Association between Aβ and tau accumulations and their influence on clinical features in aging and Alzheimer's disease spectrum brains: A [11C]PBB3-PET study

Alzheimer's and Dementia: Diagnosis, Assessment and Disease Monitoring

Volumn 6, Issue , 2017, Pages 11-20

  Shimada, Hitoshi ^a   Kitamura, Soichiro ^a   Shinotoh, Hitoshi ^a,b   Endo, Hironobu ^a,c   Niwa, Fumitoshi ^a,d   Hirano, Shigeki ^a,e   Kimura, Yasuyuki ^a   Zhang, Ming Rong ^a   Kuwabara, Satoshi ^e   Suhara, Tetsuya ^a   Higuchi, Makoto ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^b Neurology Chiba Clinic   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^e CHIBA UNIVERSITY   (Japan)

Author keywords

Aging; Alzheimer's disease; Amyloid; Biomarkers; Brain atrophy; Cognitive decline; Cognitive reserve; Dementia; MCI; Positron emission tomography; Preclinical; Tau; 11C PBB3; 11C PiB

Indexed keywords

AMYLOID BETA PROTEIN; PITTSBURGH COMPOUND B; PYRIDINYL BUTADIENYL BENZOTHIAZOLE 3 C 11; RADIOPHARMACEUTICAL AGENT; TAU PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; AGING; ALZHEIMER DISEASE; ARTICLE; BIOACCUMULATION; BRAIN SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GRAY MATTER; HUMAN; IMAGE ANALYSIS; INFORMED CONSENT; MALE; MILD COGNITIVE IMPAIRMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PATHOGENESIS; PET SCANNER; POSITRON EMISSION TOMOGRAPHY;

EID: 85009837024     PISSN: None     EISSN: 23528729     Source Type: Journal    
DOI: 10.1016/j.dadm.2016.12.009     Document Type: Article

References (53)

