Annals of Indian Academy of Neurology
ORIGINAL ARTICLE
Year
: 2009  |  Volume : 12  |  Issue : 3  |  Page : 157--161

Prevalence of typical circle of Willis and the variation in the anterior communicating artery: A study of a Sri Lankan population


K Ranil D De Silva1, Rukmal Silva1, W.S.L Gunasekera2, RW Jayesekera3,  
1 Department of Anatomy, Faculty of Medical Sciences, University of Sri Jayewardenepura, Sri Lanka
2 Department of Anatomy, National Hospital of Sri Lanka, Sri Lanka
3 Department of Anatomy, Faculty of Medicine, Colombo, Sri Lanka

Correspondence Address:
K Ranil D De Silva
Department of Anatomy, Faculty of Medical Sciences, University of Sri Jayewardenepura, Nugegoda
Sri Lanka

Abstract

Objective: To determine the extent of hypoplasia of the component vessels of the circle of Willis (CW) and the anatomical variations in the anterior communicating artery (AcomA) in the subjects who have died of causes unrelated to the brain and compare with previous autopsy studies. Materials and Methods: The external diameter of all the arteries forming the CW in 225 normal Sri Lankan adult cadaver brains was measured using a calibrated grid to determine the occurrence of źDQ╗typicalźDQ╗ CWs, where all of the component vessels had a diameter of more than 1 mm. Variations in the AcomA were classified into 12 types based on Ozaki et al., 1977. Results: 193 (86%) showed źDQ╗hypoplasiaźDQ╗, of which 127 (56.4%) were with multiple anomalies. Posterior communicating artery (PcoA) was hypoplastic bilaterally in 93 (51%) and unilaterally in 49 (13%). Precommunicating segment of the posterior cerebral arteries (P1) was hypoplastic bilaterally in 3 (2%), unilaterally in 14 (4%), and AcomA was hypoplastic in 91 (25%). The precommunicating segment of the anterior cerebral arteries (A1) was hypoplastic unilaterally in 17 (5%). Types of variations in the AcomA were: single 145 (65%), fusion 52 (23%), double 22 (10%) [V shape, Y shape, H shape, N shape], triplication 1 (0.44%), presence of median anterior cerebral artery 5 (2%), and aneurysm 1 (0.44%). Conclusion: The occurrence of źDQ╗typicalźDQ╗ CW in autopsy brains was rare. Further studies would be necessary to determine if these anatomical variations could predispose to cerebral ischemia and premature stroke in the Sri Lankan population.



How to cite this article:
De Silva K R, Silva R, Gunasekera W, Jayesekera R W. 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;12:157-161


How to cite this URL:
De Silva K R, Silva R, Gunasekera W, Jayesekera R W. 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 [serial online] 2009 [cited 2019 Dec 8 ];12:157-161
Available from: http://www.annalsofian.org/text.asp?2009/12/3/157/56314


Full Text

 Introduction



Ischemic stroke in young adults (aged 15-45 years) is proportionately more common in India (15-30%) [1] and in Sri Lanka (34%), [2] in contrast to (3−5%) [3] in the West, the etiology of the majority of strokes in young adults in Sri Lanka is unexplained. [4],[5]

The circle of Willis (CW) plays an important role in cerebral hemodynamics as a collateral anastomotic channel, and presence of an intact CW should be more effective in facilitating cross flow compared to situations where there are deficiencies in the CW. There is a close correlation between a low capacity CW and an increased risk of stroke, [6],[7],[8],[9] collateral ability of the CW be best used when an emergency supervenes, depending on the presence and the size of the luminal caliber of its component vessels. [10],[11],[12]

Many studies have repotted a wide range in variation in the anatomy of the CW and the anterior communicating artery (AcomA) among normal individuals, [13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26] hypoplasia of the component arteries of the CW has been studied in India. [17],[21],[26],[27] Hypoplasia of the component arteries of the CW and the anatomical variations of the AcomA has not been previously studied in Sri Lanka and the aim of this cadaveric study was to assess the extent of hypoplasia (diameters part of the anterior cerebral arteries (A1), AcomA, precommunicating part of the posterior cerebral arteries (P1), and posterior communicating arteries (PcoA); and the anatomical variations of the AcomA in subjects who have died of causes unrelated to the brain and compare with previous autopsy studies.

