Pattern of brain atrophy rates in autopsy-confirmed dementia with Lewy bodies

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 452-461

  Nedelska, Zuzana ^a,b,c   Ferman, Tanis J ^d   Boeve, Bradley F ^a   Przybelski, Scott A ^a   Lesnick, Timothy G ^a   Murray, Melissa E ^e   Gunter, Jeffrey L ^a   Senjem, Matthew L ^a   Vemuri, Prashanti ^a   Smith, Glenn E ^a   Geda, Yonas E ^f   Graff Radford, Jonathan ^a   Knopman, David S ^a   Petersen, Ronald C ^a   Parisi, Joseph E ^a   Dickson, Dennis W ^d,e   Jack, Clifford R ^a   Kantarci, Kejal ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY HOSPITAL MOTOL   (Czech Republic)

^c ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^d MAYO CLINIC   (United States)

^e MAYO GRADUATE SCHOOL   (United States)

^f MAYO CLINIC   (United States)

Author keywords

Alzheimer's disease; Atrophy rate; Autopsy confirmed dementia with Lewy bodies; Braak neurofibrillary tangle stage; Sample size estimate; Serial MRI

Indexed keywords

CHOLINESTERASE INHIBITOR; DOPAMINE RECEPTOR STIMULATING AGENT; MEMANTINE; BIOLOGICAL MARKER;

AGED; ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ARTICLE; AUTOPSY; BRAIN ATROPHY; BRAIN VENTRICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOTOR DYSFUNCTION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL CORTEX; TEMPORAL CORTEX; VERY ELDERLY; AMYGDALA; ATROPHY; BRAIN; COGNITION; DISEASE COURSE; ORGAN SIZE; PARIETAL LOBE; PATHOLOGY; PSYCHOLOGY; TEMPORAL LOBE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYGDALA; ATROPHY; AUTOPSY; BIOMARKERS; BRAIN; COGNITION; DISEASE PROGRESSION; FEMALE; HIPPOCAMPUS; HUMANS; LEWY BODY DISEASE; MAGNETIC RESONANCE IMAGING; MALE; NEUROFIBRILLARY TANGLES; ORGAN SIZE; PARIETAL LOBE; TEMPORAL LOBE;

EID: 84920624841     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.07.005     Document Type: Article

References (68)

