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Cerebral blood flow distribution, collateral function and pulsatility in healthy and in patients with symptomatic carotid stenosis : a magnetic resonance imaging approach
Umeå University, Faculty of Medicine, Department of Pharmacology and Clinical Neuroscience, Clinical Neuroscience. Umeå University, Faculty of Medicine, Department of Radiation Sciences.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Cerebralt blodflöde med fokus på blodflödesfördelning, kollateraler och artärpulsationer, hos friska och hos patienter med symtomatisk karotisstenos : en tillämpning med magnetisk resonanstomografi (Swedish)
Abstract [en]

Background: For the detection and treatment of early cerebral vascular disease it is of paramount importance to first understand the normal physiology of the cerebral vasculature, and subsequently, to understand how and when pathology can develop from that. This is especially important as the population above 65 years of age is increasing and aging itself is an established risk factor for the development of cerebral vascular disease. This, however, is not always an easy task, since there is a subtle balance and overlap between age-related physiological and pathophysiological changes in the arterial system. Atherosclerotic changes that lead to the development of carotid artery stenosis are responsible for about one fifth of all ischemic strokes. Today, the current state of evidence and the algorithm for carotid revascularization is mainly focused on the degree of carotid stenosis and not on its impact on cerebral hemodynamics. One reason for this is the lack of a non-invasive method, that allows for repeated investigations and provides accurate and reliable results to study cerebral hemodynamic changes. The overall aim of this thesis was to explore and develop a comprehensive approach to investigate the cerebral blood flow distribution, collateral function and pulsatility in healthy subjects and in patients with symptomatic carotid stenosis using a phase-contrast magnetic resonance imaging (PCMRI) platform. The thesis is based on four scientific papers (papers I—IV). 

Methods: In papers I and II, 49 healthy young (mean 25 years) and 45 healthy elderly (mean 71 years) subjects were included. 2D PCMRI was used to assess cerebral blood flow rate (BFR), pulsatility index (PI) and dampening factor (DF) in 15 cerebral arteries and in the ophthalmic arteries (OA). Thirty-eight patients (mean 72 years) with symptomatic carotid stenosis were included in paper III. Nineteen of these patients (mean 71 years) underwent carotid endarterectomy (CEA) (paper IV). 4D PCMRI was used for BFR assessment in papers III and IV. BFR, its distribution and collateral routes, was measured in 17 cerebral arteries and in the OA. The BFR on ipsilateral side (with symptomatic stenosis) was compared to the contralateral side (papers III and IV). BFR laterality was defined as contralateral BFR minus ipsilateral BFR in paired arteries and, BFR was compared before and after CEA (paper IV).

Results: On average, in healthy subjects, 72% of the total cerebral blood flow (tCBF) was distributed through the anterior circulation and 28% through the posterior circulation. The distribution was symmetrical and not affected by age, sex, or brain volume (paper I). Aging resulted in lower BFRs, increased pulsatility and reduced dampening capacity in cerebral arteries. Anatomical variations in the circle of Willis resulted in an asymmetrical distribution of blood flow (papers I and II). In patients with carotid stenosis, a lower BFR was found in the internal carotid artery (ICA) and its branches on the ipsilateral side. The anterior cerebral artery territory was bilaterally, primarily, supplied by the contralateral ICA. In addition to the supply through the ICA, the middle cerebral artery (MCA) territory on the ipsilateral side was secured by collateral supply from the OA and the posterior communicating arteries, seen as retrograde flow in those arteries. Despite these compensations, BFR in ipsilateral side MCA was lower, and this laterality was more pronounced in patients with severe carotid stenosis (≥70%). After CEA, the distribution of BFR going into the cerebral arteries was found to be symmetrically distributed. Total CBF increased postoperatively in patients with collateral recruitment preoperatively (n=9). The BFR laterality in MCA observed prior to CEA, was found only in the group of patients with collateral recruitment preoperatively (paper IV). The degree of stenosis did not differ between the groups with and without collateral recruitment. 

