|Year : 2022 | Volume
| Issue : 1 | Page : 3-9
Computed tomography-based angiographic evaluation of circle of willis and its variations. First documented evidence from Northern India
Shah Sumaya Jan1, Bashir Ahmad Shah1, Shabir Ahmad Bhat2, Syed Shah Faisal3, Sheikh Mohd Saleem4
1 Department of Anatomy, Government Medical College, Srinagar, Jammu and Kashmir, India
2 Department of Radiology and Imaging, Government Medical College, Srinagar, Jammu and Kashmir, India
3 Junior Resident, Department of Medicine, SKIMS Medical College, Srinagar, Jammu and Kashmir, India
4 Independent Public Health Consultant, Jammu and Kashmir, India
|Date of Submission||11-Oct-2021|
|Date of Decision||20-Nov-2021|
|Date of Acceptance||22-Nov-2021|
|Date of Web Publication||04-Feb-2022|
Prof. Bashir Ahmad Shah
Department of Anatomy, Government Medical College, Srinagar, Jammu and Kashmir
Source of Support: None, Conflict of Interest: None
Background: The circle of Willis (CW) encircles the pituitary stalk and is considered an anastomotic vascular system that links the forebrain and hindbrain. Because morphology varies between races, it was reasonable to do research on the anatomy of the CW. The purpose of this study was to determine the anatomical variations in the arteries composing the CW on computed tomography (CT angiography) in the adult Kashmiri population. Materials and Methods: This was a cross-sectional descriptive study conducted to assess the structural characteristics of CW and to estimate the prevalence of anatomical variations of CW in the adult Kashmiri population among those who were permanent residents of Kashmir Valley, aged 20 years or older, and who were referred for CT angiography from the Department of Medicine or Surgery with the diagnosis of CW. Results: A total of 50 (23.1%) studied CT angiography were having the presence of any anatomical variations, while 166 (76.9%) had normal anatomical origins. Arteries forming the CW (polygon) were found to be absent among 9 (4.16%) and 5 (2.3%) had fetal origin of arteries forming the CW. Trifurcation of arteries was found among only 2 (0.9%), hypoplastic arteries were found among 34 (15.7%), and complete circles were present in 207 (95.8%) CT angiographs. Right and left internal carotid artery, right and left anterior cerebral artery, the right middle and left middle cerebral artery, and the anterior communicating artery were all present. Conclusion: Hypoplasia was more prevalent in a posterior circle, absent arteries in the anterior circulation, while accessory vessels were common in the anterior portion of the circle.
Keywords: Anterior cerebral artery, cerebral arterial circle, middle cerebral artery, posterior cerebral artery, Willis' circle
|How to cite this article:|
Jan SS, Shah BA, Bhat SA, Faisal SS, Saleem SM. Computed tomography-based angiographic evaluation of circle of willis and its variations. First documented evidence from Northern India. Curr Med Issues 2022;20:3-9
|How to cite this URL:|
Jan SS, Shah BA, Bhat SA, Faisal SS, Saleem SM. Computed tomography-based angiographic evaluation of circle of willis and its variations. First documented evidence from Northern India. Curr Med Issues [serial online] 2022 [cited 2022 Jul 1];20:3-9. Available from: https://www.cmijournal.org/text.asp?2022/20/1/3/337310
| Introduction|| |
The circle of Willis (CW) encircles the stalk of the pituitary and is regarded as an essential anastomotic arterial system that connects the forebrain and hindbrain. It is located at the base of the brain, polygonal in shape that connects the carotid and the vertebrobasilar systems following the obliteration of primitive embryonic connections., The CW acts as a crucial collateral route for the blood supply to the brain in case of occlusion in either system. A complete polygonal configuration of the CW has been linked to reducing the risk of intracranial hemorrhage among patients with ischemic stroke undergoing intravenous thrombosis. Pertinent to mention here is that the complete polygonal morphology of CW is not present in every individual. Many have some variations that are considered normal in most individuals. The variations include duplication, hypoplasia, fenestration, or agenesis. Such variations in the CW influence the hemodynamics of the cerebral blood flow, influencing the vascular territories, arterial remodeling pathophysiology, formation or rupture of aneurysms, and development of stroke.,,, Patients with aneurysms are more likely to have asymmetry or an anomaly of the circle.