 Materials and Methods



225 brains were obtained after ethical approval from medicolegal autopsies on individuals, aged between 18 and 73 years, who had died of causes unrelated to the brain and whose brains demonstrated no gross macroscopic evidence of cerebrovascular disease . The brains were removed from the cranial cavity and fixed in 10% formaldehyde. Blood was carefully washed out from the CW with isotonic saline. The arteries comprising the CW together with the basilar artery with minute branches arising from the main vessels were then carefully removed from the base of the brain. The external diameters of A1, AcomA, PcoA, and P1 were measured using a stereomicroscope equipped with a micrometer-calibrator (Leica). The equipment was standardized according to the manufacturer's specifications. The measurements were performed three times on each segment, by the first author and the calculated average was recorded as the value, line diagrams, and photographic records made, a vessel was recorded as absent only when it was not detected following examination under the dissecting microscope. In the present study, "typical" CW was defined if all of the component vessels of the CW were present, origin of the vessels forming the CW was from its typical source and the size of a component vessel more than 1 mm in diameter. [18] Hypoplasia was defined if a component vessel/s of the CW were less than 1 mm in diameter. [18]

Variations in the AcomA were classified into 12 types: single, one point fusion, long fusion, double, V shape, Y shape, H shape, N shape, triple, plexiform, presence of median anterior cerebral artery, and aneurysms; based on Ozaki et al., 1977 [23] and compared with studies. [18],[22],[23],[24],[25],[26] Macroaneurysm of the AcomA were recorded with line diagrams and photographs.

 Results



In the present study, 'typical circles' were found only in 32 (14.2%) of the brains. 193 (85.8%) showed hypoplasia, of which 127 (56.4%) were with multiple anomalies. The most frequent site of anomaly was in the posterior half of the circle (70%). There were no instances where any of the component vessels were completely absent.

361 component arteries of the CW were hypoplastic, 255 (70%) posteriorly, and 106 (30%) anteriorly. PcoA was hypoplastic bilaterally in 93 (51.5%), unilaterally in 49 (13.5%), 24 on the left, and 25 on the right side of the CW. P1 was hypoplastic bilaterally in 3 (1.6%), unilaterally in 14 (3.8%), 8 on the left, and 6 on the right side of the CW. AcomA was hypoplastic in 91 (25%). A1 was hypoplastic unilaterally in 15 (4.1%), 5 on the left and 10 on the right side of the CW.

Variations in the AcomA are indicated in [Table 1] and [Figure 1]A−E. Hypoplasia of the AcomA was seen in 91 (25.07%) of the specimens. One (0.44%) macroaneurysm, 25 mm in diameter, was identified arising from the AcomA in a 21-year-old female whose cause of death was homicide [Figure 2].

 Discussion



Hypoplasia of the component arteries of the CW has been reported in anatomic studies ranging from 0.7 % [19] to 80.6%, [20] and the proportion of 85.8% observed in the present study, appears to be the highest observed in a population. The prevalence of the 'typical circle', the "normal" textbook polygon ranges from 4.6% [28] to 72.2%. [19] A possible reason for the wide range may be the diversity in nomenclature and the criteria used to define hypoplastic vessels. There is little unanimity in nomenclature and quantitative measurement of the diameters of all the component vessels of 'circle', which has not been measured in several studies and have relied up on rough estimations of the vessel diameter in determining the anomalies of the CW rather than actual measurements. Vessels have been described as 'thread-like', 'string-like', 'minute', and 'very small' without regards to measured diameter.

In the present study, typical configuration was found only in 14.2% of the brains compared to 26.8%, [17] 53.2%, [21] and 45.2% [26] of studies conducted in India and 52.3% in the US. [18] Quantitative measurement of the actual external diameter of all the component vessels of the CW and specimens has been done routinely in the present study. It is believed that Sri Lankans have a common origin from India. The wide range in the prevalence of typical configuration between Indian and Sri Lankan studies, warrants further studies to ascertain influence of genetic, racial, regional, environmental, hemodynamic factors, or a combination of any of them.

The minimum threshold diameter for supplying collateral flow through CW, as assessed by transcranial color-coded duplex ultrasonography (TCCD) and carotid compression tests, was compared with their unfixed postmortem anatomy lies between 0.4 and 0.6 mm. The PcoA threshold diameter for collateral function was slightly higher than the AcomA threshold diameter, possibly due to greater length of PcoA. [29] In the absence of studies showing how far the postmortem arterial diameters of fresh or fixed brains are equal to in vivo diameters and the effect of absence of perfusion pressure and possible postmortem shrinking of the arterial wall, in the present study we defined vessels less than 1 mm in diameter as "hypoplastic" or "string-like".

The most frequent site of abnormal diameters was seen in the posterior half of the circle, and the 70% proportion in the present study is similar to other reported series, [6],[18],[19],[20],[21],[26],[30] this may be related to the embryological development of the posterior half of the CW, where the basilar and the ICAs anastomose during development of the cerebral arteries.

