MRI-Visible Perivascular Spaces in the Centrum Semiovale Are Associated with Brain Amyloid Deposition in Patients with Alzheimer Disease–Related Cognitive Impairment

References

1. 1.↵
   2. Doubal FN,
   3. MacLullich AM,
   4. Ferguson KJ, et al

   . Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke 2010;41:450–54 doi:10.1161/STROKEAHA.109.564914 pmid:20056930

   Abstract/FREE Full Text
2. 2.↵
   2. Brown R,
   3. Benveniste H,
   4. Black SE, et al

   . Understanding the role of the perivascular space in cerebral small vessel disease. Cardiovasc Res 2018;114:1462–73 doi:10.1093/cvr/cvy113 pmid:29726891

   CrossRefPubMed
3. 3.↵
   2. Zhu YC,
   3. Tzourio C,
   4. Soumare A, et al

   . Severity of dilated Virchow-Robin spaces is associated with age, blood pressure, and MRI markers of small vessel disease: a population-based study. Stroke 2010;41:2483–90 doi:10.1161/STROKEAHA.110.591586 pmid:20864661

   Abstract/FREE Full Text
4. 4.↵
   2. Weller RO,
   3. Hawkes CA,
   4. Kalaria RN, et al

   . White matter changes in dementia: role of impaired drainage of interstitial fluid. Brain Pathol 2015;25:63–78 doi:10.1111/bpa.12218 pmid:25521178

   CrossRefPubMed
5. 5.↵
   2. Wardlaw JM,
   3. Benveniste H,
   4. Nedergaard M, et al

   . Colleagues from the Fondation Leducq Transatlantic Network of Excellence on the Role of the Perivascular Space in Cerebral Small Vessel Disease. Perivascular spaces in the brain: anatomy, physiology and pathology. Nat Rev Neurol 2020;16:137–53 doi:10.1038/s41582-020-0312-z pmid:32094487

   CrossRefPubMed
6. 6.↵
   2. Park YW,
   3. Shin NY,
   4. Chung SJ, et al

   . Magnetic resonance imaging–visible perivascular spaces in basal ganglia predict cognitive decline in Parkinson’s disease. Mov Disord 2019;34:1672–79 doi:10.1002/mds.27798 pmid:31322758

   CrossRefPubMed
7. 7.↵
   2. Banerjee G,
   3. Kim HJ,
   4. Fox Z, et al

   . MRI–visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain 2017;140:1107–16 doi:10.1093/brain/awx003 pmid:28335021

   CrossRefPubMed
8. 8.↵
   2. Smeijer D,
   3. Ikram MK,
   4. Hilal S

   . Enlarged perivascular spaces and dementia: a systematic review. J Alzheimers Dis 2019;72:247–56 doi:10.3233/JAD-190527 pmid:31561362

   CrossRefPubMed
9. 9.↵
   2. Inglese M,
   3. Bomsztyk E,
   4. Gonen O, et al

   . Dilated perivascular spaces: hallmarks of mild traumatic brain injury. AJNR Am J Neuroradiol 2005;26:719–24 pmid:15814911

   Abstract/FREE Full Text
10. 10.↵
    2. Martinez-Ramirez S,
    3. Pontes-Neto OM,
    4. Dumas AP, et al

    . Topography of dilated perivascular spaces in subjects from a memory clinic cohort. Neurology 2013;80:1551–56 doi:10.1212/WNL.0b013e31828f1876 pmid:23553482

    CrossRefPubMed
11. 11.↵
    2. Charidimou A,
    3. Meegahage R,
    4. Fox Z, et al

    . Enlarged perivascular spaces as a marker of underlying arteriopathy in intracerebral haemorrhage: a multicentre MRI cohort study. J Neurol Neurosurg Psychiatry 2013;84:624–29 doi:10.1136/jnnp-2012-304434 pmid:23412074

    Abstract/FREE Full Text
12. 12.↵
    2. Charidimou A,
    3. Boulouis G,
    4. Pasi M, et al

    . MRI–visible perivascular spaces in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology 2017;88:1157–64 doi:10.1212/WNL.0000000000003746 pmid:28228568

    Abstract/FREE Full Text
13. 13.↵
    2. van Veluw SJ,
    3. Biessels GJ,
    4. Bouvy WH, et al

    . Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab 2016;36:576–80 doi:10.1177/0271678X15620434 pmid:26661250

    CrossRefPubMed
14. 14.↵
    2. Raposo N,
    3. Planton M,
    4. Payoux P, et al

    . Enlarged perivascular spaces and florbetapir uptake in patients with intracerebral hemorrhage. Eur J Nucl Med Mol Imaging 2019;46:2339–47 doi:10.1007/s00259-019-04441-1 pmid:31359110

    CrossRefPubMed
15. 15.↵
    2. Martinez-Ramirez S,
    3. van Rooden S,
    4. Charidimou A, et al

