Divergent regional patterns of cerebral hypoperfusion and gray matter atrophy in mild cognitive impairment patients

Journal of Cerebral Blood Flow and Metabolism

Volumn 37, Issue 3, 2017, Pages 814-824

  Wirth, Miranka ^a   Pichet Binette, Alexa ^a,b   Brunecker, Peter ^a   Köbe, Theresa ^a   Witte, A Veronica ^a,c   Flöel, Agnes ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^c MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

Author keywords

Alzheimer's disease; Cerebral blood flow; cerebral blood volume; magnetic resonance imaging; mild cognitive impairment

Indexed keywords

BIOLOGICAL MARKER;

ADULT; AGED; ALZHEIMER DISEASE; ANATOMICAL CONCEPTS; ARTICLE; BASAL GANGLION; BRAIN ATROPHY; BRAIN BLOOD FLOW; BRAIN PERFUSION; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; INFERIOR PARIETAL CORTEX; INFERIOR TEMPORAL CORTEX; MALE; MILD COGNITIVE IMPAIRMENT; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRECUNEUS; PRIORITY JOURNAL; RISK FACTOR; ATROPHY; BRAIN CIRCULATION; CASE CONTROL STUDY; COGNITIVE DEFECT; EARLY DIAGNOSIS; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ATROPHY; CASE-CONTROL STUDIES; CEREBROVASCULAR CIRCULATION; COGNITIVE DYSFUNCTION; EARLY DIAGNOSIS; GRAY MATTER; HUMANS; MAGNETIC RESONANCE IMAGING; MIDDLE AGED;

EID: 85012117549     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X16641128     Document Type: Article

References (62)