Reported incidence of absent arteries in the CW in normal brains leading to an incomplete circle range from 0.6% [18] to 17%. [23] In the present study of 225 autopsies, a vessel was considered absent only when it was not visualized despite careful examination under the dissecting microscope and there were no such instances observed. A meticulous examination is needed to demonstrate small twigs forming the CW. This is dependent upon proper collection of samples, careful removal of the brain and the CW and thorough examination under the dissecting microscope for torn arteries before a vessel is classified as absent. The presence even of small vessels may be important for potential collateral channels.

The state of the circle becomes important in determining the adequacy of the brain circulation. The possibility of by-passing or shunting effects in occlusion of one of the cerebral vessels and the adequacy of recovery or lack of recovery after vascular occlusions may be explained in part by variations in the anatomy of the circle of Willis. [11] A rapid, high reperfusion strongly increases survival in the ischemic penumbra, inhibiting the growth of the core region.

It has been reported that in Asians, the incidence of intracranial atherosclerosis in anterior circulation stroke is much higher than Caucasians. [31] Prevalence of posterior circulation stroke among Asians has been reported much higher compared to the West. [32],[33],[34] The average age of patients in the developing countries with stroke is 15 years younger than in developed countries. [35] The reasons for these differences are not well-understood and role of anatomy and the pathology of the cerebral arteries in the pathogenesis of cerebrovascular diseases in different ethnic or racial groups are far from clear. There exist several postulates as to the underlying reasons for the anatomical variation of the CW: amplitude of the neck movements, [36] hemodynamic factors, [15],[37] postnatal development, [38] and genetic factors. [39]

The findings of the anomalies of the AcomA in the present study, studies conducted in India [21],[26] and from those of more diverse populations, [18],[19],[21],[22],[23],[24],[25],[26] reported in the literature appears to be similar and is possibly due to embryonic development.

Limitations

In the absence of studies showing relationship between functional in vivo diameters and postmortem arterial diameters of fixed brains, we used an arbitrary diameter of 1 mm of component vessels of the CW as hypoplastic. We did not measure the narrowest part of the arteries; these parts probably may determine collateral ability.

 Conclusion



The present study reveals that high incidence of hypoplastic vessels (193 of 225; 86%) and with multiple anomalies (127 of 225; 56.4%), in the CW in the Sri Lankan population, whether it acts in combination with arteriosclerotic changes and/or changes in of food habits and/or genetic difference between normal and anamalous type of cerebral arteries, would contribute to premature strokes in young adults warrants further investigations.

 Acknowledgments



This study was supported by Hiran Tillekeratne Research Fund, University Grants Commission, and Research Grant from the University of Sri Jayewadenepura. We wish to thank Dr. LBL De Alwis and Dr. Ananda Samarasekera, Judicial Medical Officers, for granting permission to inspect the samples, Mr. A. Dais for photography, and Mr. RAD Ratuwithana for data entry.

