Impaired cerebral vasoreactivity to CO 2 in Alzheimer's disease using BOLD fMRI

NeuroImage

Volumn 58, Issue 2, 2011, Pages 579-587

  Cantin, S ^a,b,c   Villien, M ^a,b   Moreaud, O ^c   Tropres, I ^c   Keignart, S ^c   Chipon, E ^a,b,c   Le Bas, J F ^a,b,c   Warnking, J ^a,b   Krainik, A ^a,b,c  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIV GRENOBLE ALPES   (France)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

Alzheimer's disease; BOLD fMRI; Carbon dioxide; Cerebral vasoreactivity; Mild cognitive impairment

Indexed keywords

ANGIOTENSIN 2 RECEPTOR ANTAGONIST; APOLIPOPROTEIN E4; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CARBOGEN; CARBON DIOXIDE; FIBRIC ACID DERIVATIVE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; THIAZIDE DIURETIC AGENT;

ADULT; AGE; AGED; ALZHEIMER DISEASE; AMNESIA; ANALYTIC METHOD; ARTICLE; BLOOD VESSEL REACTIVITY; BOLD SIGNAL; BRAIN ATROPHY; BRAIN PERFUSION; BRAIN SIZE; CEREBROVASCULAR DISEASE; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DYSLIPIDEMIA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENOTYPE; GRAY MATTER; HIPPOCAMPUS; HUMAN; HYPERTENSION; HYPERTRIGLYCERIDEMIA; IMAGE ANALYSIS; INHALATION; MALE; MENTAL PERFORMANCE; MICROANGIOPATHY; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; PATIENT MONITORING; PRIORITY JOURNAL; PULSED ARTERIAL SPIN LABELLING;

AGED; ALZHEIMER DISEASE; ATROPHY; CARBON DIOXIDE; CEREBROVASCULAR CIRCULATION; DATA INTERPRETATION, STATISTICAL; FEMALE; HEMODYNAMICS; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MILD COGNITIVE IMPAIRMENT; NEUROPSYCHOLOGICAL TESTS; OXYGEN; REGRESSION ANALYSIS; SPIN LABELS;

EID: 80051787707     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.06.070     Document Type: Article

References (56)

