Completion of the Circle of Willis Varies by Gender, Age, and Indication for Computed Tomography Angiography

doi:10.1016/j.wneu.2017.07.084

World Neurosurgery

Volume 106, October 2017, Pages 953-963

https://doi.org/10.1016/j.wneu.2017.07.084 Get rights and content

Objective

The circle of Willis (CoW) is the foremost anastomosis and blood distribution center of the brain. Its effectiveness depends on its completion and the size and patency of its vessels. Gender-related and age-related anatomic variations in the CoW may play an important role in the pathogenesis of cerebrovascular diseases. In this study, we analyzed computed tomography angiograms (CTAs) to assess for differences in CoW completion related to gender, age, and indication for CTA.

Methods

A total of 834 CTAs were retrospectively analyzed for all CoW vessels to compare the incidence of complete CoW and variation frequency based on gender, age, and indication.

Results

The incidence of complete CoW was 37.1% overall. CoW completion showed a statistically significant decrease with increasing age for all age groups in both men (47.0%, 29.4%, 18.8%) and women (59.1%, 44.2%, 30.9%). Completion was greater in women (43.8%) than in men (31.2%) overall and for all age groups. These gender differences were all statistically significant except for the 18–39 years age group. The most frequent of the 28 CoW variations were absent posterior communicating artery (PCOM) bilaterally (17.1%), right PCOM (15.3%), and left PCOM (10.9%). Ischemic stroke and the 18–39 years age group of hemorrhagic stroke showed a statistically significant reduction in completion relative to trauma.

Conclusions

The incidence of complete CoW is likely greater in women for all age groups and likely decreases with age in both genders. The most frequently absent vessel is likely the PCOM, either unilaterally or bilaterally. Completion may play a role in ischemic stroke and a subset of patients with hemorrhagic stroke.

Introduction

The circle of Willis (CoW) is the foremost anastomosis and blood distribution center of the brain. However, its effectiveness is dependent on its completeness and the size and patency of its vessels. The clinical relevance of variations in CoW morphology caused by blood redistribution is becoming increasingly evident. Hemodynamic analyses have shown that occlusion in one vessel results in blood flow redirection to the other vessels and reduced collateral flow1, 2, 3, 4, 5 and that these differences can lead to measurable and clinically relevant ischemia, including stroke.2, 3, 6, 7, 8, 9, 10

Because of this increasingly apparent role in cerebral hemodynamics and ischemia, it is possible that CoW morphology may be a significant risk factor for the development of cerebrovascular disease (CVD). Collateral circulation was found to reduce the risk of transient ischemic attack and ischemic stroke, including disabling and fatal strokes.8, 9, 11, 12, 13, 14, 15 Similarly, a complete CoW was associated with reduced stroke severity, recurrence, and death as well as better recovery.⁹ With respect to aneurysms, there is substantial evidence showing a correlation between incomplete CoW variations and higher incidence of aneurysm.4, 16, 17, 18 An incomplete CoW was also correlated with an increased rate of aneurysm in patients with a family history of stroke.¹⁹ The pathophysiologic mechanisms for the role of CoW variations in aneurysm formation are beginning to be elucidated.4, 20 For example, Nam et al.²⁰ found that CoW variations may induce aneurysm formation caused by increased shear stress on the vessel wall. These results suggest that, in addition to the many other risk factors for cardiovascular disease, incomplete CoW morphology may be an additional and potentially major risk factor for CVD development and severity as well as recovery from its sequelae.

There is substantial evidence for both age-dependent and gender-dependent differences in parameters related to CVD. Di Carlo et al.²¹ and Appelros et al.²² found that males had a significantly higher incidence and prevalence of ischemic stroke than did females, were younger at the time of their first stroke, and had a higher incidence of TIA before stroke. However, females had increased stroke severity and case fatality and were more likely to develop disability and handicap.21, 22 In contrast, women have been found to have a higher incidence of cerebral aneurysm and subarachnoid hemorrhage.16, 22 Importantly, gender-related differences in the locations of aneurysms have also been found. Horikoshi et al.¹⁶ found that men had more aneurysms along the anterior communicating artery (ACOM) and middle cerebral artery, whereas women had more on the internal carotid artery and vertebrobasilar system. Men were also found to have a significantly higher rate of aneurysm rupture at the ACOM, whereas women had a higher rupture rate at the internal carotid artery.²³ Similarly, the rate of hospitalizations for stroke also increases with age.²⁴

An emerging hypothesis is that gender- and age-related anatomic variations in the CoW may play an important role in the pathogenesis of gender- and age-related differences in the rates and distribution patterns of CVD. In this study, we conducted the largest imaging analysis of CoW morphology with respect to gender- and age-related differences to date.

