Arterial spin labeling imaging reveals widespread and Aβ-independent reductions in cerebral blood flow in elderly apolipoprotein epsilon-4 carriers

Journal of Cerebral Blood Flow and Metabolism

Volumn 36, Issue 3, 2016, Pages 581-595

  Michels, Lars ^a,b   Warnock, Geoffrey ^a   Buck, Alfred ^a   Macauda, Gianluca ^a,d   Leh, Sandra E ^c   Kaelin, Andrea M ^c   Riese, Florian ^c   Meyer, Rafael ^c   O'gorman, Ruth ^b   Hock, Christoph ^c   Kollias, Spyros ^a   Gietl, Anton F ^c  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

amnestic; apolipoprotein E; arterial spin labeling; beta amyloid; Mild cognitive impairment

Indexed keywords

ACETYLSALICYLIC ACID; AMYLOID BETA PROTEIN; ANTIHYPERTENSIVE AGENT; APOLIPOPROTEIN E4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PITTSBURGH COMPOUND B; SPIN LABEL;

AGED; ARTICLE; BRAIN BLOOD FLOW; BRAIN PERFUSION; CAUDATE NUCLEUS; CINGULATE GYRUS; CLINICAL ARTICLE; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GROUP DYNAMICS; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; MALE; MIDDLE FRONTAL GYRUS; MIDDLE OCCIPITAL GYRUS; MILD COGNITIVE IMPAIRMENT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PUTAMEN; SPIN LABELING; THALAMUS; VISUAL CORTEX; BRAIN CIRCULATION; COGNITIVE DEFECT; GENETICS; GENOTYPE; METABOLISM; PATHOPHYSIOLOGY;

AGED; AMYLOID BETA-PEPTIDES; APOLIPOPROTEIN E4; CEREBROVASCULAR CIRCULATION; COGNITIVE DYSFUNCTION; FEMALE; GENOTYPE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; POSITRON-EMISSION TOMOGRAPHY; SPIN LABELS;

EID: 84959333462     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X15605847     Document Type: Article

References (53)