Eighty-five percent of saccular aneurysms arise from arteries of the CW, with 35% from the anterior communicating artery (ACOM), 30% from the internal carotid artery (ICA), 22% from the middle cerebral artery (MCA), and the rest from the posterior circulation. The presence of a nonfunctional anterior collateral pathway in the CW in patients with the ICA occlusive disease is strongly associated with ischemic stroke. Vertebral artery dominance may also contribute to basilar artery curvature and posterior circulation infarctions. Uncommonly, the persistence of fetal anastomoses involving the CW is found, including persistent trigeminal, otic, hypoglossal, and pro-atlantal arteries. These arteries more or less unite the internal carotid and vertebrobasilar systems. The persistent primitive trigeminal artery is the most common persistent fetal anastomoses (83%) and connects the cavernous sinus to the basilar artery. The persistent otic artery is the least common and connects the petrous carotid to the basilar artery. The persistent primitive hypoglossal artery connects the petrous or distal cervical ICA to the vertebral artery. The persistent pro-atlantal inter-segmental artery connects the cervical ICA to the vertebral artery.
Computed tomography (CT) angiography is regarded as a highly sensitive, specific, fast, reliable, and noninvasive method compared to catheter angiography, which is considered the gold standard. The classification of CW has been proposed using various methods because of the complexity in the anterior and posterior circulation., As the morphology differs in distinct races, it was justifiable to study the anatomy of CW. To the best of our knowledge, there is no published data regarding the study of the anatomy of the CW in the Kashmiri population; for this reason, we conducted this study with the objectives to find the anatomical and any variation in the arteries forming the CW on CT angiography in adult Kashmiri population.
| Materials and Methods|| |
This was a cross-sectional descriptive study done to assess the structural characteristics of CW and to estimate the prevalence of anatomical variations of CW in the adult Kashmiri population. The study was conducted in the Postgraduate Department of Anatomy in collaboration with the Department of Radiodiagnosis and Imaging, Government Medical College, Srinagar. The research was done for a period of 18 months from March 2018 up to September 2019 among those who were permanent residents of Kashmir Valley, aged ≥20 years, and who were referred for CT angiography from the Department of Medicine or Surgery for suspected tumors, lesions of brain, brain injury, intracranial bleed or structural anomalies, persistent headache, etc. We included only those brain CT labeled as normal by an experienced radiologist (having ≥5 years specialization in brain imaging). Patients with the conditions such as congenital brain abnormalities, skull base tumors, cerebrovascular malformations such as aneurysm, arteriovenous malformation, arteriovenous fistula, acute ischemic, hemorrhagic, cerebrovascular strokes were excluded.
For calculating the sample size for estimation of prevalence with specified absolute precision, the formula n = Z2pq/d2 was used. In this study, the anticipated prevalence of 10%, absolute accuracy at 4%, and confidence level at 95%, the sample size calculated was 216.
Before CT, written informed consent was taken from the patient before the procedure. Contrast CT was performed using Siemens Emotion 16 slice multidetector spiral CT scan and 256-slice SOMATOM Definition flash CT scan.
The study looked at the completeness of the circle and the presence of any variations in the anterior and posterior circulation of the CW. The study also analyzed the external diameters of arteries and <1 mm in external diameter were considered hypoplastic, except for the communicating arteries, where <0.5 mm was considered hypoplastic.
Data were entered into a Microsoft Excel spreadsheet. Continuous variables were summarized as mean and standard deviation. Categorical variables were summarized as percentages. All statistical analysis was done using BM Corp. Released 2020. IBM SPSS Statistics for Windows, Version 27.0. Armonk, NY: IBM Corp.