Section snippets

Patients

This study was approved by the institutional review board at the Banner University Medical Center-Tucson. All CT angiograms (CTAs) of the head or the head/neck performed at Banner University Medical Center-Tucson in 2014–2016 were retrospectively assessed for the presence of all of CoW vessels by the first and senior authors. Exclusion criteria consisted of pediatric cases, cases in which vessels could not be visualized, and cases in which CTA slices were >1 mm thick. A total of 834 individual

Demographics

A total of 834 patients (age range, 18–95.9 years; mean, 55.8 years) were included in this study, consisting of 446 men (mean, 55.4 years) and 388 women (mean, 56.4 years). These patients were categorized into 6 groups consisting of 115 men aged 18–39.9 years (mean, 29.9 years), 214 men aged 40–69.9 years (mean, 56.3 years), 117 men aged ≥70 years (mean, 78.8 years), 88 women aged 18–39.9 years (mean, 28.6 years), 190 women aged 40–69.9 years (mean, 55.7 years), and 110 women aged ≥70 years

Discussion

The relevance of the collateral circulation afforded by a complete CoW in clinical disease is becoming increasingly evident. In recent years, there has been growing interest in the study of CoW morphology in an effort to elucidate potentially clinically relevant variations in different populations. In this study, we analyzed 834 CTAs and found an overall CoW completion rate of 37.1%. Several other studies have assessed the rate of CoW completion; however, their results vary substantially (

Conclusions

There is increasing evidence of the clinical importance of CoW completion with respect to CVD. However, variations from the classic, functionally complete CoW are common and are likely more common as a group than is the classic CoW. There are few studies reporting gender- or age-related differences in CoW completion. Our results are consistent with the overall trends of previous studies that seem to be that CoW completion decreases with increasing age and is more common in women than in men.

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Cited by (33)

