Blood-brain barrier impairment in dementia: Current and future in vivo assessments

Neuroscience and Biobehavioral Reviews

Volumn 49, Issue , 2015, Pages 71-81

  van de Haar, Harm J ^a,b   Burgmans, Saartje ^a,b   Hofman, Paul A M ^a,b   Verhey, Frans R J ^a,b   Jansen, Jacobus F A ^a,b   Backes, Walter H ^a,b,c  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Alzheimer's disease; Blood brain barrier; Contrast enhanced; CT; DCE MRI; Dementia; PET; Vascular dementia

Indexed keywords

ALBUMIN; AMYLOID BETA PROTEIN; WATER;

ALBUMIN BLOOD LEVEL; ALZHEIMER DISEASE; AUTOPSY; BLOOD BRAIN BARRIER; BLOOD BRAIN BARRIER IMPAIRMENT; BRAIN METABOLISM; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROSPINAL FLUID; CEREBROVASCULAR DISEASE; COGNITIVE DEFECT; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; DEMENTIA; FLUID BALANCE; HUMAN; IN VIVO STUDY; MULTIINFARCT DEMENTIA; NERVOUS SYSTEM PARAMETERS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERMEABILITY BARRIER; POSITRON EMISSION TOMOGRAPHY; REVIEW; WHITE MATTER; WHITE MATTER HYPERINTENSITY; ANIMAL; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; BLOOD-BRAIN BARRIER; DEMENTIA; HUMANS;

EID: 84921312706     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2014.11.022     Document Type: Review

References (97)

1. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53. DOI: 10.1038/nrn1824.
2. Abraham M.H. The factors that influence permeation across the blood-brain barrier. Eur. J. Med. Chem. 2004, 39:235-240. DOI: 10.1016/j.ejmech.2003.12.004.
3. Agdeppa E.D., Spilker M.E. A review of imaging agent development. AAPS J. 2009, 11:286-299. DOI: 10.1208/s12248-009-9104-5.
4. Agyare E., Leonard S., Curran G. Traffic jam at the blood-brain barrier promotes greater accumulation of Alzheimer's disease Amyloid-β proteins in the cerebral vasculature. Mol. Pharm. 2013, 10:1557-1565.
5. Alafuzoff I., Adolfsson R., Grundke-Iqbal I., Winblad B. Blood-brain barrier in Alzheimer dementia and in non-demented elderly. Acta Neuropathol. 1987, 73:160-166.
6. Algotsson A., Winblad B. The integrity of the blood-brain barrier in Alzheimer's disease. Acta Neurol. Scand. 2007, 115:403-408. DOI: 10.1111/j.1600-0404.2007.00823.x.
7. Babikian V., Ropper a.H. Binswanger's disease: a review. Stroke 1987, 18:2-12. DOI: 10.1161/01.STR.18.1.2.
8. Bell R.D.R., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009, 118:103-113. DOI: 10.1007/s00401-009-0522-3.
9. Blennow K., Fredman P., Wallin A., Gottfries C.G., Karlsson I., Långström G., Skoog I., Svennerholm L., Wikkelsö C. Protein analysis in cerebrospinal fluid II. Reference values derived from healthy individuals 18-88 years of age. Eur. Neurol. 1993, 33:129-133.
10. Blennow K., Wallin A., Fredman P., Karlsson I., Gottfries C.G., Svennerholm L. Blood-brain barrier disturbance in patients with Alzheimer's disease is related to vascular factors. Acta Neurol. Scand. 1990, 81:323-326.
11. Blumenthal H.T. Immunological aspects of the aging brain. Neurobiology of aging 1976, 313-334. Raven Press, New York. R.D. Terry, S. Gersbon (Eds.).
12. Bowman G.L., Kaye J.a, Quinn J.F. Dyslipidemia and blood-brain barrier integrity in Alzheimer's disease. Curr. Gerontol. Geriatr. Res. 2012, 2012:184042. DOI: 10.1155/2012/184042.