Conclusions: This thesis provides a new and comprehensive approach to mapping and quantifying normal cerebral blood flow and pulsatility. By presenting the distribution of tCBF going into cerebral arteries, instead of using absolute values, the effect of age could be neutralized and the results can be applicable when describing healthy cerebral blood flow, regardless of age. 4D PCMRI made it possible to describe the altered blood flow distribution and collateral ranking in patients with carotid stenosis prior to CEA and its normalization after the procedure. Our findings highlight the importance of BFR quantification for understanding cerebral hemodynamics in patients with carotid stenosis. 4D PCMRI technique is a promising clinical tool for investigations of cerebral hemodynamics in patients with stroke.

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2019. , p. 63
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2023
Keywords [en]
Aging, Arterial pulsatility, Carotid stenosis, Cerebral arteries, Cerebral blood flow, Cerebral collateral blood flow, Circle of Willis, Phase contrast magnetic resonance imaging
National Category
Neurology
Identifiers
URN: urn:nbn:se:umu:diva-158834ISBN: 978-91-7855-036-4 (print)OAI: oai:DiVA.org:umu-158834DiVA, id: diva2:1314809
Public defence
2019-06-05, Hörsal B, Unod T9, Norrlands universitetssjukhus, Umeå, 13:00 (English)
Opponent
Supervisors
Funder
Swedish Heart Lung Foundation, 20140592Swedish Research Council, 2015-05616Available from: 2019-05-15 Created: 2019-05-09 Last updated: 2019-05-14Bibliographically approved
List of papers
1. Blood flow distribution in cerebral arteries
Open this publication in new window or tab >>Blood flow distribution in cerebral arteries
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2015 (English)In: Journal of Cerebral Blood Flow and Metabolism, ISSN 0271-678X, E-ISSN 1559-7016, Vol. 35, no 4, p. 648-654Article in journal (Refereed) Published
Abstract [en]

High-resolution phase-contrast magnetic resonance imaging can now assess flow in proximal and distal cerebral arteries. The aim of this study was to describe how total cerebral blood flow (tCBF) is distributed into the vascular tree with regard to age, sex and anatomic variations. Forty-nine healthy young (mean 25 years) and 45 elderly (mean 71 years) individuals were included. Blood flow rate (BFR) in 21 intra-and extracerebral arteries was measured. Total cerebral blood flow was defined as BFR in the internal carotid plus vertebral arteries and mean cerebral perfusion as tCBF/brain volume. Carotid/vertebral distribution was 72%/28% and was not related to age, sex, or brain volume. Total cerebral blood flow (717 +/- 123 mL/min) was distributed to each side as follows: middle cerebral artery (MCA), 21%; distal MCA, 6%; anterior cerebral artery (ACA), 12%, distal ACA, 4%; ophthalmic artery, 2%; posterior cerebral artery (PCA), 8%; and 20% to basilar artery. Deviating distributions were observed in subjects with 'fetal' PCA. Blood flow rate in cerebral arteries decreased with increasing age (P < 0.05) but not in extracerebral arteries. Mean cerebral perfusion was higher in women (women: 61 +/- 8; men: 55 +/- 6 mL/min/100 mL, P < 0.001). The study describes a new method to outline the flow profile of the cerebral vascular tree, including reference values, and should be used for grading the collateral flow system.