    . Perivascular spaces volume in sporadic and hereditary (Dutch-Type) cerebral amyloid angiopathy. Stroke 2018;49:1913–19 doi:10.1161/STROKEAHA.118.021137 pmid:30012821

    Abstract/FREE Full Text
16. 16.↵
    2. Roher AE,
    3. Kuo YM,
    4. Esh C, et al

    . Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer’s disease. Mol Med 2003;9:112–22 doi:10.1007/BF03402043 pmid:12865947

    CrossRefPubMedWeb of Science
17. 17.↵
    2. Charidimou A,
    3. Hong YT,
    4. Jager HR, et al

    . White matter perivascular spaces on magnetic resonance imaging: marker of cerebrovascular amyloid burden? Stroke 2015;46:1707–09 doi:10.1161/STROKEAHA.115.009090 pmid:25908461

    Abstract/FREE Full Text
18. 18.↵
    2. Rowe CC,
    3. Ackerman U,
    4. Browne W, et al

    . Imaging of amyloid beta in Alzheimer’s disease with 18F-BAY94-9172, a novel PET tracer: proof of mechanism. Lancet Neurol 2008;7:129–35 doi:10.1016/S1474-4422(08)70001-2 pmid:18191617

    CrossRefPubMedWeb of Science
19. 19.↵
    2. Hawkes CA,
    3. Jayakody N,
    4. Johnston DA, et al

    . Failure of perivascular drainage of beta-amyloid in cerebral amyloid angiopathy. Brain Pathol 2014;24:396–403 doi:10.1111/bpa.12159 pmid:24946077

    CrossRefPubMed
20. 20.↵
    2. Ramirez J,
    3. Berezuk C,
    4. McNeely AA, et al

    . Visible Virchow-Robin spaces on magnetic resonance imaging of Alzheimer’s disease patients and normal elderly from the Sunnybrook Dementia Study. J Alzheimers Dis 2014;43:415–24 doi:10.3233/JAD-132528 pmid:25096616

    CrossRefPubMed
21. 21.↵
    2. Marcus C,
    3. Mena E,
    4. Subramaniam RM

    . Brain PET in the diagnosis of Alzheimer’s disease. Clin Nucl Med 2014;39:e413–22; quiz e23–26 doi:10.1097/RLU.0000000000000547 pmid:25199063

    CrossRefPubMed
22. 22.↵
    2. Murphy MP,
    3. LeVine H 3rd.

    . Alzheimer’s disease and the amyloid-beta peptide. J Alzheimers Dis 2010;19:311–23 doi:10.3233/JAD-2010-1221 pmid:20061647

    CrossRefPubMedWeb of Science
23. 23.↵
    2. McKhann G,
    3. Drachman D,
    4. Folstein M, et al

    . 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;34:939–44 doi:10.1212/wnl.34.7.939 pmid:6610841

    Abstract/FREE Full Text
24. 24.↵
    2. Petersen RC,
    3. Smith GE,
    4. Waring SC, et al

    . Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 1999;56:303–08 doi:10.1001/archneur.56.3.303 pmid:10190820

    CrossRefPubMedWeb of Science
25. 25.↵
    2. Ahn HJ,
    3. Chin J,
    4. Park A, et al

    . Seoul Neuropsychological Screening Battery-dementia version (SNSB-D): a useful tool for assessing and monitoring cognitive impairments in dementia patients. J Korean Med Sci 2010;25:1071–76 doi:10.3346/jkms.2010.25.7.1071 pmid:20592901

    CrossRefPubMedWeb of Science
26. 26.↵
    2. Wardlaw JM,
    3. Smith EE,
    4. Biessels GJ, et al

    . STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1). Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013;12:822–38 doi:10.1016/S1474-4422(13)70124-8 pmid:23867200

    CrossRefPubMedWeb of Science
27. 27.↵
    2. Maclullich AM,
    3. Wardlaw JM,
    4. Ferguson KJ, et al

    . Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry 2004;75:1519–23 doi:10.1136/jnnp.2003.030858 pmid:15489380

    Abstract/FREE Full Text
28. 28.↵
    2. Fazekas F,
    3. Chawluk JB,
    4. Alavi A, et al

    . MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 1987;149:351–56 doi:10.2214/ajr.149.2.351 pmid:3496763

    CrossRefPubMedWeb of Science
29. 29.↵
    2. Barthel H,
    3. Gertz HJ,
    4. Dresel S, et al

    . Cerebral amyloid-beta PET with florbetaben (18F) in patients with Alzheimer’s disease and healthy controls: a multicentre phase 2 diagnostic study. Lancet Neurol 2011;10:424–35 doi:10.1016/S1474-4422(11)70077-1 pmid:21481640