Ethical approval was obtained from the Institutional ethical committee before the commencement of the study. The committee permitted the same per-protocol presented and described in the proposal to vide no: Acad/6579-87/MC dated March 09, 2016.
| Results|| |
The description of arteries forming the anterior and posterior circulation of CW is shown in [Table 1]. The right and left ICA, right and left anterior cerebral artery, and right middle and left MCA were present in all the studied CT angiographs (100%). The ACOM was present in 210 (97.2%) studied CT angiography and absent in 6 (2.8%). A worth mentioning finding was the hypoplastic nature of the ACOM, which was found among 11 (5.0%) of studied CT angiographs. Moreover, it was found that the right posterior communicating artery (PCOM) was absent among 2 (0.9%) [Figure 1] with 13 (6.0%) showing the hypoplastic nature of the right PCOM, whereas the left PCOM was absent among 1 (0.5%) and hypoplastic among 8 (3.7%) studied CT angiographs. Right and left vertebral artery, basilar artery, right and left PCA were found to be present in all the studied CT angiographs (100%) while 2 (0.9%) CT angiographs had hypoplastic right vertebral artery.
|Table 1: Description of arteries forming the anterior and posterior circulation of circle of Willis in the studied population (n=216)|
Click here to view
|Figure 1: Computed tomography angiographic image of absent bilateral posterior communication artery.|
Click here to view
The mean diameter of the arteries forming the anterior and posterior circulation of the CW is shown in [Table 2]. Among the studied CT angiographs, the right and left ICA had a mean diameter of 4.48 ± 0.69 mm and 4.63 ± 0.78 mm, right and left anterior cerebral arteries had a mean diameter of 1.77 ± 0.47 mm and 1.95 ± 0.43 mm, right and left MCA had a mean diameter of 2.53 ± 0.46 mm and 2.48 ± 0.55 mm while the ACOM was having a mean diameter of 1.15 ± 0.59 mm, respectively. On a similar note, the mean diameter of right and left PCOM was 1.24 ± 0.66 mm and 1.16 ± 0.67 mm, respectively. Among the studied CT angiographs, the right and left vertebral artery were having a mean diameter of 2.35 ± 0.91 mm and 2.67 ± 0.93 mm, basilar artery with a mean diameter of 3.02 ± 0.65 mm, right and left PCA had a mean diameter of 1.94 ± 0.47 mm and 1.98 ± 0.46 mm, respectively.
|Table 2: Measurement of diameter of arteries (mm) forming the anterior and circulation of circle of Willis among the studied population|
Click here to view
[Table 3] shows the prevalence of arteries of the CW forming the complete polygon [Figure 2]. Among the studied CT angiographs, 216, a complete CW (polygon) was present in 207 (95.8%) studied CT angiographs and absent in 9 (4.2%) CT angiographs. Among the studied CT angiographs, a total of 211 (97.7%) CT angiographs had the usual origin of the arteries forming the CW, while only 5 (2.3%) had fetal origin of arteries [Figure 3].
|Table 3: Completeness of circle of Willis, origin of arteries, and prevalence of anatomical variations encountered in the circle of Willis among the studied population in the studied population (n=216)|
Click here to view
|Figure 2: Computed tomography angiographic image of usual circle of Willis (complete polygon).|
Click here to view
|Figure 3: Computed tomography angiographic image of fetal origin of left posterior cerebral artery. NB: Fetal-type posterior cerebral artery is a common anatomic variation observed in the CW and defined as a posterior cerebral artery that originates from the internal carotid artery with or without a small connection with the basilar artery.|
Click here to view
Furthermore, among the studied CT angiographs, a total of 50 (23.1%) had the presence of any anatomical variations, while 166 (76.9%) were having common anatomical origins. [Table 3] also shows the different types of anatomical variation in the CW encountered during our study. Hypoplastic arteries were found among 34 (15.7%) CT angiographs, arteries forming the CW were found to be absent among 9 (4.16%) CT angiographs, 5 (2.3%) had fetal origin of the arteries. Trifurcation of arteries was found only among 2 (0.9%) studied CT angiographs [Figure 4].
|Figure 4: Computed tomography angiographic image of trifurcation of anterior cerebral artery.|
Click here to view
| Discussion|| |
The CW is formed at the base of the brain to preserve cerebral perfusion and avoid the symptoms of ischemia in case of blockage of a part of the cerebral arterial system. The CW and its branches are subjected to numerous variations. The variations differ from person to person and on the right and left sides of the same individual. The role of an arterial circle is to equalize the pressure. Under normal conditions, little interchange of blood occurs along the anastomotic channel due to equality of blood pressure. In occlusion, the arterial circle tends to equalize the pressure, thereby maintaining the circulation.