1. [1] Trojanowski, J.Q., Lee, V.M., “Fatal attractions” of proteins. A comprehensive hypothetical mechanism underlying Alzheimer's disease and other neurodegenerative disorders. Ann N Y Acad Sci 924 (2000), 62–67.
2. [2] Hardy, J.A., Higgins, G.A., Alzheimer's disease: the amyloid cascade hypothesis. Science 256 (1992), 184–185.
3. [3] Bensaïdane, M.R., Beauregard, J.M., Poulin, S., Buteau, F.A., Guimond, J., Bergeron, D., et al. Clinical utility of amyloid PET imaging in the differential diagnosis of atypical dementias and its impact on caregivers. J Alzheimers Dis 52 (2016), 1251–1262.
4. [4] Sha, S.J., Ghosh, P.M., Lee, S.E., Corbetta-Rastelli, C., Jagust, W.J., Kornak, J., et al. Predicting amyloid status in corticobasal syndrome using modified clinical criteria, magnetic resonance imaging and fluorodeoxyglucose positron emission tomography. Alzheimers Res Ther, 7, 2015, 8.
5. [5] Okello, A., Koivunen, J., Edison, P., Archer, H.A., Turkheimer, F.E., Någren, K., et al. Conversion of amyloid positive and negative MCI to AD over 3 years: An 11C-PIB PET study. Neurology 73 (2009), 754–760.
6. [6] Sperling, R.A., Laviolette, P.S., O'Keefe, K., O'Brien, J., Rentz, D.M., Pihlajamaki, M., et al. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63 (2009), 178–188.
7. [7] Jack, C.R. Jr., Knopman, D.S., Jagust, W.J., Shaw, L.M., Aisen, P.S., Weiner, M.W., et al. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol 9 (2010), 119–128.
8. [8] Shimada, H., Shinotoh, H., Hirano, S., Miyoshi, M., Sato, K., Tanaka, N., et al. β-Amyloid in Lewy body disease is related to Alzheimer's disease-like atrophy. Mov Disord 28 (2013), 169–175.
9. [9] Villemagne, V.L., Burnham, S., Bourgeat, P., Brown, B., Ellis, K.A., Salvado, O., et al., Australian Imaging Biomarkers and Lifestyle (AIBL) Research Group. Amyloid β deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol 12 (2013), 357–367.
10. [10] Liu, E., Schmidt, M.E., Margolin, R., Sperling, R., Koeppe, R., Mason, N.S., et al. Bapineuzumab 301 and 302 Clinical Trial Investigators. Amyloid-β 11C-PiB-PET imaging results from 2 randomized bapineuzumab phase 3 AD trials. Neurology 85 (2015), 692–700.
11. [11] Sevigny, J., Chiao, P., Bussière, T., Weinreb, P.H., Williams, L., Maier, M., et al. The antibody aducanumab reduces Aβ plaques in Alzheimer's disease. Nature 537 (2016), 50–56.
12. [12] Frisoni, G.B., Lorenzi, M., Caroli, A., Kemppainen, N., Någren, K., Rinne, J.O., In vivo mapping of amyloid toxicity in Alzheimer disease. Neurology 72 (2009), 1504–1511.
13. [13] Marshall, G.A., Donovan, N.J., Lorius, N., Gidicsin, C.M., Maye, J., Pepin, L.C., et al. Apathy is associated with increased amyloid burden in mild cognitive impairment. J Neuropsychiatry Clin Neurosci 25 (2013), 302–307.
14. [14] Mori, T., Shimada, H., Shinotoh, H., Hirano, S., Eguchi, Y., Yamada, M., et al. Apathy correlates with prefrontal amyloid β deposition in Alzheimer's disease. J Neurol Neurosurg Psychiatry 85 (2014), 449–455.
15. [15] Katzman, R., Terry, R., DeTeresa, R., Brown, T., Davies, P., Fuld, P., et al. Clinical, pathological, and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann Neurol 23 (1988), 138–144.
16. [16] Rowe, C.C., Ng, S., Ackermann, U., Gong, S.J., Pike, K., Savage, G., et al. Imaging beta-amyloid burden in aging and dementia. Neurology 68 (2007), 1718–1725.
17. [17] Price, J.L., McKeel, D.W. Jr., Buckles, V.D., Roe, C.M., Xiong, C., Grundman, M., et al. Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease. Neurobiol Aging 30 (2009), 1026–1036.
18. [18] Quigley, H., Colloby, S.J., O'Brien, J.T., PET imaging of brain amyloid in dementia: a review. Int J Geriatr Psychiatry 26 (2011), 991–999.
19. [19] Higuchi, M., Lee, V.M., Trojanowski, J.Q., Tau and axonopathy in neurodegenerative disorders. Neuromolecular Med 2 (2002), 131–150.
20. [20] Crary, J.F., Trojanowski, J.Q., Schneider, J.A., Abisambra, J.F., Abner, E.L., Alafuzoff, I., et al. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol 128 (2014), 755–766.
21. [21] Arriagada, P.V., Growdon, J.H., Hedley-Whyte, E.T., Hyman, B.T., Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42 (1992), 631–639.
22. [22] Nelson, P.T., Alafuzoff, I., Bigio, E.H., Bouras, C., Braak, H., Cairns, N.J., et al. Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol 71 (2012), 362–381.
23. [23] van Rossum, I.A., Vos, S.J., Burns, L., Knol, D.L., Scheltens, P., Soininen, H., et al. Injury markers predict time to dementia in subjects with MCI and amyloid pathology. Neurology 79 (2012), 1809–1816.
24. [24] Chien, D.T., Bahri, S., Szardenings, A.K., Walsh, J.C., Mu, F., Su, M.Y., et al. Early clinical PET imaging results with the novel PHF-tau radioligand [F-18]-T807. J Alzheimers Dis 34 (2013), 457–468.
25. [25] Ishiki, A., Okamura, N., Furukawa, K., Furumoto, S., Harada, R., Tomita, N., et al. Longitudinal assessment of tau pathology in patients with Alzheimer's disease using [18F]THK-5117 positron emission tomography. PLoS One, 10, 2015, e0140311.
