Cerebrospinal fluid markers of neurodegeneration and rates of brain atrophy in early Alzheimer disease

JAMA Neurology

Volumn 72, Issue 6, 2015, Pages 656-665

  Tarawneh, Rawan ^a,b   Head, Denise ^a,c   Allison, Samantha ^a   Buckles, Virginia ^a   Fagan, Anne M ^a   Ladenson, Jack H ^d   Morris, John C ^a,d   Holtzman, David M ^a,d  

^a WASHINGTON UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABETA42 PROTEIN; BIOLOGICAL MARKER; TAU 181 PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG; VISININ; VISININ LIKE PROTEIN 1; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); NEUROCALCIN; PEPTIDE FRAGMENT; VSNL1 PROTEIN, HUMAN;

AGED; AGING; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; CEREBROSPINAL FLUID; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; FOLLOW UP; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OBSERVATIONAL STUDY; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; ATROPHY; BRAIN; LONGITUDINAL STUDY; PATHOLOGY; SEVERITY OF ILLNESS INDEX;

AGED; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ATROPHY; BIOMARKERS; BRAIN; FEMALE; HUMANS; LONGITUDINAL STUDIES; MALE; NEUROCALCIN; PEPTIDE FRAGMENTS; SEVERITY OF ILLNESS INDEX; TAU PROTEINS;

EID: 84931089913     PISSN: 21686149     EISSN: 21686157     Source Type: Journal    
DOI: 10.1001/jamaneurol.2015.0202     Document Type: Article

References (70)