13. Bowman G.L., Kaye J.A., Moore M., Waichunas D., Carlson N.E., Quinn J.F. Blood-brain barrier impairment in Alzheimer disease: stability and functional significance. Neurology 2007, 68:1809-1814. DOI: 10.1212/01.wnl.0000262031.18018.1a.
14. Bronge L., Wahlund L.-O.O. Contrast-enhanced MRI of White Matter Lesions in patients with blood-brain barrier dysfunction. Dement. Geriatr. Cognit. Disord. 2000, 11:477-481. DOI: 17248.
15. Burgmans S., van de Haar H.J., Verhey F.R.J., Backes W.H. Amyloid-β Interacts with blood-brain barrier function in dementia: a systematic review. J. Alzheimers Dis. 2013, 35:859-873. DOI: 10.3233/JAD-122155.
16. Caserta M.T., Caccioppo D., Lapin G.D., Ragin A., Groothuis D.R., Caserta M.T., Caccioppo D., Lapin G.D. Blood-brain barrier integrity in Alzheimer's disease patients and elderly control subjects. J. Neuropsychiatry Clin. Neurosci. 1998, 10:78-84.
17. Choi S.R., Schneider J.A., Bennett D.A., Beach T.G., Bedell B.J., Zehntner S.P., Krautkramer M.J., Kung H.F., Skovronsky D.M., Hefti F., Clark C.M. Correlation of amyloid PET ligand florbetapir F 18 binding with Aβ aggregation and neuritic plaque deposition in postmortem brain tissue. Alzheimer Dis. Assoc. Disord. 2013, 26:8-16. DOI: 10.1097/WAD.0b013e31821300bc.
18. Claudio L. Ultrastructural features of the blood-brain barrier in biopsy tissue from Alzheimer's disease patients. Acta Neuropathol. 1996, 91:6-14.
19. De Backer M.E., Nabuurs R.J.a, van Buchem M.A., van der Weerd L. MR-based molecular imaging of the brain: the next frontier. AJNR Am. J. Neuroradiol. 2010, 31:1577-1583. DOI: 10.3174/ajnr.A2264.
20. 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. DOI: 10.1016/S1474-4422(04)00683-0.
21. Deane R., Bell R., Sagare A., Zlokovic B. Clearance of Amyloid-β peptide across the blood-brain barrier: implication for therapies in Alzheimers disease. CNS Neurol. Disord.-Drug Targets 2009, 8:16-30. DOI: 10.2174/187152709787601867.
22. Deane R., Wu Z., Zlokovic B.V. RAGE (Yin) versus LRP (Yang) balance regulates Alzheimer amyloid β-peptide clearance through transport across the blood-brain barrier. Stroke 2004, 35:2628-2631.
23. Deschaintre Y., Richard F., Leys D., Pasquier F. Treatment of vascular risk factors is associated with slower decline in Alzheimer disease. Neurology 2009, 73:674-680. DOI: 10.1212/WNL.0b013e3181b59bf3.
24. Didziapetris R., Japertas P. Classification analysis of P-glycoprotein substrate specificity. J. Drug Target. 2003, 11:391-406.
25. Duan J.-H., Wang H.-Q., Xu J., Lin X., Chen S.-Q., Kang Z., Yao Z.-B. White matter damage of patients with Alzheimer's disease correlated with the decreased cognitive function. Surg. Radiol. Anat. 2006, 28:150-156. DOI: 10.1007/s00276-006-0111-2.
26. Dyrna F., Hanske S., Krueger M., Bechmann I. The blood-brain barrier. J. Neuroimmune Pharmacol. 2013, 1-11. DOI: 10.1007/s11481-013-9473-5.
27. Dysken M.W., Nelson M.J., Hoover K.M., Kuskowski M., McGeachie R. Rapid dynamic CT scanning in primary degenerative dementia and age-matched controls. Biol. Psychiatry 1990, 28:425-434.