    CrossRefPubMedWeb of Science
30. 30.↵
    2. Lopresti BJ,
    3. Klunk WE,
    4. Mathis CA, et al

    . Simplified quantification of Pittsburgh Compound B amyloid imaging PET studies: a comparative analysis. J Nucl Med 2005;46:1959–72 doi:10.1016/j.nicl.2017.04.025 pmid:16330558

    Abstract/FREE Full Text
31. 31.↵
    2. Bullich S,
    3. Seibyl J,
    4. Catafau AM, et al

    . Optimized classification of (18)F-Florbetaben PET scans as positive and negative using an SUVR quantitative approach and comparison to visual assessment. Neuroimage Clin 2017;15:325–32 doi:10.1016/j.nicl.2017.04.025 pmid:28560157

    CrossRefPubMed
32. 32.↵
    2. Duara R,
    3. Loewenstein DA,
    4. Lizarraga G, et al

    . Effect of age, ethnicity, sex, cognitive status and APOE genotype on amyloid load and the threshold for amyloid positivity. Neuroimage Clin 2019;22:101800 doi:10.1016/j.nicl.2019.101800 pmid:30991618

    CrossRefPubMed
33. 33.↵
    2. Francis F,
    3. Ballerini L,
    4. Wardlaw JM

    . Perivascular spaces and their associations with risk factors, clinical disorders and neuroimaging features: a systematic review and meta-analysis. Int J Stroke 2019;14:359–71 doi:10.1177/1747493019830321 pmid:30762496

    CrossRefPubMed
34. 34.↵
    2. Chen W,
    3. Song X,
    4. Zhang Y

    ; Alzheimer’s Disease Neuroimaging Initiative. Assessment of the Virchow-Robin Spaces in Alzheimer disease, mild cognitive impairment, and normal aging, using high-field MR imaging. AJNR Am J Neuroradiol 2011;32:1490–95 doi:10.3174/ajnr.A2541 pmid:21757525

    Abstract/FREE Full Text
35. 35.↵
    2. Weller RO,
    3. Djuanda E,
    4. Yow HY, et al

    . Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 2009;117:1–14 doi:10.1007/s00401-008-0457-0 pmid:19002474

    CrossRefPubMedWeb of Science
36. 36.↵
    2. Palmqvist S,
    3. Zetterberg H,
    4. Mattsson N, et al

    . Alzheimer’s Disease Neuroimaging Initiative. Detailed comparison of amyloid PET and CSF biomarkers for identifying early Alzheimer disease. Neurology 2015;85:1240–49 doi:10.1212/WNL.0000000000001991 pmid:26354982

    Abstract/FREE Full Text
37. 37.↵
    2. Buchhave P,
    3. Minthon L,
    4. Zetterberg H, et al

    . Cerebrospinal fluid levels of beta-amyloid 1-42, but not of tau, are fully changed already 5 to 10 years before the onset of Alzheimer dementia. Arch Gen Psychiatry 2012;69:98–106 doi:10.1001/archgenpsychiatry.2011.155 pmid:22213792

    CrossRefPubMedWeb of Science
38. 38.↵
    2. Hansson O,
    3. Zetterberg H,
    4. Buchhave P, et al

    . Association between CSF biomarkers and incipient Alzheimer’s disease in patients with mild cognitive impairment: a follow-up study. Lancet Neurol 2006;5:228–34 doi:10.1016/S1474-4422(06)70355-6 pmid:16488378

    CrossRefPubMedWeb of Science
39. 39.↵
    2. Hughes TM,
    3. Craft S,
    4. Lopez OL

    . Review of ‘the potential role of arterial stiffness in the pathogenesis of Alzheimer’s disease.’ Neurodegener Dis Manag 2015;5:121–35 doi:10.2217/nmt.14.53 pmid:25894876

    CrossRefPubMed
40. 40.↵
    2. Adams HH,
    3. Hilal S,
    4. Schwingenschuh P, et al

    . A priori collaboration in population imaging: the Uniform Neuro-Imaging of Virchow-Robin Spaces Enlargement Consortium. Alzheimers Dement (Amst) 2015;1:513–20 doi:10.1016/j.dadm.2015.10.004 pmid:27239529

    CrossRefPubMed
41. 41.↵
    2. Minoshima S,
    3. Drzezga AE,
    4. Barthel H, et al

    . SNMMI Procedure Standard/EANM Practice Guideline for Amyloid PET Imaging of the Brain 1.0. J Nucl Med 2016;57:1316–22 doi:10.2967/jnumed.116.174615 pmid:27481605

    FREE Full Text
42. 42.↵
    2. Seibyl J,
    3. Barthel H,
    4. Stephens A, et al

    . Reliability, reproducibility and efficacy of the 18F florbetaben β-amyloid PET scan visual assessment method as trained via a computer-based instructional tool. J Nucl Med 2013;54(Suppl 2):300