Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis: A cross-sectional preliminary report

Paolo Zamboni, Erica Menegatti, Bianca Weinstock-Guttman, Michael G. Dwyer, Claudiu V. Schirda, Anna M. Malagoni, David Hojnacki, Cheryl Kennedy, Ellen Carl, Niels Bergsland, Christopher Magnano, Ilaria Bartolomei, Fabrizio Salvi, Robert Zivadinov

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Abstract

Background: Several studies have reported hypoperfusion of the brain parenchyma in multiple sclerosis (MS) patients. We hypothesized a possible relationship between abnormal perfusion in MS and hampered venous outflow at the extracranial level, a condition possibly associated with MS and known as chronic cerebrospinal venous insufficiency (CCSVI).Methods: We investigated the relationship between CCSVI and cerebral perfusion in 16 CCSVI MS patients and 8 age- and sex-matched healthy controls. Subjects were scanned in a 3-T scanner using dynamic susceptibility, contrast-enhanced, perfusion-weighted imaging. Cerebral blood flow (CBF), cerebral blood volume (CBV) and mean transit time (MTT) were measured in the gray matter (GM), white matter (WM) and the subcortical GM (SGM). The severity of CCSVI was assessed according to the venous hemodynamic insufficiency severity score (VHISS) on the basis of the number of venous segments exhibiting flow abnormalities.Results: There was a significant association between increased VHISS and decreased CBF in the majority of examined regions of the brain parenchyma in MS patients. The most robust correlations were observed for GM and WM (r = -0.70 to -0.71, P <0.002 and P corrected = 0.022), and for the putamen, thalamus, pulvinar nucleus of thalamus, globus pallidus and hippocampus (r = -0.59 to -0.71, P <0.01 and P corrected <0.05). No results for correlation between VHISS and CBV or MTT survived multiple comparison correction.Conclusions: This pilot study is the first to report a significant relationship between the severity of CCSVI and hypoperfusion in the brain parenchyma. These preliminary findings should be confirmed in a larger cohort of MS patients to ensure that they generalize to the MS population as a whole. Reduced perfusion could contribute to the known mechanisms of virtual hypoxia in degenerated axons.

Original languageEnglish
Article number22
JournalBMC Medicine
Volume9
DOIs
Publication statusPublished - Mar 7 2011

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Venous Insufficiency
Multiple Sclerosis
Brain
Cerebrovascular Circulation
Pulvinar
Perfusion
Hemodynamics
Globus Pallidus
Perfusion Imaging
Putamen
Thalamus
Axons
Hippocampus

ASJC Scopus subject areas

  • Medicine(all)

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Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis : A cross-sectional preliminary report. / Zamboni, Paolo; Menegatti, Erica; Weinstock-Guttman, Bianca; Dwyer, Michael G.; Schirda, Claudiu V.; Malagoni, Anna M.; Hojnacki, David; Kennedy, Cheryl; Carl, Ellen; Bergsland, Niels; Magnano, Christopher; Bartolomei, Ilaria; Salvi, Fabrizio; Zivadinov, Robert.

In: BMC Medicine, Vol. 9, 22, 07.03.2011.

Research output: Contribution to journalArticle

Zamboni, P, Menegatti, E, Weinstock-Guttman, B, Dwyer, MG, Schirda, CV, Malagoni, AM, Hojnacki, D, Kennedy, C, Carl, E, Bergsland, N, Magnano, C, Bartolomei, I, Salvi, F & Zivadinov, R 2011, 'Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis: A cross-sectional preliminary report', BMC Medicine, vol. 9, 22. https://doi.org/10.1186/1741-7015-9-22
Zamboni, Paolo ; Menegatti, Erica ; Weinstock-Guttman, Bianca ; Dwyer, Michael G. ; Schirda, Claudiu V. ; Malagoni, Anna M. ; Hojnacki, David ; Kennedy, Cheryl ; Carl, Ellen ; Bergsland, Niels ; Magnano, Christopher ; Bartolomei, Ilaria ; Salvi, Fabrizio ; Zivadinov, Robert. / Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis : A cross-sectional preliminary report. In: BMC Medicine. 2011 ; Vol. 9.
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abstract = "Background: Several studies have reported hypoperfusion of the brain parenchyma in multiple sclerosis (MS) patients. We hypothesized a possible relationship between abnormal perfusion in MS and hampered venous outflow at the extracranial level, a condition possibly associated with MS and known as chronic cerebrospinal venous insufficiency (CCSVI).Methods: We investigated the relationship between CCSVI and cerebral perfusion in 16 CCSVI MS patients and 8 age- and sex-matched healthy controls. Subjects were scanned in a 3-T scanner using dynamic susceptibility, contrast-enhanced, perfusion-weighted imaging. Cerebral blood flow (CBF), cerebral blood volume (CBV) and mean transit time (MTT) were measured in the gray matter (GM), white matter (WM) and the subcortical GM (SGM). The severity of CCSVI was assessed according to the venous hemodynamic insufficiency severity score (VHISS) on the basis of the number of venous segments exhibiting flow abnormalities.Results: There was a significant association between increased VHISS and decreased CBF in the majority of examined regions of the brain parenchyma in MS patients. The most robust correlations were observed for GM and WM (r = -0.70 to -0.71, P <0.002 and P corrected = 0.022), and for the putamen, thalamus, pulvinar nucleus of thalamus, globus pallidus and hippocampus (r = -0.59 to -0.71, P <0.01 and P corrected <0.05). No results for correlation between VHISS and CBV or MTT survived multiple comparison correction.Conclusions: This pilot study is the first to report a significant relationship between the severity of CCSVI and hypoperfusion in the brain parenchyma. These preliminary findings should be confirmed in a larger cohort of MS patients to ensure that they generalize to the MS population as a whole. Reduced perfusion could contribute to the known mechanisms of virtual hypoxia in degenerated axons.",
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T1 - Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis

