Small vessel disease is associated with altered cerebrovascular pulsatility but not resting cerebral blood flow

Shi, Yulu; Thrippleton, Michael J.; Blair, Gordon W.; Dickie, David Alexander; Marshall, Ian; Hamilton, I.; Doubal, Fergus; Chappell, Francesca M

doi:10.1177/0271678x18803956

Cited by 94 publications

(96 citation statements)

References 53 publications

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“…We also demonstrated that reduction in white matter CVR was associated with increased intracranial vascular pulsatility, most clearly seen in the intracranial venous sinuses and internal jugular veins, and with increased PVS visibility. (23) Importantly, we also found that reduced CVR was associated with reduced CSF stroke volume at the foramen magnum, and also that reduced CSF stroke volume was associated with increased basal ganglia PVS, showing for the first time in the intact human cranium, a possible link between dysfunctional brain interstitial fluid drainage (evidenced by increased PVS visibility) and impaired CSF pulsation (thought to help flush interstitial fluid through the glymphatic system). (30) We saw no association of reduced CVR in white or grey matter with resting CBF, or of resting CBF with any measures of SVD.…”

Section: Discussionsupporting

confidence: 52%

“…We are the first to describe an association of increased PVS with reduced CVR and CSF stroke volume, in addition to increased intracranial vascular pulsatility. (23) Visible PVS are associated with hypertension, increasing age, systemic and intracerebral inflammation, other SVD features like WMH and microbleeds, and increased risk of dementia. (1) Longitudinal studies are required to demonstrate if PVS visibility precedes or follows impairments in CVR or changes in vascular or CSF pulsatility.…”

Section: Discussionmentioning

confidence: 99%

“…(11) We performed phase contrast MRI to measure pulsatility in the internal carotid arteries, intracranial venous sinuses, CSF flow (aqueduct, foramen magnum) and total CBF, as described in detail. (23) Full parameters of all MR sequences are in Supplementary Table 1.…”

Section: Methodsmentioning

confidence: 99%

“…Arterial and venous flow waveforms were measured as described previously. (23-25) Briefly, we used a 2D cine phase-contrast sequence with retrospective peripheral pulse gating to acquire 32 velocity images per cardiac cycle. We used the following slice locations to measure flow in the different structures: a slice superior to the carotid bifurcation and perpendicular to the internal carotid artery (ICA) walls to measure flow in the ICA, vertebral arteries (VA) and internal jugular veins (IJV); a coronal-oblique slice intersecting the superior sagittal sinus approximately 2cm above the torcular and through the midpoint of the straight sinus to measure superior sagittal sinus (SSS), straight sinus (StS) and transverse sinus (TS) flow; a slice perpendicular to the aqueduct for aqueduct CSF flow and an axial slice at the cranio-cervical junction for foramen magnum CSF flow.…”

Section: Methodsmentioning

confidence: 99%

“…We calculated WMH volumes using a validated semi-quantitative technique described previously. (23) Briefly we generated WMH probability maps for each subject using FLAIR and T1W image data. Hyperintense outliers within the white matter surface were defined as voxels with a z score ≥ 1.5 on FLAIR to create an initial estimate of WMH volume.…”

Section: Methodsmentioning

confidence: 99%

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Intracranial functional haemodynamic relationships in patients with cerebral small vessel disease

Blair

Thrippleton

Shi

et al. 2019

Preprint

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BackgroundCerebral small vessel disease (SVD) is a major cause of stroke and dementia. The underlying cerebrovascular dysfunction is poorly understood. We investigated cerebrovascular reactivity, blood flow, vascular and cerebrospinal fluid (CSF) pulsatility, and their independent relationship to SVD features, in patients with minor ischaemic stroke and MRI evidence of SVD.MethodsWe recruited patients with minor ischaemic stroke and assessed CVR using Blood Oxygen Level Dependent (BOLD) MRI during a hypercapnic challenge, cerebral blood flow, vascular and CSF pulsatility using phase contrast MRI, and structural MR brain imaging to quantify white matter hyperintensities (WMH) and perivascular spaces (PVS). We quantified CVR in seven white matter and six subcortical grey matter regions, measured blood flow in carotid and vertebral arteries, intracranial venous sinuses, internal jugular veins and CSF flow at the aqueduct and foramen magnum. We used multiple regression to identify SVD features, blood flow and pulsatility parameters associated with CVR, controlling for patient characteristics.ResultsIn 53 of 60 patients with complete data (age 68.0±8.8, 74% male, 75% hypertensive), CVR in grey and white matter decreased with increasing blood pressure (BP, respectively −0.001%/mmHg, p=0.01 and −0.006%/mmHg, p=0.01, per mmHg increase in BP). After controlling for age, gender and systolic BP, white matter CVR decreased with increasing WMF volume (−0.01%/mmHg per log10 increase in WMH volume, p=0.02) and basal ganglia PVS (−0.01%/mmHg per point increase in PVS score, p=0.02). White matter CVR decreased with increasing venous pulsatility (superior sagittal sinus −0.03%/mmHg, p=0.02, per unit increase in pulsatility index) but not with cerebral blood flow (p=0.58). Lower foramen magnum CSF stroke volume was associated with worse white matter CVR (0.04%/mmHg per ml increase in stroke volume, p=0.04) and increased basal ganglia PVS.ConclusionsContemporaneous assessment of CVR, intracranial vascular and CSF pulsatility demonstrates important interrelationships of these vascular functions in humans. Decreased CVR, increased venous pulsatility and reduced foramen magnum CSF stroke volume suggests that dynamic vascular dysfunctions underpin PVS dysfunction and WMH development. Improved understanding of microvascular dysfunction and CSF dynamics offers new intervention targets to reduce SVD lesion development and their impact on cognitive dysfunction and stroke.