References

1Anand K, Chowdhury D, Singh KB, Pandav CS, Kapoor SK. Estimation of mortality and morbidity of strokes in India. Neuroepidemiology 2001;20:208-11.
2Gunatilake SB, Gunatilake HC. Young strokes: An increasing problem. Oral presentation, 104 th Anniversary Academic Sessions of the Sri Lanka Medical Association, Sri Lanka. 1991 March: 25.
3Blecic S, Bogousslavsky J. Stroke in young adults. In: Barnett HJ, Mohr JP, Stein BM, Atsu FM, editors. Stroke-path physiology, diagnosis and management. 3 rd ed. New York: Churchill Livingstone; 1998. p. 1001-12.
4Seneviratne BI, Ameratunga B. Strokes in young adults. Br Med J 1972;3:791-3.
5De Silva KRD, Gamage R, Wewelwala CC, Gunarathna D, Kittner SJ, Sirisena D, et al. Young strokes in Sri Lanka: An unsolved problem. J Stroke Cerebrovasc Dis.2009; 14:304-308.
6Fetterman GH, Moran TJ. Anomalies of the circle of Willis in relation to cerebral softening. Arch Pathol. 1941; 32: 251-7.
7Alpers BJ, Berry RG. Circle of Willis in cerebral vascular disorders. Arch Neurol. 1963;8:398-402.
8Battacharji SK, Hutchinson EC, McCall AJ. The circle of Willis: The incidence of developmental abnormalities in normal and infracted brains. Brain. 1967; 90: 747-58.
9Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 2000;31:128-32.
10Mull M, Schwarz M, Thron A. Cerebral hemispheric low-flow infarcts in arterial occlusive disease: Lesion patterns and angiomorphological conditions. Stroke 1997;28:118-23.
11Miralles M, Dolz JL, Cotillas J, Aldoma J, Santiso MA, Gimenez A, et al. The role of the circle of Willis in carotid occlusion: Assessment with phase contrast MR angiography and transcranial duplex. Eur J Vasc Endovasc Surg 1995;10:424-30.
12Shomer 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.
13Barboriak DP, Provenzale JM. Pictorial review: Magnetic resonance angiography of arterial variants at the circle of Willis. Clin Radiol 1997;52:429-36.
14Hillen B. The variability of the circle of Willis: Univariate and bivariate analysis. Acta Morphol Neth Scand 1986;24:87-101.
15Hillen B. The variability of the circulus arteriosus (Willisii): Order or anarchy. Acta Anat (Basel) 1987;129:74-80.
16Krabbe-Hartkamp MJ, Van der Grond J, de Leeuw FE, de Groot JC, Algra A, Hillen B, et al. Circle of Willis: Morphological variation on MR angiograms. Radiology 1998;207:103-11.
17Vare AM, Bansal PC. Arterial Pattern at the base of the human brain. J Anat Soc India 1970;19:71-9.
18Alpers BJ, Berry RG, Paddison RM. Anatomical studies of the circle of Willis in normal brain. Arch Neurol Psychiat 1959;81:409-18.
19Fawcett E, Blachford JV. The circle of Willis. An examination of 700 specimens. J Anat and Physiol 1905;40:63-70.
20Riggs HE, Rupp C. Variations in form of circle of Willis. Arch Neurol. 1963;8:8-14.
21Reddy DR, Prabhakar V, Rao BD. Anatomical Study of Circle of Willis. Neurology India 1972;20:8-12.
22Puchades-Orts A, Nombela-Gomez M, Ortuno-Pacheco G. Variation in form of Circle of Willis: Some anatomical and embryological considerations. Anat Rec 1976;185:119-23.
23Ozaki T, Handa H, Tomomoto K, Hazama F. Anatomical variations of the arterial system of the base of the brain. Arch Jap Chir 1977;46:3-17.
24Fujimoto K, Tanaka O. Morphological examination of the circulus arteriosus cerebri humani (circle of Willis) I. Anterior and posterior communicating arteries. Acta Anatomica (Nippon) 1989;64:481-9.
25Eftekhar 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.
26Kapoor K, Singh B, Dewan LI. Variations in the configuration of the circle of Willis. Anat Sci Int 2008;83:96-106.
27Tandon PN. Epidemological study on subarachnoid haemorrhage in India (1972-75). ICMR.1987; 1-34.
28Fisher CM. The circle of Willis: Anatomical variations. Vasc Dis 1965;2:99-105.
29Hoksbergen AW, Fulesdi 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.
30Kamath S. Observations on the length and diameter of vessels forming the circle of Willis. J Anat 1981;133:419-23.
31Moossy J. Pathology of cerebral atherosclerosis. Influence of age, race, and gender. Stroke 1993;24:I22-3; I31-2.
32Lee JH, Han SJ, Yun YH, Choi HC, Jung S, Cho SJ, et al. Posterior circulation ischemic stroke in Korean population. Eur J Neurol 2006;13:742-8.
33Bogousslavsky J, Melle GV, Regli F. The Lausanne stroke registry: analysis of 1000 consecutive patients with first stroke. Stroke 1988;19:1083-92.
34Moulin T, Tatu L, Crιpin-Leblond T, Chavot D, Bergθs S, Rumbach T. The BesanΗon stroke registry: An acute stroke registry of 2500 consecutive patients. European Neurology 1997;38:10-20.
35Truelsen T, Bonita R, Jamrozik K. Surveillance of stroke: A global perspective. Int J Epidemiol 2001;30:S11-6.
36Lazorthes G, Gouaze A, Santini JJ, Salamon G. The arterial circle of the brain (circulus arteriosus cerebri). Anatomia Clinica 1979;1:241-57.
37Milenkovic Z, Vucetic R, Puzic M. Asymmetry and anomalies of the circle of Willis in fetal brain. Microsurgical study and functional remarks. Surg Neurol 1985;24:563-70.
38Stehbens WE. Etiology of intracranial berry aneurysms. J Neurosurg 1989;70:823-31.
39Vasovic L, Milenkovic Z, Pavlovic S. Comparative morphological variations and abnormalities of circles of Willis: A mini review including two personal cases. Neurosurg Rev 2002;25:247-51.