28. Echávarri C., Burgmans S., Caballero M.C., García-Bragado F., Verhey F.R.J., Uylings H.B.M. Co-occurrence of different pathologies in dementia: implications for dementia diagnosis. J. Alzheimers Dis. 2012, 30:1-9. DOI: 10.3233/JAD-2012-111400.
29. Elovaara I., Icén A., Palo J., Erkinjuntti T., Icen A. CSF in Alzheimer's disease. Studies on blood-brain barrier function and intrathecal protein synthesis. J. Neurol. Sci. 1985, 70:73-80.
30. Elovaara I., Palo J., Erkinjuntti T., Sulkava R. Serum and cerebrospinal fluid proteins and the blood-brain barrier in Alzheimer's disease and multi-infarct dementia. Eur. Neurol. 1987, 26:229-234.
31. Erickson M.a., Banks W.a. Blood-brain barrier dysfunction as a cause and consequence of Alzheimer's disease. J. Cereb. Blood Flow Metab. 2013, 33:1500-1513. DOI: 10.1038/jcbfm.2013.135.
32. Farrall A.J., Wardlaw J.M. Blood-brain barrier: ageing and microvascular disease-systematic review and meta-analysis. Neurobiol. Aging 2009, 30:337-352. DOI: 10.1016/j.neurobiolaging.2007.07.015.
33. Fiala M., Liu Q.N., Sayre J., Pop V., Brahmandam V., Graves M.C., Vinters H.V. Cyclooxygenase-2-positive macrophages infiltrate the Alzheimer's disease brain and damage the blood-brain barrier. Eur. J. Clin. Invest. 2002, 32:360-371. DOI: 10.1046/j.1365-2362.2002.00994.x.
34. Frölich L., Kornhuber J., Ihl R., Fritze J., Maurer K., Riederer P., Frolich L. Integrity of the blood-CSF barrier in dementia of Alzheimer type: CSF/serum ratios of albumin and IgG. Eur. Arch. Psychiatry Clin. Neurosci. 1991, 240:363-366.
35. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.a, Raju S., Prada C., Greenberg S.M., Bacskai B.J., Frosch M.P. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol. Dis. 2006, 24:516-524. DOI: 10.1016/j.nbd.2006.08.017.
36. Giulian D., Haverkamp L., Li J., Karshin W. Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer brain. Neurochem. Int. 1995, 27:119-137.
37. Götz J., Ittner L.M. Animal models of Alzheimer's disease and frontotemporal dementia. Nat. Rev. Neurosci. 2008, 9:532-544. DOI: 10.1038/nrn2420.
38. Günzel D., Yu A.S.L. Claudins and the modulation of tight junction permeability. Physiol. Rev. 2013, DOI: 10.1152/physrev.00019.2012.
39. Hales P.W., Clark C.a. Combined arterial spin labeling and diffusion-weighted imaging for noninvasive estimation of capillary volume fraction and permeability-surface product in the human brain. J. Cereb. Blood Flow Metab. 2013, 33:67-75. DOI: 10.1038/jcbfm.2012.125.
40. Hanyu H., Asano T., Tanaka Y., Iwamoto T., Takasaki M., Abe K. Increased blood-brain barrier permeability in white matter lesions of Binswanger's disease evaluated by contrast-enhanced MRI. Dement. Geriatr. Cognit. Disord. 2002, 14:1-6. DOI: 10.1159/000058326.
41. Hardy J. The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J. Neurochem. 2009, 110:1129-1134. DOI: 10.1111/j.1471-4159.2009.06181.x.
42. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356. DOI: 10.1126/science.1072994.
43. Harik S., Kalaria R.N. Blood-brain barrier abnormalities in Alzheimer's disease. Ann. N.Y. Acad. Sci. 1990, 640:47-52.
