J Stroke.  2024 Sep;26(3):415-424. 10.5853/jos.2023.04203.

Early Improvement in Interstitial Fluid Flow in Patients With Severe Carotid Stenosis After Angioplasty and Stenting

Affiliations
  • 1Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan
  • 2School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan
  • 3Department of Neurology, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan
  • 4Brain Research Center, National Yang Ming Chiao Tung University, Taipei, Taiwan
  • 5Institute of Clinical Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan
  • 6Division of Translational Research, Department of Medical Research, Taipei Veterans General Hospital, Taipei, Taiwan
  • 7Department of Biomedical Engineering, Yuanpei University of Medical Technology, Hsinchu, Taiwan
  • 8Department of Radiology, National Defense Medical Center, Taipei, Taiwan

Abstract

Background and Purpose
This study aimed to investigate early changes in interstitial fluid (ISF) flow in patients with severe carotid stenosis after carotid angioplasty and stenting (CAS).
Methods
We prospectively recruited participants with carotid stenosis ≥80% undergoing CAS at our institute between October 2019 and March 2023. Magnetic resonance imaging (MRI), including diffusion tensor imaging (DTI), and the Mini-Mental State Examination (MMSE) were performed 3 days before CAS. MRI with DTI and MMSE were conducted within 24 hours and 2 months after CAS, respectively. The diffusion tensor image analysis along the perivascular space (DTI-ALPS) index was calculated from the DTI data to determine the ISF status. Increments were defined as the ratio of the difference between post- and preprocedural values to preprocedural values.
Results
In total, 102 participants (age: 67.1±8.9 years; stenosis: 89.5%±5.7%) with longitudinal data were evaluated. The DTI-ALPS index increased after CAS (0.85±0.15; 0.85 [0.22] vs. 0.86±0.14; 0.86 [0.21]; P=0.022), as did the MMSE score (25.9±3.7; 24.0 [4.0] vs. 26.9±3.4; 26.0 [3.0]; P<0.001). Positive correlations between increments in the DTI-ALPS index and MMSE score were found in all patients (rs=0.468; P<0.001).
Conclusion
An increased 24-hour post-CAS DTI-ALPS index suggests early improvement in ISF flow efficiency. The positive correlation between the 24-hour DTI-ALPS index and 2-month MMSE score increments suggests that early ISF flow improvement may contribute to long-term cognitive improvement after CAS.

Keyword

Diffusion tensor imaging; Prospective studies; Cognition; Magnetic resonance imaging

Figure

  • Figure 1. Imaging process in this study. (A) Diffusion tensor imaging (DTI) was performed on a 3-T magnetic resonance imaging (MRI) machine along with susceptibility-weighted angiography (SWAN), time-of-flight MR angiography (TOF-MRA), T2-weighted imaging (T2WI), and postcontrast T1-weighted imaging (T1WI+C) in the same session. Any patients with visible intracranial space-occupying lesions depicted on T1WI+C were excluded. T2WI data were then used as a reference to avoid placing regions of interest (ROIs) on areas of white matter hyperintensity. SWAN and TOF-MRA data were used as references to avoid placing ROIs on slow-flow and arterial vessels. The pink and yellow circles indicate ROI registration onto the projection and association area, respectively, as on DTI. (B) Diagnostic digital angiography (DSA) was performed to calculate the stenosis grade based on the North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria. Arrows on the diagnostic DSA image indicate carotid stenosis. A control angiogram was obtained after carotid stenting. Technical success was defined as residual stenosis <30%. Arrowheads on the control angiogram depict the proximal and distal ends of the carotid stent. (C) The diffusion tensor image analysis along the perivascular space (DTI-ALPS) index was calculated as the ratio of the mean diffusivity of projection and association areas on the x-axis to the mean diffusivity of projection on the y-axis and association on the z-axis. (D) Detailed analysis pipeline for the DTI-ALPS analysis was demonstrated. We first applied the coordinates of (23, -13, 22), (-23, -13, 22), (34, -13, 22), and (-34, -13, 22) to the right projection, left projection, right association, and left association areas, respectively, on the preprocedural DTI. Corrections were made to avoid these ROIs being placed on areas with slow-flow, arterial vessels, or apparent white matter intensities on SWAN, TOF-MRA, or T2WI. The ROIs with the same locations were copied onto the postprocedural DTI in the same patients, and the locations were confirmed manually again on the postprocedural DTI. The DTI-ALPS index of both preprocedural and postprocedural imaging was then calculated and compared for each patient.

  • Figure 2. Correlations of and longitudinal changes in the MMSE score and DTI-ALPS index before and after CAS. (A) A positive correlation between the preprocedural MMSE score and DTI-ALPS index is depicted. (B) The MMSE score increased 2 months after carotid stenting. (C) The DTI-ALPS index increased within 24 hours after carotid stenting. The gray lines in (B) and (C) connect the preprocedural and postprocedural values in patients with increased postprocedural values. MMSE, Mini-Mental State Examination; DTI-ALPS, diffusion tensor image analysis along the perivascular space; CAS, carotid angioplasty and stenting.

  • Figure 3. Increments in the DTI-ALPS index and MMSE score. Increments in the DTI-ALPS index and MMSE score were positively correlated in (A) all patients and (B) patients with increased MMSE scores after CAS. The increment was defined as the ratio of differences between postprocedural and preprocedural values (DTI-ALPS index or MMSE scores) to preprocedural values. DTI-ALPS, diffusion tensor image analysis along the perivascular space; MMSE, Mini-Mental State Examination; CAS, carotid angioplasty and stenting.


Reference

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