1. Serrano-Pozo A, Frosch MP, Masliah E, et al. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 2011; 1: A006189.
2. Jack CR Jr, Knopman DS, Jagust WJ, et al. Hypothetical model of dynamic biomarkers of the Alzheimers pathological cascade. Lancet Neurol 2010; 9: 119-128.
3. Iadecola C. The overlap between neurodegenerative and vascular factors in the pathogenesis of dementia. Acta Neuropathol 2010; 120: 287-296.
4. Girouard H and Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol (1985) 2006; 100: 328-335.
5. Iadecola C. Cerebrovascular effects of amyloid-beta peptides: mechanisms and implications for Alzheimers dementia. Cell Mol Neurobiol 2003; 23: 681-689.
6. Austin BP, Nair VA, Meier TB, et al. Effects of hypoperfusion in Alzheimers disease. J Alzheimers Dis: JAD 2011; 26Suppl 3: 123-133.
7. Wierenga CE, Hays CC and Zlatar ZZ. Cerebral blood flow measured by arterial spin labeling MRI as a preclinical marker of Alzheimers disease. J Alzheimers Dis: JAD 2014; 42: S411-S419.
8. Hirao K, Ohnishi T, Hirata Y, et al. The prediction of rapid conversion to Alzheimers disease in mild cognitive impairment using regional cerebral blood flow SPECT. Neuroimage 2005; 28: 1014-1021.
9. Matsuda H. Cerebral blood flow and metabolic abnormalities in Alzheimers disease. Ann Nucl Med 2001; 15: 85-92.
10. Luckhaus C, Cohnen M, Fluss MO, et al. The relation of regional cerebral perfusion and atrophy in mild cognitive impairment (MCI) and early Alzheimers dementia. Psychiatry Res 2010; 183: 44-51.
11. Lacalle-Aurioles M, Mateos-Perez JM, Guzman-De-Villoria JA, et al. Cerebral blood flow is an earlier indicator of perfusion abnormalities than cerebral blood volume in Alzheimers disease. J Cereb Blood Flow Metab 2014; 34: 654-659.
12. Visser PJ, Scheltens P, Verhey FR, et al. Medial temporal lobe atrophy and memory dysfunction as predictors for dementia in subjects with mild cognitive impairment. J Neurol 1999; 246: 477-485.
13. Alsop DC, Casement M, de Bazelaire C, et al. Hippocampal hyperperfusion in Alzheimers disease. Neuroimage 2008; 42: 1267-1274.
14. Calamante F, Thomas DL, Pell GS, et al. Measuring cerebral blood flow using magnetic resonance imaging techniques. J Cereb Blood Flow Metab 1999; 19: 701-735.
15. Essig M, Shiroishi MS, Nguyen TB, et al. Perfusion MRI: The five most frequently asked technical questions. AJR Am J Roentgenol 2013; 200: 24-34.
16. 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.
17. Reiman EM, Chen K, Liu X, et al. Fibrillar amyloid-beta burden in cognitively normal people at 3 levels of genetic risk for Alzheimers disease. Proc Natl Acad Sci USA 2009; 106: 6820-6825.
18. Wirth M, Madison CM, Rabinovici GD, et al. Alzheimers disease neurodegenerative biomarkers are associated with decreased cognitive function but not beta-Amyloid in cognitively normal older individuals. J Neurosci 2013; 33: 5553-5563.
19. Petersen RC and Negash S. Mild cognitive impairment: An overview. CNS Spectr 2008; 13: 45-53.
20. Petersen RC, Smith GE, Waring SC, et al. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 1999; 56: 303-308.
21. 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: 1159-1165.
22. Folstein M, Folstein S and McHugh P. Mini-mental state: A practical method for grading the cognitive state of patients for the clinicians. J Psychiatr Res 1975; 12: 189-198.
23. McKhann G, Drachman D, Folstein M, et al. Clinical diagnosis of Alzheimers disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimers Disease. Neurology 1984; 34: 939-944.
24. McKhann GM, Knopman DS, Chertkow H, et al. The diagnosis of dementia due to Alzheimers disease: recommendations from the National Institute on Aging-Alzheimers Association workgroups on diagnostic guidelines for Alzheimers disease. Alzheimers Dement 2011; 7: 263-269.
25. Kerti L, Witte AV, Winkler A, et al. Higher glucose levels associated with lower memory and reduced hippocampal microstructure. Neurology 2013; 81: 1746-1752.
26. Beck AT and Beamesderfer A. Assessment of depression: The depression inventory. Mod Prob Pharmacopsychiatr 1974; 7: 151-169.
27. Morris JC, Roe CM, Xiong C, et al. APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Ann Neurol 2010; 67: 122-131.
28. Corder EH, Saunders AM, Risch NJ, et al. Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat Genet 1994; 7: 180-184.
29. Helmstaedter C, Lendt M and Lux S. Verbaler Lern-und Merkfähigkeitstest. Hogrefe: Goettingen, 2001.
30. DAgostino RB Sr, Vasan RS, Pencina MJ, et al. General cardiovascular risk profile for use in primary care: The Framingham Heart Study. Circulation 2008; 117: 743-753.
31. ODwyer L, Lamberton F, Matura S, et al. Reduced hippocampal volume in healthy young ApoE4 carriers: An MRI study. PLoS One 2012; 7: e48895.
32. Dale AM, Fischl B and Sereno MI. Cortical surfacebased analysis. I. Segmentation and surface reconstruction. Neuroimage 1999; 9: 179-194.