44. Hawkins R.a, Phelps M.E., Huang S.C., Wapenski J.a, Grimm P.D., Parker R.G., Juillard G., Greenberg P. A kinetic evaluation of blood-brain barrier permeability in human brain tumors with [68Ga]EDTA and positron computed tomography. J. Cereb. Blood Flow Metab. 1984, 4:507-515. DOI: 10.1038/jcbfm.1984.75.
45. Jack C.R., Knopman D.S., Jagust W.J., Shaw L.M., Aisen P.S., Weiner M.W., Petersen R.C., Trojanowski J.Q. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 2010, 9:119-128. DOI: 10.1016/S1474-4422(09)70299-6.
46. Jonker C., Eikelenboom P., Tavenier P. Immunological indices in the cerebrospinal fluid of patients with presenile dementia of the Alzheimer type. Br. J. Psychiatry 1982, 140:44-49.
47. Kalaria R.N. The blood-brain barrier and cerebrovascular pathology in Alzheimer's disease. Ann. N.Y. Acad. Sci. 1999, 893:113-125. DOI: 10.1111/j.1749-6632.1999.tb07821.x.
48. Kay A., May C., Papadopoulos N. CSF and serum concentrations of albumin and IgG in Alzheimer's disease. Neurobiol. Aging 1987, 8:21-25.
49. Kessler R.M., Goble J.C., Bird J.H., Girton M.E., Doppman J.L., Rapoport S.I., Barranger J.a Measurement of blood-brain barrier permeability with positron emission tomography and [68Ga]EDTA. J. Cereb. Blood Flow Metab. 1984, 4:323-328. DOI: 10.1038/jcbfm.1984.48.
50. Kimelberg H.K. Water homeostasis in the brain: basic concepts. Neuroscience 2004, 129:851-860. DOI: 10.1016/j.neuroscience.2004.07.033.
51. Klunk W.E., Engler H., Nordberg A., Wang Y., Blomqvist G., Holt D.P., Bergstro M., Savitcheva I., Debnath M.L., Barletta J., Price J.C., Sandell J., Lopresti B.J., Wall A., Koivisto P., Antoni G., Mathis C.A., Långstro B. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann. Neurol. 2004, 55:306-319.
52. Le Bihan D., Breton E., Lallemand D. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986, 161:401-407.
53. Leonardi A., Gandolfo C., Caponnetto C., Arata L., Vecchia R. The integrity of the blood-brain barrier in Alzheimer's type and multi-infarct dementia evaluated by the study of albumin and IgG in serum and cerebrospinal fluid. J. Neurol. Sci. 1985, 67:253-261.
54. Matsumoto Y., Yanase D., Noguchi-Shinohara M., Ono K., Yoshita M., Yamada M. Blood-brain barrier permeability correlates with medial temporal lobe atrophy but not with amyloid-beta protein transport across the blood-brain barrier in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 2007, 25:144-147. DOI: 10.1159/000112555.
55. Mattila K.M., Pirttilä T., Blennow K., Wallin A., Viitanen M., Frey H. Altered blood-brain-barrier function in Alzheimer's disease?. Acta Neurol. Scand. 1994, 89:192-198.
56. Mecocci P., Parnetti L., Reboldi G.P., Santucci C., Gaiti A., Ferri C., Gernini I., Romagnoli M., Cadini D., Senin U. Blood-brain-barrier in a geriatric population: barrier function in degenerative and vascular dementias. Acta Neurol. Scand. 1991, 84:210-213.
57. Minoshima S., Giordani B., Berent S., Frey K.a, Foster N.L., Kuhl D.E. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann. Neurol. 1997, 42:85-94. DOI: 10.1002/ana.410420114.
58. Munoz D.G., Erkinjuntti T., Gaytan-Garcia S., Hachinski V., GaytanGarcia S. Serum protein leakage in Alzheimer's disease revisited. Ann. N.Y. Acad. Sci. 1997, 826:173-189. DOI: 10.1111/j.1749-6632.1997.tb48469.x.