Complete circle of Willis
De Silva et al. in 2009 defined a circle as typical if all the component vessels of the CW were present, the origin of the vessels forming the CW was from its typical source and the size of a component vessel was more than 1 mm in diameter. In the present study, “We adapted the criteria for considering the circle as complete, which involved all the component vessels of the CW and vessels forming the CW had origin from its typical source.” This is supported by Hartkamp et al., who based their classification system on the continuity of the circular configuration (morphological completeness) to assess the potential for collateral flow development.
The prevalence of the typical circle as described in textbooks ranges from 4.6% to 7.2% as reported by Ranil et al. and Iqbal. The difference in range could have been due to the diversity in classification and the definition of hypoplastic vessels. In the present study, a high proportion of completeness of the CW was observed (95.8%). These findings were consistent with a study by Sande and Wanjari who found a high prevalence of completeness of CW in 80% study population. This was compared to studies by Iqbal, Kapoor et al., both in India, Maally and Ismail et al., in Egypt, who found that almost half of the circles were complete. On the other hand, De Silva et al. in Sri Lanka found a low prevalence of completeness in the CW (14.2%). Iqbal pointed out that the wide range in the prevalence of the typical configuration could be attributed to the influence of genetic, regional, environmental, hemodynamic factors and the diversity in the classification of hypoplastic vessels.
On the other hand, in the present study, the CW was found to be incomplete in 9 (4.2%) cases, and this was primarily due to the absence of the ACOM in 6 (2.8%) and PCOM in 3 (1.4%) unilaterally or bilaterally. This incompleteness could pose a risk factor for ischemic stroke, especially in internal carotid occlusion. A recent study by Hindenes et al. identified 47 unique CW variants, of which five variants constituted 68.5% of the sample. The complete variant was found in 11.9% of the subjects, and the most common variant (27.8%) was missing both posterior communicating arteries.
Hypoplasia in the artery
Raghavendren et al. studied morphometric variation in the CW in 50 adult brains. Among the 50 cases, 28 cases (56%) had a regular pattern of CW, while the remaining 22 cases (44%) showed variations. The typical variation reported is the hypoplastic PCOM with a percentage of 31.8%. Of the 22 cases, 7 variations were seen in the anterior circulation, and 15 variations were seen in the posterior circulation in the present study.
In the present study, the ACOM, one of the components of CW, has been found to exhibit abnormalities such as hypoplasia in 11 (5%) cases and absence in 6 (2.8%) CT angiograms observed. Fusion of the anterior cerebral artery may cause a lack of ACOM. The absence of an ACOM is also possible without fusion of the anterior cerebral artery.
The present observations largely corroborate with those of Windle and Alpers et al., who recorded 3% and 2% cases of absence of the ACOM due to fusion of the two anterior cerebral arteries, respectively. The present observations demonstrate the complete lack of ACOM without fusion of ACA and are similar to Fawcett and Blachford, who found a complete absence of ACOM in 0.14% cases.
The PCOM connects the two systems that supply the brain (internal carotid and vertebrobasilar systems). They provide collaterals in the cerebral circulation so that if one system is blocked, the other can take over, as reported by Saha et al. To define the hypoplasia of the PCOM, various authors used different measurements. Radiological studies by three-dimensional time of flight magnetic resonance angiography considered hypoplasia if the diameter of the vessel is <0.8 mm. The vessel was considered hypoplastic in the present study if the external diameter was <1 mm, chosen based on previous studies.,
PCOM variations are regarded as the most common variations in brain circulations. They are either hypoplastic or missing in 10%–46% of the cases., Similarly, in the present study, hypoplasia was seen in 3.7% and 6% in the left and right PCOM, respectively. At the same time, absent vessels were seen in 1.4%. This is also in line with Standring.
Moreover, the findings in the present study are not in agreement with the study by Saha et al., who found 37 cases (61.6%) out of 60 cases of the PCOM were either absent or hypoplastic. Furthermore, they reported that the average diameter of PCOM varied between 1.0 and 1.5 mm, with some having very narrow diameters of <0.5 mm. The mean diameter of the vessels in the present study varied from 1.16 mm and 1.24 mm for the left and right PCOM, respectively. According to most literature, hypoplasia of PCOM is a genetic variation and does not lead to any symptoms if other component vessels of the CW are functioning normally.
