A Review of the Circle of Willis: Investigative Methods, Anatomical Variations and Correlated Ischemic Brain Diseases
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Published
May 10, 2020
Abstract
The Circle of Willis (CoW) is the most important collateral pathway communicating between the bilateral carotid system and the posterior circulation. Many techniques have been used to investigate the configuration and function of the CoW and their advantages and disadvantages are reviewed here. In previous studies, morphometric variation in CoW has been widely detected; however, the frequency of variation ranges largely, between 10% and 85%. Some differences in reported frequency may reflect differences in: the definition of CoW variation, the methods used to examine variation and study populations. Two conclusions, however, are clear: (i) the prevalence of variation in the posterior circle is higher than in that of the anterior circle; and (ii) variations in the CoW are correlated with cerebral or carotid vessel diseases. Although the cause of the variants remains unclear, both genetic background and hemodynamics could play important roles. Lastly, the correlation between the CoW and ischemic brain diseases is discussed. In future, artificial intelligence will be helpful for evaluating the CoW.
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Keywords
Circle of Willis, Diagnostic Imaging, Dissection; Anatomic Variation, Brain Ischemia
Supporting Agencies
Science and Technology Innovation Project of Foshan (FS0AA-KJ218-1301-0021) to Dr. Pan.
References
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2.Krabbe-Hartkamp MJ, van der Grond J, de Leeuw FE, de Groot JC, Algra A, Hillen B, Breteler MM, Mali WP. Circle of Willis: Morphologic variation on three-dimensional time-of-flight MR angiograms. Radiology 1998; 207(1):103-111.
3.Manninen H, Makinen K, Vanninen R, Ronkainen A, Tulla H. How often does an incomplete circle of Willis predispose to cerebral ischemia during closure of carotid artery? Postmortem and clinical imaging studies. Acta Neurochirurg 2009; 151(9):1099-1105.
4.Eftekhar B, Dadmehr M, Ansari S, Ghodsi M, Nazparvar B, Ketabchi E. Are the distributions of variations of circle of Willis different in different populations? - Results of an anatomical study and review of literature. BMC Neurol 2006; 6:22.
5.Ryan DJ, Byrne S, Dunne R, Harmon M, Harbison J. White matter disease and an incomplete circle of Willis. Int J Stroke 2015; 10(4):547-552.
6.Vasovic L, Milenkovic Z, Pavlovic S. Comparative morphological variations and abnormalities of circles of Willis: A minireview including two personal cases. Neurosurg Rev 2002; 25(4):247-251.
7.Saba L, Raz E, Fatterpekar G, Montisci R, di Martino M, Bassareo PP, Piga M. Correlation between leukoaraiosis volume and circle of Willis variants. J Neuroimag 2015; 25(2):226-231.
8.Kapoor K, Kak VK, Singh B. Morphology and comparative anatomy of circulus arteriosus cerebri in mammals. Anat Histol Embryol 2003; 32(6):347-355.
9.Hoksbergen AW, Legemate DA, Ubbink DT, Jacobs MJ. Collateral variations in circle of willis in atherosclerotic population assessed by means of transcranial color-coded duplex ultrasonography. Stroke 2000; 31(7):1656-1660.
10.Hata A, Yanagawa M, Honda O, Kikuchi N, Miyata T, Tsukagoshi S, Uranishi A, Tomiyama N. Effect of Matrix Size on the Image Quality of Ultra-high-resolution CT of the Lung: Comparison of 512 x 512, 1024 x 1024, and 2048 x 2048. Acad Radiol 2018; 25(7):869-876.
11.Nguyen-Huynh MN, Wintermark M, English J, Lam J, Vittinghoff E, Smith WS, Johnston SC. How accurate is CT angiography in evaluating intracranial atherosclerotic disease? Stroke 2008; 39(4):1184-1188.
12.Varga A, Di Leo G, Banga PV, Csobay-Novak C, Kolossvary M, Maurovich-Horvat P, Huttl K. Multidetector CT angiography of the Circle of Willis: Association of its variants with carotid artery disease and brain ischemia. Eur Radiol 2019; 29(1):46-56.
13.Malhotra A, Wu X, Chugh A, Mustafa A, Matouk CC, Gandhi D, Sanelli P. Risk of radiation-induced cancer from computed tomography angiography use in imaging surveillance for unruptured cerebral aneurysms. Stroke 2018:STROKEAHA118022454.