59. Nitta T., Hata M., Gotoh S., Seo Y., Sasaki H., Hashimoto N., Furuse M., Tsukita S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 2003, 161:653-660. DOI: 10.1083/jcb.200302070.
60. Pahnke J., Walker L.C., Scheffler K., Krohn M. Alzheimer's disease and blood-brain barrier function-Why have anti-beta-amyloid therapies failed to prevent dementia progression?. Neurosci. Biobehav. Rev. 2009, 33:1099-1108. DOI: 10.1016/j.neubiorev.2009.05.006.
61. Patlak C.S., Blasberg R.G., Fenstermacher J.D. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J. Cereb. Blood Flow Metab. 1983, 3:1-7. DOI: 10.1038/jcbfm.1983.1.
62. Pimplikar S.W. Reassessing the amyloid cascade hypothesis of Alzheimer's disease. Int. J. Biochem. Cell Biol. 2009, 41:1261-1268. DOI: 10.1016/j.biocel.2008.12.015.
63. Poduslo J.F., Curran G.L., Wengenack T.M., Malester B., Duff K. Permeability of proteins at the blood-brain barrier in the normal adult mouse and double transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 2001, 8:555-567. DOI: 10.1006/nbdi.2001.0402.
64. Romanitan M.O., Popescu B.O., Spulber S., Băjenaru O., Popescu L.M., Winblad B., Bogdanovic N. Altered expression of claudin family proteins in Alzheimer's disease and vascular dementia brains. J. Cell. Mol. Med. 2010, 14:1088-1100. DOI: 10.1111/j.1582-4934.2009.00999.x.
65. Rozemuller J.M., Eikelenboom P., Kamphorst W., Stam F.C. Lack of evidence for dysfunction of the blood-brain barrier in Alzheimer's disease: an immunohistochemical study. Neurobiol. Aging 1988, 9:383-391.
66. Ryu J.K., McLarnon J.G. A leaky blood-brain barrier, fibrinogen infiltration and microglial reactivity in inflamed Alzheimer's disease brain. J. Cell. Mol. Med. 2009, 13:2911-2925. DOI: 10.1111/j.1582-4934.2008.00434.x.
67. Schabel M.C., Parker D.L. Uncertainty and bias in contrast concentration measurements using spoiled gradient echo pulse sequences. Phys. Med. Biol. 2008, 53:2345-2373. DOI: 10.1088/0031-9155/53/9/010.
68. Schlageter N.L., Carson R.E., Rapoport S.I. Examination of blood-brain barrier permeability in dementia of the Alzheimer type with [68Ga]EDTA and positron emission tomography. J. Cereb. Blood Flow Metab. 1987, 7:1-8. DOI: 10.1038/jcbfm.1987.1.
69. Seelig A., Gottschlich R., Devant R.M. A method to determine the ability of drugs to diffuse through the blood-brain barrier. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:68-72.
70. Simons E.R., Marshall D.C., Long H.J., Otto K., Billingslea A., Tibbles H., Wells J., Eisenhauer P., Fine R.E., Cribbs D.H., Davies T.a, Abraham C.R. Blood brain barrier endothelial cells express candidate amyloid precursor protein-cleaving secretases. Amyloid 1998, 5:153-162.
71. Skoog I., Wallin A., Fredman P., Wallin A., Skoog I., Fredman P., Hesse C., Aevarsson O., Karlsson I., Gottfries C.G., Blennow K. A population study on blood-brain barrier function in 85-year-olds: relation to Alzheimer's disease and vascular dementia. Neurology 1998, 50:966-971.
72. Small G.W., Kepe V., Ercoli L.M., Siddarth P., Bookheimer S.Y., Miller K.J., Lavretsky H., Burggren A.C., Cole G.M., Vinters H.V., Thompson P.M., Huang S.-C., Satyamurthy N., Phelps M.E., Barrio J.R. PET of brain amyloid and tau in mild cognitive impairment. N. Engl. J. Med. 2006, 355:2652-2663. DOI: 10.1056/NEJMoa054625.
