THE INNER DIAMETER OF ARTERIES OF THE CIRCLE OF WILLIS REGARDING GENDER AND AGE ON MAGNETIC RESONANCE ANGIOGRAPHY

Headnote

Introduction: The collateral potential of the circle of Willis (CW) is believed to be dependent on the presence and size of its arteries. The aim of the study was to determine the inner diameter of the arteries of the CW in the Bosnian population, in relation to gender and age.

Examinees and methods: This prospective-retrospective study included 1000 examinees who underwent Magnetic resonance angiography (MRA) of the cerebral arteries. 3D-time of flight angiograms were performed according to the standard protocol, with axial slicethickness of 0.9 mm. We measured the inner diameter of all arteries of the CW except the anterior communicating artery.

Results: The average inner diameter of the arteries of the CW were: internal carotid artery: 4.24 mm, anterior cerebral artery: 2.09 mm, posterior communicating artery: 1.32 mm, posterior cerebral artery: 1.94 mm, diameter of the basilar artery: 3.22 mm. The average diameter of all the arteries, except the posterior communicating artery, was significantly higher in men (p < 0.05) than in women. There was a weak negative correlation between the value of the inner diameter of the anterior cerebral artery and the age of the examinees in all groups (r = -0.212, r = -0.197, r = -0.228). In females there was a weak positive correlation between the value of the diameter of the internal carotid artery and age (r = 0.121; p < 0.0001).

Conclusion: Our results showed that the average diameter of most arteries of the CW is higher in men than in women, without any significant correlation between the value of the diameter of most arteries and age.

Key words: diameter, artery, circle of Willis.

INTRODUCTION

The circle of Willis (CW) is located at the base of the brain and is considered to be the main cerebral collateral pathway that allows flow redistribution in response to low perfusion pressure in a major feeding artery [1]. The CW is the most important anastomosis between the carotid and vertebrobasilar circulation, and it also connects the circulation of the right and left cerebral hemisphere (Figure 1, 2). It is a potential collateral pathway of blood flow in cases of reduced cerebral perfusion through the carotid or vertebrobasilar system [2, 3]. The collateral potential of the CW is believed to be dependent on the presence and size of its component vessels, which vary in calibre, being often partially developed, sometimes even absent, and about 60% of circles show anomalies [4,5,6,7].

The mean diameter of the arteries of the CW, as well as the other cerebral arteries, is the most frequent parameter analysed by different authors, mostly in autopsy studies [8,9,10]. These studies show that diameters may be dependent on the pressure exerted by a plastic mass, such as latex, while the blood vessel is being injected, or during another technique of filling the vessels [11]. In these cases the obtained diameter values refer to the external diameter of the blood vessel, which partly depends on the elasticity of the blood vessels, and is not an entirely accurate value. Diagnostic radiological imaging, such as: digital subtraction angiography (DSA), three-dimensional cerebral angiography, computed tomography angiography (CTA) and magnetic resonance angiography (MRA), determine the internal diameter of the blood vessel, which is a more accurate value. CTA and MRA with the possibility of 3D image reconstruction, which allows detailed morphometric examination of the blood vessels, have become more precise and accurate than anatomical methods of examination [12, 13]. These methods enable us to set new standards for the normal size of the intracranial blood vessels (inner diameter, length, volume), tortuosity and stereoscopic relationships between the blood vessels in 3D space (Figure 2). However, compared to anatomical studies, there are considerably fewer published studies related to the normal diameter of the blood vessels of the brain based on CT or MR angiograms [14, 15, 16, 17, 18]. Some radiological studies previously conducted, that dealt with the measurement of the diameter of arteries of the CW, showed gender and age-related differences in the vessel diameter [18, 19, 20] while others found no gender and age related differences [17].

The aim of this study was to determine the normal inner diameter of the arteries of the CW in the Bosnian population according to gender, to determine the correlation between age and the artery diameter values, and to compare our results with previous radiological studies.

EXAMINEES AND METHODS

Examinees: In a prospective-retrospective study, performed in the period from July 2008 to May 2013 at the Department of Radiology and Nuclear Medicine of the University Clinical Centre, Tuzla 1000 subjects were included (376 men and 624 women), older than 18 years, who consecutively underwent MRA of the cerebral arteries. Patients with cerebrovascular disease, vascular malformations and brain tumours were excluded from the study.