14.Zhu G, Yuan Q, Yang J, Yeo JH. The role of the circle of Willis in internal carotid artery stenosis and anatomical variations: A computational study based on a patient-specific three-dimensional model. Biomed Engineer Online 2015; 14:107.
15.Klimek-Piotrowska W, Rybicka M, Wojnarska A, Wojtowicz A, Koziej M, Holda MK. A multitude of variations in the configuration of the circle of Willis: An autopsy study. Anat Sci Int 2016; 91(4):325-333.
16.De Silva KR, Silva R, Amaratunga D, Gunasekera WS, Jayesekera RW. Types of the cerebral arterial circle (circle of Willis) in a Sri Lankan population. BMC Neurol 2011; 11:5.
17.Van Overbeeke JJ, Hillen B, Tulleken CA. A comparative study of the circle of Willis in fetal and adult life. The configuration of the posterior bifurcation of the posterior communicating artery. J Anat 1991; 176:45-54.
18.Li Q, Li J, Lv F, Li K, Luo T and Xie P. A multidetector CT angiography study of variations in the circle of Willis in a Chinese population. J Clin Neurosci 2011; 18(3):379-383.
19.Kapoor K, Singh B, Dewan LI. Variations in the configuration of the circle of Willis. Anat Sci Int 2008; 83(2):96-106.
20.Macchi C, Catini C, Federico C, Gulisano M, Pacini P, Cecchi F, Corcos L, Brizzi E. Magnetic resonance angiographic evaluation of circulus arteriosus cerebri (circle of Willis): A morphologic study in 100 human healthy subjects. Ital J Anat Embryol 1996; 101(2):115-123.
21.Horikoshi T, Akiyama I, Yamagata Z, Sugita M, Nukui H. Magnetic resonance angiographic evidence of sex-linked variations in the circle of Willis and the occurrence of cerebral aneurysms. J Neurosurg 2002; 96(4):697-703.
22.Fields WS. Aortocranial occlusive vascular disease (stroke). Clin Symposia 1974; 26(4):3-31.
23.Puchades-Orts A, Nombela-Gomez M, Ortuno-Pacheco G. Variation in form of circle of Willis: Some anatomical and embryological considerations. Anat Rec 1976; 185(1):119-123.
24.Chrzanowska G, Mierzwa J. Variation of the cerebral arterial circle (of Willis) in man. Folia Morphol 1979; 38(3):365-373.
25.Brunereau L, Levy C, Arrive L, Bousson V, Marsot-Dupuch K, Bousser MG, Tubiana JM. Anatomy of the circle of Willis with 3D time of flight magnetic resonance angiography and analysis of partitions. J Radiol 1995; 76(9):573-577.
26.Waaijer A, van Leeuwen MS, van der Worp HB, Verhagen HJ, Mali WP, Velthuis BK. Anatomic variations in the circle of Willis in patients with symptomatic carotid artery stenosis assessed with multidetector row CT angiography. Cerebrovas Dis 2007; 23(4):267-274.
27.Schomer DF, Marks MP, Steinberg GK, Johnstone IM, Boothroyd DB, Ross MR, Pelc NJ, Enzmann DR. The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Eng J Med 1994; 330(22):1565-1570.
28.Miralles M, Dolz JL, Cotillas J, Aldoma J, Santiso MA, Gimenez A, Capdevila A, Cairols MA. The role of the circle of Willis in carotid occlusion: assessment with phase contrast MR angiography and transcranial duplex. Eur J Vas Endovas Surg 1995; 10(4):424-430.
29.Kluytmans M, van der Grond J, van Everdingen KJ, Klijn CJ, Kappelle LJ, Viergever MA. Cerebral hemodynamics in relation to patterns of collateral flow. Stroke 1999; 30(7):1432-1439.
30.Hartkamp MJ, van Der Grond J, van Everdingen KJ, Hillen B, Mali WP. Circle of Willis collateral flow investigated by magnetic resonance angiography. Stroke 1999; 30(12):2671-2678.
31.Arjal RK, Zhu T, Zhou Y. The study of fetal-type posterior cerebral circulation on multislice CT angiography and its influence on cerebral ischemic strokes. Clin Imag 2014; 38(3):221-225.