Keywords
aging, cerebral blood flow, circle of Willis, cognitive impairment, phase-contrast MRI, stroke
National Category
Clinical Medicine
Identifiers
urn:nbn:se:umu:diva-103545 (URN)10.1038/jcbfm.2014.241 (DOI)000352027900015 ()25564234 (PubMedID)
Available from: 2015-05-25 Created: 2015-05-21 Last updated: 2019-05-09Bibliographically approved
2. Aging alters the dampening of pulsatile blood flow in cerebral arteries
Open this publication in new window or tab >>Aging alters the dampening of pulsatile blood flow in cerebral arteries
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2016 (English)In: Journal of Cerebral Blood Flow and Metabolism, ISSN 0271-678X, E-ISSN 1559-7016, Vol. 36, no 9, p. 1519-1527Article in journal (Refereed) Published
Abstract [en]

Excessive pulsatile flow caused by aortic stiffness is thought to be a contributing factor for several cerebrovascular diseases. The main purpose of this study was to describe the dampening of the pulsatile flow from the proximal to the distal cerebral arteries, the effect of aging and sex, and its correlation to aortic stiffness. Forty-five healthy elderly (mean age 71 years) and 49 healthy young (mean age 25 years) were included. Phase-contrast magnetic resonance imaging was used for measuring blood flow pulsatility index and dampening factor (proximal artery pulsatility index/distal artery pulsatility index) in 21 cerebral and extra-cerebral arteries. Aortic stiffness was measured as aortic pulse wave velocity. Cerebral arterial pulsatility index increased due to aging and this was more pronounced in distal segments of cerebral arteries. There was no difference in pulsatility index between women and men. Dampening of pulsatility index was observed in all cerebral arteries in both age groups but was significantly higher in young subjects than in elderly. Pulse wave velocity was not correlated with cerebral arterial pulsatility index. The increased pulsatile flow in elderly together with reduced dampening supports the pulse wave encephalopathy theory, since it implies that a higher pulsatile flow is reaching distal arterial segments in older subjects.

National Category
Radiology, Nuclear Medicine and Medical Imaging
Identifiers
urn:nbn:se:umu:diva-126505 (URN)10.1177/0271678X16629486 (DOI)000382996800004 ()26823470 (PubMedID)
Available from: 2016-10-27 Created: 2016-10-10 Last updated: 2019-05-09Bibliographically approved
3. Blood flow lateralization and collateral compensatory mechanisms in patients with carotid artery stenosis
Open this publication in new window or tab >>Blood flow lateralization and collateral compensatory mechanisms in patients with carotid artery stenosis
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2019 (English)In: Stroke, ISSN 0039-2499, E-ISSN 1524-4628, Vol. 50, no 5, p. 1081-1088Article in journal (Refereed) Published
Abstract [en]

Background and Purpose: Four-dimensional phase-contrast magnetic resonance imaging enables quantification of blood flow rate (BFR; mL/min) in multiple cerebral arteries simultaneously, making it a promising technique for hemodynamic investigation in patients with stroke. The aim of this study was to quantify the hemodynamic disturbance and the compensatory pattern of collateral flow in patients with symptomatic carotid stenosis.

Methods: Thirty-eight patients (mean, 72 years; 27 men) with symptomatic carotid stenosis (>/=50%) or occlusion were investigated using 4-dimensional phase-contrast magnetic resonance imaging. For each patient, BFR was measured in 19 arteries/locations. The ipsilateral side to the symptomatic carotid stenosis was compared with the contralateral side.

Results: Internal carotid artery BFR was lower on the ipsilateral side (134+/-87 versus 261+/-95 mL/min; P<0.001). BFR in anterior cerebral artery (A1 segment) was lower on ipsilateral side (35+/-58 versus 119+/-72 mL/min; P<0.001). Anterior cerebral artery territory bilaterally was primarily supplied by contralateral internal carotid artery. The ipsilateral internal carotid artery mainly supplied the ipsilateral middle cerebral artery (MCA) territory. MCA was also supplied by a reversed BFR found in the ophthalmic and the posterior communicating artery routes on the ipsilateral side (-5+/-28 versus 10+/-28 mL/min, P=0.001, and -2+/-12 versus 6+/-6 mL/min, P=0.03, respectively). Despite these compensations, BFR in MCA was lower on the ipsilateral side, and this laterality was more pronounced in patients with severe carotid stenosis (>/=70%). Although comparing ipsilateral MCA BFR between stenosis groups (<70% and >/=70%), there was no difference ( P=0.95).