1. Alsop D.C., Detre J.A., Grossman M. Assessment of cerebral blood flow in Alzheimer's disease by spin-labeled magnetic resonance imaging. Ann. Neurol. 2000, 47:93-100.
2. Ashkanian M., Borghammer P., Gjedde A., Ostergaard L., Vafaee M. Improvement of brain tissue oxygenation by inhalation of carbogen. Neuroscience 2008, 156:932-938.
3. Ashkanian M., Gjedde A., Mouridsen K., Vafaee M., Hansen K.V., Ostergaard L., Andersen G. Carbogen inhalation increases oxygen transport to hypoperfused brain tissue in patients with occlusive carotid artery disease: increased oxygen transport to hypoperfused brain. Brain Res. 2009, 1304:90-95.
4. Bell R.D., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009, 118:103-113.
5. Benarroch E.E. Neurovascular unit dysfunction: a vascular component of Alzheimer disease?. Neurology 2007, 68:1730-1732.
6. Boche D., Zotova E., Weller R.O., Love S., Neal J.W., Pickering R.M., Wilkinson D., Holmes C., Nicoll J.A. Consequence of Abeta immunization on the vasculature of human Alzheimer's disease brain. Brain 2008, 131:3299-3310.
7. Brown G.G., Eyler Zorrilla L.T., Georgy B., Kindermann S.S., Wong E.C., Buxton R.B. BOLD and perfusion response to finger-thumb apposition after acetazolamide administration: differential relationship to global perfusion. J. Cereb. Blood Flow Metab. 2003, 23:829-837.
8. Buxton R.B., Uludag K., Dubowitz D.J., Liu T.T. Modeling the hemodynamic response to brain activation. Neuroimage 2004, 23(Suppl. 1):S220-S233.
9. Chao L.L., Buckley S.T., Kornak J., Schuff N., Madison C., Yaffe K., Miller B.L., Kramer J.H., Weiner M.W. ASL perfusion MRI predicts cognitive decline and conversion from MCI to dementia. Alzheimer Dis. Assoc. Disord. 2010, 24:19-27.
10. Claassen J.A., Jansen R.W. Cholinergically mediated augmentation of cerebral perfusion in Alzheimer's disease and related cognitive disorders: the cholinergic-vascular hypothesis. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61:267-271.
11. Cohen E.R., Ugurbil K., Kim S.G. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J. Cereb. Blood Flow Metab. 2002, 22:1042-1053.
12. Dai W., Lopez O.L., Carmichael O.T., Becker J.T., Kuller L.H., Gach H.M. Mild cognitive impairment and Alzheimer disease: patterns of altered cerebral blood flow at MR imaging. Radiology 2009, 250:856-866.
13. de la Torre J.C. Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol. 2004, 3:184-190.
14. de la Torre J.C. Alzheimer's disease is incurable but preventable. J. Alzheimers Dis. 2010, 20:861-870.
15. de la Torre J.C., Stefano G.B. Evidence that Alzheimer's disease is a microvascular disorder: the role of constitutive nitric oxide. Brain Res. Brain Res. Rev. 2000, 34:119-136.
16. Du A.T., Jahng G.H., Hayasaka S., Kramer J.H., Rosen H.J., Gorno-Tempini M.L., Rankin K.P., Miller B.L., Weiner M.W., Schuff N. Hypoperfusion in frontotemporal dementia and Alzheimer disease by arterial spin labeling MRI. Neurology 2006, 67:1215-1220.
17. Farkas E., De Jong G.I., de Vos R.A., Jansen Steur E.N., Luiten P.G. Pathological features of cerebral cortical capillaries are doubled in Alzheimer's disease and Parkinson's disease. Acta Neuropathol. 2000, 100:395-402.
18. Farkas E., Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol. 2001, 64:575-611.
19. Ferri C.P., Prince M., Brayne C., Brodaty H., Fratiglioni L., Ganguli M., Hall K., Hasegawa K., Hendrie H., Huang Y., Jorm A., Mathers C., Menezes P.R., Rimmer E., Scazufca M. Global prevalence of dementia: a Delphi consensus study. Lancet 2005, 366:2112-2117.
20. Fox A.J. How to measure carotid stenosis. Radiology 1993, 186:316-318.
21. 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.
22. Frontczak-Baniewicz M., Walski M. Ultrastructural features of the neurovascular unit in Alzheimer's neurodegeneration. J. Physiol. Pharmacol. 2006, 57(Suppl. 4):91-96.
23. Gauthier S., Reisberg B., Zaudig M., Petersen R.C., Ritchie K., Broich K., Belleville S., Brodaty H., Bennett D., Chertkow H., Cummings J.L., de Leon M., Feldman H., Ganguli M., Hampel H., Scheltens P., Tierney M.C., Whitehouse P., Winblad B. Mild cognitive impairment. Lancet 2006, 367:1262-1270.
24. Girouard H., Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J. Appl. Physiol. 2006, 100:328-335.
25. Haller S., Bonati L.H., Rick J., Klarhofer M., Speck O., Lyrer P.A., Bilecen D., Engelter S.T., Wetzel S.G. Reduced cerebrovascular reserve at CO2 BOLD MR imaging is associated with increased risk of periinterventional ischemic lesions during carotid endarterectomy or stent placement: preliminary results. Radiology 2008, 249:251-258.
26. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R.W., Bullock R., Love S., Neal J.W., Zotova E., Nicoll J.A. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 2008, 372:216-223.
27. Hornblow A.R., Kidson M.A. The visual analogue scale for anxiety: a validation study. Aust. N. Z. J. Psychiatry 1976, 10:339-341.
28. Hughes C.P., Berg L., Danziger W.L., Coben L.A., Martin R.L. A new clinical scale for the staging of dementia. Br. J. Psychiatry 1982, 140:566-572.
29. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
30. Iadecola C. The overlap between neurodegenerative and vascular factors in the pathogenesis of dementia. Acta Neuropathol. 2010, 120:287-296.