26. [26] Lockhart, S.N., Baker, S.L., Okamura, N., Furukawa, K., Ishiki, A., Furumoto, S., et al. Dynamic PET measures of tau accumulation in cognitively normal older adults and Alzheimer's disease patients measured using [18F] THK-5351. PLoS One, 11, 2016, e0158460.
27. [27] Maruyama, M., Shimada, H., Suhara, T., Shinotoh, H., Ji, B., Maeda, J., et al. Imaging of tau pathology in a tauopathy mouse model and in Alzheimer patients compared to normal controls. Neuron 79 (2013), 1094–1108.
28. [28] McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., Stadlan, E.M., Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34 (1984), 939–944.
29. [29] Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E.G., Kokmen, E., Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56 (1999), 303–308.
30. [30] Hashimoto, H., Kawamura, K., Igarashi, N., Takei, M., Fujishiro, T., Aihara, Y., et al. Radiosynthesis, photoisomerization, biodistribution, and metabolite analysis of 11C-PBB3 as a clinically useful PET probe for imaging of tau pathology. J Nucl Med 55 (2014), 1532–1538.
31. [31] Kimura, Y., Ichise, M., Ito, H., Shimada, H., Ikoma, Y., Seki, C., et al. Quantification of tau pathology in human brain with 11C-PBB3. J Nucl Med 56 (2015), 1359–1365.
32. [32] Ashburner, J., A fast diffeomorphic image registration algorithm. Neuroimage 38 (2007), 95–113.
33. [33] Maldjian, J.A., Laurienti, P.J., Kraft, R.A., Burdette, J.H., An automated method for neuroanatomic and cytoarchitectonic atlas-based inter- rogation of fMRI data sets. Neuroimage 19 (2003), 1233–1239.
34. [34] Ashburner, J., Friston, K.J., Voxel-based morphometry—the methods. Neuroimage 11 (2000), 805–821.
35. [35] Ashburner, J., Friston, K.J., Unified segmentation. Neuroimage 26 (2005), 839–851.
36. [36] Schöll, M., Lockhart, S.N., Schonhaut, D.R., O'Neil, J.P., Janabi, M., Ossenkoppele, R., et al. PET imaging of tau deposition in the aging human brain. Neuron 89 (2016), 971–982.
37. [37] Savva, G.M., Wharton, S.B., Ince, P.G., Forster, G., Matthews, F.E., Brayne, C., Medical Research Council Cognitive Function and Ageing Study. Age, neuropathology, and dementia. N Engl J Med 360 (2009), 2302–2309.
38. [38] Migliaccio, R., Agosta, F., Possin, K.L., Canu, E., Filippi, M., Rabinovici, G.D., et al. Mapping the Progression of Atrophy in Early- and Late-Onset Alzheimer's Disease. J Alzheimers Dis 46 (2015), 351–364.
39. [39] Ossenkoppele, R., Schonhaut, D.R., Schöll, M., Lockhart, S.N., Ayakta, N., Baker, S.L., et al. Tau PET patterns mirror clinical and neuroanatomical variability in Alzheimer's disease. Brain 139 (2016), 1551–1567.
40. [40] Zhang, M., Katzman, R., Salmon, D., Jin, H., Cai, G., Wang, Z., et al. The prevalence of dementia and Alzheimer's disease in Shanghai, China: impact of age, gender and education. Ann Neurol 27 (1990), 428–437.
41. [41] Snowdon, D.A., Aging and Alzheimer's disease: lessons from the Nun Study. Gerontologist 37 (1997), 150–156.
42. [42] Stern, Y., What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8 (2002), 448–460.
43. [43] Stern, Y., Cognitive reserve in ageing and Alzheimer's disease. Lancet Neurol 11 (2012), 1006–1012.
44. [44] Stern, Y., Cognitive reserve. Neuropsychologia 47 (2009), 2015–2028.
45. [45] Stern, Y., Habeck, C., Moeller, J., Scarmeas, N., Anderson, K.E., Hilton, H.J., et al. Brain networks associated with cognitive reserve in healthy young and old adults. Cereb Cortex 15 (2005), 394–402.
46. [46] Iacono, D., Markesbery, W.R., Gross, M., Pletnikova, O., Rudow, G., Zandi, P., et al. The Nun study: clinically silent AD, neuronal hypertrophy, and linguistic skills in early life. Neurology 73 (2009), 665–673.
47. [47] Almeida, R.P., Schultz, S.A., Austin, B.P., Boots, E.A., Dowling, N.M., Gleason, C.E., et al. Effect of cognitive reserve on age-related changes in cerebrospinal fluid biomarkers of Alzheimer disease. JAMA Neurol 72 (2015), 699–706.
48. [48] Bauckneht, M., Picco, A., Nobili, F., Morbelli, S., Amyloid positron emission tomography and cognitive reserve. World J Radiol 7 (2015), 475–483.
49. [49] Jack, C.R. Jr., Knopman, D.S., Chételat, G., Dickson, D., Fagan, A.M., Frisoni, G.B., et al. Suspected non-Alzheimer disease pathophysiology—concept and controversy. Nat Rev Neurol 12 (2016), 117–124.
50. [50] Good, C.D., Johnsrude, I.S., Ashburner, J., Henson, R.N., Friston, K.J., Frackowiak, R.S., A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14 (2001), 21–36.
51. [51] Wang, L., Benzinger, T.L., Su, Y., Christensen, J., Friedrichsen, K., Aldea, P., et al. Evaluation of tau imaging in staging Alzheimer disease and revealing interactions between β-amyloid and tauopathy. JAMA Neurol 73 (2016), 1070–1077.
52. [52] Johnson, K.A., Schultz, A., Betensky, R.A., Becker, J.A., Sepulcre, J., Rentz, D., et al. Tau positron emission tomographic imaging in aging and early Alzheimer disease. Ann Neurol 79 (2016), 110–119.
53. [53] Brier, M.R., Gordon, B., Friedrichsen, K., McCarthy, J., Stern, A., Christensen, J., et al. Tau and Aβ imaging, CSF measures, and cognition in Alzheimer's disease. Sci Transl Med, 8, 2016, 338ra66.