Skip to main content
Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging 11/2019

29.07.2019 | Original Article

Enlarged perivascular spaces and florbetapir uptake in patients with intracerebral hemorrhage

verfasst von: Nicolas Raposo, Mélanie Planton, Pierre Payoux, Patrice Péran, Jean François Albucher, Lionel Calviere, Alain Viguier, Vanessa Rousseau, Anne Hitzel, François Chollet, Jean Marc Olivot, Fabrice Bonneville, Jérémie Pariente

Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging | Ausgabe 11/2019

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Enlarged perivascular spaces in the centrum semiovale (CSO-EPVS) have been linked to cerebral amyloid angiopathy (CAA). To get insight into the underlying mechanisms of this association, we investigated the relationship between amyloid-β deposition assessed by 18F-florbetapir PET and CSO-EPVS in patients with acute intracerebral hemorrhage (ICH).

Methods

We prospectively enrolled 18 patients with lobar ICH (suggesting CAA) and 20 with deep ICH (suggesting hypertensive angiopathy), who underwent brain MRI and 18F-florbetapir PET. EPVS were assessed on MRI using a validated 4-point visual rating scale in the centrum semiovale and the basal ganglia (BG-EPVS). PET images were visually assessed, blind to clinical and MRI data. We evaluated the association between florbetapir PET positivity and high degree (score> 2) of CSO-EPVS and BG-EPVS.

Results

High CSO-EPVS degree was more common in patients with lobar ICH than deep ICH (55.6% vs. 20.0%; p = 0.02). Eight (57.1%) patients with high CSO-EPVS degree had a positive florbetapir PET compared with 4 (16.7%) with low CSO-EPVS degree (p = 0.01). In contrast, prevalence of florbetapir PET positivity was similar between patients with high vs. low BG-EPVS. In multivariable analysis adjusted for age, hypertension, and MRI markers of CAA, florbetapir PET positivity (odds ratio (OR) 6.44, 95% confidence interval (CI) 1.32–38.93; p = 0.03) was independently associated with high CSO-EPVS degree.

