Spatial patterns of longitudinal gray matter change as predictors of concurrent cognitive decline in amyloid positive healthy subjects

Journal of Alzheimer's Disease

Volumn 55, Issue 1, 2016, Pages 343-358

  Caballero, Miguel Ángel Araque ^a   Klöppel, Stefan ^b   Dichgans, Martin ^a,c   Ewers, Michael ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c Technische Universität München Munich Cluster for Systems Neurology   (Germany)

Author keywords

Aging; Alzheimer's disease; atrophy; gray matter; longitudinal; magnetic resonance imaging; multivariate; pattern recognition; relevance vector regression

Indexed keywords

AMYLOID BETA PROTEIN; BIOLOGICAL MARKER; APOLIPOPROTEIN E;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; CEREBROSPINAL FLUID ANALYSIS; COGNITION ASSESSMENT; COGNITIVE DEFECT; EPISODIC MEMORY; EXECUTIVE FUNCTION; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RELEVANCE VECTOR MACHINE; ATROPHY; BRAIN; CEREBROSPINAL FLUID; DIAGNOSTIC IMAGING; FOLLOW UP; GENETICS; LONGITUDINAL STUDY; METABOLISM; NERVE TRACT; PROGNOSIS; REGRESSION ANALYSIS; THREE DIMENSIONAL IMAGING;

AGED; AMYLOID BETA-PEPTIDES; APOLIPOPROTEINS E; ATROPHY; BIOMARKERS; BRAIN; COGNITIVE DYSFUNCTION; EXECUTIVE FUNCTION; FEMALE; FOLLOW-UP STUDIES; GRAY MATTER; HUMANS; IMAGING, THREE-DIMENSIONAL; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; NEURAL PATHWAYS; POSITRON-EMISSION TOMOGRAPHY; PROGNOSIS; REGRESSION ANALYSIS;

EID: 84994655852     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-160327     Document Type: Article

References (58)

1. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, 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.
2. Jack CR, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, Shaw LM, Vemuri P, Wiste HJ, Weigand SD, Lesnick TG, Pankratz VS, Donohue MC, Trojanowski JQ (2013) Tracking pathophysiological processes in Alzheimer?s disease: An updated hypothetical model of dynamic biomarkers. Lancet Neurol 12, 207-216.
3. Dubois B, Hampel H, Feldman HH, Scheltens P, Aisen P, Andrieu S, Bakardjian H, Benali H, Bertram L, Blennow K, Broich K, Cavedo E, Crutch S, Dartigues JF, Duyck aerts C, Epelbaum S, Frisoni GB, Gauthier S, Genthon R, Gouw AA, Habert MO, Holtzman DM, Kivipelto M, Lista S, Molinuevo JL, O?Bryant SE, Rabinovici GD, Rowe C, Salloway S, Schneider LS, Sperling R, Teichmann M, Carrillo MC, Cummings J, Jack CR Jr (2016) Proceedings of the Meeting of the International Working Group (IWG) and the American Alzheimer?s Association on The Preclinical State of AD; July 23, 2015; Washington DC, USA, Preclinical Alzheimer?s disease: Definition, natural history, and diagnostic criteria. Alzheimers Dement 12, 292-323.
4. Vos SJ, Xiong C, Visser PJ, Jasielec MS, Hassenstab J, Grant EA, Cairns NJ, Morris JC, Holtzman DM, Fagan AM (2013) Preclinical Alzheimer?s disease and its outcome: A longitudinal cohort study. Lancet Neurol 12, 957-965.
5. Knopman DS, Jack CR Jr, Wiste HJ, Weigand SD, Vemuri P, Lowe V, Kantarci K, Gunter JL, Senjem ML, Ivnik RJ, Roberts RO, Boeve BF, Petersen RC (2012) Short-Term clinical outcomes for stages of NIA-AA preclinical Alzheimer disease. Neurology 78, 1576-1582.
6. Mormino EC, Betensky RA, Hedden T, Schultz AP, Amariglio RE, Rentz DM, Johnson KA, Sperling RA (2014) Synergistic effect of beta-Amyloid and neurodegeneration on cognitive decline in clinically normal individuals. JAMA Neurol 71, 1379-1385.
7. Wirth M, Villeneuve S, Haase CM, Madison CM, Oh H, Landau SM, Rabinovici GD, Jagust WJ (2013) Associations between Alzheimer disease biomarkers, neurodegeneration, and cognition in cognitively normal older people. JAMA Neurol 70, 1512-1519.
8. Mattsson N, Insel PS, Nosheny R, Tosun D, Trojanowski JQ, Shaw LM, Jack CR Jr, Donohue MC, Weiner MW, Alzheimer?s Disease Neuroimaging Initiative (2014) Emerging beta-Amyloid pathology and accelerated cortical atrophy. JAMA Neurol 71, 725-734.
9. Nosheny RL, Insel PS, Truran D, Schuff N, Jack CR Jr, Aisen PS, Shaw LM, Trojanowski JQ, Weiner MW, Alzheimer?s Disease Neuroimaging (2015) Variables associated with hippocampal atrophy rate in normal aging and mild cognitive impairment. Neurobiol Aging 36, 273-282.
10. Jack CR Jr, Wiste HJ, Weigand SD, Knopman DS, Lowe V, Vemuri P, Mielke MM, Jones DT, Senjem ML, Gunter JL, Gregg BE, Pankratz VS, Petersen RC (2013) Amyloid-first and neurodegeneration-first profiles characterize incident amyloid PET positivity. Neurology 81, 1732-1740.
11. Chetelat G, Villemagne VL, Villain N, Jones G, Ellis KA, Ames D, Martins RN, Masters CL, Rowe CC, AIBL Research Group (2012) Accelerated cortical atrophy in cognitively normal elderly with high beta-Amyloid deposition. Neurology 78, 477-484.
12. Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Blennow K, Brewer JB, Dale AM, Alzheimer?s Disease Neuroimaging Initiative (2010) Brain atrophy in healthy aging is related to CSF levels of Abeta1-42. Cereb Cortex 20, 2069-2079.
13. Jack CR Jr, Wiste HJ, Knopman DS, Vemuri P, Mielke MM, Weigand SD, Senjem ML, Gunter JL, Lowe V, Gregg BE, Pankratz VS, Petersen RC (2014) Rates of beta-Amyloid accumulation are independent of hippocampal neurodegeneration. Neurology 82, 1605-1612.
14. Araque Caballero MA, Brendel M, Delker A, Ren J, Rominger A, Bartenstein P, Dichgans M, Weiner MW, Ewers M, Alzheimer?s Disease Neuroimaging Initiative (ADNI) (2015) Mapping 3-year changes in gray matter and metabolism in Abeta-positive nondemented subjects. Neurobiol Aging 36, 2913-2924.
15. Lim YY, Maruff P, Pietrzak RH, Ames D, Ellis KA, Harrington K, Lautenschlager NT, Szoeke C, Martins RN, Masters CL, Villemagne VL, Rowe CC, AIBL Research Group (2014) Effect of amyloid on memory and non-memory decline from preclinical to clinical Alzheimer?s disease. Brain 137(Pt 1), 221-231.
16. Ewers M, Insel P, Jagust WJ, Shaw L, Trojanowski JJ, Aisen P, Petersen RC, Schuff N, Weiner MW (2012) Alzheimer?s Disease Neuroimaging Initiative (ADNI), CSF biomarker and PIB-PET-derived beta-Amyloid signature predicts metabolic, gray matter, and cognitive changes in nondemented subjects. Cereb Cortex 22, 1993-2004.