32.Banga PV, Varga A, Csobay-Novak C, Kolossvary M, Szanto E, Oderich GS, Entz L, Sotonyi P. Incomplete circle of Willis is associated with a higher incidence of neurologic events during carotid eversion endarterectomy without shunting. J Vas Surg 2018; 68(6):1764-1771.
33.Montisci R, Sanfilippo R, Bura R, Branca C, Piga M, Saba L. Status of the circle of Willis and intolerance to carotid cross-clamping during carotid endarterectomy. Eur J Vas Endovas Surg 2013; 45(2):107-112.
2.Krabbe-Hartkamp MJ, van der Grond J, de Leeuw FE, de Groot JC, Algra A, Hillen B, Breteler MM, Mali WP. Circle of Willis: Morphologic variation on three-dimensional time-of-flight MR angiograms. Radiology 1998; 207(1):103-111.
3.Manninen H, Makinen K, Vanninen R, Ronkainen A, Tulla H. How often does an incomplete circle of Willis predispose to cerebral ischemia during closure of carotid artery? Postmortem and clinical imaging studies. Acta Neurochirurg 2009; 151(9):1099-1105.
4.Eftekhar B, Dadmehr M, Ansari S, Ghodsi M, Nazparvar B, Ketabchi E. Are the distributions of variations of circle of Willis different in different populations? - Results of an anatomical study and review of literature. BMC Neurol 2006; 6:22.
5.Ryan DJ, Byrne S, Dunne R, Harmon M, Harbison J. White matter disease and an incomplete circle of Willis. Int J Stroke 2015; 10(4):547-552.
6.Vasovic L, Milenkovic Z, Pavlovic S. Comparative morphological variations and abnormalities of circles of Willis: A minireview including two personal cases. Neurosurg Rev 2002; 25(4):247-251.
7.Saba L, Raz E, Fatterpekar G, Montisci R, di Martino M, Bassareo PP, Piga M. Correlation between leukoaraiosis volume and circle of Willis variants. J Neuroimag 2015; 25(2):226-231.
8.Kapoor K, Kak VK, Singh B. Morphology and comparative anatomy of circulus arteriosus cerebri in mammals. Anat Histol Embryol 2003; 32(6):347-355.
9.Hoksbergen AW, Legemate DA, Ubbink DT, Jacobs MJ. Collateral variations in circle of willis in atherosclerotic population assessed by means of transcranial color-coded duplex ultrasonography. Stroke 2000; 31(7):1656-1660.
10.Hata A, Yanagawa M, Honda O, Kikuchi N, Miyata T, Tsukagoshi S, Uranishi A, Tomiyama N. Effect of Matrix Size on the Image Quality of Ultra-high-resolution CT of the Lung: Comparison of 512 x 512, 1024 x 1024, and 2048 x 2048. Acad Radiol 2018; 25(7):869-876.
11.Nguyen-Huynh MN, Wintermark M, English J, Lam J, Vittinghoff E, Smith WS, Johnston SC. How accurate is CT angiography in evaluating intracranial atherosclerotic disease? Stroke 2008; 39(4):1184-1188.
12.Varga A, Di Leo G, Banga PV, Csobay-Novak C, Kolossvary M, Maurovich-Horvat P, Huttl K. Multidetector CT angiography of the Circle of Willis: Association of its variants with carotid artery disease and brain ischemia. Eur Radiol 2019; 29(1):46-56.
13.Malhotra A, Wu X, Chugh A, Mustafa A, Matouk CC, Gandhi D, Sanelli P. Risk of radiation-induced cancer from computed tomography angiography use in imaging surveillance for unruptured cerebral aneurysms. Stroke 2018:STROKEAHA118022454.
14.Zhu G, Yuan Q, Yang J, Yeo JH. The role of the circle of Willis in internal carotid artery stenosis and anatomical variations: A computational study based on a patient-specific three-dimensional model. Biomed Engineer Online 2015; 14:107.
15.Klimek-Piotrowska W, Rybicka M, Wojnarska A, Wojtowicz A, Koziej M, Holda MK. A multitude of variations in the configuration of the circle of Willis: An autopsy study. Anat Sci Int 2016; 91(4):325-333.
16.De Silva KR, Silva R, Amaratunga D, Gunasekera WS, Jayesekera RW. Types of the cerebral arterial circle (circle of Willis) in a Sri Lankan population. BMC Neurol 2011; 11:5.