The Importance of the Circle of Willis in Carotid Interventions Outcomes: A Real-Life Study
2024, Annals of Vascular Surgery
The main objective of this study is to evaluate and compare the outcomes regarding operative mortality rate, ipsilateral stroke, and overall survival rate among patients with internal carotid artery stenosis submitted to carotid endarterectomy (CEA) or stenting regarding the completeness of circle of Willis (CoW).
Prospective, consecutive cohort study of patients submitted to carotid interventions (CEA and carotid stenting: CAS) for internal carotid artery stenosis diagnosis evaluated according complete or incomplete CoW. The patients were divided into 2 groups: group I, the patients with complete CoW and group II, the patients with incomplete CoW, with the disruption of anterior and/or ipsilateral posterior circulation, regarding the ipsilateral significant carotid stenosis.
Overall, 98 patients submitted to carotid intervention were evaluated. Two groups of patients were identified: group CoW complete with 54 patients and group CoW incomplete with 44 patients. Regarding the type of intervention, the prevalence of CAS in CoW complete group and CoW incomplete group were statistically similar (54.1% vs. 55.1%, P = 0.22). Notwithstanding, CEA was also statistically similar in CoW incomplete group and CoW complete group (44.2% vs. 45.9%, P = 0.22). The perioperative mortality rate was 2% in total cohort (2 patients), with no differences among CoW complete and incomplete groups (3.7% vs. 0%, P = 0.50, respectively). Furthermore, the incidence of postoperative stroke was 3.1% (asymptomatic 2%, symptomatic 1.1%), with no differences among CoW complete and incomplete groups (3.7% vs. 2.3%, P = 0.68, respectively). A univariate and multivariate linear regression showed that among the factors evaluated, only chronic kidney failure was related with hazard ratio = 1.89, P = 0.003, confidence interval 1.058–2.850.
The completeness of the CoW, independently of the type of carotid intervention (CEA and CAS), did not interfere in the results regarding postoperative outcomes for stroke and death. Chronic kidney disease was associated to increased risk of perioperative stroke.
Anatomical variations in the circle of Willis are associated with increased odds of intracranial aneurysms: The Tromsø study
2023, Journal of the Neurological Sciences
Studies on patients suggest an association between anatomical variations in the Circle of Willis (CoW) and intracranial aneurysms (IA), but it is unclear whether this association is present in the general population. In this cross-sectional population study, we investigated the associations between CoW anatomical variations and IA.
We included 1667 participants from a population sample with 3 T MRI time-of-flight angiography (40–84 years, 46.5% men). Saccular IAs were defined as protrusions in the intracranial arteries ≥2 mm, while variants of the CoW were classified according to whether segments were missing or hypoplastic (< 1 mm). We used logistic regression, adjusting for age and IA risk factors, to assess whether participants with incomplete CoW variants had a greater prevalence of IA and whether participants with specific incomplete variants had a greater prevalence of IA.
Participants with an incomplete CoW had an increased prevalence of IA (OR, 2.3 [95% CI 1.05–5.04]). This was mainly driven by the variant missing all three communicating arteries (OR, 4.2 [95% CI 1.7–1 0.3]) and the variant missing the P1 segment of the posterior cerebral artery (OR, 3.6 [95% CI 1.2–10.1]). The combined prevalence of the two variants was 15.4% but accounted for 28% of the IAs.
The findings suggest that an incomplete CoW is associated with an increased risk of IA for adults in the general population.
Incomplete circle of Willis variants and stroke outcome
2022, European Journal of Radiology
Citation Excerpt :
Vertebral artery A/H was not related to stroke outcome. The reported prevalence of CoW variants may vary greatly depending on assessment methods [4,22,23]. In this study, 34% of patients had an incomplete CoW, a lower rate than reported in many other studies.
There is considerable variation in circle of Willis morphology among the general population, and these variations have been correlated with risk of aneurysms, cerebral ischemia, and other clinical events.
To investigate the relationship between circle of Willis variants and stroke outcome.
We performed a retrospective study involving 297 patients from our institution’s acute stroke academic registry. All received MRA examinations of the head upon admission for acute strokes. All imaging was reviewed to assess for circle of Willis variants (particularly A1 and P1 aplasia or hypoplasia) along with vertebral artery aplasia or hypoplasia. Stroke outcome was defined as good (walking independently at the time of discharge) or poor (inability to walk at discharge, assistance needed to walk at discharge, or death). Severity of stroke was assessed using the National Institute of Health Stroke Scale.
An incomplete circle of Willis was seen in 34% of subjects. There was no significant association between age, gender, hypertension, or presence of arterial stenosis and circle of Willis completeness. Using logistic regression, we found that the presence of an incomplete circle of Willis decreased the odds of a stroke patient having a good outcome by 47% (p = 0.046, OR 0.53, 95% CI 0.281–0.988), after adjusting for age and severity of stroke at admission.
This study suggests that an incomplete circle of Willis may be associated with a poorer prognosis for stroke patients.
Validation of an Oscillation Test for the Sonographic Assessment of Fetal-Type Posterior Cerebral Artery Variants in Migraine Patients with Visual Aura
2022, Ultrasound in Medicine and Biology