73. Sourbron S.P., Buckley D.L. Classic models for dynamic contrast-enhanced MRI. NMR Biomed. 2013, 26:1004-1027. DOI: 10.1002/nbm.2940.
74. Spulber S., Bogdanovic N., Romanitan M.O., Bajenaru O.a, Popescu B.O. Claudin expression profile separates Alzheimer's disease cases from normal aging and from vascular dementia cases. J. Neurol. Sci. 2012, 322:184-186. DOI: 10.1016/j.jns.2012.05.031.
75. Starr J.M., Farrall A.J., Armitage P.a, McGurn B., Wardlaw J.M. Blood-brain barrier permeability in Alzheimer's disease: a case-control MRI study. Psychiatry Res. 2009, 171:232-241. DOI: 10.1016/j.pscychresns.2008.04.003.
76. Stewart P.A., Hayakawa K., Akers M.A., Vinters H.V. A morphometric study of the blood-brain barrier in Alzheimer's disease. Lab. Invest. 1992, 67:734-742.
77. Tabert M.H., Manly J.J., Liu X., Pelton G.H., Rosenblum S., Jacobs M., Zamora D., Goodkind M., Bell K., Stern Y., Devanand D.P. Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Arch. Gen. Psychiatry 2006, 63:916-924. DOI: 10.1001/archpsyc.63.8.916.
78. Taheri S., Gasparovic C., Huisa B.N., Adair J.C., Edmonds E., Prestopnik J., Grossetete M., Shah N.J., Wills J., Qualls C., Rosenberg G.A. Blood-brain barrier permeability abnormalities in vascular cognitive impairment. Stroke 2011, 42:2158-2563. DOI: 10.1161/STROKEAHA.110.611731.
79. Taheri S., Gasparovic C., Shah N.J., Rosenberg G.a Quantitative measurement of blood-brain barrier permeability in human using dynamic contrast-enhanced MRI with fast T1 mapping. Magn. Reson. Med. 2011, 65:1036-1042. DOI: 10.1002/mrm.22686.
80. Thomsen H.S., Morcos S.K., Almén T., Bellin M.-F., Bertolotto M., Bongartz G., Clement O., Leander P., Heinz-Peer G., Reimer P., Stacul F., van der Molen A., Webb J.aW. Nephrogenic systemic fibrosis and gadolinium-based contrast media: updated ESUR contrast medium safety committee guidelines. Eur. Radiol. 2013, 23:307-318. DOI: 10.1007/s00330-012-2597-9.
81. Tibbling G., Link H., Öhman S. Principles of albumin and IgG analyses in neurological disorders I. Establishment of reference values. Scand. J. Clin. Lab. Investig. 1977, 37:385-390.
82. Tofts P.S., Brix G., Buckley D.L., Evelhoch J.L., Henderson E., Knopp M.V., Larsson H.B.W., Lee T., Mayr N.A., Parker G.J.M., Port R.E., Taylor J., Weisskoff R.M. Contrast-enhanced T1-weighted MRI of a diffusable tracer: standardized quantities and symbols. J. Magn. Reson. Imaging 1999, 10:223-232. DOI: 10.1002/(SICI)1522-2586(199909)10:3<223::AID-JMRI2>3.0.CO;2-S.
83. Tomimoto H., Akiguchi I., Suenaga T., Nishimura M., Wakita H., Nakamura S., Kimura J., Akiguchi H., Suenaga I.T. Alterations of the blood-brain barrier and glial cells in white-matter lesions in cerebrovascular and Alzheimer's disease patients. Stroke 1996, 27:2069-2074.