17.Van Overbeeke JJ, Hillen B, Tulleken CA. A comparative study of the circle of Willis in fetal and adult life. The configuration of the posterior bifurcation of the posterior communicating artery. J Anat 1991; 176:45-54.
18.Li Q, Li J, Lv F, Li K, Luo T and Xie P. A multidetector CT angiography study of variations in the circle of Willis in a Chinese population. J Clin Neurosci 2011; 18(3):379-383.
19.Kapoor K, Singh B, Dewan LI. Variations in the configuration of the circle of Willis. Anat Sci Int 2008; 83(2):96-106.
20.Macchi C, Catini C, Federico C, Gulisano M, Pacini P, Cecchi F, Corcos L, Brizzi E. Magnetic resonance angiographic evaluation of circulus arteriosus cerebri (circle of Willis): A morphologic study in 100 human healthy subjects. Ital J Anat Embryol 1996; 101(2):115-123.
21.Horikoshi T, Akiyama I, Yamagata Z, Sugita M, Nukui H. Magnetic resonance angiographic evidence of sex-linked variations in the circle of Willis and the occurrence of cerebral aneurysms. J Neurosurg 2002; 96(4):697-703.
22.Fields WS. Aortocranial occlusive vascular disease (stroke). Clin Symposia 1974; 26(4):3-31.
23.Puchades-Orts A, Nombela-Gomez M, Ortuno-Pacheco G. Variation in form of circle of Willis: Some anatomical and embryological considerations. Anat Rec 1976; 185(1):119-123.
24.Chrzanowska G, Mierzwa J. Variation of the cerebral arterial circle (of Willis) in man. Folia Morphol 1979; 38(3):365-373.
25.Brunereau L, Levy C, Arrive L, Bousson V, Marsot-Dupuch K, Bousser MG, Tubiana JM. Anatomy of the circle of Willis with 3D time of flight magnetic resonance angiography and analysis of partitions. J Radiol 1995; 76(9):573-577.
26.Waaijer A, van Leeuwen MS, van der Worp HB, Verhagen HJ, Mali WP, Velthuis BK. Anatomic variations in the circle of Willis in patients with symptomatic carotid artery stenosis assessed with multidetector row CT angiography. Cerebrovas Dis 2007; 23(4):267-274.
27.Schomer DF, Marks MP, Steinberg GK, Johnstone IM, Boothroyd DB, Ross MR, Pelc NJ, Enzmann DR. The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Eng J Med 1994; 330(22):1565-1570.
28.Miralles M, Dolz JL, Cotillas J, Aldoma J, Santiso MA, Gimenez A, Capdevila A, Cairols MA. The role of the circle of Willis in carotid occlusion: assessment with phase contrast MR angiography and transcranial duplex. Eur J Vas Endovas Surg 1995; 10(4):424-430.
29.Kluytmans M, van der Grond J, van Everdingen KJ, Klijn CJ, Kappelle LJ, Viergever MA. Cerebral hemodynamics in relation to patterns of collateral flow. Stroke 1999; 30(7):1432-1439.
30.Hartkamp MJ, van Der Grond J, van Everdingen KJ, Hillen B, Mali WP. Circle of Willis collateral flow investigated by magnetic resonance angiography. Stroke 1999; 30(12):2671-2678.
31.Arjal RK, Zhu T, Zhou Y. The study of fetal-type posterior cerebral circulation on multislice CT angiography and its influence on cerebral ischemic strokes. Clin Imag 2014; 38(3):221-225.
32.Banga PV, Varga A, Csobay-Novak C, Kolossvary M, Szanto E, Oderich GS, Entz L, Sotonyi P. Incomplete circle of Willis is associated with a higher incidence of neurologic events during carotid eversion endarterectomy without shunting. J Vas Surg 2018; 68(6):1764-1771.
33.Montisci R, Sanfilippo R, Bura R, Branca C, Piga M, Saba L. Status of the circle of Willis and intolerance to carotid cross-clamping during carotid endarterectomy. Eur J Vas Endovas Surg 2013; 45(2):107-112.
How to Cite
Wang, W., Wang, Q., Yang, G., Qiu, M., & Pan, A. (2020). A Review of the Circle of Willis: Investigative Methods, Anatomical Variations and Correlated Ischemic Brain Diseases. Science Insights, 33(2), 159–166. https://doi.org/10.15354/si.20.re069
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Review
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