1. Ashburner J., Ridgway G.R. Symmetric diffeomorphic modeling of longitudinal structural MRI. Front. Neurosci. 2013, 5:197. eCollection 2012.
2. Ballmaier M., O'Brien J.T., Burton E.J., Thompson P.M., Rex D.E., Narr K.L., McKeith I.G., DeLuca H., Toga A.W. Comparing gray matter loss profiles between dementia with Lewy bodies and Alzheimer's disease using cortical pattern matching: diagnosis and gender effects. Neuroimage 2004, 23:25-35.
3. Barber R., Ballard C., McKeith I.G., Gholkar A., O'Brien J.T. MRI volumetric study of dementia with Lewy bodies: a comparison with AD and vascular dementia. Neurology 2000, 54:1304-1309.
4. Barkhof F., Polvikoski T.M., van Straaten E.C., Kalaria R.N., Sulkava R., Aronen H.J., Niinistö L., Rastas S., Oinas M., Scheltens P., Erkinjuntti T. The significance of medial temporal lobe atrophy: a postmortem MRI study in the very old. Neurology 2007, 69:1521-1527.
5. Braak H., Braak E. Evolution of the neuropathology of Alzheimer's disease. Acta Neurol. Scand. Suppl. 1996, 165:3-12.
6. Brenneis C., Wenning G.K., Egger K.E., Schocke M., Trieb T., Seppi K., Marksteiner J., Ransmayr G., Benke T., Poewe W. Basal forebrain atrophy is a distinctive pattern in dementia with Lewy bodies. Neuroreport 2004, 15:1711-1714.
7. Burton E.J., Karas G., Paling S.M., Barber R., Williams E.D., Ballard C.G., McKeith I.G., Scheltens P., Barkhof F., O'Brien J.T. Patterns of cerebral atrophy in dementia with Lewy bodies using voxel-based morphometry. Neuroimage 2002, 17:618-630.
8. Burton E.J., McKeith I.G., Burn D.J., Williams E.D., O'Brien J.T. Cerebral atrophy in Parkinson's disease with and without dementia: a comparison with Alzheimer's disease, dementia with Lewy bodies and controls. Brain 2004, 127(Pt 4):791-800.
9. Burton E.J., Barber R., Mukaetova-Ladinska E.B., Robson J., Perry R.H., Jaros E., Kalaria R.N., O'Brien J.T. Medial temporal lobe atrophy on MRI differentiates Alzheimer's disease from dementia with Lewy bodies and vascular cognitive impairment: a prospective study with pathological verification of diagnosis. Brain 2009, 132(Pt 1):195-203.
10. Burton E.J., Mukaetova-Ladinska E.B., Perry R.H., Jaros E., Barber R., O'Brien J.T. Neuropathological correlates of volumetric MRI in autopsy-confirmed Lewy body dementia. Neurobiol. Aging 2012, 33:1228-1236.
11. Fahn S., Elton R.L. Unified Parkinson's disease rating scale. Recent Developments in Parkinson's Disease 1987, 2:153-163. UPDRS program members, Macmillan Healthcare Information, Florham Park, NJ, 293-304.
12. Ferrer I., Santpere G., van Leeuwen F.W. Argyrophilic grain disease. Brain 2008, 131(Pt6):1416-1432.
13. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., van der Kouwe A., Killiany R., Kennedy D., Klaveness S., Montillo A., Makris N., Rosen B., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
14. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J.Psychiatr. Res. 1975, 12:189-198.
15. Fox N.C., Freeborough P.A., Rossor M.N. Visualisation and quantification of rates of atrophy in Alzheimer's disease. Lancet 1996, 348:94-97.
16. Fox N.C., Cousens S., Scahill R., Harvey R.J., Rossor M.N. Using serial registered brain magnetic resonance imaging to measure disease progression in Alzheimer disease: power calculations and estimates of sample size to detect treatment effects. Arch. Neurol. 2000, 57:339-344.
17. Graff-Radford J., Boeve B.F., Pedraza O., Ferman T.J., Przybelski S., Lesnick T.G., Vemuri P., Senjem M.L., Smith G.E., Knopman D.S., Lowe V., Jack C.R., Petersen R.C., Kantarci K. Imaging and acetylcholinesterase inhibitor response in dementia with Lewy bodies. Brain 2012, 135(Pt 8):2470-2477.
18. Gunter J.L., Shiung M.M., Manduca A., Jack C.R. Methodological considerations for measuring rates of brain atrophy. J.Magn. Reson. Imaging 2003, 18:16-24.