Conclusions: With a novel approach using 4-dimensional phase-contrast magnetic resonance imaging, we could simultaneously quantify and rank the importance of collateral routes in patients with carotid stenosis. An important observation was that contralateral internal carotid artery mainly secured the bilateral anterior cerebral artery territory. Because of the collateral recruitment, compromised BFR in MCA is not necessarily related to the degree of carotid stenosis. These findings highlight the importance of simultaneous investigation of the hemodynamics of the entire cerebral arterial tree.

Place, publisher, year, edition, pages
Philadelphia: Lippincott Williams & Wilkins, 2019
Keywords
carotid stenosis, circle of Willis, humans, magnetic resonance imaging, cine, middle cerebral artery
National Category
Cardiac and Cardiovascular Systems
Identifiers
urn:nbn:se:umu:diva-158003 (URN)10.1161/STROKEAHA.119.024757 (DOI)000469350000029 ()30943887 (PubMedID)
Funder
Swedish Research Council, 2015-05616Swedish Research Council, 2017-04949Västerbotten County CouncilSwedish Heart Lung Foundation, 20140592
Available from: 2019-04-10 Created: 2019-04-10 Last updated: 2019-11-19Bibliographically approved
4. Quantification and mapping of cerebral hemodynamics before and after carotid endarterectomy: a 4D PCMRI study
Open this publication in new window or tab >>Quantification and mapping of cerebral hemodynamics before and after carotid endarterectomy: a 4D PCMRI study
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Background and purpose: A carotid stenosis can have a profound impact on the cerebral hemodynamics that cannot be inferred from the degree of stenosis by itself. We aimed to quantify and map the distribution of blood flow rate (BFR) in cerebral arteries before and after carotid endarterectomy (CEA), using four-dimensional phase-contrast magnetic resonance imaging (4D PCMRI).

Methods: Nineteen patients (71±6 years, 2 women) with symptomatic carotid stenosis (≥50%)undergoing CEA were investigated using 4D PCMRI before and after surgery. BFR was measured in 17 cerebral arteries and in the ophthalmic arteries (OA). Collateral recruitment through the anterior and posterior communicating arteries, OA and the leptomeningeal arterial route was identified and quantified. BFR laterality was described as contralateral BFR minus ipsilateral BFR in paired arteries.

Results: Total cerebral blood flow increased by 15% (p<0.01) after CEA. On the ipsilateral side, increased BFR was found after CEA in internal carotid artery (ICA) (246±62mL/min vs. 135±80mL/min; p<0.001), anterior cerebral artery (87±mL/min vs. 38±58mL/min; p<0.01) and middle cerebral artery (MCA) (149±43mL/min vs. 119±34mL/min; p<0.01), resulting in a postoperative BFR distribution without signs of laterality. In patients with preoperatively recruited collaterals (n=9), BFR laterality was found in MCA before, but not after, CEA (p<0.01). This laterality was not found in patients without collateral recruitment (n=10) (p=0.2). The degree of stenosis did not differ between the groups with vs. without collateral recruitment (p=0.85). 

Conclusion: 4D PCMRI is a useful technique to quantify cerebral hemodynamic changes seen in patients with carotid stenosis before and after CEA. MCA laterality, seen in patients with collateral recruitment before CEA, pointed towards a hemodynamic disturbance in MCA territory for those patients. This study introduces a new and non-invasive way to evaluate cerebral hemodynamics due to carotid stenosis prior to and after CEA.

Keywords
Stroke, Carotid stenosis, Carotid endarterectomy, Cerebral blood flow, Phase-contrast MRI, Circle of Willis
National Category
Neurology
Identifiers
urn:nbn:se:umu:diva-158833 (URN)
Funder
Swedish Research Council, 2015-05616Swedish Heart Lung Foundation, 20140592
Available from: 2019-05-09 Created: 2019-05-09 Last updated: 2019-05-14

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