Anatomic variants of the posterior circle of Willis, including the fetal-type posterior cerebral artery (FPCA), may contribute to the formation of visual aura in migraine. We sought to validate an oscillation test to investigate FPCA frequency in migraine using transcranial color-coded duplex ultrasonography (TCCS). First, the diagnostic accuracy of the oscillation test used to identify FPCA variants by TCCS was assessed in stroke patients with available computed tomography angiography (CTA) as the set gold standard. Second, in a cross-sectional study, patients with migraine with visual aura (MWVA) and migraine without aura (MWOA), as well as healthy controls, were prospectively recruited for sonographic assessment of FPCA variants. We compared FPCA frequency between migraine patients and controls using χ²-testing and performed logistic regression analysis to investigate a potential association between MWVA and the presence of FPCA variants. Specificity, sensitivity and positive and negative predictive values for sonographic identification of FPCA with CTA as the set gold standard were 93%, 77%, 63% and 96% (partial FPCA) and 99%, 78%, 88% and 98% (complete FPCA), respectively. One hundred forty-two migraine patients (39 ± 12 y, 90 MWVA and 52 MWOA) and 49 healthy controls (31 ± 12 y) were recruited. The χ² testing did not reveal significant differences in FPCA frequency as assessed by TCCS (unilateral or bilateral, partial and/or complete) between migraine patients and controls (MWVA: 40/90 or 44.4%, MWOA: 22/52 or 42.3%, controls: 24/49 or 49%, p = 0.79). Similarly, the frequencies of partial FPCA (p = 0.61) and complete FPCA (p = 0.27) did not vary significantly among groups. Logistic regression analysis revealed no interaction effect between migraine diagnosis and FPCA prevalence (any FPCA), when adjusted for age and sex. The sonographic oscillation test can be used as a non-invasive method to identify partial and complete FPCA variants with high specificity and reasonable sensitivity. Our findings suggest that FPCA variants do not contribute to the formation of visual migraine aura.
Posterior Communicating Artery Hypoplasia: A Risk Factor for Vertebral Artery Dissection Causing Subarachnoid Hemorrhage
2022, Journal of Stroke and Cerebrovascular Diseases
Citation Excerpt :
Zaninovich et al. reported that bilateral absence of PCoA was detected in approximately 19% of patients. However, they assessed a population that included 36% stroke patients and 7% patients with unruptured aneurysms.13 Li et al. conducted a CTA study among 160 Chinese healthy adults.
Subarachnoid hemorrhage due to vertebral artery dissection is often fatal; however, its anatomical predictors remain unclear. We conducted a retrospective hospital-based case-control study to evaluate whether variations in the posterior communicating artery are associated with the risk of vertebral artery dissection with subarachnoid hemorrhage.
We obtained data from patients who underwent computed tomography angiography at our hospital between April 2010 and March 2020. Based on the connection between the anterior and posterior circulation of the arterial circle of Willis, the patients were categorized into a separated group (posterior communicating artery hypoplasia) and a connected group (all others). We evaluated the association between the development of posterior communicating artery and subarachnoid hemorrhage due to vertebral artery dissection using multivariate logistic regression analysis.
Thirty-eight patients had subarachnoid hemorrhage due to vertebral artery dissection and 76 were identified as age- and sex-matched controls. In conditional multivariate logistic regression analysis, the separated group showed a significant association with subarachnoid hemorrhage due to vertebral artery dissection, with an adjusted odds ratio of 2.8 (95% confidence interval, 1.2–6.5; P = 0.021).
The present study demonstrates that posterior communicating artery hypoplasia may be associated with subarachnoid hemorrhage due to vertebral artery dissection. Our results highlight the importance of anatomical variations in the cerebral artery and provide evidence to help develop preventive measures against strokes.
The role of diffuse correlation spectroscopy and frequency-domain near-infrared spectroscopy in monitoring cerebral hemodynamics during hypothermic circulatory arrests
2021, JTCVS Techniques
Citation Excerpt :
However, these established flow rates are largely based on the empiric data and retrospective studies, with no direct cerebral perfusion measurements supporting it. Also, older patients may have a partially degraded circle of Willis, potentially compromising contralateral brain perfusion.34 If the contralateral SO2 levels drop during HCA with ACP, the clinicians may ask to raise perfusion pressure or increase CPB flow to facilitate left brain hemisphere perfusion.
Real-time noninvasive monitoring of cerebral blood flow (CBF) during surgery is key to reducing mortality rates associated with adult cardiac surgeries requiring hypothermic circulatory arrest (HCA). We explored a method to monitor cerebral blood flow during different brain protection techniques using diffuse correlation spectroscopy (DCS), a noninvasive optical technique which, combined with frequency-domain near-infrared spectroscopy (FDNIRS), also provides a measure of oxygen metabolism.
We used DCS in combination with FDNIRS to simultaneously measure hemoglobin oxygen saturation (SO₂), an index of cerebral blood flow (CBF_i), and an index of cerebral metabolic rate of oxygen (CMRO_2i) in 12 patients undergoing cardiac surgery with HCA.
Our measurements revealed that a negligible amount of blood is delivered to the cerebral cortex during HCA with retrograde cerebral perfusion, indistinguishable from HCA-only cases (median CBF_i drops of 93% and 95%, respectively) with consequent similar decreases in SO₂ (mean decrease of 0.6 ± 0.1% and 0.9 ± 0.2% per minute, respectively); CBF_i and SO₂ are mostly maintained with antegrade cerebral perfusion; the relationship of CMRO_2i to temperature is given by CMRO_2i = 0.052e^0.079T.
FDNIRS-DCS is able to detect changes in CBF_i, SO₂, and CMRO_2i with intervention and can become a valuable tool for optimizing cerebral protection during HCA.