1. Johnson KA, Jones K, Holman BL, et al. Preclinical prediction of Alzheimers disease using SPECT. Neurology 1998; 50(6): 1563-1571
2. Ishii K, Sasaki M, Yamaji S, et al. Demonstration of decreased posterior cingulate perfusion in mild Alzheimers disease by means of H215O positron emission tomography. Eur J Nucl Med 1997; 24(6): 670-673
3. Landau SM, Harvey D, Madison CM, et al. Associations between cognitive, functional, and FDG-PET measures of decline in AD, and MCI. Neurobiol Aging 2011; 32(7): 1207-1218
4. Detre JA, Leigh JS, Williams DS, et al. Perfusion imaging. Magn Reson Med 1992; 23(1): 37-45
5. Alexopoulos P, Sorg C, Forschler A, et al. Perfusion abnormalities in mild cognitive impairment, and mild dementia in Alzheimers disease measured by pulsed arterial spin labeling MRI. Eur Arch Psychiatry Clin Neurosci 2012; 262(1): 69-77
6. Mattsson N, Tosun D, Insel PS, et al. Association of brain amyloid-beta with cerebral perfusion, and structure in Alzheimers disease, and mild cognitive impairment. Brain 2014; 137(Pt 5): 1550-1561
7. Chao LL, Buckley ST, Kornak J, et al. ASL perfusion MRI predicts cognitive decline, and conversion from MCI to dementia. Alzheimer Dis Assoc Disord 2010; 24(1): 19-27
8. Wang Z, Das SR, Xie SX, et al. Arterial spin labeled MRI in prodromal Alzheimers disease: A multi-site study. NeuroImage Clin 2013; 2: 630-636
9. Walsh DM, Klyubin I, Fadeeva JV, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002; 416(6880): 535-539
10. Scheff SW, Price DA, Schmitt FA, et al. Synaptic loss in the inferior temporal gyrus in mild cognitive impairment, and Alzheimers disease. JAD 2011; 24(3): 547-557
11. Dubois B, Feldman HH, Jacova C, et al. Advancing research diagnostic criteria for Alzheimers disease: the IWG-2 criteria. Lancet Neurol 2014; 13(6): 614-629
12. Sperling RA, Aisen PS, Beckett LA, et al. Toward defining the preclinical stages of Alzheimers disease: recommendations from the National Institute on Aging-Alzheimers Association workgroups on diagnostic guidelines for Alzheimers disease. Alzheimers Dementia: J Alzheimers Assoc 2011; 7(3): 280-292
13. Sojkova J, Beason-Held L, Zhou Y, et al. Longitudinal cerebral blood flow, and amyloid deposition: an emerging pattern?. J Nucl Med 2008; 49(9): 1465-1471
14. Abrahamson EE, Foley LM, Dekosky ST, et al. Cerebral blood flow changes after brain injury in human amyloidbeta knock-in mice. J Cereb Blood Flow Metab 2013; 33(6): 826-833
15. Hu NW, Smith IM, Walsh DM, et al. Soluble amyloidbeta peptides potently disrupt hippocampal synaptic plasticity in the absence of cerebrovascular dysfunction in vivo. Brain 2008; 131(Pt 9): 2414-2424
16. Maier FC, Wehrl HF, Schmid AM, et al. Longitudinal PET-MRI reveals beta-amyloid deposition, and rCBF dynamics, and connects vascular amyloidosis to quantitative loss of perfusion. Nature Med 2014; 20(12): 1485-1492
17. Farrer LA, Cupples LA, Haines JL, et al. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype, and Alzheimer disease. A meta-analysis. APOE, and Alzheimer Disease Meta Analysis Consortium. JAMA 1997; 278(16): 1349-1356
18. Mielke MM, Wiste HJ, Weigand SD, et al. Indicators of amyloid burden in a population-based study of cognitively normal elderly. Neurology 2012; 79(15): 1570-1577
19. Fleisher AS, Podraza KM, Bangen KJ, et al. Cerebral perfusion, and oxygenation differences in Alzheimers disease risk. Neurobiol Aging 2009; 30(11): 1737-1748
20. Kim SM, Kim MJ, Rhee HY, et al. Regional cerebral perfusion in patients with Alzheimers disease, and mild cognitive impairment: effect of APOE epsilon4 allele. Neuroradiol 2013; 55(1): 25-34
21. Hogh P, Knudsen GM, Kjaer KH, et al. Single photon emission computed tomography, and apolipoprotein E in Alzheimers disease: impact of the epsilon4 allele on regional cerebral blood flow. J Geriatric Psych Neurol 2001; 14(1): 42-51
22. Thambisetty M, Beason-Held L, An Y, et al. APOE epsilon4 genotype, and longitudinal changes in cerebral blood flow in normal aging. Arch Neurol 2010; 67(1): 93-98
23. Lowe VJ, Weigand SD, Senjem ML, et al. Association of hypometabolism, and amyloid levels in aging, normal subjects. Neurology 2014; 82(22): 1959-1967
24. Gietl AF, Warnock G, Riese F, et al. Regional cerebral blood flow estimated by early PiB uptake is reduced in mild cognitive impairment, and associated with age in an amyloid-dependent manner. Neurobiol Aging 2015; 36(4): 1619-1628
25. Winblad B, Palmer K, Kivipelto M, et al. Mild cognitive impairment-beyond controversies, towards a consensus: report of the international working group on mild cognitive impairment. J Intern Med 2004; 256(3): 240-246
26. Morris JC, Heyman A, Mohs RC, et al. The consortium to establish a registry for alzheimers disease (CERAD). Part I. clinical, and neuropsychological assessment of Alzheimers disease. Neurology 1989; 39(9): 1159-1165