Conclusions

Among patients with spontaneous ICH, high degree of CSO-EPVS but not BG-EPVS is associated with amyloid PET positivity. The findings provide further evidence that CSO-EPVS are markers of vascular amyloid burden that may be useful in diagnosing CAA.
Literatur
1.
Zurück zum Zitat Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344(19):1450–60.CrossRef Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344(19):1450–60.CrossRef
2.
Zurück zum Zitat Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701.CrossRef Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701.CrossRef
3.
Zurück zum Zitat Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry. 2012;83(2):124–37.CrossRef Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry. 2012;83(2):124–37.CrossRef
4.
Zurück zum Zitat Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol. 2013;12(5):483–97.CrossRef Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol. 2013;12(5):483–97.CrossRef
5.
Zurück zum Zitat Viswanathan A, Rakich SM, Engel C, Snider R, Rosand J, Greenberg SM, et al. Antiplatelet use after intracerebral hemorrhage. Neurology. 2006;66(2):206–9.CrossRef Viswanathan A, Rakich SM, Engel C, Snider R, Rosand J, Greenberg SM, et al. Antiplatelet use after intracerebral hemorrhage. Neurology. 2006;66(2):206–9.CrossRef
6.
Zurück zum Zitat Biffi A, Halpin A, Towfighi A, Gilson A, Busl K, Rost N, et al. Aspirin and recurrent intracerebral hemorrhage in cerebral amyloid angiopathy. Neurology. 2010;75(8):693–8.CrossRef Biffi A, Halpin A, Towfighi A, Gilson A, Busl K, Rost N, et al. Aspirin and recurrent intracerebral hemorrhage in cerebral amyloid angiopathy. Neurology. 2010;75(8):693–8.CrossRef
7.
Zurück zum Zitat Greenberg SM, Vernooij MW, Cordonnier C, Viswanathan A, Al-Shahi Salman R, Warach S, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol. 2009;8(2):165–74.CrossRef Greenberg SM, Vernooij MW, Cordonnier C, Viswanathan A, Al-Shahi Salman R, Warach S, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol. 2009;8(2):165–74.CrossRef
8.
Zurück zum Zitat Linn J, Halpin A, Demaerel P, Ruhland J, Giese AD, Dichgans M, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010;74(17):1346–50.CrossRef Linn J, Halpin A, Demaerel P, Ruhland J, Giese AD, Dichgans M, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010;74(17):1346–50.CrossRef
9.
Zurück zum Zitat Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–38.CrossRef Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–38.CrossRef
10.
Zurück zum Zitat Weller RO, Hawkes CA, Kalaria RN, Werring DJ, Carare RO. White matter changes in dementia: role of impaired drainage of interstitial fluid. Brain Pathol. 2015;25(1):63–78.CrossRef Weller RO, Hawkes CA, Kalaria RN, Werring DJ, Carare RO. White matter changes in dementia: role of impaired drainage of interstitial fluid. Brain Pathol. 2015;25(1):63–78.CrossRef
11.
Zurück zum Zitat Charidimou A, Boulouis G, Pasi M, Auriel E, van Etten ES, Haley K, et al. MRI-visible perivascular spaces in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology. 2017;88(12):1157–64.CrossRef Charidimou A, Boulouis G, Pasi M, Auriel E, van Etten ES, Haley K, et al. MRI-visible perivascular spaces in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology. 2017;88(12):1157–64.CrossRef
12.
Zurück zum Zitat Hawkes CA, Jayakody N, Johnston DA, Bechmann I, Carare RO. Failure of perivascular drainage of beta-amyloid in cerebral amyloid angiopathy. Brain Pathol. 2014;24(4):396–403.CrossRef Hawkes CA, Jayakody N, Johnston DA, Bechmann I, Carare RO. Failure of perivascular drainage of beta-amyloid in cerebral amyloid angiopathy. Brain Pathol. 2014;24(4):396–403.CrossRef
13.
Zurück zum Zitat Gurol ME, Becker JA, Fotiadis P, Riley G, Schwab K, Johnson KA, et al. Florbetapir-PET to diagnose cerebral amyloid angiopathy: a prospective study. Neurology. 2016;87(19):2043–9.CrossRef Gurol ME, Becker JA, Fotiadis P, Riley G, Schwab K, Johnson KA, et al. Florbetapir-PET to diagnose cerebral amyloid angiopathy: a prospective study. Neurology. 2016;87(19):2043–9.CrossRef
14.
Zurück zum Zitat Raposo N, Planton M, Peran P, Payoux P, Bonneville F, Lyoubi A, et al. Florbetapir imaging in cerebral amyloid angiopathy-related hemorrhages. Neurology. 2017;89(7):697–704.CrossRef Raposo N, Planton M, Peran P, Payoux P, Bonneville F, Lyoubi A, et al. Florbetapir imaging in cerebral amyloid angiopathy-related hemorrhages. Neurology. 2017;89(7):697–704.CrossRef
15.
Zurück zum Zitat Jorm AF. The Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): a review. Int Psychogeriatr. 2004;16(3):275–93.CrossRef Jorm AF. The Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): a review. Int Psychogeriatr. 2004;16(3):275–93.CrossRef
16.
Zurück zum Zitat Charidimou A, Linn J, Vernooij MW, Opherk C, Akoudad S, Baron JC, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain. 2015;138(Pt 8):2126–39.CrossRef Charidimou A, Linn J, Vernooij MW, Opherk C, Akoudad S, Baron JC, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain. 2015;138(Pt 8):2126–39.CrossRef
17.
Zurück zum Zitat Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–6.CrossRef Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–6.CrossRef
18.
Zurück zum Zitat Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke. 2010;41(3):450–4.CrossRef Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke. 2010;41(3):450–4.CrossRef