T2 - A cross-sectional preliminary report

AU - Zamboni, Paolo

AU - Menegatti, Erica

AU - Weinstock-Guttman, Bianca

AU - Dwyer, Michael G.

AU - Schirda, Claudiu V.

AU - Malagoni, Anna M.

AU - Hojnacki, David

AU - Kennedy, Cheryl

AU - Carl, Ellen

AU - Bergsland, Niels

AU - Magnano, Christopher

AU - Bartolomei, Ilaria

AU - Salvi, Fabrizio

AU - Zivadinov, Robert

PY - 2011/3/7

Y1 - 2011/3/7

N2 - Background: Several studies have reported hypoperfusion of the brain parenchyma in multiple sclerosis (MS) patients. We hypothesized a possible relationship between abnormal perfusion in MS and hampered venous outflow at the extracranial level, a condition possibly associated with MS and known as chronic cerebrospinal venous insufficiency (CCSVI).Methods: We investigated the relationship between CCSVI and cerebral perfusion in 16 CCSVI MS patients and 8 age- and sex-matched healthy controls. Subjects were scanned in a 3-T scanner using dynamic susceptibility, contrast-enhanced, perfusion-weighted imaging. Cerebral blood flow (CBF), cerebral blood volume (CBV) and mean transit time (MTT) were measured in the gray matter (GM), white matter (WM) and the subcortical GM (SGM). The severity of CCSVI was assessed according to the venous hemodynamic insufficiency severity score (VHISS) on the basis of the number of venous segments exhibiting flow abnormalities.Results: There was a significant association between increased VHISS and decreased CBF in the majority of examined regions of the brain parenchyma in MS patients. The most robust correlations were observed for GM and WM (r = -0.70 to -0.71, P <0.002 and P corrected = 0.022), and for the putamen, thalamus, pulvinar nucleus of thalamus, globus pallidus and hippocampus (r = -0.59 to -0.71, P <0.01 and P corrected <0.05). No results for correlation between VHISS and CBV or MTT survived multiple comparison correction.Conclusions: This pilot study is the first to report a significant relationship between the severity of CCSVI and hypoperfusion in the brain parenchyma. These preliminary findings should be confirmed in a larger cohort of MS patients to ensure that they generalize to the MS population as a whole. Reduced perfusion could contribute to the known mechanisms of virtual hypoxia in degenerated axons.

AB - Background: Several studies have reported hypoperfusion of the brain parenchyma in multiple sclerosis (MS) patients. We hypothesized a possible relationship between abnormal perfusion in MS and hampered venous outflow at the extracranial level, a condition possibly associated with MS and known as chronic cerebrospinal venous insufficiency (CCSVI).Methods: We investigated the relationship between CCSVI and cerebral perfusion in 16 CCSVI MS patients and 8 age- and sex-matched healthy controls. Subjects were scanned in a 3-T scanner using dynamic susceptibility, contrast-enhanced, perfusion-weighted imaging. Cerebral blood flow (CBF), cerebral blood volume (CBV) and mean transit time (MTT) were measured in the gray matter (GM), white matter (WM) and the subcortical GM (SGM). The severity of CCSVI was assessed according to the venous hemodynamic insufficiency severity score (VHISS) on the basis of the number of venous segments exhibiting flow abnormalities.Results: There was a significant association between increased VHISS and decreased CBF in the majority of examined regions of the brain parenchyma in MS patients. The most robust correlations were observed for GM and WM (r = -0.70 to -0.71, P <0.002 and P corrected = 0.022), and for the putamen, thalamus, pulvinar nucleus of thalamus, globus pallidus and hippocampus (r = -0.59 to -0.71, P <0.01 and P corrected <0.05). No results for correlation between VHISS and CBV or MTT survived multiple comparison correction.Conclusions: This pilot study is the first to report a significant relationship between the severity of CCSVI and hypoperfusion in the brain parenchyma. These preliminary findings should be confirmed in a larger cohort of MS patients to ensure that they generalize to the MS population as a whole. Reduced perfusion could contribute to the known mechanisms of virtual hypoxia in degenerated axons.

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