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Section: Discussionsupporting

confidence: 52%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Intracranial functional haemodynamic relationships in patients with cerebral small vessel disease

Blair

Thrippleton

Shi

et al. 2019

Preprint

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Enlarged perivascular spaces in patients with migraine: a case–control study based on 3T MRI

Yuan,

Li,

Tang

et al. 2023

Ann Clin Transl Neurol

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Objective To explore whether MRI‐visible enlarged perivascular spaces (EPVS) are associated with migraine and may serve as a predictor of migraine. Then further explore its correlation with migraine chronification. Methods A total of 231 participants (healthy control [HC] = 57, episodic migraine [EM] = 59, chronic migraine [CM] = 115) were included in this case–control study. A 3T MRI device and the validated visual rating scale were used to assess the grades of EPVS in centrum semiovale (CSO), midbrain (MB), and basal ganglia (BG). Comparisons between the two groups were made using the chi‐square or Fisher's exact tests to initially determine whether high‐grade EPVS were associated with migraine and migraine chronification. A multivariate logistic regression model was constructed to further investigate the role of high‐grade EPVS in migraine. Results The prevalence of high‐grade EPVS in CSO and MB were significantly higher in patients with migraine than in HCs (CSO: 64.94% vs. 42.11%, P = 0.002; MB: 55.75% vs. 29.82%, P = 0.001). Subgroup analysis showed no statistical difference between patients with EM and CM (CSO: 69.94% vs. 62.61%, P = 0.368; MB: 50.85% vs. 58.26%, P = 0.351). Individuals with high‐grade EPVS in CSO (odds ratio [OR]: 2.324; 95% confidence interval [CI]: 1.136–4.754; P = 0.021) and MB (OR: 3.261; 95% CI: 1.534–6.935; P = 0.002) were more likely to suffer from migraine. Interpretation This case–control study showed that high‐grade EPVS in CSO and MB in clinical practice with the underlying mechanism of dysfunction of the glymphatic system could be a predictor of migraine, but no significant correlation had been found with migraine chronification.

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High‐Spatiotemporal‐Resolution Ultrasound Flow Imaging to Determine Cerebrovascular Hemodynamics in Alzheimer's Disease Mice Model

Huang,

Hsu,

Tsai

et al. 2023

Advanced Science

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Although the relationships of cerebrovascular hemodynamic dysfunction with neurodegenerative diseases remain unclear, many studies have indicated that poor cerebral perfusion accelerates the progression of neurodegenerative diseases, such as Alzheimer's disease (AD). Small animal models are widely used in AD research. However, providing an imaging modality with a high spatiotemporal resolution and sufficiently large field of view to assess cerebrovascular hemodynamics in vivo remains a challenge. The present study proposes a novel technique for high‐spatiotemporal‐resolution vector micro‐Doppler imaging (HVμDI) based on contrast‐free ultrafast high frequency ultrasound imaging to visualize the cerebrovascular hemodynamics of the mouse, with a data acquisition time of 0.4 s, a minimal detectable vessel size of 38 µm, and a temporal resolution of 500 Hz. In vivo experiments are conducted on wild‐type and AD mice. Cerebrovascular hemodynamics are quantified using the cerebral vascular density, diameter, velocity, tortuosity, cortical flow pulsatility, and instant flow direction variations. Results reveal that AD significantly change the cerebrovascular hemodynamics. HVμDI offers new opportunities for in vivo analysis of cerebrovascular hemodynamics in neurodegenerative pathologies in preclinical animal research.

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Small vessel disease is associated with altered cerebrovascular pulsatility but not resting cerebral blood flow

Cited by 94 publications

References 53 publications

Intracranial functional haemodynamic relationships in patients with cerebral small vessel disease

Intracranial functional haemodynamic relationships in patients with cerebral small vessel disease

Enlarged perivascular spaces in patients with migraine: a case–control study based on 3T MRI

High‐Spatiotemporal‐Resolution Ultrasound Flow Imaging to Determine Cerebrovascular Hemodynamics in Alzheimer's Disease Mice Model

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