17. Wang Y, Goh JO, Resnick SM, Davatzikos C (2013) Imaging-based biomarkers of cognitive performance in older adults constructed via high-dimensional pattern regression applied to MRI and PET. PLoS One 8, e85460.
18. Chu C, Mourao-Miranda J, Chiu Y-C, Kriegeskorte N, Tan G, Ashburner J (2011) Utilizing temporal information in fMRI decoding: Classifier using kernel regression methods. Neuroimage 58, 560-571.
19. Stonnington CM, Chu C, Klöppel S, Jack CR, Ashburner J, Frackowiak RSJ (2010) Predicting clinical scores from magnetic resonance scans in Alzheimer?s disease. Neuroimage 51, 1405-1413.
20. Gaser C, Franke K, Kloppel S, Koutsouleris N, Sauer H, Alzheimer?s Disease Neuroimaging Initiative (2013) Brain AGE in mild cognitive impaired patients: Predicting the conversion to Alzheimer?s disease. PLoS One 8, e67346.
21. Franke K, Ziegler G, Kloppel S, Gaser C (2010) Estimating the age of healthy subjects from T1-weighted MRI scans using kernel methods: Exploring the influence of various parameters. Neuroimage 50, 883-892.
22. Davatzikos C, Xu F, AnY, Fan Y, Resnick SM (2009) Longitudinal progression of Alzheimer?s-like patterns of atrophy in normal older adults: The SPARE-AD index. Brain 132, 2026-2035.
23. Plant C, Teipel SJ, Oswald A, Bohm C, Meindl T, Mourao-Miranda J, Bokde AW, Hampel H, Ewers M (2010) Automated detection of brain atrophy patterns based onMRI for the prediction of Alzheimer?s disease. Neuroimage 50, 162-174.
24. Clark VH, Resnick SM, Doshi J, Beason-Held LL, Zhou Y, Ferrucci L, Wong DF, Kraut MA, Davatzikos C (2012) Longitudinal imaging pattern analysis (SPARE-CD index) detects early structural and functional changes before cognitive decline in healthy older adults. Neurobiol Aging 33, 2733-2745.
25. Dickerson BC, Bakkour A, Salat DH, Feczko E, Pacheco J, Greve DN, Grodstein F, Wright CI, Blacker D, Rosas HD, Sperling RA, Atri A, Growdon JH, Hyman BT, Morris JC, Fischl B, Buckner RL (2009) The cortical signature of Alzheimer?s disease: Regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloidpositive individuals. Cereb Cortex 19, 497-510.
26. Mueller SG, Weiner MW, Thal LJ, Petersen RC, Jack C, Jagust W, Trojanowski JQ, Toga AW, Beckett L (2005) The Alzheimer?s disease neuroimaging initiative. Neuroimaging Clin N Am 15, 869-877, xi-xii.
27. Petersen RC, Aisen PS, Beckett LA, Donohue MC, Gamst AC, Harvey DJ, Jack CR Jr, Jagust WJ, Shaw LM, Toga AW, Trojanowski JQ, Weiner MW (2010) Alzheimer?s Disease Neuroimaging Initiative (ADNI): Clinical characterization. Neurology 74, 201-209.
28. Rosen WG, Mohs RC, Davis KL (1984) A new rating scale for Alzheimer?s disease. Am J Psychiatry 141, 1356-1364.
29. Crane PK, Carle A, Gibbons LE, Insel P, Mackin RS, Gross A, Jones RN, Mukherjee S, Curtis SM, Harvey D, Weiner M, Mungas D (2012) Development and assessment of a composite score for memory in the Alzheimer?s Disease Neuroimaging Initiative (ADNI). Brain Imaging Behav 6, 502-516.
30. Gibbons LE, Carle AC, Mackin RS, Harvey D, Mukherjee S, Insel P, Curtis SM, Mungas D, Crane PK (2012) A composite score for executive functioning, validated in Alzheimer?s Disease Neuroimaging Initiative (ADNI) participants with baseline mild cognitive impairment. Brain Imaging Behav 6, 517-527.
31. Shaw LM, Vanderstichele H, Knapik-Czajka M, Clark CM, Aisen PS, Petersen RC, Blennow K, Soares H, Simon A, Lewczuk P, Dean R, Siemers E, Potter W, Lee VM, Trojanowski JQ, Alzheimer?s Disease Neuroimaging Initiative (2009) Cerebrospinal fluid biomarker signature in Alzheimer?s disease neuroimaging initiative subjects. Ann Neurol 65, 403-413.
32. Jagust WJ, Bandy D, Chen K, Foster NL, Landau SM, Mathis CA, Price JC, Reiman EM, Skovronsky D, Koeppe RA, Alzheimer?s Disease Neuroimaging Initiative (2010) The Alzheimer?s Disease Neuroimaging Initiative positron emission tomography core. Alzheimers Dement 6, 221-229.
33. Landau SM, Breault C, Joshi AD, Pontecorvo M, Mathis CA, Jagust WJ, Mintun MA, Alzheimer?s Disease Neuroimaging Initiative (2013) Amyloid-beta imaging with Pittsburgh compound B and florbetapir: Comparing radiotracers and quantification methods. J Nucl Med 54, 70-77.
34. Fagan AM, Mintun MA, Mach RH, Lee SY, Dence CS, Shah AR, LaRossa GN, Spinner ML, Klunk WE, Mathis CA, DeKosky ST, Morris JC, Holtzman DM (2006) Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann Neurol 59, 512-519.
35. Villemagne VL, Burnham S, Bourgeat P, Brown B, Ellis KA, Salvado O, Szoeke C, Macaulay SL, Martins R, Maruff P, Ames D, Rowe CC, Masters CL (2013) Amyloid-deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer?s disease: A prospective cohort study. Lancet Neurol 12, 357-367.