However, a hypoplastic PCOM may be a risk factor for developing neurological deficit in patients with ICA occlusion. Schomer et al. also found a definitive correlation between narrow or absent PCOM and cerebral infarction in persons with ICA occlusion.
In the present study, accessory vessels in the form of triplication were found in the CW. Among the accessory vessels, the incidence of triplication of the ACA was 0.9% in a total of two cases. The accessory vessels were not seen in the posterior circulation. Apart from two normal anterior cerebral arteries, it is also accompanied by a midline third ACA. This finding was comparable with Iqbal, but the incidence of accessory arteries was lower in the present study.
In the present study, the embryonic origin of the PCA from the ICA was found in 5 (2.3%) cases. Such a vessel is connected to the basilar artery by a small communicating artery. S. Iqbal reported 10% embryonic origin of arteries, Riggs and Rupp reported 22%, Alpers et al. reported 15%. In contrast, in the present study, the incidence of embryonic arteries was only 2.3% which is much lower than the published literature.
Use in the clinical practice
Understanding potential variations are critical for clinicians treating ischemic attacks, strokes, and aneurysms. For example, clinicians treating aneurysms must understand that the anatomy is highly likely to differ from Willis' original description. It is important to determine the state of the circle when considering the adequacy of the brain circulation since bypass/shunts can occur after occlusion of one of the cerebral vessels and the recovery or lack thereof after vascular occlusions may be affected by various factors.
Strengths and limitations
Our study has provided the baseline data of knowledge of the diameter and the length of the arteries of the CW among the Kashmiri population, which has great importance in interventional radiology for various endovascular interventions as well as during anatomy lessons. By analyzing the patient's angiograms with normal cerebrovascular status, we could not get a complete picture of the true hemodynamic capabilities of the CW during obstruction. The results of our study showed baseline dimensions of the vessels of CW, but the association with age and sex of the patient was not compared as they were out of the scope of our study.
| Conclusion|| |
Some of the anomalies seen in the study included hypoplasia of component vessels such as ACOM, right and left PCOM and right vertebral artery, triplication of anterior cerebral arteries, embryonic origin of left PCA, and absence of anterior and (left and right) PCOM. Hypoplasia was more prevalent in a posterior circle, absent arteries in the anterior circulation, while accessory vessels were common in the anterior portion of the circle. The neurosurgical importance lies during the exposure of the region for different purposes. Thorough knowledge of the vascular variants will increase the success of the procedure. It is recommended to include a larger number of sample size in future studies to create a database for dimensions of arteries of the CW in the Kashmiri population more accurately.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Alpers BJ, Berry RG, Paddison RM. Anatomical studies of the circle of Willis in normal brain. AMA Arch Neurol Psychiatry 1959;81:409-18.
Kathuria S, Gregg L, Chen J, Gandhi D. Normal cerebral arterial development and variations. Semin Ultrasound CT MR 2011;32:242-51.
Takakuwa T, Koike T, Muranaka T, Uwabe C, Yamada S. Formation of the circle of Willis during human embryonic development. Congenit Anom (Kyoto) 2016;56:233-6.
Qiu C, Zhang Y, Xue C, Jiang S, Zhang W. MRA study on variation of the circle of Willis in healthy Chinese male adults. Biomed Res Int 2015;2015:8.
Chuang YM, Chan L, Lai YJ, Kuo KH, Chiou YH, Huang LW, et al
. Configuration of the circle of Willis is associated with less symptomatic intracerebral hemorrhage in ischemic stroke patients treated with intravenous thrombolysis. J Crit Care 2013;28:166-72.
Menshawi K, Mohr JP, Gutierrez J. A functional perspective on the embryology and anatomy of the cerebral blood supply. J Stroke 2015;17:144-58.
Lazzaro MA, Ouyang B, Chen M. The role of circle of Willis anomalies in cerebral aneurysm rupture. J Neurointerv Surg 2012;4:22-6.
van Seeters T, Hendrikse J, Biessels GJ, Velthuis BK, Mali WP, Kappelle LJ, et al
. Completeness of the circle of Willis and risk of ischemic stroke in patients without cerebrovascular disease. Neuroradiology 2015;57:1247-51.
Polguj M, Majos M, Topol M, Majos A. An asymmetrical fenestration of the basilar artery coexisting with two aneurysms in a patient with Subarachnoid haemorrhage: Case report and review of the literature. Folia Morphol (Poland) 2014;73:229-33.
