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Arterial transit artifacts on arterial spin labeling MRI can predict cerebral hyperperfusion after carotid endarterectomy: an initial study

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Abstract

Objectives

To investigate whether preoperative arterial spin labeling (ASL) MRI can predict cerebral hyperperfusion after carotid endarterectomy (CEA) in patients with carotid stenosis.

Methods

Consecutive patients with carotid stenosis who underwent CEA between May 2015 and July 2021 were included. For each patient, a cerebral blood flow ratio (rCBF) map was obtained by dividing postoperative CBF with preoperative CBF images from two pseudo-continuous ASL scans. Hyperperfusion regions with rCBF > 2 were extracted and weighted with rCBF to calculate the hyperperfusion index. According to the distribution of the hyperperfusion index, patients were divided into hyperperfusion and non-hyperperfusion groups. Preoperative ASL images were scored based on the presence of arterial transit artifacts (ATAs) in 10 regions of interest corresponding to the Alberta Stroke Programme Early Computed Tomography Score methodology. The degree of stenosis and primary and secondary collaterals were evaluated to correlate with the ASL score. Logistic regression and receiver operating characteristic curve analyses were performed to assess the predictive ability of the ASL score for cerebral hyperperfusion.

Results

Of 86 patients included, cerebral hyperperfusion was present in 17 (19.8%) patients. Carotid near occlusion, opening of posterior communicating arteries with incomplete anterior semicircle, and leptomeningeal collaterals were associated with lower ASL scores (p < 0.05). The preoperative ASL score was an independent predictor of cerebral hyperperfusion (OR = 0.48 [95% CI [0.33–0.71]], p < 0.001) with the optimal cutoff value of 25 points (AUC = 0.98, 94.1% sensitivity, 88.4% specificity).

Conclusions

Based on the presence of ATAs, ASL can non-invasively predict cerebral hyperperfusion after CEA in patients with carotid stenosis.

Key Points

• Carotid near occlusion, opening of posterior communicating arteries with incomplete anterior semicircle, and leptomeningeal collaterals were associated with lower ASL scores.

• The ASL score performed better than the degree of stenosis, type of CoW, and leptomeningeal collaterals, as well as the combination of the three factors for the prediction of cerebral hyperperfusion.

• For patients with carotid stenosis, preoperative ASL can non-invasively identify patients at high risk of cerebral hyperperfusion after carotid endarterectomy without complex post-processing steps.

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Abbreviations

ASL:

Arterial spin labeling

ATA:

Arterial transit artifact

BP:

Blood pressure

CBF:

Cerebral blood flow

CEA:

Carotid endarterectomy

CHS:

Cerebral hyperperfusion syndrome

CoW:

Circle of Willis

CVR:

Cerebrovascular reactivity

FHV:

Fluid-attenuated inversion recovery hyperintense vessel

FLAIR:

Fluid-attenuated inversion recovery

HI:

Hyperperfusion index

PLD:

Post-labeling delay

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Acknowledgements

We thank Lifang Zhang from the Clinical Epidemiology Unit, International Epidemiology Network, Peking Union Medical College Hospital, Chinese Academy of Medical Science, for statistical advice.

Funding

This work was supported in part by the National Nature Science Foundation of China grant (82071899), the Beijing Natural Science Foundation grant (L182067), and the Fundamental Research Funds for the Central Universities (3332020009).

Author information

Authors and Affiliations

  1. Department of Radiology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, No. 1 Shuaifuyuan, Wangfujing, Dongcheng District, Beijing, 100730, China

    Xiaoyuan Fan, Tianye Lin, Hui You & Feng Feng

  2. State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

    Zhentao Zuo

  3. Sino-Danish College, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, China

    Zhentao Zuo

  4. Department of Vascular Surgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, No. 1 Shuaifuyuan, Wangfujing, Dongcheng District, Beijing, 100730, China

    Zhichao Lai & Bao Liu

  5. GE Healthcare, MR Research China, Beijing, China

    Jianxun Qu & Juan Wei

  6. State Key Laboratory of Difficult, Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

    Feng Feng

Authors
  1. Xiaoyuan Fan
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  2. Zhentao Zuo
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  3. Tianye Lin
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  4. Zhichao Lai
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  5. Hui You
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  7. Juan Wei
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  9. Feng Feng
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Corresponding authors

Correspondence to Zhichao Lai or Feng Feng.

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Guarantor

The scientific guarantor of this publication is Feng Feng.

Conflict of interest

The authors of this manuscript declare that they have no conflict of interest.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all patients in this study.

Ethical approval

This prospective study was approved by the Medical Ethics Committee of the Peking Union Medical College Hospital.

Study subjects or cohorts overlap

Some study subjects or cohorts have been previously reported in:

• Lin T, Lai Z, Lv Y, et al (2018) Effective collateral circulation may indicate improved perfusion territory restoration after carotid endarterectomy. Eur Radiol 28:727–735.

• Lin T, Lai Z, Zuo Z et al (2019) ASL perfusion features and type of circle of Willis as imaging markers for cerebral hyperperfusion after carotid revascularization: a preliminary study. Eur Radiol 29:2651-2658.

• Fan X, Zhang X, Lai Z et al (2021) Cerebral small vessel disease burden related to carotid intraplaque hemorrhage serves as an imaging marker for clinical symptoms in carotid stenosis. Front Neurol 12:731237.

• Fan X, Lai Z, Lin T et al (2021) Pre-operative cerebral small vessel disease on MR imaging is associated with cerebral hyperperfusion after carotid endarterectomy. Front Cardiovasc Med 8:734392.

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Fan, X., Zuo, Z., Lin, T. et al. Arterial transit artifacts on arterial spin labeling MRI can predict cerebral hyperperfusion after carotid endarterectomy: an initial study. Eur Radiol 32, 6145–6157 (2022). https://doi.org/10.1007/s00330-022-08755-x

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