33. Ostergaard L, Weisskoff RM, Chesler DA, et al. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn Reson Med: Off J Soc Magn Reson Med/Soc Magn Reson Med 1996; 36: 715-725.
34. 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: 968-980.
35. Pickut BA, Dierckx RA, Dobbeleir A, et al. Validation of the cerebellum as a reference region for SPECT quantification in patients suffering from dementia of the Alzheimer type. Psychiatry Res 1999; 90: 103-112.
36. Bozzao A, Floris R, Baviera ME, et al. Diffusion and perfusion MR imaging in cases of Alzheimers disease: correlations with cortical atrophy and lesion load. AJNR Am J Neuroradiol 2001; 22: 1030-1036.
37. Winkler AM, Kochunov P, Blangero J, et al. Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 2010; 53: 1135-1146.
38. Van Petten C. Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-Analysis. Neuropsychologia 2004; 42: 1394-1413.
39. Smith EE, Salat DH, Jeng J, et al. Correlations between MRI white matter lesion location and executive function and episodic memory. Neurology 2011; 76: 1492-1499.
40. Wirth M, Haase CM, Villeneuve S, et al. Neuroprotective pathways: lifestyle activity, brain pathology, and cognition in cognitively normal older adults. Neurobiol Aging 2014; 35: 1873-1882.
41. Olsson E, Klasson N, Berge J, et al. White matter lesion assessment in patients with cognitive impairment and healthy controls: Reliability comparisons between visual rating, a manual, and an automatic volumetrical MRI method-The Gothenburg MCI study. J Aging Res 2013; 2013: 198471.
42. Benjamini Y and Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Stat Soc Series B (Method) 1995; 57: 289-300.
43. Johnson NA, Jahng GH, Weiner MW, et al. Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: initial experience. Radiology 2005; 234: 851-859.
44. Dai W, Lopez OL, Carmichael OT, et al. Mild cognitive impairment and alzheimer disease: patterns of altered cerebral blood flow at MR imaging. Radiology 2009; 250: 856-866.
45. 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: 69-77.
46. 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: 1977-1985.
47. Chetelat G, Desgranges B, Landeau B, et al. Direct voxelbased comparison between grey matter hypometabolism and atrophy in Alzheimers disease. Brain 2008; 131(Pt 1): 60-71.
48. Mazza M, Marano G, Traversi G, et al. Primary cerebral blood flow deficiency and Alzheimers disease: shadows and lights. J Alzheimers Dis: JAD 2011; 23: 375-389.
49. Khan UA, Liu L, Provenzano FA, et al. Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimers disease. Nat Neurosci 2014; 17: 304-311.
50. Whitwell JL, Josephs KA, Murray ME, et al. MRI correlates of neurofibrillary tangle pathology at autopsy: A voxel-based morphometry study. Neurology 2008; 71: 743-749.
51. Luckhaus C, Flub MO, Wittsack HJ, et al. Detection of changed regional cerebral blood flow in mild cognitive impairment and early Alzheimers dementia by perfusion-weighted magnetic resonance imaging. Neuroimage 2008; 40: 495-503.
52. Altmann A, Ng B, Landau SM, et al. Regional brain hypometabolism is unrelated to regional amyloid plaque burden. Brain 2015; 138 (Pt 12): 3734-3746.
53. Binnewijzend MA, Benedictus MR, Kuijer JP, et al. Cerebral perfusion in the predementia stages of Alzheimers disease. Eur Radiol 2015.
54. Michels L, Warnock G, Buck A, et al. Arterial spin labeling imaging reveals widespread and Abeta-independent reductions in cerebral blood flow in elderly apolipoprotein epsilon-4 carriers. J Cereb Blood Flow Metab 2015.
55. Villemagne VL, Furumoto S, Fodero-Tavoletti MT, et al. In vivo evaluation of a novel tau imaging tracer for Alzheimers disease. Eur J Nucl Med Mol Imaging 2014; 41: 816-826.
56. Small SA and Duff K. Linking A beta and Tau in lateonset Alzheimers Disease: A dual pathway hypothesis. Neuron 2008; 60: 534-542.
57. Villain N, Desgranges B, Viader F, et al. Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimers disease. J Neurosci 2008; 28: 6174-6181.
58. Villeneuve S, Wirth M and La Joie R. Are AD-Typical regions the convergence point of multiple pathologies? Front Aging Neurosci 2015; 7: 42: 1-4.
59. La Joie R, Perrotin A, Barre L, et al. Region-specific hierarchy between atrophy, hypometabolism, and betaamyloid (Abeta) load in Alzheimers disease dementia. J Neurosci 2012; 32: 16265-16273.
60. Varallyay CG, Nesbit E, Fu R, et al. High-resolution steady-state cerebral blood volume maps in patients with central nervous system neoplasms using ferumoxytol, a superparamagnetic iron oxide nanoparticle. J Cereb Blood Flow Metab 2013; 33: 780-786.
61. Stonnington CM, Tan G, Kloppel S, et al. Interpreting scan data acquired from multiple scanners: A study with Alzheimers disease. Neuroimage 2008; 39: 1180-1185.
62. Jovicich J, Czanner S, Han X, et al. MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. Neuroimage 2009; 46: 177-192.