Characterizing a perfusion-based periventricular small vessel region of interest

Dolui, Sudipto; Tisdall, M. Dylan; Vidorreta, Marta; Jacobs, David R.; Nasrallah, Ilya M.; Bryan, R. Nick; Wolk, David A.; Detre, John A.

doi:10.1016/j.nicl.2019.101897

Cited by 30 publications

(45 citation statements)

References 66 publications

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“…Use of healthy subject DTI data with virtual lesions circumvented the challenges associated with performing DTI tractography in lesioned brains (24,25) and progressive ischemic PVWM lesions were simulated by varying the CBF threshold on a mean CBF map from a large cohort of middle-aged subjects, allowing the connectivity effects of PVWM lesions to be isolated from deep WM lesions that are typically seen clinically with advancing age and subcortical ischemic lesion burden. We showed that sub-threshold CBF recapitulates the pattern of PVWM lesion burden seen in an elderly cohort, as demonstrated in our prior work (28).…”

Section: Discussionsupporting

confidence: 84%

“…Fig. 1B shows a map of cerebral blood flow (CBF) in standard space derived from arterial spin labeled perfusion MRI data in 436 middle aged subjects, as described in our prior work (28). This map has been overlaid onto the same slices shown in Fig.…”

Section: White Matter Lesion Frequency Versus Periventricular Cerebramentioning

confidence: 99%

“…To simulate progressive ischemic PVWM lesions, we created a series of masks using the white matter CBF distribution map from a previous study of a large cohort of middle-aged subjects (28) and by masking that map with thresholds from 8 to 20 ml/100g/min in steps of 1 ml/100g/min. At each step, we used the mask as a region of avoidance (ROA) for DTI structural connectivity tracking on N = 30 DTI scans from young healthy subjects in the HCP S900 release.…”

Section: Virtual-lesion Dti Structural Disconnectomementioning

confidence: 99%

“…To simulate PVWM lesions, we built upon our recent work demonstrating that the distribution of PVWM hyperintensities corresponds to the distribution of white matter perfusion, which is lowest in the periventricular region (28). In our prior study, we characterized spatial variations in white matter CBF using a group CBF map obtained from a large cohort (N = 436) of middle-aged adults from the Coronary Artery Risk Development in Young Adults (CARDIA) study.…”

Section: Introductionmentioning

confidence: 99%

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Disconnectome Associated with Progressive Ischemic Periventricular White Matter Lesions

Dolui

Habes

et al. 2019

Preprint

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Periventricular white matter (PVWM) hyperintensities on T2-weighted MRI are ubiquitous in older adults and associated with dementia. Efforts to determine how PVWM lesions impact structural connectivity to impinge on brain function remain challenging in part because white matter tractography algorithms for diffusion tensor imaging (DTI) may lose fidelity in the presence of lesions. We used a “virtual lesion” approach to characterize the “disconnectome” associated with periventricular white matter (PVWM) lesions. We simulated progressive ischemic PVWM lesions using sub-threshold cerebral blood flow (CBF) masks derived from a previously published group-averaged map acquired from N=436 middle aged subjects in which the lowest CBF values were seen in PVWM and morphologically recapitulated the spatial pattern of PVWM hyperintensities seen in typical aging. We mimicked the age-dependent evolution of PVWM lesion burden by varying the threshold applied to the CBF map. We found that the optic radiations, inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, corpus callosum, temporopontine tract and fornix were affected in early simulated PVWM lesion burdens, and that the connectivity of subcortical, cerebellar, and visual regions were significantly disrupted with increasing simulated PVWM lesion burdens. We also validated the use of virtual lesions to simulate the disconnectome due to WM hyperintensities in a cognitively normal elderly cohort (N=46) by evaluating correlations between structural and functional connectomes. The virtual lesion approach provides new insights into the spatial-temporal changes of the brain structural connectome under progressive PVWM burdens during normal aging.Significance StatementWe determined the disconnectomes caused by periventricular white matter (PVWM) lesions using the “virtual lesion” approach. We validated the approach using lesions, DTI and resting-state fMRI data from elderly subjects. We simulated disconnectome of progressive PVWM lesions using cerebral blood flow (CBF) masks in PVWM region with normative DTI data, which provides specificity for an ischemic mechanism and begins to address the possibility that connectivity may be affected by reduced CBF prior to the development of overt lesions on T2-weighted FLAIR MRI. The current study presented new insights into the spatial-temporal evolutions of the brain structural connectome under progressive PVWM burdens under normal aging.