27. Wong EC, Buxton RB, and Frank LR. Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed 1997; 10(4-5): 237-249
28. Wang Z, Aguirre GK, Rao H, et al. Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn Reson Imag 2008; 26(2): 261-269
29. Buxton RB, Frank LR, Wong EC, et al. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 1998; 40(3): 383-396
30. Herscovitch P, and Raichle ME. What is the correct value for the brain-blood partition coefficient for water?. J Cereb Blood Flow Metab 1985; 5(1): 65-69
31. Lu H, Clingman C, Golay X, et al. Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla. Magn Reson Med 2004; 52(3): 679-682
32. Dai W, Garcia D, de Bazelaire C, et al. Continuous flowdriven inversion for arterial spin labeling using pulsed radio frequency, and gradient fields. Magn Reson Med 2008; 60(6): 1488-1497
33. Liu TT, and Wong EC. A signal processing model for arterial spin labeling functional MRI. Neuroimage 2005; 24(1): 207-215
34. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002; 15(1): 273-289
35. Riese F, Gietl A, Zolch N, et al. Posterior cingulate gamma-aminobutyric acid, and glutamate/glutamine are reduced in amnestic mild cognitive impairment, and are unrelated to amyloid deposition, and apolipoprotein E genotype. Neurobiol Aging 2015; 36(1): 53-59
36. Hixson JE, and Vernier DT. Restriction isotyping of human apolipoprotein E by gene amplification, and cleavage with HhaI. J Lipid Res 1990; 31(3): 545-548
37. Binnewijzend MA, Kuijer JP, Benedictus MR, et al. Cerebral blood flow measured with 3D pseudocontinuous arterial spin-labeling MR imaging in Alzheimer disease, and mild cognitive impairment: a marker for disease severity. Radiology 2013; 267(1): 221-230
38. Costafreda SG, Fu CH, Lee L, et al. A systematic review, and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Hum Brain Mapp 2006; 27(10): 799-810
39. Liakakis G, Nickel J, and Seitz RJ. Diversity of the inferior frontal gyrus-a meta-analysis of neuroimaging studies. Behav Brain Res 2011; 225(1): 341-347
40. Katzev M, Tuscher O, Hennig J, et al. Revisiting the functional specialization of left inferior frontal gyrus in phonological, and semantic fluency: the crucial role of task demands, and individual ability. J Neuroscience 2013; 33(18): 7837-7845
41. Mosconi L, Tsui WH, Herholz K, et al. Multicenter standardized 18F-FDG PET diagnosis of mild cognitive impairment, Alzheimers disease, and other dementias. J Nucl Med 2008; 49(3): 390-398
42. Chen Y, Wolk DA, Reddin JS, et al. Voxel-level comparison of arterial spin-labeled perfusion MRI, and FDGPET in Alzheimer disease. Neurology 2011; 77(22): 1977-1985
43. Qiu A, Fennema-Notestine C, Dale AM, et al. Alzheimers disease neuroimaging I. regional shape abnormalities in mild cognitive impairment, and Alzheimers disease. Neuroimage 2009; 45(3): 656-661
44. Tang X, Holland D, Dale AM, et al. Baseline shape diffeomorphometry patterns of subcortical, and ventricular structures in predicting conversion of mild cognitive impairment to Alzheimers disease. JAD 2015; 44(2): 599-611
45. Tang X, Holland D, Dale AM, et al. Alzheimers disease neuroimaging I. Shape abnormalities of subcortical, and ventricular structures in mild cognitive impairment, and Alzheimers disease: detecting, quantifying, and predicting. Hum Brain Mapp 2014; 35(8): 3701-3725
46. Knopman DS, Jack CR Jr., Wiste HJ, et al. 18)F-fluorodeoxyglucose positron emission tomography, aging, and apolipoprotein E genotype in cognitively normal persons. Neurobiol Aging 2014; 35(9): 2096-106
47. Reiman EM, Chen K, Alexander GE, et al. Correlations between apolipoprotein E epsilon4 gene dose, and brainimaging measurements of regional hypometabolism. Proc Natl Acad Sci USA 2005; 102(23): 8299-8302
48. Liu Y, Yu JT, Wang HF, et al. APOE genotype, and neuroimaging markers of Alzheimers disease: systematic review, and meta-analysis. J Neurol Neurosurg Psych 2015; 86(2): 127-134
49. Jagust WJ, and Landau SM, Alzheimers Disease Neuroimaging I. Apolipoprotein E, not fibrillar betaamyloid, reduces cerebral glucose metabolism in normal aging. J Neurosci 2012; 32(50): 18227-18233
50. Zlokovic BV. Cerebrovascular effects of apolipoprotein E: implications for Alzheimer disease. JAMA Neurol 2013; 70(4): 440-444
51. Bell RD, Winkler EA, Singh I, et al. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature 2012; 485(7399): 512-516
52. Liu CC, Kanekiyo T, Xu H, et al. Apolipoprotein E, and Alzheimer disease: risk, mechanisms, and therapy. Nat Rev Neurol 2013; 9(2): 106-118
53. Alsop DC, Detre JA, Golay X, et al. Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: A consensus of the ISMRM perfusion study group, and the European consortium for ASL in dementia. Magnetic Reson Med. Epub ahead of print 8 April 2014. DOI: 10.1002/mrm.25197