis DG, Wekstein DR, Smith CD, Ashford JW, Markesbery WR. "Preclinical" AD revisited: Neuropathology of cognitively normal older adults. Neurology 2000; 55: 370-6. (Pubitemid 30654797)
65. Schmitt FA, Wetherby MM, Wekstein DR, Dearth CM, Markesbery WR. Brain donation in normal ageing: Procedures, motivations, and donor characteristics from the Biologically Resilient Adults in Neurological Studies (BRAiNS) Project. Gerontologist 2001; 41: 716-22. (Pubitemid 33139628)
66. Sonnen JA, Larson EB, Crane PK, Haneuse S, Li G, Schellenberg GD, et al. Pathological correlates of dementia in a longitudinal, population-based sample of ageing. Ann Neurol 2007; 62: 406-13. (Pubitemid 350105954)
67. Thom M. Hippocampal sclerosis: Progress since Sommer. Brain Pathol 2009; 19: 565-72.
68. van Dijk EJ, Prins ND, Vermeer SE, Koudstaal PJ, Breteler MM. Frequency of white matter lesions and silent lacunar infarcts. J Neural Transm Suppl 2002; 62: 25-39. (Pubitemid 37046649)
69. Welsh KA, Butters N, Hughes JP, Mohs RC, Heyman A. Detection and stageing of dementia in Alzheimer's disease. Use of the neuropsychological measures developed for the Consortium to Establish a Registry for Alzheimer's Disease. Arch Neurol 1992; 49: 448-52.
70. Wolf DS, Gearing M, Snowdon DA, Mori H, Markesbery WR, Mirra SS. Progression of regional neuropathology in Alzheimer disease and normal elderly: Findings from the Nun study. Alzheimer Dis Assoc Disorders 1999; 13: 226-31. (Pubitemid 30011381)
71. Zarow C, Sitzer TE, Chui HC. Understanding hippocampal sclerosis in the elderly: Epidemiology, characterization, and diagnostic issues. Curr Neurol Neurosci Rep 2008; 8: 363-70.