The Vascular Steal Phenomenon is an Incomplete Contributor to Negative Cerebrovascular Reactivity in Patients with Symptomatic Intracranial Stenosis

Abstract

'Vascular steal' has been proposed as a compensatory mechanism in hemodynamically compromised ischemic parenchyma. Here, independent measures of cerebral blood flow (CBF) and blood oxygenation level-dependent (BOLD) magnetic resonance imaging (MRI) responses to a vascular stimulus in patients with ischemic cerebrovascular disease are recorded. Symptomatic intracranial stenosis patients (n ¼ 40) underwent a multimodal 3.0T MRI protocol including structural (T 1 -weighted and T 2 -weighted fluidattenuated inversion recovery) and hemodynamic (BOLD and CBF-weighted arterial spin labeling) functional MRI during room air and hypercarbic gas administration. CBF changes in regions demonstrating negative BOLD reactivity were recorded, as well as clinical correlates including symptomatic hemisphere by infarct and lateralizing symptoms. Fifteen out of forty participants exhibited negative BOLD reactivity. Of these, a positive relationship was found between BOLD and CBF reactivity in unaffected (stenosis degreeo50%) cortex. In negative BOLD cerebrovascular reactivity regions, three patients exhibited significant (Po0.01) reductions in CBF consistent with vascular steal; six exhibited increases in CBF; and the remaining exhibited no statistical change in CBF. Secondary findings were that negative BOLD reactivity correlated with symptomatic hemisphere by lateralizing clinical symptoms and prior infarcts(s). These data support the conclusion that negative hypercarbia-induced BOLD responses, frequently assigned to vascular steal, are heterogeneous in origin with possible contributions from autoregulation and/or metabolism.

The Effects of Perturbed Cerebral Blood Flow and Cerebrovascular Reactivity on Structural MRI and Behavioral Readouts in Mild Traumatic Brain Injury

“…Such a blood-stealing phenomenon has been observed in ischemic stroke, and ischemic cerebrovascular disease. [30][31][32] Attenuated CBF responses to vasodilation have been reported using both the CCI 33,34 and fluid percussion injury models. 35 However, negative CBF responses to hypercapnia have not been reported previously.…”

Arterial Spin Labeling and Blood Oxygen Level-Dependent MRI Cerebrovascular Reactivity in Cerebrovascular Disease: A Systematic Review and Meta-Analysis

“…The third and last study, which found a higher CVR ipsilaterally, was the study by Altamura et al [21] who attributed this to the decreased fMRI signal detection in hemodynamic impaired patients resulting in more noise within the data. A reason as to why studies could find a higher CVR ipsilaterally could be cerebral metabolic rate of oxygen (CMRO 2 ) upregulation in the ipsilateral hemisphere [48] . CMRO 2 upregulation can be caused by a hypercarbic hyperoxia stimulus (carbogen) in which the tissue that is hypoxic at baseline metabolizes the additional oxygen provided and therefore artificially decreases the relative amount of dHb being present, thus creating a falsely increased CVR.…”

Prior Infarcts, Reactivity, and Angiography in Moyamoya Disease (PIRAMD): a scoring system for moyamoya severity based on multimodal hemodynamic imaging

“…In healthy parenchyma, CVR primarily derives from a large increase in cerebral blood flow (CBF) and volume (CBV) in response to a vasostimulatory agent such as carbon dioxide (i.e., hypercapnia). Significantly diminished or negative changes in CVR after during hypercapnia have previously been shown to correlate with regions affected by prior infarct and symptomatology 1,26,30 . However, owing to the relative novelty of hypercapnic CVR mapping using MRI compared to more established clinical measures such as acetazolamide SPECT, interpretation of hypercapnic CVR maps has not been standardized.…”

“…Cerebrovascular reactivity (CVR) is a well-documented and valuable surrogate marker of cerebrovascular reserve in patients with previously identified intravascular pathology 1,9,10,12,13 . In healthy parenchyma, CVR primarily derives from a large increase in cerebral blood flow (CBF) and volume (CBV) in response to a vasostimulatory agent such as carbon dioxide (i.e., hypercapnia).…”