31. Inzitari D., Pracucci G., Poggesi A., Carlucci G., Barkhof F., Chabriat H., Erkinjuntti T., Fazekas F., Ferro J., Hennerici M., Langhorne P., O'Brien J., Schletens P., Visser M., Wahlund L., Waldemar G., Wallin A., Pantoni L., Group L.S. Changes in white matter as determinant of global functional decline in older independent outpatients: three year follow-up of LADIS (leukoaraiosis and disability) study cohort. BMJ 2009, 339:b2477.
32. Jiang Z., Krainik A., David O., Salon C., Tropres I., Hoffmann D., Pannetier N., Barbier E.L., Bombin E.R., Warnking J., Pasteris C., Chabardes S., Berger F., Grand S., Segebarth C., Gay E., Le Bas J.F. Impaired fMRI activation in patients with primary brain tumors. Neuroimage 2010, 52:538-548.
33. Johnson N.A., Jahng G.H., Weiner M.W., Miller B.L., Chui H.C., Jagust W.J., Gorno-Tempini M.L., Schuff N. 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.
34. Kato H., Shimosegawa E., Oku N., Kitagawa K., Kishima H., Saitoh Y., Kato A., Yoshimine T., Hatazawa J. MRI-based correction for partial-volume effect improves detectability of intractable epileptogenic foci on 123I-iomazenil brain SPECT images. J. Nucl. Med. 2008, 49:383-389.
35. Kogure D., Matsuda H., Ohnishi T., Asada T., Uno M., Kunihiro T., Nakano S., Takasaki M. Longitudinal evaluation of early Alzheimer's disease using brain perfusion SPECT. J. Nucl. Med. 2000, 41:1155-1162.
36. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453:869-878.
37. Luzzi S., Vella L., Bartolini M., Provinciali L., Silvestrini M. Atherosclerosis in the evolution of Alzheimer's disease: can treatment reduce cognitive decline?. J. Alzheimers Dis. 2010, 20:893-901.
38. Mandell D.M., Han J.S., Poublanc J., Crawley A.P., Stainsby J.A., Fisher J.A., Mikulis D.J. Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in Patients with arterial steno-occlusive disease: comparison with arterial spin labeling MRI. Stroke 2008, 39:2021-2028.
39. 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.
40. Meltzer C.C., Leal J.P., Mayberg H.S., Wagner H.N., Frost J.J. Correction of PET data for partial volume effects in human cerebral cortex by MR imaging. J. Comput. Assist. Tomogr. 1990, 14:561-570.
41. Mueggler T., Sturchler-Pierrat C., Baumann D., Rausch M., Staufenbiel M., Rudin M. Compromised hemodynamic response in amyloid precursor protein transgenic mice. J. Neurosci. 2002, 15:7218-7224.
42. Noth U., Meadows G.E., Kotajima F., Deichmann R., Corfield D.R., Turner R. Cerebral vascular response to hypercapnia: determination with perfusion MRI at 1.5 and 3.0Tesla using a pulsed arterial spin labeling technique. J. Magn. Reson. Imaging 2006, 24:1229-1235.
43. Oishi M., Mochizuki Y., Takasu T. Regional differences in cerebrovascular reactivity to acetazolamide in Alzheimer's disease. J. Clin. Neurosci. 1999, 6:380-381.
44. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
45. Petersen R.C. Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 2004, 256:183-194.
46. Princz-Kranz F.L., Mueggler T., Knobloch M., Nitsch R.M., Rudin M. Vascular response to acetazolamide decreases as a function of age in the arcA beta mouse model of cerebral amyloidosis. Neurobiol. Dis. 2010, 40:284-292.
47. Rombouts S.A., Goekoop R., Stam C.J., Barkhof F., Scheltens P. Delayed rather than decreased BOLD response as a marker for early Alzheimer's disease. Neuroimage 2005, 26:1078-1085.
48. Scheltens P., Leys D., Barkhof F., Huglo D., Weinstein H.C., Vermesch P., Kuiper M., Steinling M., Wolters E.C., Valk J. Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates. J. Neurol. Neurosurg. Psychiatry 1992, 55:967-972.
49. Shin H.K., Jones P.B., Garcia-Alloza M., Borrelli L., Greenberg S.M., Bacskai B.J., Frosch M.P., Hyman B.T., Moskowitz M.A., Ayata C. Age-dependent cerebrovascular dysfunction in a transgenic mouse model of cerebral amyloid angiopathy. Brain 2007, 130:2310-2319.
50. Silvestrini M., Pasqualetti P., Baruffaldi R., Bartolini M., Handouk Y., Matteis M., Moffa F., Provinciali L., Vernieri F. Cerebrovascular reactivity and cognitive decline in patients with Alzheimer disease. Stroke 2006, 37:1010-1015.
51. Thomason M.E., Glover G.H. Controlled inspiration depth reduces variance in breath-holding-induced BOLD signal. Neuroimage 2008, 39:206-214.
52. Tong X.K., Hamel E. Regional cholinergic denervation of cortical microvessels and nitric oxide synthase-containing neurons in Alzheimer's disease. Neuroscience 1999, 92:163-175.
53. van der Zande F.H., Hofman P.A., Backes W.H. Mapping hypercapnia-induced cerebrovascular reactivity using BOLD MRI. Neuroradiology 2005, 47:114-120.
54. Yezhuvath, U.S., Uh, J., Cheng, Y., Martin-Cook, K., Weiner, M., Diaz-Arrastia, R., van Osch, M., Lu, H., in press. Forebrain-dominant deficit in cerebrovascular reactivity in Alzheimer's disease. Neurobiol. Aging., electronic publication ahead of print. doi:10.1016/j.neurobiolaging.2010.02.005.
55. Ziyeh S., Rick J., Reinhard M., Hetzel A., Mader I., Speck O. Blood oxygen level-dependent MRI of cerebral CO2 reactivity in severe carotid stenosis and occlusion. Stroke 2005, 36:751-756.
56. Zlokovic B.V. Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci. 2005, 28:202-208.