View all citing articles on Scopus

: Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Original ArticleCompletion of the Circle of Willis Varies by Gender, Age, and Indication for Computed Tomography Angiography

Objective

Methods

Results

Conclusions

Introduction

Section snippets

Patients

Demographics

Discussion

Conclusions

J Vasc Surg

J Clin Neurosci

Dev Biol

J Clin Neurosci

Clin Radiol

Computation of hemodynamics in the circle of Willis

Stroke

SPECT measurements of regional cerebral perfusion and carbondioxide reactivity: correlation with cerebral collaterals in internal carotid artery occlusive disease

J Neurol

Planning-free cerebral blood flow territory mapping in patients with intracranial arterial stenosis

J Cereb Blood Flow Metab

An experimental investigation of the hemodynamic variations due to aplastic vessels within three-dimensional phantom models of the circle of Willis

Ann Biomed Eng

Circle of Willis collateral flow investigated by magnetic resonance angiography

Stroke

Anterior cerebral artery A1 segment hypoplasia may contribute to A1 hypoplasia syndrome

Eur Neurol

The clinical relevance of fetal variant of the circle of Willis and its influence on the cerebral collateral circulation

Acta Neurol Taiwan

Absent collateral function of the circle of Willis as risk factor for ischemic stroke

Cerebrovasc Dis

Correlation between the integrity of the circle of Willis and the severity of initial noncardiac cerebral infarction and clinical prognosis

Medicine (Baltimore)

Clinical significance of the circle of Willis in intracranial atherosclerotic stenosis

J Neurointerv Surg

Group for the NASCET (NASCET). Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis

Stroke

The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation

Ann Intern Med

The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction

N Engl J Med

The variable clinical and CT findings after carotid occlusion: the role of collateral blood supply

J Neurol Neurosurg Psychiatry

Magnetic resonance angiographic evidence of sex-linked variations in the circle of willis and the occurrence of cerebral aneurysms

J Neurosurg

Association of aneurysms and variation of the A1 segment

J Neurointerv Surg

Cerebral aneurysms and variations in the circle of Willis

Stroke

CTA Characteristics of the circle of Willis and intracranial aneurysm in a Chinese crowd with family history of stroke

Biomed Res Int

Evaluation of aneurysm-associated wall shear stress related to morphological variations of circle of Willis using a microfluidic device

J Biomech

Sex differences in the clinical presentation, resource use, and 3-month outcome of acute stroke in Europe: data from a multicenter multinational hospital-based registry

Stroke

Sex differences in stroke epidemiology: a systematic review

Stroke

Presence of anatomical variations of the circle of Willis in patients undergoing surgical treatment for ruptured intracranial aneurysms

Vojnosanit Pregl Mil Med Pharm J Serbia

Hospitalization for Stroke in Key Findings in U.S. hospitals, 1989–2009. NCHS Data Brief, No 95

Age patterns of geriatric disease incidences in the U.S. elderly population: Medicare-based analysis

J Am Geriatr Soc

Magnetic resonance angiographic evaluation of circulus arteriosus cerebri (circle of Willis): a morphologic study in 100 human healthy subjects

Ital J Anat Embryol

Assessment of the circle of Willis with cranial tomography angiography

Med Sci Monit Int Med J Exp Clin Res

Original Article
Completion of the Circle of Willis Varies by Gender, Age, and Indication for Computed Tomography Angiography