Psychiatry Research: Neuroimaging
Volume 171, Issue 3 , Pages 232-241 , 31 March 2009

Blood–brain barrier permeability in Alzheimer's disease: a case–control MRI study

  • John M. Starr

      Affiliations

    • Geriatric Medicine Unit, University of Edinburgh, Scotland, UK
    • Corresponding Author InformationCorresponding author. Royal Victoria Hospital, Craigleith Road, Edinburgh, Scotland, EH4 2DN, UK. Tel.: +44 131 537 5023; fax: +44 131 537 5140.
  • ,
  • Andrew J. Farrall

      Affiliations

    • Division of Clinical Neurosciences, of Edinburgh, Scotland, UK
  • ,
  • Paul Armitage

      Affiliations

    • Division of Clinical Neurosciences, of Edinburgh, Scotland, UK
  • ,
  • Brian McGurn

      Affiliations

    • Geriatric Medicine Unit, University of Edinburgh, Scotland, UK
  • ,
  • Joanna Wardlaw

      Affiliations

    • Division of Clinical Neurosciences, of Edinburgh, Scotland, UK

Received 10 November 2006 ,Revised 17 March 2008 ,Accepted 29 April 2008.

References 

  1. Armitage P, Behrenbruch C, Brady M, Moore N. Extracting and visualizing physiological parameters using dynamic contrast-enhanced magnetic resonance imaging of the breast. Medical Image Analysis. 2005;9:315–329
  2. Bickel U. How to measure drug transport across the blood–brain barrier. Neurotherapeutics. 2005;2:15–26
  3. Blennow K, Wallin A, Chong JK. Cerebrospinal fluid ‘neuronal thread protein’ comes from serum by passage over the blood–brain barrier. Neurodegeneration. 1995;4:187–193
  4. Buckley DL. Uncertainty in the analysis of tracer kinetics using dynamic contrast-enhanced T1-weighted MRI. Magnetic Resonance in Medicine. 2002;47:601–606
  5. Caserta MT, Caccioppo D, Lapin GD, Ragin A, Groothuis DR. Blood–brain barrier integrity in Alzheimer's disease patients and elderly control subjects. Journal of Neuropsychiatry & Clinical Neurosciences. 1998;10:78–84
  6. Claudio L. Ultrastructural features of the blood–brain barrier in biopsy tissue from Alzheimer's disease patients. Acta Neuropathologica. 1996;91:6–14
  7. Deane R, Yan SD, Submamaryan RK, et al. RAGE mediates amyloid-β peptide transport across the blood–brain barrier and accumulation in brain. Nature Medicine. 2003;9:907–913
  8. Deane R, Wu Z, Sagare A, et al. LRP/amyloid β-peptide interaction mediates differential brain efflux of Aβ isoforms. Neuron. 2004;43:333–344
  9. Dimicoli J-L, Patry J, Poupon J, Volk A. On the use of R1 and R2 for measurement of contrast agent concentration in isolated perfused rat liver. NMR in Biomedicine. 2003;16:276–285
  10. Donahue KM, Burstein D, Manning WJ, Gray ML. Studies of Gd-DTPA relaxivity and proton exchange rates in tissue. Magnetic Resonance in Medicine. 1994;32:66–76
  11. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5T in Alzheimer's disease and normal aging. American Journal of Neuroradiology. 1987;8:421–426
  12. Fiala M, Liu QN, Sayre J, Pop V, Brahmandam V, Graves MC, et al. Cyclooxygenase-2-positive macrophages infiltrate the Alzheimer's disease brain and damage the blood–brain barrier. European Journal of Clinical Investigation. 2002;32:360–371
  13. Hampel H, Kotter HU, Moller HJ. Blood–cerebrospinal fluid barrier dysfunction for high molecular weight proteins in Alzheimer disease and major depression: Indication for disease subsets. Alzheimer Disease & Associated Disorders. 1997;11:78–87
  14. 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. Dementia & Geriatric Cognitive Disorders. 2002;14:1–6
  15. Harik SI, Kalaria RN. Blood–brain barrier abnormalities in Alzheimer's disease. Annals of the New York Academy of Sciences. 1991;640:47–52
  16. Ibrahim MA, Emerson JF, Cotman CW. Magnetic resonance imaging relaxation times and gadolinium-DTPA relaxivity values in human cerebrospinal fluid. Investigative Radiology. 1998;33:153–162
  17. Jenkinson M, Smith S. A global optimization method for robust affine registration of brain images. Medical Image Analysis. 2001;5:143–156
  18. MacLullich AMJ, Ferguson KJ, Deary IJ, Seckl JR, Starr JM, Wardlaw JM. Intracranial capacity and brain volumes are associated with cognition in healthy elderly men. Neurology. 2002;59:169–174
  19. Mattila KM, Pirttila T, Blennow K, Wallin A, Viitanen M, Frey H. Altered blood–brain-barrier function in Alzheimer's disease?. Acta Neurologica Scandinavica. 1994;89:192–198