19. Gunter J.L., Senjem M.L., Vemuri P., Jack C.R. Comparison of mask-based differences, boundary shift integral and symmetric normalization Jacobian integration. MICCAI 2012 Workshop on Novel Imaging Biomarkers for Alzheimer's Disease and Related Disorders 2012, Nice, France.
20. Hamilton R.L. Lewy bodies in Alzheimer's disease: a neuropathological review of 145 cases using alpha-synuclein immunohistochemistry. Brain Pathol. 2000, 10:378-384.
21. Hansen L., Salmon D., Galasko D., Masliah E., Katzman R., DeTeresa R., Thal J., Pay M.M., Hofstetter R., Klauber M., Rice V., Butters N., Alford M. The Lewy body variant of Alzheimer's disease: a clinical and pathologic entity. Neurology 1990, 40:1-8.
22. Hanyu H., Tanaka Y., Shimizu S., Sakurai H., Iwamoto T., Abe K. Differences in MR features of the substantia innominata between dementia with Lewy bodies and Alzheimer's disease. J.Neurol. 2005, 252:482-484.
23. Harvey G.T., Hughes J., McKeith I.G., Briel R., Ballard C., Gholkar A., Scheltens P., Perry R.H., Ince P., O'Brien J.T. Magnetic resonance imaging differences between dementia with Lewy bodies and Alzheimer's disease: a pilot study. Psychol. Med. 1999, 29:181-187.
24. Hashimoto M., Kitagaki H., Imamura T., Hirono N., Shimomura T., Kazui H., Tanimukai S., Hanihara T., Mori E. Medial temporal and whole-brain atrophy in dementia with Lewy bodies: a volumetric MRI study. Neurology 1998, 51:357-362.
25. Ho A.J., Hua X., Lee S., Leow A.D., Yanovsky I., Gutman B., Dinov I.D., Leporé N., Stein J.L., Toga A.W., Jack C.R., Bernstein M.A., Reiman E.M., Harvey D.J., Kornak J., Schuff N., Alexander G.E., Weiner M.W., Thompson P.M. Comparing 3 T and 1.5 T MRI for tracking Alzheimer's disease progression with tensor-based morphometry. Hum. Brain Mapp. 2010, 31:499-514. Alzheimer's Disease Neuroimaging Initiative.
26. Horvath J., Hermann F.R., Burkhard P.R., Bouras C., Kovari C. Neuropathology of dementia in a large cohort of patients with Parkinson's disease. Parkinsonism Relat. Disord. 2013, 19:864-868.
27. Hua X., Lee S., Yanovsky I., Leow A.D., Chou Y.Y., Ho A.J., Gutman B., Toga A.W., Jack C.R., Bernstein M.A., Reiman E.M., Harvey D.J., Kornak J., Schuff N., Alexander G.E., Weiner M.W., Thompson P.M. Optimizing power to track brain degeneration in Alzheimer's disease and mild cognitive impairment with tensor-based morphometry: an ADNI study of 515 subjects. Neuroimage 2009, 48:668-681. Alzheimer's Disease Neuroimaging Initiative.
28. Jack C.R., Petersen R.C., Xu Y., O'Brien P.C., Smith G.E., Ivnik R.J., Boeve B.F., Tangalos E.G., Kokmen E. Rates of hippocampal atrophy correlate with change in clinical status in aging and AD. Neurology 2000, 55:484-489.
29. Jack C.R., Slomkowski M., Gracon S., Hoover T.M., Felmlee J.P., Stewart K., Xu Y., Shiung M.M., O'Brien P.C., Cha R., Knopman D.S., Petersen R.C. MRI as a biomarker of disease progression in a therapeutic trial of milameline for AD. Neurology 2003, 60:253-260.
30. Jack C.R., Shiung M.M., Gunter J.L., O'Brien P.C., Weigand S.D., Knopman D.S., Boeve B.F., Ivnik R.J., Smith G.E., Cha R.H., Tangalos E.G., Petersen R.C. Comparison of different MRI brain atrophy rate measures with clinical disease progression in AD. Neurology 2004, 62:591-600.
31. Jack C.R., Petersen R.C., Grundman M., Jin S., Gamst A., Ward C.P., Sencakova D., Doody R.S., Thal L.J. Longitudinal MRI findings from the vitamin E and donepezil treatment study for MCI. Neurobiol. Aging 2008, 29:1285-1295. Members of the Alzheimer's Disease Cooperative Study (ADCS).
32. Jellinger K.A., Wenning G.K., Seppi K. Predictors of survival in dementia with lewy bodies and Parkinson dementia. Neurodegener. Dis. 2007, 4:428-430.
33. Josephs K.A., Whitwell J.L., Ahmed Z., Shiung M.M., Weigand S.D., Knopman D.S., Boeve B.F., Parisi J.E., Petersen R.C., Dickson D.W., Jack C.R. Beta-amyloid burden is not associated with rates of brain atrophy. Ann. Neurol. 2008, 63:204-212.
