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June 06, 2017; 88 (23) Article

Distribution of lacunes in cerebral amyloid angiopathy and hypertensive small vessel disease

Marco Pasi, Gregoire Boulouis, Panagiotis Fotiadis, Eitan Auriel, Andreas Charidimou, Kellen Haley, Alison Ayres, Kristin M. Schwab, Joshua N. Goldstein, Jonathan Rosand, Anand Viswanathan, Leonardo Pantoni, Steven M. Greenberg, M. Edip Gurol
First published May 5, 2017, DOI: https://doi.org/10.1212/WNL.0000000000004007
Marco Pasi
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Gregoire Boulouis
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Panagiotis Fotiadis
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Eitan Auriel
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Andreas Charidimou
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Kellen Haley
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Alison Ayres
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Kristin M. Schwab
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Joshua N. Goldstein
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Jonathan Rosand
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Anand Viswanathan
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Leonardo Pantoni
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Steven M. Greenberg
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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M. Edip Gurol
From the Hemorrhagic Stroke Research Program (M.P., G.B., P.F., E.A., A.C., K.H., A.A., K.M.S., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; NEUROFARBA Department (M.P., L.P.), Neuroscience Section, University of Florence, Italy; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Full PDF
Citation
Distribution of lacunes in cerebral amyloid angiopathy and hypertensive small vessel disease
Marco Pasi, Gregoire Boulouis, Panagiotis Fotiadis, Eitan Auriel, Andreas Charidimou, Kellen Haley, Alison Ayres, Kristin M. Schwab, Joshua N. Goldstein, Jonathan Rosand, Anand Viswanathan, Leonardo Pantoni, Steven M. Greenberg, M. Edip Gurol
Neurology Jun 2017, 88 (23) 2162-2168; DOI: 10.1212/WNL.0000000000004007

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Abstract

Objective: To evaluate whether the burden of deep and lobar lacunes differs between patients with intracerebral hemorrhage (ICH) with definite/probable cerebral amyloid angiopathy (CAA) per the Boston criteria and hypertensive small vessel disease (HTN-SVD; ICH in basal ganglia, thalami, brainstem).

Methods: We defined lobar and deep lacunes similar to the topographic distribution used for ICH and cerebral microbleeds (CMBs). We then compared their distribution between patients with CAA-ICH and those with strictly deep CMB and ICH (HTN-ICH). The independent associations of lacune location with the diagnosis of CAA-ICH and HTN-ICH were evaluated with multivariable models. The relationship between lobar lacunes and white matter hyperintensity (WMH) volume was evaluated by means of partial correlation analyses adjusted for age and a validated visual scale.

Results: In our final cohort of 316 patients with ICH, lacunes were frequent (24.7%), with similar rates in 191 patients with CAA and 125 with HTN-ICH (23% vs 27.2%, p = 0.4). Lobar lacunes were more commonly present in CAA (20.4% vs 5.7%, p < 0.001), while deep lacunes were more frequent in HTN-ICH (15.2% vs 2.1%, p < 0.001). After correction for demographics and clinical and neuroimaging markers of SVD, lobar lacunes were associated with CAA (p = 0.003) and deep lacunes with HTN-ICH (p < 0.001). Lobar lacunes in 80% of the cases were at least in contact with WMH, and after adjustment for age, they were highly correlated to WMH volume (r = 0.42, p < 0.001).

Conclusions: Lobar lacunes are associated with CAA, whereas deep lacunes are more frequent in HTN-SVD. Lobar lacunes seem to have a close relationship with WMH, suggesting a possible common origin.

GLOSSARY

BG=
basal ganglia;
CAA=
cerebral amyloid angiopathy;
CI=
confidence interval;
CMB=
cerebral microbleed;
CSO=
centrum semiovale;
cSS=
cortical superficial siderosis;
EPVS=
enlarged perivascular spaces;
HTN=
hypertensive;
ICH=
intracerebral hemorrhage;
MGH=
Massachusetts General Hospital;
OR=
odds ratio;
SVD=
small vessel disease;
WM=
white matter;
WMH=
white matter hyperintensities;
WMHP=
white matter hyperintensity pattern

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 2158

  • Received October 5, 2016.
  • Accepted in final form February 16, 2017.
  • © 2017 American Academy of Neurology
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