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Section: Discussionsupporting

confidence: 84%

Section: White Matter Lesion Frequency Versus Periventricular Cerebramentioning

confidence: 99%

Section: Virtual-lesion Dti Structural Disconnectomementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Disconnectome Associated with Progressive Ischemic Periventricular White Matter Lesions

Dolui

Habes

et al. 2019

Preprint

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“…Seven of the 27 newly identified cross-sectional studies investigated patients with cognitive impairment or dementia; including Alzheimer's disease (AD), 18,19 mild cognitive impairment (MCI) 8, 10, 20 and vascular cognitive impairment (VCI). 9,21 Thirteen of the 27 added cross-sectional studies investigated patients without cognitive impairment including patients with varying degrees of WMH burden, 7,16,22,23 hypertensive patients with and without SVD, 6,24,25 individuals with Cerebral Autosomal Dominant Arteriopathy with Subcortical Infarcts and Leukoencephalopathy (CADASIL), 26 cognitively normal older subjects 14,27 and patients with ischaemic stroke. 28 Two of these 13 studies investigated the effect of blood pressure reduction on CBF in SVD, from which only baseline data on CBF and WMH burden, prior to any treatment, were extracted.…”

Section: Characteristics Of Included Studiesmentioning

confidence: 99%

Associations between white matter hyperintensity burden, cerebral blood flow and transit time in small vessel disease: an updated meta-analysis

Stewart

Stringer

Shi

et al. 2020

Preprint

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Cerebral small vessel disease is a major contributor to stroke and dementia, characterised by white matter hyperintensities (WMH) on neuroimaging. WMH are associated with reduced cerebral blood flow (CBF) cross-sectionally, though longitudinal associations remain unclear. We updated a 2016 meta-analysis, identifying 30 studies, 27 cross-sectional (n=2956) and 3 longitudinal (n=440), published since 2016. Cross-sectionally, we meta-analysed 10 new studies with 24 previously reported studies, total 34 (n=2180), finding lower CBF to be associated with worse WMH burden (mean global CBF: standardised mean difference: -0.45, 95% confidence interval (CI): -0.64,-0.27). Longitudinally, the association of baseline CBF with WMH progression varied: the largest study (5 years, n=252) found no associations, while another small study (4.5 years, n=52) found that low CBF in the periventricular WMH penumbra predicted WMH progression. We could not meta-analyse longitudinal studies due to different statistical and methodological approaches. We found lower CBF within WMH compared to normal appearing white matter (novel meta-analysis; 5 cross-sectional studies; n=295; SMD: -1.51, 95% CI: -1.94,-1.07). These findings highlight that relationships between resting CBF and WMH are complex and that more longitudinal studies analysing regional CBF and subsequent WMH change are required to determine the role of CBF in small vessel disease progression.

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Association of Intensive vs Standard Blood Pressure Control With Cerebral Blood Flow

et al. 2022

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IMPORTANCEAntihypertensive treatments benefit cerebrovascular health and cognitive function in patients with hypertension, but it is uncertain whether an intensive blood pressure target leads to potentially harmful cerebral hypoperfusion.OBJECTIVE To investigate the association of intensive systolic blood pressure (SBP) control vs standard control with whole-brain cerebral blood flow (CBF). DESIGN, SETTING, AND PARTICIPANTSThis substudy of the Systolic Blood Pressure Intervention Trial (SPRINT) randomized clinical trial compared the efficacy of 2 different blood pressure-lowering strategies with longitudinal brain magnetic resonance imaging (MRI) including arterial spin labeled perfusion imaging to quantify CBF. A total of 1267 adults 50 years or older with hypertension and increased cardiovascular risk but free of diabetes or dementia were screened for the SPRINT substudy from 6 sites in the US. Randomization began in November 2010 with final follow-up MRI in July 2016. Analyses were performed from September 2020 through December 2021.INTERVENTIONS Study participants with baseline CBF measures were randomized to an intensive SBP target less than 120 mm Hg or standard SBP target less than 140 mm Hg. MAIN OUTCOMES AND MEASURESThe primary outcome was change in whole-brain CBF from baseline. Secondary outcomes were change in gray matter, white matter, and periventricular white matter CBF. RESULTS Among 547 participants with CBF measured at baseline, the mean (SD) age was 67.5 (8.1) years and 219 (40.0%) were women; 315 completed follow-up MRI at a median (IQR) of 4.0 (3.7-4.1) years after randomization. Mean whole-brain CBF increased from 38.90 to 40.36 (difference, 1.46 [95% CI,) mL/100 g/min in the intensive treatment group, with no mean increase in the standard treatment group (37.96 to 37.12; difference, -0.84 [95% CI, -2.30 to 0.61] mL/100 g/min; between-group difference, 2.30 [95% CI, 0.30-4.30; P = .02]). Gray, white, and periventricular white matter CBF showed similar changes. The association of intensive vs standard treatment with CBF was generally similar across subgroups defined by age, sex, race, chronic kidney disease, SBP, orthostatic hypotension, and frailty, with the exception of an indication of larger mean increases in CBF associated with intensive treatment among participants with a history of cardiovascular disease (interaction P = .05). CONCLUSIONS AND RELEVANCEIntensive vs standard antihypertensive treatment was associated with increased, rather than decreased, cerebral perfusion, most notably in participants with a history of cardiovascular disease.

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Characterizing a perfusion-based periventricular small vessel region of interest

Cited by 30 publications

References 66 publications

Disconnectome Associated with Progressive Ischemic Periventricular White Matter Lesions

Disconnectome Associated with Progressive Ischemic Periventricular White Matter Lesions

Associations between white matter hyperintensity burden, cerebral blood flow and transit time in small vessel disease: an updated meta-analysis

Association of Intensive vs Standard Blood Pressure Control With Cerebral Blood Flow

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