1. Price JL, Morris JC. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol. 1999;45(3):358-368.
2. Jack CR Jr, Knopman DS, Jagust WJ, et al. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 2010;9(1):119-128.
3. Price JL, Ko AI, Wade MJ, Tsou SK, McKeel DW, Morris JC. Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch Neurol. 2001;58(9):1395-1402.
4. Jack CR Jr, Shiung MM, Weigand SD, et al. Brain atrophy rates predict subsequent clinical conversion in normal elderly and amnestic MCI. Neurology. 2005;65(8):1227-1231.
5. Vemuri P, Wiste HJ, Weigand SD, et al; Alzheimer's Disease Neuroimaging Initiative. MRI and CSF biomarkers in normal, MCI, and AD subjects: predicting future clinical change. Neurology. 2009;73(4):294-301.
6. Braunewell KH, Klein-Szanto AJ. Visinin-like proteins (VSNLs): interaction partners and emerging functions in signal transduction of a subfamily of neuronal Ca2+-sensor proteins. Cell Tissue Res. 2009;335(2):301-316.
7. Laterza OF, Modur VR, Crimmins DL, et al. Identification of novel brain biomarkers. Clin Chem. 2006;52(9):1713-1721.
8. Tarawneh R, D'Angelo G, Macy E, et al. Visinin-like protein-1: diagnostic and prognostic biomarker in Alzheimer disease. Ann Neurol. 2011;70(2):274-285.
9. Tarawneh R, Lee JM, Ladenson JH, Morris JC, Holtzman DM. CSF VILIP-1 predicts rates of cognitive decline in early Alzheimer disease. Neurology. 2012;78(10):709-719.
10. Fagan AM, Xiong C, Jasielec MS, et al; Dominantly Inherited Alzheimer Network. Longitudinal change in CSF biomarkers in autosomal-dominant Alzheimer's disease. Sci Transl Med. 2014;6(226):226ra30.
11. Talbot C, Lendon C, Craddock N, Shears S, Morris JC, Goate A. Protection against Alzheimer's disease with apoE epsilon 2. Lancet. 1994;343(8910):1432-1433.
12. Morris JC. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology. 1993;43(11):2412-2414.
13. Storandt M, Grant EA, Miller JP, Morris JC. Longitudinal course and neuropathologic outcomes in original vs revised MCI and in pre-MCI. Neurology. 2006;67(3):467-473.
14. Morris JC, Blennow K, Froelich L, et al. Harmonized diagnostic criteria for Alzheimer's disease: recommendations. J Intern Med. 2014;275(3):204-213.
15. Berg L, Miller JP, Baty J, Rubin EH, Morris JC, Figiel G. Mild senile dementia of the Alzheimer type, 4: evaluation of intervention. Ann Neurol. 1992;31(3):242-249.
16. 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(3):189-198.
17. Morris JC, Weintraub S, Chui HC, et al. The Uniform Data Set (UDS): clinical and cognitive variables and descriptive data from Alzheimer Disease Centers. Alzheimer Dis Assoc Disord. 2006;20(4):210-216.
18. Berg L, McKeel DW Jr, Miller JP, et al. Clinicopathologic studies in cognitively healthy aging and Alzheimer's disease: relation of histologic markers to dementia severity, age, sex, and apolipoprotein E genotype. Arch Neurol. 1998;55(3):326-335.
19. Fagan AM, Mintun MA, Mach RH, et al. Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Aβ42 in humans. Ann Neurol. 2006;59(3):512-519.
20. Cirrito JR, May PC, O'Dell MA, et al. In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-βmetabolism and half-life. J Neurosci. 2003;23(26):8844-8853.
21. Buckner RL, Head D, Parker J, et al. A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage. 2004;23(2):724-738.
22. Head D, Snyder AZ, Girton LE, Morris JC, Buckner RL. Frontal-hippocampal double dissociation between normal aging and Alzheimer's disease. Cereb Cortex. 2005;15(6):732-739.
23. Zhang Y, Brady M, Smith S. Segmentation of brainMR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 2001;20(1):45-57.
24. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17(3):143-155.
25. Desikan RS, Segonne F, Fischl B, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31(3):968-980.
26. Fischl B, Salat DH, Busa E, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33(3):341-355.
27. Braak H, Braak E, Bohl J. Staging of Alzheimer-related cortical destruction. Eur Neurol. 1993;33(6):403-408.
28. Tosun D, Schuff N, Truran-Sacrey D, et al; Alzheimer's Disease Neuroimaging Initiative. Relations between brain tissue loss, CSF biomarkers, and the ApoE genetic profile: a longitudinal MRI study. Neurobiol Aging. 2010;31(8):1340-1354.
29. Hostage CA, Choudhury KR, Murali Doraiswamy P, Petrella JR; Alzheimer's Disease Neuroimaging Initiative. Mapping the effect of the apolipoprotein E genotype on 4-year atrophy rates in an Alzheimer disease.related brain network. Radiology. 2014;271(1):211-219.
30. Braunewell K, Riederer P, Spilker C, Gundelfinger ED, Bogerts B, Bernstein HG. Abnormal localization of two neuronal calcium sensor proteins, visinin-like proteins (VILIPs)-1 and -3, in neocortical brain areas of Alzheimer disease patients. Dement Geriatr Cogn Disord. 2001;12(2):110-116.
31. Schnurra I, Bernstein HG, Riederer P, Braunewell KH. The neuronal calcium sensor protein VILIP-1 is associated with amyloid plaques and extracellular tangles in Alzheimer's disease and promotes cell death and tau phosphorylation in vitro: a link between calcium sensors and Alzheimer's disease? Neurobiol Dis. 2001;8(5):900-909.
32. Lee JM, Blennow K, Andreasen N, et al. The brain injury biomarker VLP-1 is increased in the cerebrospinal fluid of Alzheimer disease patients. Clin Chem. 2008;54(10):1617-1623.
33. Luo X, Hou L, Shi H, et al. CSF levels of the neuronal injury biomarker visinin-like protein-1 in Alzheimer's disease and dementia with Lewy bodies. J Neurochem. 2013;127(5):681-690.
34. Braunewell KH. The visinin-like proteins VILIP-1 and VILIP-3 in Alzheimer's disease: old wine in new bottles. Front Mol Neurosci. 2012;5:20.
35. Henneman WJ, Vrenken H, Barnes J, et al. Baseline CSF p-tau levels independently predict progression of hippocampal atrophy in Alzheimer disease. Neurology. 2009;73(12):935-940.
36. Hampel H, Burger K, Pruessner JC, et al. Correlation of cerebrospinal fluid levels of tau protein phosphorylated at threonine 231 with rates of hippocampal atrophy in Alzheimer disease. Arch Neurol. 2005;62(5):770-773.