34. Josephs K.A., Whitwell J.L., Parisi J.E., Knopman D.S., Boeve B.F., Geda Y.E., Jack C.R., Petersen R.C., Dickson D.W. Argyrophilic grains: a distinct disease or an additive pathology?. Neurobiol. Aging 2008, 29:566-573.
35. Kantarci K., Senjem M.L., Lowe V.J., Wiste H.J., Weigand S.D., Kemp B.J., Frank A.R., Shiung M.M., Boeve B.F., Knopman D.S., Petersen R.C., Jack C.R. Effects of age on the glucose metabolic change in mild cognitive impairment. AJNR Am. J. Neuroradiol. 2010, 31:1247-1253.
36. Kantarci K., Ferman T.J., Boeve B.F., Weigand S.D., Przybelski S., Vemuri P., Murray M.E., Senjem M.L., Smith G.E., Knopman D.S., Petersen R.C., Jack C.R., Parisi J.E., Dickson D.W. Focal atrophy on MRI and neuropathologic classification of dementia with Lewy bodies. Neurology 2012, 79:553-560.
37. Knopman D.S., Parisi J.E., Salviati A., Floriach-Robert M., Boeve B.F., Ivnik R.J., Smith G.E., Dickson D.W., Johnson K.A., Petersen L.E., McDonald W.C., Braak H., Petersen R.C. Neuropathology of cognitively normal elderly. J.Neuropathol. Exp. Neurol. 2003, 62:1087-1095.
38. Kosaka K. Lewy bodies in cerebral cortex, report of three cases. Acta Neuropathol. 1978, 42:127-134.
39. Lashley T., Holton J.L., Gray E., Kirkham K., O'Sullivan S.S., Hilbig A., Wood N.W., Lees A.J., Revesz T. Acta Neuropathol. 2008, 115:417-425.
40. Lewy F. Paralysis agitans. I. Pathologische Anatomie. Handbuch der Neurologie 1912, 3:920-933. Springer-Verlag, Berlin.
41. Mattis S. Dementia Rating Scale (DRS) 1988, Psychological Assessment Resources, Odessa, FL:.
42. McKeith I.G., Mintzer J., Aarsland D., Burn D., Chiu H., Cohen-Mansfield J., Dickson D., Dubois B., Duda J.E., Feldman H., Gauthier S., Halliday G., Lawlor B., Lippa C., Lopez O.L., Carlos Machado J., O'Brien J., Playfer J., Reid W. Dementia with Lewy bodies. Lancet Neurol. 2004, 3:19-28. International Psychogeriatric Association Expert Meeting on DLB.
43. McKeith I.G., Dickson D.W., Lowe J., Emre M., O'Brien J.T., Feldman H., Cummings J., Duda J.E., Lippa C., Perry E.K., Aarsland D., Arai H., Ballard C.G., Boeve B., Burn D.J., Costa D., Del Ser T., Dubois B., Galasko D., Gauthier S., Goetz C.G., Gomez-Tortosa E., Halliday G., Hansen L.A., Hardy J., Iwatsubo T., Kalaria R.N., Kaufer D., Kenny R.A., Korczyn A., Kosaka K., Lee V.M., Lees A., Litvan I., Londos E., Lopez O.L., Minoshima S., Mizuno Y., Molina J.A., Mukaetova-Ladinska E.B., Pasquier F., Perry R.H., Schulz J.B., Trojanowski J.Q., Yamada M. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005, 65:1863-1872. Consortium on DLB.
44. 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 1984, 34:939-944.
45. Merdes A.R., Hansen L.A., Jeste D.V., Galasko D., Hofstetter C.R., Ho G.J., Thal L.J., Corey-Bloom J. Influence of Alzheimer pathology on clinical diagnostic accuracy in dementia with Lewy bodies. Neurology 2003, 60:1586-1590.
46. Middelkoop H.A., van der Flier W.M., Burton J., Lloyd A.J., Paling S., Barber R., Ballard C., McKeith I.G., O'Brien J.T. Dementia with Lewy bodies and AD are not associated with occipital lobe atrophy on MRI. Neurology 2001, 57:2117-2120.
47. Mirra S.S., Heyman A., McKeel D., Sumi S.M., Crain B.J., Brownlee L.M., Vogel F.S., Hughes J.P., van Belle G., Berg L. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991, 41:479-486.
48. Murray M.E., Ferman T.J., Boeve B.F., Przybelski S.A., Lesnick T.G., Liesinger A.M., Senjem M.L., Gunter J.L., Preboske G.M., Lowe V.J., Vemuri P., Dugger B.N., Knopman D.S., Smith G.E., Parisi J.E., Silber M.H., Graff-Radford N.R., Petersen R.C., Jack C.R., Dickson D.W., Kantarci K. MRI and pathology of REM sleep behavior disorder in dementia with Lewy bodies. Neurology 2013, 81:1681-1689.