36. Wyman BT, Harvey DJ, Crawford K, Bernstein MA, Carmichael O, Cole PE, Crane PK, DeCarli C, Fox NC, Gunter JL, Hill D, Killiany RJ, Pachai C, Schwarz AJ, Schuff N, Senjem ML, Suhy J, Thompson PM, Weiner M, Jack CR, Jr, Alzheimer?s Disease Neuroimaging Initiative (2013) Standardization of analysis sets for reporting results from ADNI MRI data. Alzheimers Dement 9, 332-337.
37. Luders E, Gaser C, Jancke L, Schlaug G (2004) A voxelbased approach to gray matter asymmetries. Neuroimage 22, 656-664.
38. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26, 839-851.
39. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38, 95-113.
40. Dore V, Villemagne VL, Bourgeat P, Fripp J, Acosta O, Chetelat G, Zhou L, Martins R, Ellis KA, Masters CL, Ames D, Salvado O, Rowe CC (2013) Cross-sectional and longitudinal analysis of the relationship between Abeta deposition, cortical thickness, and memory in cognitively unimpaired individuals and in Alzheimer disease. JAMA Neurol 70, 903-911.
41. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain?s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106, 13040-13045.
42. Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS (2012) Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32, 8988-8999.
43. Tipping ME (2001) Sparse Bayesian learning and the relevance vector machine. J Mach Learn Res 1, 211-244.
44. Schrouff J, Rosa MJ, Rondina JM, Marquand AF, Chu C, Ashburner J, Phillips C, Richiardi J, Mourao-Miranda J (2013) PRoNTo: Pattern recognition for neuroimaging toolbox. Neuroinformatics 11, 319-337.
45. Dickerson BC, Stoub TR, Shah RC, Sperling RA, Killiany RJ, Albert MS, Hyman BT, Blacker D, Detoledo-Morrell L (2011) Alzheimer-signature MRI biomarker predicts AD dementia in cognitively normal adults. Neurology 76, 1395-1402.
46. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289.
47. Oh H, Madison C, Villeneuve S, Markley C, Jagust WJ (2014) Association of gray matter atrophy with age, beta-Amyloid, and cognition in aging. Cereb Cortex 24, 1609-1618.
48. Schuff N, Tosun D, Insel PS, Chiang GC, Truran D, Aisen PS, Jack CR, Weiner MW, Alzheimer?s Disease Neuroimaging Initiative (2012) Nonlinear time course of brain volume loss in cognitively normal and impaired elders. Neurobiol Aging 33, 845-855.
49. La Joie R, Perrotin A, Barre L, Hommet C, Mezenge F, Ibazizene M, Camus V, Abbas A, Landeau B, Guilloteau D, de La Sayette V, Eustache F, Desgranges B, Chetelat G (2012) Region-specific hierarchy between atrophy, hypometabolism, and beta-Amyloid (Abeta) load in Alzheimer?s disease dementia. J Neurosci 32, 16265-16273.
50. Pfefferbaum A, Rohlfing T, Rosenbloom MJ, Chu W, Colrain IM, Sullivan EV (2013) Variation in longitudinal trajectories of regional brain volumes of healthy men and women (ages 10 to 85 years) measured with atlas-based parcellation of MRI. Neuroimage 65, 176-193.
51. DeCarli C, Massaro J, Harvey D, Hald J, Tullberg M, Au R, Beiser A, D?Agostino R, Wolf PA (2005) Measures of brain morphology and infarction in the framingham heart study: Establishing what is normal. Neurobiol Aging 26, 491-510.
52. Lockhart SN, DeCarli C (2014) Structural imaging measures of brain aging. Neuropsychol Rev 24, 271-289.
53. Toledo JB, Bjerke M, Chen K, Rozycki M, Jack CR Jr, Weiner MW, Arnold SE, Reiman EM, Davatzikos C, Shaw LM, Trojanowski JQ (2015) Alzheimer?s Disease Neuroimaging Initiative, Memory, executive, and multidomain subtle cognitive impairment: Clinical and biomarker findings. Neurology 85, 144-153.
54. Peter J, Scheef L, Abdulkadir A, Boecker H, Heneka M, Wagner M, Koppara A, Klöppel S, Jessen F (2014) Gray matter atrophy pattern in elderly with subjective memory impairment. Alzheimers Dement 10, 99-108.
55. Shaffer JL, Petrella JR, Sheldon FC, Choudhury KR, Calhoun VD, Coleman RE, Doraiswamy PM (2013) Predicting cognitive decline in subjects at risk for Alzheimer disease by using combined cerebrospinal fluid, MR imaging, and PET biomarkers. Radiology 266, 583-591.
56. Tipping M (2000) The relevance vector machine. In Advances in Neural Information Processing Systems, Solla SA, Leen TK, Müller K-R, eds.MITPress, Cambridge, MA, pp. 652-658.
57. Mwangi B, Matthews K, Steele JD (2012) Prediction of illness severity in patients with major depression using structural MRbrain scans. JMagn Reson Imaging 35, 64-71.
58. Mwangi B, Hasan KM, Soares JC (2013) Prediction of individual subject?s age across the human lifespan using diffusion tensor imaging: A machine learning approach. Neuroimage 75, 58-67.