37. Wahlund LO, Blennow K. Cerebrospinal fluid biomarkers for disease stage and intensity in cognitively impaired patients. Neurosci Lett. 2003;339(2):99-102.
38. Tosun D, Schuff N, Shaw LM, Trojanowski JQ, Weiner MW; Alzheimer's Disease NeuroImaging Initiative. Relationship between CSF biomarkers of Alzheimer's disease and rates of regional cortical thinning in ADNI data. J Alzheimers Dis. 2011;26(suppl 3):77-90.
39. Josephs KA, Whitwell JL, Ahmed Z, et al. Beta-amyloid burden is not associated with rates of brain atrophy. Ann Neurol. 2008;63(2):204-212.
40. Schuff N, Woerner N, Boreta L, et al; Alzheimer's Disease Neuroimaging Initiative. MRI of hippocampal volume loss in early Alzheimer's disease in relation to ApoE genotype and biomarkers. Brain. 2009;132(pt 4):1067-1077.
41. Tarawneh R, Holtzman DM. Biomarkers in translational research of Alzheimer's disease. Neuropharmacology. 2010;59(4-5):310-322.
42. Tarawneh R, Holtzman DM. Critical issues for successful immunotherapy in Alzheimer's disease: development of biomarkers and methods for early detection and intervention. CNS Neurol Disord Drug Targets. 2009;8(2):144-159.
43. Csernansky JG, Hamstra J, Wang L, et al. Correlations between antemortem hippocampal volume and postmortem neuropathology in AD subjects. Alzheimer Dis Assoc Disord. 2004;18(4):190-195.
44. Whitwell JL, Josephs KA, Murray ME, et al. MRI correlates of neurofibrillary tangle pathology at autopsy: a voxel-based morphometry study. Neurology. 2008;71(10):743-749.
45. Silbert LC, Quinn JF, Moore MM, et al. Changes in premorbid brain volume predict Alzheimer's disease pathology. Neurology. 2003;61(4):487-492.
46. Bobinski M, De Leon MJ, Wegiel J, et al. The histological validation of post mortem magnetic resonance imaging.determined hippocampal volume in Alzheimer's disease. Neuroscience. 2000;95(3):721-725.
47. Zarow C, Vinters HV, Ellis WG, et al. Correlates of hippocampal neuron number in Alzheimer's disease and ischemic vascular dementia. Ann Neurol. 2005;57(6):896-903.
48. Chetelat G, Villemagne VL, Bourgeat P, et al; Australian Imaging Biomarkers and Lifestyle Research Group. Relationship between atrophy and β-amyloid deposition in Alzheimer disease. Ann Neurol. 2010;67(3):317-324.
49. Ingelsson M, Fukumoto H, Newell KL, et al. Early Aβ accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology. 2004;62(6):925-931.
50. Andreasen N, Hesse C, Davidsson P, et al. Cerebrospinal fluid β-amyloid (1-42) in Alzheimer disease: differences between early- and late-onset Alzheimer disease and stability during the course of disease. Arch Neurol. 1999;56(6):673-680.
51. Blennow K, Zetterberg H, Minthon L, et al. Longitudinal stability of CSF biomarkers in Alzheimer's disease. Neurosci Lett. 2007;419(1):18-22.
52. Van Rossum IA, Visser PJ, Knol DL, et al. Injury markers but not amyloid markers are associated with rapid progression frommild cognitive impairment to dementia in Alzheimer's disease. J Alzheimers Dis. 2012;29(2):319-327.
53. Bennett DA, Schneider JA, Wilson RS, Bienias JL, Arnold SE. Neurofibrillary tangles mediate the association of amyloid load with clinical Alzheimer disease and level of cognitive function. Arch Neurol. 2004;61(3):378-384.
54. De Leon MJ, George AE, Stylopoulos LA, Smith G, Miller DC. Early marker for Alzheimer's disease: the atrophic hippocampus. Lancet. 1989;2(8664):672-673.
55. Risacher SL, Saykin AJ. Neuroimaging and other biomarkers for Alzheimer's disease: the changing landscape of early detection. Annu Rev Clin Psychol. 2013;9:621-648.
56. Baron JC, Chetelat G, Desgranges B, et al. In vivo mapping of gray matter loss with voxel-based morphometry inmild Alzheimer's disease. Neuroimage. 2001;14(2):298-309.
57. Chetelat G, Desgranges B, De La Sayette V, Viader F, Eustache F, Baron JC. Mapping gray matter loss with voxel-based morphometry inmild cognitive impairment. Neuroreport. 2002;13(15):1939-1943.
58. Braak H, Braak E, Bohl J, Bratzke H. Evolution of Alzheimer's disease related cortical lesions. J Neural Transm Suppl. 1998;54:97-106.
59. Whitwell JL, Shiung MM, Przybelski SA, et al. MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology. 2008;70(7):512-520.
60. Fan Y, Resnick SM, Wu X, Davatzikos C. Structural and functional biomarkers of prodromal Alzheimer's disease: a high-dimensional pattern classification study. Neuroimage. 2008;41(2):277-285.
61. Misra C, Fan Y, Davatzikos C. Baseline and longitudinal patterns of brain atrophy in MCI patients, and their use in prediction of short-term conversion to AD: results from ADNI. Neuroimage. 2009;44(4):1415-1422.
62. Bobinski M, De Leon MJ, Tarnawski M, et al. Neuronal and volume loss in CA1 of the hippocampal formation uniquely predicts duration and severity of Alzheimer disease. Brain Res. 1998;805(1-2):267-269.
63. Fjell AM, Walhovd KB, Fennema-Notestine C, et al; Alzheimer's Disease Neuroimaging Initiative. CSF biomarkers in prediction of cerebral and clinical change in mild cognitive impairment and Alzheimer's disease. J Neurosci. 2010;30(6):2088-2101.
64. Jack CR Jr, Dickson DW, Parisi JE, et al. Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology. 2002;58(5):750-757.
65. Jack CR Jr, Holtzman DM. Biomarker modeling of Alzheimer's disease. Neuron. 2013;80(6):1347-1358.
66. Sperling RA, Aisen PS, Beckett LA, et al. 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. 2011;7(3):280-292.
67. Desikan RS, McEvoy LK, Thompson WK, et al; Alzheimer's Disease Neuroimaging Initiative. Amyloid-β-associated clinical decline occurs only in the presence of elevated p-tau. Arch Neurol. 2012;69(6):709-713.
68. Ridha BH, Barnes J, Bartlett JW, et al. Tracking atrophy progression in familial Alzheimer's disease: a serial MRI study. Lancet Neurol. 2006;5(10):828-834.
69. Schott JM, Fox NC, Frost C, et al. Assessing the onset of structural change in familial Alzheimer's disease. Ann Neurol. 2003;53(2):181-188.
70. Holtzman DM, Goate A, Kelly J, Sperling R. Mapping the road forward in Alzheimer's disease. Sci Transl Med. 2011;3(114):114ps48.