Impaired cerebrovascular reactivity in multiple sclerosis

Olga Marshall, Hanzhang Lu, Jean Christophe Brisset, Feng Xu, Peiying Liu, Joseph Herbert, Robert I. Grossman, Yulin Ge

Research output: Contribution to journalArticle

55 Citations (Scopus)

Abstract

IMPORTANCE Cerebrovascular reactivity (CVR) is an inherent indicator of the dilatory capacity of cerebral arterioles for a vasomotor stimulus for maintaining a spontaneous and instant increase of cerebral blood flow (CBF) in response to neural activation. The integrity of this mechanism is essential to preserving healthy neurovascular coupling; however, to our knowledge, no studies have investigated whether there are CVR abnormalities in multiple sclerosis (MS).

OBJECTIVE To use hypercapnic perfusion magnetic resonance imaging to assess CVR impairment in patients with MS.

Design, Setting, and Participants A total of 19 healthy volunteers and 19 patients with MS underwent perfusion magnetic resonance imaging based on pseudocontinuous arterial spin labeling to measure CBF at normocapnia (ie, breathing room air) and hypercapnia. The hypercapnia condition is achieved by breathing 5%carbon dioxide gas mixture, which is a potent vasodilator causing an increase of CBF.

Main Outcomes and Measures Cerebrovascular reactivitywas calculated as the percent increase of normocapnic to hypercapnic CBF normalized by the change in end-tidal carbon dioxide, which was recorded during both conditions. Group analysis was performed for regional and global CVR comparison between patients and controls. Regression analysis was also performed between CVR values, lesion load, and brain atrophy measures in patients with MS.

Results A significant decrease of mean (SD) global gray matter CVR was found in patients with MS (3.56 [0.81]) compared with healthy controls (5.08 [1.56]; P = .001). Voxel-by-voxel analysis showed diffuse reduction of CVR in multiple regions of patients with MS. There was a significant negative correlation between gray matter CVR and lesion volume (R = 0.6, P = .004) and a significant positive correlation between global gray matter CVR and gray matter atrophy index (R = 0.5, P = .03).

Conclusions and Relevance Our quantitative imaging findings suggest impairment in functional cerebrovascular pathophysiology, by measuring a diffuse decrease in CVR, which may be the underlying cause of neurodegeneration in MS.

Original languageEnglish (US)
Pages (from-to)1275-1281
Number of pages7
JournalJAMA Neurology
Volume71
Issue number10
DOIs
StatePublished - Oct 1 2014

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Cerebrovascular Circulation
Multiple Sclerosis
Hypercapnia
Magnetic Resonance Angiography
Carbon Dioxide
Atrophy
Respiration
Arterioles
Reactivity
Vasodilator Agents
Healthy Volunteers
Gases
Air
Regression Analysis
Outcome Assessment (Health Care)
Gray Matter
Brain
Cerebral Blood Flow
Grey Matter

ASJC Scopus subject areas

  • Arts and Humanities (miscellaneous)
  • Clinical Neurology
  • Medicine(all)

Cite this

Marshall, O., Lu, H., Brisset, J. C., Xu, F., Liu, P., Herbert, J., ... Ge, Y. (2014). Impaired cerebrovascular reactivity in multiple sclerosis. JAMA Neurology, 71(10), 1275-1281. https://doi.org/10.1001/jamaneurol.2014.1668

Impaired cerebrovascular reactivity in multiple sclerosis. / Marshall, Olga; Lu, Hanzhang; Brisset, Jean Christophe; Xu, Feng; Liu, Peiying; Herbert, Joseph; Grossman, Robert I.; Ge, Yulin.

In: JAMA Neurology, Vol. 71, No. 10, 01.10.2014, p. 1275-1281.

Research output: Contribution to journalArticle

Marshall, O, Lu, H, Brisset, JC, Xu, F, Liu, P, Herbert, J, Grossman, RI & Ge, Y 2014, 'Impaired cerebrovascular reactivity in multiple sclerosis', JAMA Neurology, vol. 71, no. 10, pp. 1275-1281. https://doi.org/10.1001/jamaneurol.2014.1668
Marshall O, Lu H, Brisset JC, Xu F, Liu P, Herbert J et al. Impaired cerebrovascular reactivity in multiple sclerosis. JAMA Neurology. 2014 Oct 1;71(10):1275-1281. https://doi.org/10.1001/jamaneurol.2014.1668
Marshall, Olga ; Lu, Hanzhang ; Brisset, Jean Christophe ; Xu, Feng ; Liu, Peiying ; Herbert, Joseph ; Grossman, Robert I. ; Ge, Yulin. / Impaired cerebrovascular reactivity in multiple sclerosis. In: JAMA Neurology. 2014 ; Vol. 71, No. 10. pp. 1275-1281.
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