  20. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA work group. Neurology. 1984;34:939–944
  21. Morkenborg J, Pedersen M, Jensen FT, Stodkilde-Jorgensen H, Djurhuus JC, Frokiaer J. Quantitative assessment of Gd-DTPA contrast agent from signal enhancement: an in-vitro study. Magnetic Resonance Imaging. 2003;21:637–643
  22. Munoz DG, Erkinjuntti T, Gaytan-Garcia S, Hachinski V. Serum protein leakage in Alzheimer's disease revisited. Annals of the New York Academy of Sciences. 1997;826:173–189
  23. The Neuropathology Group MRC CFAS. Pathological correlates of late-onset dementia in a multicentre, community-based population in England and Wales. Lancet. 2001;357:169–175
  24. Ott A, Stolk RP, Van Harskamp F, Pols HAP, Hofman A, Breteler MMB. Diabetes mellitus and the risk of dementia — the Rotterdam Study. Neurology. 1999;53:1937–1942
  25. Pickup S, Wood AKW, Kundel HL. Gadodiamide T1 relaxivity in brain tissue in vivo is lower than in saline. Magnetic Resonance in Medicine. 2005;53:35–40
  26. Poduslo JF, Curran GL, Wengenack TM, 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. Neurobiology of Disease. 2001;8:555–567
  27. Preston SD, Steart PV, Wilkinson A, Nicoll JAR, Weller RO. Capillary and arterial cerebral amyloid angiopathy in Alzheimer's disease: Defining the perivascular route for the elimination of amyloid beta from the human brain. Neuropathology & Applied Neurobiology. 2003;29:106–117
  28. Shuter B, Tofts PS, Wang SC, Pope JM. The relaxivity of Gd-EOB-DTPA and Gd-DTPA in liver and kidney of the Wistar rat. Magnetic Resonance Imaging. 1996;14:243–253
  29. Skoog I, Wallin A, Fredman P, Hesse C, Aevarsson O, Karlsson I, et al. 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
  30. Snowden DA. Healthy aging and dementia: findings from the Nun study. Annals of Internal Medicine. 2003;139:450–454
  31. Starr JM, Ferguson K, Wardlaw JM, MacLullich A, Deary I, Marshall I. Increased blood brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. Journal of Neurology, Neurosurgery, and Psychiatry. 2003;74:70–76
  32. Stewart PA, Hayakawa K, Akers MA, Vinters HV. A morphometric study of the blood–brain barrier in Alzheimer's disease. Laboratory Investigation. 1992;67:734–742
  33. Su MY, Head E, Brooks WM, Wang Z, Muggenburg BA, Adam GE, et al. Magnetic resonance imaging of anatomic and vascular characteristics in a canine model of human aging. Neurobiology of Aging. 1998;19:479–485
  34. Tofts PS, Kermode AG. Measurement of the blood–brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magnetic Resonance in Medicine. 1991;17:357–367
  35. Tomimoto H, Akiguchi I, Suenaga T, Nishimura M, Wakita H, Nakamura S, et al. 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
  36. Ujiie M, Dickstein DL, Carlow DA, Jefferies WA. Blood–brain barrier permeability precedes senile plaque formation in an Alzheimer disease model. Microcirculation. 2003;10:463–470
  37. Wada H. Blood–brain barrier permeability of the demented elderly as studied by cerebrospinal fluid–serum albumin ratio. Internal Medicine. 1998;37:509–513
  38. Wahlund LO, Bronge L. Contrast-enhanced MRI of white matter lesions in patients with blood–brain barrier dysfunction. Annals of the New York Academy of Sciences. 2000;903:477–481
  39. Wardlaw JM, Sandercock PAG, Dennis MS, Starr JM. Is breakdown of the blood–brain barrier responsible for lacunar stroke, leukoaraiosis and dementia?. Stroke. 2003;34:806–812
  40. Wardlaw JM, Ferguson KJ, Graham C. White matter hyperintensities and rating scales — observer reliability varies with lesion load. Journal of Neurology. 2004;251:584–590
  41. Wisniewski HM, Vorbrodt AW, Wegiel J. Amyloid angiopathy and blood–brain barrier changes in Alzheimer's disease. Annals of the New York Academy of Sciences. 1997;826:161–172
  42. Wu Z, Guo H, Chow N, et al. Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nature Medicine. 2005;11:959–965
  43. Zlokovic BV. Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends in Neuroscience. 2005;28:202–208

PII: S0925-4927(08)00073-5

doi: 10.1016/j.pscychresns.2008.04.003

Psychiatry Research: Neuroimaging
Volume 171, Issue 3 , Pages 232-241 , 31 March 2009