Leptomeningeal collateral activation indicates severely impaired cerebrovascular reserve capacity in patients with symptomatic unilateral carotid artery occlusion

J Cereb Blood Flow Metab. 2021 Nov;41(11):3039-3051. doi: 10.1177/0271678X211024373. Epub 2021 Jun 10.

Abstract

For patients with symptomatic unilateral internal carotid artery (ICA) occlusion, impaired cerebrovascular reactivity (CVR) indicates increased stroke risk. Here, the role of collateral activation remains a matter of debate, whereas angio-anatomical collateral abundancy does not necessarily imply sufficient compensatory flow provided. We aimed to further elucidate the role of collateral activation in the presence of impaired CVR. From a prospective database, 62 patients with symptomatic unilateral ICA occlusion underwent blood oxygenation-level dependent (BOLD) fMRI CVR imaging and a transcranial Doppler (TCD) investigation for primary and secondary collateral activation. Descriptive statistic and multivariate analysis were used to evaluate the relationship between BOLD-CVR values and collateral activation. Patients with activated secondary collaterals exhibited more impaired BOLD-CVR values of the ipsilateral hemisphere (p = 0.02). Specifically, activation of leptomeningeal collaterals showed severely impaired ipsilateral hemisphere BOLD-CVR values when compared to activation of ophthalmic collaterals (0.05 ± 0.09 vs. 0.12 ± 0.04, p = 0.005). Moreover, the prediction analysis showed leptomeningeal collateral activation as a strong independent predictor for ipsilateral hemispheric BOLD-CVR. In our study, ipsilateral leptomeningeal collateral activation is the sole collateral pathway associated with severely impaired BOLD-CVR in patients with symptomatic unilateral ICA occlusion.

Keywords: BOLD fMRI; TCD; carotid artery occlusion; cerebrovascular reactivity; collaterals.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Carotid Artery, Internal / pathology*
  • Cerebrovascular Circulation / physiology
  • Cerebrovascular Disorders / diagnostic imaging*
  • Collateral Circulation / physiology*
  • Female
  • Humans
  • Ischemic Attack, Transient / diagnosis
  • Ischemic Attack, Transient / physiopathology
  • Ischemic Stroke / diagnosis
  • Ischemic Stroke / physiopathology
  • Magnetic Resonance Imaging / methods*
  • Male
  • Meninges / blood supply*
  • Meninges / diagnostic imaging
  • Middle Aged
  • Multivariate Analysis
  • Oxygen Saturation / physiology
  • Prospective Studies
  • Ultrasonography, Doppler, Transcranial / methods