84. Ujiie M., Dickstein D.L., Carlow D.A., Jefferies W.A. Blood-brain barrier permeability precedes senile plaque formation in an Alzheimer disease model. Microcirculation 2003, 10:463-470. DOI: 10.1038/sj.mn.7800212.
85. Umutlu L., Kraff O., Orzada S. Dynamic contrast-enhanced renal MRI at 7 Tesla: preliminary results. Invest. Radiol. 2011, 46:425-433.
86. Umutlu L., Maderwald S., Kraff O., Theysohn J.M., Kuemmel S., Hauth E.a, Forsting M., Antoch G., Ladd M.E., Quick H.H., Lauenstein T.C. Dynamic contrast-enhanced breast MRI at 7 Tesla utilizing a single-loop coil: a feasibility trial. Acad. Radiol. 2010, 17:1050-1056. DOI: 10.1016/j.acra.2010.03.017.
87. Van Assema D.M.E., Goos J.D.C., van der Flier W.M., Lubberink M., Boellaard R., Windhorst A.D., Scheltens P., Lammertsma A.A., van Berckel B.N.M. No evidence for additional blood-brain barrier P-glycoprotein dysfunction in Alzheimer's disease patients with microbleeds. J. Cereb. Blood Flow Metab. 2012, 32:1468-1471. DOI: jcbfm201264 [pii] 10.1038/jcbfm.2012.64.
88. Van Assema D.M.E., Lubberink M., Bauer M., van der Flier W.M., Schuit R.C., Windhorst A.D., Comans E.F.I., Hoetjes N.J., Tolboom N., Langer O., Müller M., Scheltens P., Lammertsma A.A., van Berckel B.N.M., Muller M. Blood-brain barrier P-glycoprotein function in Alzheimer's disease. Brain 2012, 135:181-189. DOI: 10.1093/brain/awr298.
89. 18F-flutemetamol amyloid imaging in Alzheimer disease and mild cognitive impairment: a phase 2 trial. Ann. Neurol. 2010, 68:319-329. DOI: 10.1002/ana.22068.
90. Wada H. Blood-brain barrier permeability of the demented elderly as studied by cerebrospinal fluid-serum albumin ratio. Intern. Med. 1998, 37:509-513. DOI: 10.2169/internalmedicine.37.509.
91. Wallin A., Blennow K., Fredman P., Gottfries C.G., Karlsson I., Svenner-holm L., Svennerholm L. Blood brain barrier function in vascular dementia. Acta Neurol. Scand. 1990, 81:318-322. DOI: 10.1111/j.1600-0404.1990.tb01562.x.
92. Wang H., Golob E.J., Su M.-Y. Vascular volume and blood-brain barrier permeability measured by dynamic contrast enhanced MRI in hippocampus and cerebellum of patients with MCI and normal controls. J. Magn. Reson. Imaging 2006, 24:695-700. DOI: 10.1002/jmri.20669.
93. Wardlaw J.M. Blood-brain barrier and cerebral small vessel disease. J. Neurol. Sci. 2010, 299:66-71. DOI: 10.1016/j.jns.2010.08.042.
94. Wisniewski H.M., Kozlowski P.B. Evidence for blood-brain barrier changes in senile dementia of the Alzheimer type (SDAT). Ann. N.Y. Acad. Sci. 1982, 396:119-129.
95. Wunder A., Schoknecht K., Stanimirovic D.B., Prager O., Chassidim Y. Imaging blood-brain barrier dysfunction in animal disease models. Epilepsia 2012, 53(Suppl. 6):14-21. DOI: 10.1111/j.1528-1167.2012.03698.x.
96. Zipser B.D., Johanson C.E., Gonzalez L., Berzin T.M., Tavares R., Hulette C.M., Vitek M.P., Hovanesian V., Stopa E.G. Microvascular injury and blood-brain barrier leakage in Alzheimer's disease. Neurobiol. Aging 2007, 28:977-986.
97. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201. DOI: 10.1016/j.neuron.2008.01.003.