49. The National Institute on Aging and Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer's disease. Neurobiol. Aging 1997, 18(4 Suppl):S1-S2. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease.
50. O'Brien J.T., Paling S., Barber R., Williams E.D., Ballard C., McKeith I.G., Gholkar A., Crum W.R., Rossor M.N., Fox N.C. Progressive brain atrophy on serial MRI in dementia with Lewy bodies, AD, and vascular dementia. Neurology 2001, 56:1386-1388.
51. O'Donovan J., Watson R., Colloby S.J., Firbank M.J., Burton E.J., Barber R., Blamire A.M., O'Brien J.T. Does posterior cortical atrophy on MRI discriminate between Alzheimer's disease, dementia with Lewy bodies, and normal aging?. Int. Psychogeriatr. 2013, 25:111-119.
52. Patenaude B., Smith S.M., Kennedy D.N., Jenkinson M. ABayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 2011, 56:907-922.
53. Petersen R.C. Mild cognitive impairment as a diagnostic entity. J.Intern. Med. 2004, 256:183-194.
54. Petersen R.C., Kokmen E., Tangalos E., Ivnik R.J., Kurland L.T. Mayo clinic Alzheimer's disease patient registry. Aging (Milano) 1990, 2:408-415.
55. Ridha B.H., Barnes J., Bartlett J.W., Godbolt A., Pepple T., Rossor M.N., Fox N.C. Tracking atrophy progression in familial Alzheimer's disease: a serial MRI study. Lancet Neurol. 2006, 5:828-834.
56. Saito Y., Ruberu N.N., Sawabe M., Arai T., Tanaka N., Kakuta Y., Yamanouchi H., Murayama S. Staging of argyrophilic grains: an age-associated tauopathy. J.Neuropathol. Exp. Neurol. 2004, 63:911-918.
57. Scahill R.I., Schott J.M., Stevens J.M., Rossor M.N., Fox N.C. Mapping the evolution of regional atrophy in Alzheimer's disease: unbiased analysis of fluid-registered serial MRI. Proc. Natl. Acad. Sci. U.S.A 2002, 99:4703-4707.
58. Schneider J.A., Arvanitakis Z., Bang W., Bennett D.A. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology 2007, 69:2197-2204.
59. Schneider J.A., Arvanitakis Z., Leurgans S.E., Bennett D.A. The neuropathology of probable Alzheimer disease and mild cognitive impairment. Ann. Neurol. 2009, 66:200-208.
60. Silbert L.C., Quinn J.F., Moore M.M., Corbridge E., Ball M.J., Murdoch G., Sexton G., Kaye J.A. Changes in premorbid brain volume predict Alzheimer's disease pathology. Neurology 2003, 61:487-492.
61. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nat. Neurosci. 2003, 6:309-315.
62. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997, 388:839-840.
63. Thompson P.M., Hayashi K.M., de Zubicaray G., Janke A.L., Rose S.E., Semple J., Herman D., Hong M.S., Dittmer S.S., Doddrell D.M., Toga A.W. Dynamics of gray matter loss in Alzheimer's disease. J.Neurosci. 2003, 23:994-1005.
64. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
65. Vemuri P., Whitwell J.L., Kantarci K., Josephs K.A., Parisi J.E., Shiung M.S., Knopman D.S., Boeve B.F., Petersen R.C., Dickson D.W., Jack C.R. Antemortem MRI based STructural Abnormality iNDex (STAND)-scores correlate with postmortem Braak neurofibrillary tangle stage. Neuroimage 2008, 42:559-567.
66. Vemuri P., Simon G., Kantarci K., Whitwell J.L., Senjem M.L., Przybelski S.A., Gunter J.L., Josephs K.A., Knopman D.S., Boeve B.F., Ferman T.J., Dickson D.W., Parisi J.E., Petersen R.C., Jack C.R. Antemortem differential diagnosis of dementia pathology using structural MRI: differential-STAND. Neuroimage 2011, 55:522-531.
67. Whitwell J.L., Jack C.R., Parisi J.E., Knopman D.S., Boeve B.F., Petersen R.C., Ferman T.J., Dickson D.W., Josephs K.A. Rates of cerebral atrophy differ in different degenerative pathologies. Brain 2007, 130(Pt 4):1148-1158.
68. Whitwell J.L., Weigand S.D., Shiung M.M., Boeve B.F., Ferman T.J., Smith G.E., Knopman D.S., Petersen R.C., Benarroch E.E., Josephs K.A., Jack C.R. Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer's disease. Brain 2007, 130(Pt 3):708-719.