Amyloid burden in cognitively normal elderly is associated with preferential hippocampal subfield volume loss

Journal of Alzheimer's Disease

Volumn 45, Issue 1, 2015, Pages 27-33

  Hsu, Phillip J ^a   Shou, Haochang ^c   Benzinger, Tammie ^a,b   Marcus, Daniel ^a   Durbin, Tony ^a   Morris, John C ^b   Sheline, Yvette I ^a,b,c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Amyloid accumulation; cognitively normal elderly; hippocampal subfield volumes; presubiculum; subiculum

Indexed keywords

AMYLOID BETA PROTEIN; 2-(4'-(METHYLAMINO)PHENYL)-6-HYDROXYBENZOTHIAZOLE; AMYLOID PROTEIN; ANILINE DERIVATIVE; THIAZOLE DERIVATIVE;

AGED; ARTICLE; BRAIN SIZE; COGNITION; CONTROLLED STUDY; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRESUBICULUM; PRIORITY JOURNAL; SUBICULUM; COGNITION DISORDERS; DIAGNOSTIC IMAGING; MENTAL HEALTH; METABOLISM; MIDDLE AGED; PATHOLOGY; THREE DIMENSIONAL IMAGING;

AGED; AMYLOIDOGENIC PROTEINS; ANILINE COMPOUNDS; COGNITION DISORDERS; FEMALE; HIPPOCAMPUS; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MALE; MENTAL STATUS SCHEDULE; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; THIAZOLES;

EID: 84924186786     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-141743     Document Type: Article

References (63)

1. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356.
2. Gravina SA, Ho L, Eckman CB, Long KE, Otvos L, Younkin LH, Suzuki N, Younkin SG (1995) Amyloid aβ protein (Aβ) in Alzheimer's disease brain. Nature 270, 7013-7016.
3. Yates P, a, Sirisriro R, Villemagne VL, Farquharson S, Masters CL, Rowe CC (2011) Cerebral microhemorrhage and brain β-amyloid in aging and Alzheimer disease. Neurology 77, 48-54.
4. Jack CR, Knopman DS, Jagust WJ, Shaw LM, Aisen PS, WeinerW, Petersen RC, Trojanowski JQ (2010) Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol 9, 1-20.
5. Jack CR, Knopman DS, Jagust WJ, Peterson RC, Weiner MW, Aisen PS, Shaw LM, Vemuri P, Wiste HJ, Weigand SD, Lesnick TG, Pankratz VS, Donohue MC, Trojanowski JQ (2013) Update on hypothetical model of Alzheimer's disease biomarkers. Lancet Neurol 12, 207-216.
6. Perrin RJ, Fagan AM, HoltzmanDM (2009) Multimodal techniques for diagnosis and prognosis of Alzheimer's disease. Nature 461, 916-922.
7. Holmes C, Boche D, Wilkinson D (2008) Long-term effects of Aβ 42 immunisation in Alzheimer's disease: Follow-up of a randomised, placebo-controlled phase I trial. Lancet 372, 11-14.
8. Sperling R, a, Aisen PS, Beckett L, a, Bennett D, a, Craft S, Fagan AM, Iwatsubo T, Jack CR, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M, Wagster MV, Phelps CH (2011) Toward defining the preclinical stages of Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7, 280-292.
9. Katzman R, Terry R, Deteresa R, Brown T, Davies P, Fuld P, Renbing X, PeckA (1988) Neurochemical changes in dementia: A subgroup with preserved mental status and numerous neocortical plaques. Ann Neurol 23, 138-144.
10. Price JL, Morris JC (1999) Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol 45, 358-368.
11. Crystal H, Dickson D, Fuld P, Masur D, Scott R, Mehler M, Masdeu J, Kawas C, Aronson M, Wolfson L (1988) Clinicopathologic studies in dementia: Nondemented subjects with pathologically confirmed Alzheimer's disease. Neurology 38, 1682-1687.
12. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, Bergstro M, Savitcheva I, Debnath ML, Barletta J, Price JC, Sandell J, Lopresti BJ, Wall A, Koivisto P, Antoni G, Mathis CA, Langstro B (2004) Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol 55, 306-319.
13. Grimmer T, Henriksen G, Wester H-J, Förstl H, Klunk WE, Mathis C, a, Kurz A, Drzezga A (2009) Clinical severity of Alzheimer's disease is associated with PIB uptake in PET. Neurobiol Aging 30, 1902-1909.
14. Jack CR, Lowe VJ, Senjem ML, Weigand SD, Kemp BJ, Shiung MM, Knopman DS, Boeve BF, Klunk WE, Mathis C, a, Petersen RC (2008) 11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment. Brain 131, 665-680.
15. Morris JC, Roe CM, Grant EA, Head D, Storandt M, Goate AM, Fagan AM, Holtzman DM, Mintun MA (2009) Pittsburgh compound B imaging and prediction of progression from cognitive normality to symptomatic Alzheimer disease. Arch Neurol 66, 1469-1475.
16. Mintun M, a, Larossa GN, Sheline YI, Dence CS, Lee SY, Mach RH, Klunk WE, Mathis C, a, DeKosky ST, Morris JC (2006) [11C]PIB in a nondemented population: Potential antecedent marker of Alzheimer disease. Neurology 67, 446-452.
17. Killiany RJ, Moss MB, Albert MS, Sandor T, Tieman J, Jolesz F (1993) Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer's disease. Arch Neurol 50, 949-954.
18. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82, 239-259.
19. Hyman B, Hoesen G, Van, Damasio A, Barnes C (1984) Alzheimer's disease: Cell-specific pathology isolates the hippocampal formation. Science 225, 1168-1170.
20. Ball M, Hachinski V, Fox A, Kirshen A (1985) A new definition of Alzheimer's disease:Ahippocampal dementia. Lancet 325, 14-16.
21. Bourgeat P, Chételat G, Villemagne VL, Fripp J, Raniga P, Pike K, Acosta O, Szoeke C, Ourselin S, Ames D, Ellis K, a, Martins RN, Masters CL, Rowe CC, Salvado O (2010) Beta-amyloid burden in the temporal neocortex is related to hippocampal atrophy in elderly subjects without dementia. Neurology 74, 121-127.
22. Andrews K, Modat M, Macdonald K (2013) Atrophy rates in asymptomatic amyloidosis: Implications for Alzheimer prevention trials. PLoS One 8, e58816.
23. Frisoni G, Fox N, Jack C, Scheltens P, Thompson P (2010) The clinical use of structural MRI in Alzheimer disease. Nat Rev Neurol 6, 67-77.
24. Lindberg O, Walterfang M, Looi JCL, Malykhin N, Ostberg P, Zandbelt B, Styner M, Paniagua B, Velakoulis D, Omdahl E, Wahlund L-O (2012) Hippocampal shape analysis in Alzheimer's disease and frontotemporal lobar degeneration subtypes. J Alzheimers Dis 30, 355-365.
25. Tondelli M, Wilcock GK, Nichelli P, De Jager. C a, Jenkinson M, Zamboni G (2012) Structural MRI changes detectable up to ten years before clinical Alzheimer's disease. Neurobiol Aging 33, 825.e25-825.e36.
26. La Joie R, Perrotin A, De La Sayette V, Egret S, Doeuvre L, Belliard S, Eustache F, Desgranges B, Chételat G (2013) Hippocampal subfield volumetry in mild cognitive impairment, Alzheimer's disease and semantic dementia. Neuroimage Clin 3, 155-162.
27. Van Leemput K, Bakkour A, Benner T (2009) Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 19, 549-557.
28. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I: Segmentation and surface reconstruction. Neuroimage 9, 179-194.
29. Dale A, Sereno M (1993) Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction. J Cogn Neurosci 5, 162-176.
30. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97, 11050-11055.
31. Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20, 70-80.
32. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, Van derKouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355.
33. Fischl B (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14, 11-22.
34. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. J Cogn Neurosci 9, 195-207.
35. Fischl B, Sereno MI, Tootell RB, Dale AM (1999) Highresolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8, 272-284.