Zhou H, Sun J, Ji X, Lin J, Tang S, Zeng J, et al
. Correlation between the integrity of the circle of Willis and the severity of initial noncardiac cerebral infarction and clinical prognosis. Medicine (Baltimore) 2016;95:e2892.
Keedy A. An overview of intracranial aneurysms. Mcgill J Med 2006;9:141-6.
Dimmick SJ, Faulder KC. Normal variants of the cerebral circulation at multidetector CT angiography. Radiographics 2009;29:1027-43.
Yang ZL, Ni QQ, Schoepf UJ, De Cecco CN, Lin H, Duguay TM, et al
. Small intracranial aneurysms: Diagnostic accuracy of CT angiography. Radiology 2017;285:941-52.
Dorcas HP. The development of the cranial arteries in the human embryo. Contrib Embryol 1948;32:205-62.
Zurada A, Gielecki JS. A novel formula for the classification of blood vessels according to symmetry, asymmetry and hypoplasia. Folia Morphol (Warsz) 2007;66:339-45.
Zhu W, Wang YF, Dong XF, Feng HX, Zhao HQ, Liu CF. Study on the correlation of vertebral artery dominance, basilar artery curvature and posterior circulation infarction. Acta Neurol Belg 2016;116:287-93.
Fawcett E, Blachford JV. The circle of Willis: An examination of 700 specimens. J Anat Physiol 1905;40:63.2-70.
De Silva KR, Silva R, Gunasekera WS, Jayesekera RW. Prevalence of typical circle of Willis and the variation in the anterior communicating artery: A study of a Sri Lankan population. Ann Indian Acad Neurol 2009;12:157-61.
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;30:2671-8.
Iqbal S. A comprehensive study of the anatomical variations of the circle of willis in adult human brains. J Clin Diagn Res 2013;7:2423-7.
Sande V, Wanjari SP. Variations in the arterial circle of Willis in cadaver: A dissection study. IJHSR 2014;4:132-8.
Kapoor K, Singh B, Dewan LI. Variations in the configuration of the circle of Willis. Anat Sci Int 2008;83:96-106.
Maally MA, Ismail AA. Three dimensional magnetic resonance angiography of the circle of Willis: Anatomical variations in general Egyptian population. Egypt J Radiol Nucl Med 2011;42:405-12.
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.
Hindenes LB, Håberg AK, Johnsen LH, Mathiesen EB, Robben D, Vangberg TR. Variations in the Circle of Willis in a large population sample using 3D TOF angiography: The Tromsø Study. PLoS One 2020;15:e0241373.
Raghavendra, Shirol V, Dixit D, Reddy YAK, Desai S. Circle of willis and its variations; morphometric study in adult human cadavers. Int J Med Res Heal Sci. 2014;3(2):394.
Nordon DG. Rodrigues junior of- variation in the brain circulation – The circle of Willis. J Morphol Sci 2012;29:243-7.
Windle BC. The arteries forming the circle of Willis. J Anat Physiol 1888;22:289-93.
Saha A, Bhagyalakshmi B, Mandal S, Banopadhyaya M. Variation of posterior communicating artery in human brain: A morphological study. Gomal J Med Sci 2013;11:42-6.
Hoksbergen AW, Fülesdi B, Legemate DA, Csiba L. Collateral configuration of the circle of Willis: Transcranial color-coded duplex ultrasonography and comparison with postmortem anatomy. Stroke 2000;31:1346-51.
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.
Merkkola P, Tulla H, Ronkainen A, Soppi V, Oksala A, Koivisto T, et al
. Incomplete circle of Willis and right axillary artery perfusion. Ann Thorac Surg 2006;82:74-9.
Standring S. Gray's Anatomy, “The Anatomical Basis of Clinical Practice”. 40th
ed. Oxford: Churchill Livingstone, Elsevier; 2008.
Schomer DF, Marks MP, Steinberg GK, Johnstone IM, Boothroyd DB, Ross MR, et al
. The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Engl J Med 1994;330:1565-70.
Riggs HE, Rupp C. Variation in form of circle of Willis. The relation of the variations to collateral circulation: Anatomic analysis. Arch Neurol 1963;8:8-14.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3]