19.
Zurück zum Zitat Maclullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry. 2004;75(11):1519–23.CrossRef Maclullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry. 2004;75(11):1519–23.CrossRef
20.
Zurück zum Zitat Johnson KA, Sperling RA, Gidicsin CM, Carmasin JS, Maye JE, Coleman RE, et al. Florbetapir (F18-AV-45) PET to assess amyloid burden in Alzheimer’s disease dementia, mild cognitive impairment, and normal aging. Alzheimers Dement. 2013;9(5 Suppl):S72–83.CrossRef Johnson KA, Sperling RA, Gidicsin CM, Carmasin JS, Maye JE, Coleman RE, et al. Florbetapir (F18-AV-45) PET to assess amyloid burden in Alzheimer’s disease dementia, mild cognitive impairment, and normal aging. Alzheimers Dement. 2013;9(5 Suppl):S72–83.CrossRef
21.
Zurück zum Zitat Zhu YC, Tzourio C, Soumare A, Mazoyer B, Dufouil C, Chabriat H. 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(11):2483–90.CrossRef Zhu YC, Tzourio C, Soumare A, Mazoyer B, Dufouil C, Chabriat H. 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(11):2483–90.CrossRef
22.
Zurück zum Zitat Banerjee G, Kim HJ, Fox Z, Jager HR, Wilson D, Charidimou A, et al. MRI-visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain. 2017;140(4):1107–16.CrossRef Banerjee G, Kim HJ, Fox Z, Jager HR, Wilson D, Charidimou A, et al. MRI-visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain. 2017;140(4):1107–16.CrossRef
23.
Zurück zum Zitat Martinez-Ramirez S, Pontes-Neto OM, Dumas AP, Auriel E, Halpin A, Quimby M, et al. Topography of dilated perivascular spaces in subjects from a memory clinic cohort. Neurology. 2013;80(17):1551–6.CrossRef Martinez-Ramirez S, Pontes-Neto OM, Dumas AP, Auriel E, Halpin A, Quimby M, et al. Topography of dilated perivascular spaces in subjects from a memory clinic cohort. Neurology. 2013;80(17):1551–6.CrossRef
24.
Zurück zum Zitat Charidimou A, Meegahage R, Fox Z, Peeters A, Vandermeeren Y, Laloux P, 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(6):624–9.CrossRef Charidimou A, Meegahage R, Fox Z, Peeters A, Vandermeeren Y, Laloux P, 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(6):624–9.CrossRef
25.
Zurück zum Zitat Charidimou A, Jaunmuktane Z, Baron JC, Burnell M, Varlet P, Peeters A, et al. White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology. 2014;82(1):57–62.CrossRef Charidimou A, Jaunmuktane Z, Baron JC, Burnell M, Varlet P, Peeters A, et al. White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology. 2014;82(1):57–62.CrossRef
26.
Zurück zum Zitat Charidimou A, Hong YT, Jager HR, Fox Z, Aigbirhio FI, Fryer TD, et al. White matter perivascular spaces on magnetic resonance imaging: marker of cerebrovascular amyloid burden? Stroke. 2015;46(6):1707–9.CrossRef Charidimou A, Hong YT, Jager HR, Fox Z, Aigbirhio FI, Fryer TD, et al. White matter perivascular spaces on magnetic resonance imaging: marker of cerebrovascular amyloid burden? Stroke. 2015;46(6):1707–9.CrossRef
27.
Zurück zum Zitat Martinez-Ramirez S, van Rooden S, Charidimou A, van Opstal AM, Wermer M, Gurol ME, et al. Perivascular spaces volume in sporadic and hereditary (Dutch-type) cerebral amyloid angiopathy. Stroke. 2018;49(8):1913–9.CrossRef Martinez-Ramirez S, van Rooden S, Charidimou A, van Opstal AM, Wermer M, Gurol ME, et al. Perivascular spaces volume in sporadic and hereditary (Dutch-type) cerebral amyloid angiopathy. Stroke. 2018;49(8):1913–9.CrossRef
28.
Zurück zum Zitat van Veluw SJ, Biessels GJ, Bouvy WH, Spliet WG, Zwanenburg JJ, Luijten PR, et al. Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab. 2016;36(3):576–80.CrossRef van Veluw SJ, Biessels GJ, Bouvy WH, Spliet WG, Zwanenburg JJ, Luijten PR, et al. Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab. 2016;36(3):576–80.CrossRef
29.
Zurück zum Zitat Ly JV, Donnan GA, Villemagne VL, Zavala JA, Ma H, O’Keefe G, et al. 11C-PIB binding is increased in patients with cerebral amyloid angiopathy-related hemorrhage. Neurology. 2010;74(6):487–93.CrossRef Ly JV, Donnan GA, Villemagne VL, Zavala JA, Ma H, O’Keefe G, et al. 11C-PIB binding is increased in patients with cerebral amyloid angiopathy-related hemorrhage. Neurology. 2010;74(6):487–93.CrossRef
30.
Zurück zum Zitat Boyle PA, Yu L, Nag S, Leurgans S, Wilson RS, Bennett DA, et al. Cerebral amyloid angiopathy and cognitive outcomes in community-based older persons. Neurology. 2015;85(22):1930–6.CrossRef Boyle PA, Yu L, Nag S, Leurgans S, Wilson RS, Bennett DA, et al. Cerebral amyloid angiopathy and cognitive outcomes in community-based older persons. Neurology. 2015;85(22):1930–6.CrossRef
Metadaten
Titel
Enlarged perivascular spaces and florbetapir uptake in patients with intracerebral hemorrhage
verfasst von
Nicolas Raposo
Mélanie Planton
Pierre Payoux
Patrice Péran
Jean François Albucher
Lionel Calviere
Alain Viguier
Vanessa Rousseau
Anne Hitzel
François Chollet
Jean Marc Olivot
Fabrice Bonneville
Jérémie Pariente
Publikationsdatum
29.07.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nuclear Medicine and Molecular Imaging / Ausgabe 11/2019
Print ISSN: 1619-7070
Elektronische ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-019-04441-1

Weitere Artikel der Ausgabe 11/2019

European Journal of Nuclear Medicine and Molecular Imaging 11/2019 Zur Ausgabe