36. Fischl B, Salat DH, Van Der Kouwe AJW, Makris N, Ségonne F, Quinn BT, Dale AM (2004) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23 (Suppl 1), S69-S84.
37. Han X, Jovicich J, Salat D, Van Der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killiany R, Maguire P, Rosas D, Makris N, Dale A, Dickerson B, Fischl B (2006) Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. Neuroimage 32, 180-194.
38. Jovicich J, Czanner S, Greve D, Haley E, Van Der Kouwe A, Gollub R, Kennedy D, Schmitt F, Brown G, Macfall J, Fischl B, Dale A (2006) Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data. Neuroimage 30, 436-443.
39. Ségonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22, 1060-1075.
40. Simón A-M, Schiapparelli L, Salazar-Colocho P, Cuadrado-Tejedor M, Escribano L, López De Maturana R, Del Río J, Pérez-Mediavilla A, Frechilla D (2009) Overexpression of wild-type human APP in mice causes cognitive deficits and pathological features unrelated to Abeta levels. Neurobiol Dis 33, 369-378.
41. Beauquis J, Vinuesa A, Pavio P, Galvan V, Saravia F (2014) Neuronal and glial alterations, increased anxiety, and cognitive impairment before hippocampal amyloid deposition in PDAPP mice, model of Alzheimer's disease. Hippocampus 24, 257-269.
42. Loreth D, Ozmen L, Revel FG, Knoflach F, Wetzel P, Frotscher M, Metzger F, Kretz O (2012) Selective degeneration of septal and hippocampal GABAergic neurons in a mouse model of amyloidosis and tauopathy. Neurobiol Dis 47, 1-12.
43. Baglietto-Vargas D, Moreno-Gonzalez I, Sanchez-Varo R, Jimenez S, Trujillo-Estrada L, Sanchez-Mejias E, Torres M, Romero-Acebal M, Ruano D, Vizuete M, Vitorica J, Gutierrez A (2010) Calretinin interneurons are early targets of extracellular amyloid-beta pathology in PS1/AbetaPP Alzheimer mice hippocampus. J Alzheimers Dis 21, 119-132.
44. Scahill RI, Schott JM, Stevens JM, Rossor MN, Fox NC (2002) Mapping the evolution of regional atrophy in Alzheimer's disease: Unbiased analysis of fluid-registered serial MRI. Proc Natl Acad Sci U S A 99, 4703-4707.
45. Fox N, Warrington E (1996) Presymptomatic hippocampal atrophy in Alzheimer's disease: A longitudinal MRI study. Brain 119, 2001-2007.
46. Apostolova LG, Dutton RA, Dinov ID, Hayashi KM, Toga AW, Cummings JL, Thompson PM (2006) Conversion of mild cognitive impairment to Alzheimer disease predicted by hippocampal atrophy maps. Arch Neurol 63, 693-699.
47. Den Heijer T, Geerlings MI, Hoebeek FE, Hofman A, Koudstaal PJ, Breteler MMB (2006) Use of hippocampal and amygdalar volumes on magnetic resonance imaging to predict dementia in cognitively intact elderly people. Arch Gen Psychiatry 63, 57-62.
48. Jack CR, Petersen RC, Xu YC, O'Brien PC, Smith GE, Ivnik RJ, Boeve BF, Waring SC, Tangalos EG, Kokmen E (1999) Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 52, 1397.
49. Scher AI, Xu Y, Korf ESC, White LR, Scheltens P, Toga AW, Thompson PM, Hartley SW, Witter MP, Valentino DJ, Launer LJ (2007) Hippocampal shape analysis in Alzheimer's disease: A population-based study. Neuroimage 36, 8-18.
50. West MJ, Kawas CH, Stewart WF, Rudow GL, Troncoso JC (2004) Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 25, 1205-1212.
51. Price JL, Ko a I, Wade MJ, Tsou SK, McKeel DW, Morris JC (2001) Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch Neurol 58, 1395-1402.
52. Hanseeuw BJ, Van Leemput K, Kavec M, Grandin C, Seron X, Ivanoiu A (2011) Mild cognitive impairment: Differential atrophy in the hippocampal subfields. AJNRAmJ Neuroradiol 32, 1658-1661.
53. Rössler M, Zarski R, Bohl J, OhmTG (2002) Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer's disease. Acta Neuropathol 103, 363-369.
54. Frisoni GB, Ganzola R, Canu E, Rüb U, Pizzini FB, Alessandrini F, Zoccatelli G, Beltramello A, Caltagirone C, ThompsonPM (2008) Mapping local hippocampal changes in Alzheimer's disease and normal ageing with MRI at 3 Tesla. Brain 131, 3266-3276.
55. Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW (2010) Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 31, 1339-1347.
56. Mueller SG, Weiner MW (2009) Selective effect of age, Apo β4, and Alzheimer's disease on hippocampal subfields. Hippocampus 19, 558-564.
57. Amaral DG (1990) Hippocampal formation. In The Human Nervous System, Paxinos G, ed. Academic Press, Inc., San Diego, pp. 711-755.
58. Yushkevich PA, Pluta J, Wang H, Xie L, Ding S, Gertje E, Mancusco L, Kliot D, Das SR, Wolk D (2014) Automated volumetry and regional thickness analysis of hippocampal subfields and medial temporal cortical structures in mild cognitive impairment. Hum Brain Mapp, doi: 10.1002/hbm.22627
59. Li S, Shi F, Pu F, Li X, Jiang T, Xie S, Wang Y (2007) Hippocampal shape analysis of Alzheimer disease based on machine learning methods. AJNR Am J Neuroradiol 28, 1339-1345.
60. Ferrarini L, Frisoni GB, Pievani M, Reiber JHC, Ganzola R, Milles J (2009) Morphological hippocampal markers for automated detection of Alzheimer's disease and mild cognitive impairment converters in magnetic resonance images. J Alzheimers Dis 17, 643-659.
61. Gerardin E, Chételat G, Chupin M, Cuingnet R, Desgranges B, Kim H-S, Niethammer M, Dubois B, Lehéricy S, Garnero L, Eustache F, Colliot O (2009) Multidimensional classification of hippocampal shape features discriminates Alzheimer's disease and mild cognitive impairment from normal aging. Neuroimage 47, 1476-1486.
62. Achterberg HC, Van Der Lijn F, Den Heijer T, Vernooij MW, Ikram MA, Niessen WJ, De Bruijne M (2014) Hippocampal shape is predictive for the development of dementia in a normal, elderly population. Hum Brain Mapp 35, 2359-2371.
63. Csernansky JG, Wang L, Swank J, Miller JP, Gado M, McKeel D, Miller MI, Morris JC (2005) Preclinical detection of Alzheimer's disease: Hippocampal shape and volume predict dementia onset in the elderly. Neuroimage 25, 783-792.