Methods: MRA was performed using one of two machines, strength 1.5 Tesla (Siemens, model Avanto, Germany or Philips, model Achieva, The Netherlands). The MR angiography protocol consisted of non-contrast three-dimensional time of flight (3D TOF) angiograms with axial slice thickness at 0.9 mm, covering the area of the first cervical vertebra to the upper contour of the corpus callosum MRA. On the Siemens 1.5T machine, the following imaging parameters were set: 25 ms time of repetition (TR), 7ms time of echo (TE); 20° flip angle; 256x256 matrix size; 220 mm field of view (FOV). The imaging parameters on Phillips machine were: TR 23 ms; TE 6.91 ms, flip angle 20°; matrix 328x208; FOV 180 mm. In the study, the axial 3D TOF angiograms, maximum intensity projection (MIP) images, and 3D reconstruction of the axial angiograms were analysed by Voxar system. All images were analysed by a single radiologist with five years' experience in MRI, and all unclear cases were further analysed by a neuro-radiologist with many years' experience. The diameter of the following CW components were measured: internal carotid artery (ICA), A1 segment of the anterior cerebral artery (ACA), posterior communicating artery (PCOA), P1 segment of the posterior cerebral artery (PCA), and diameter of the basilar artery (BA). Due to the small diameter of the anterior communicating artery (ACOA), which is insufficient to be adequately analysed by MRA, that artery was not analysed in the study. The inner diameter of the ICA was measured at the C4, C5 and C6 segments. The BA was measured at its proximal, middle and distal segments. Three measurements were carried out to obtain the average value. The A1 segment of the ACA, the P1 segment of the PCA and the PCOA were measured in the middle part, and if the width of these arteries was uneven longitudinally, measurement was done at the proximal, middle and distal segments of the vessel, and the diameter of the artery was taken to be the arithmetic average mean of those three measurements. Some arteries of the CW were not always visualized on MR angiogram (aplastic arteries) and the average artery diameter is calculated according to the number of arteries that were visualized.

Statistical analysis: The collected data were stored in the Microsoft Access database while statistical analysis was performed using MedCalc statistical software.

The standard methods of descriptive statistics were used for statistical data processing (mean, standard deviation, minimum and maximum values ). As the inner diameter differences between right and left side cerebral arteries, as well as between males and females, were approximately normally distributed variables, they were tested with the parametric t-test for independent samples. Correlation between the inner diameter of the individual cerebral artery and age were tested by Pearson's linear correlation. Differences on the level of p < 0.05 were considered statistically significant.

RESULTS

The inner diameter of the measured CW arteries (including all right and left arteries) in all examinees is shown in Table 1. Side related differences between vessel diameters in all examinees and their statistical significance are shown in Table 2, in males in Table 3, and in females in Table 4. The mean inner diameter of the left PCA was statistically significantly larger than diameter of the right PCA in the in females, while in males the mean diameter of the right and left PCA was equal. There were no statistically significant differences between mean vessel diameters of the right and left arteries of the ICA, ACA and PCOA.

Gender related differences and their statistical significance in the diameters of the arteries of the CW are shown in Table 5. There were statistically significant differences between the mean vessel diameters between males and females in the ICA, ACA, PCA and BA. The average diameters of these arteries in males were significantly larger than in females, while the average diameter of the PCOA was almost equal in males and females.

The correlation between the artery diameters and the age of the examinees is shown in Table 6. In the group comprising all examinees, the diameters of all the arteries of the CW, except the ACA, were not correlated with age. There was a weak negative age-diameter correlation in the case of the ACA in the group comprising all examinees, as well as in males and in females. In the case of the ICA in females, a weak positive age-diameter correlation was demonstrated. The diameter of the PCA in females and the diameter of the PCOA in males were not correlated with age. In the cases of the ICA and the PCA in males, the PCOA in females, as well as the diameter of the BA in both sexes, there was no adequate evidence to show whether the two factors correlated or not, since the P value was greater than 0.05 in all cases.

Discussion

MRA is a non-invasive, very sensitive radiological technique for detecting the anatomy of the CW [21]. 3D TOF MRA can provide valuable information about the diameters and variations of the CW arteries regarding the collateral anatomy and function of this circle [22]. In the last 15 years, several radiological studies have dealt with the determination of the inner diameter arteries of the CW, correlated with side, gender and age [17, 18, 19, 20]. Most of the angiographic studies observed less than 200 subjects, except the study by Chen et al. [17], while 1000 examinees were included in the present study, making this study one of the larger ones.

Side-related difference in artery diameter

In this study the average diameter of the ICA was larger than in previous studies, and the reason for this is probably the different methodologies and measurement locations. In the present study the inner diameter of the ICA was measured at the C4, C5 and C6 segments and three measurements were carried out to obtain the average value, while in previous studies the place of measurement is not explicitly stated [17, 19, 20]. It is possible that it was measured at the distal segment of the ICA, on the C6 segment before the terminal branching artery, which is smaller than the proximal parts. Other artery diameters of the CW correspond to the results of other authors, except the diameter of the PCOA, which is slightly larger than the diameters listed in other presented studies [17, 19, 20, 23].

In the present study, of all the measured arteries of the CW, only the average inner diameter of the left PCA was statistically significantly larger than the diameter of the right PCA in females, while in males the diameters of the right and left PCA were equal. The mean diameter of the left and right ICA was equal in all groups, while the diameter of the left PCOA in all groups was not significantly larger than the right PCOA. There were no statistically significant differences between the mean vessel diameters of the right and left arteries of the ICA, ACA and PCOA in the present study. In previous angiographic studies, the authors have also found only small fluctuations in diameters between the right and left arteries of the CW [17, 18, 19, 20].

Gender-related differences in artery diameters

CW artery diameters measured in our study were comparable with other angiographic studies, especially MRA, as shown in Table 7.

In this study the average diameters of the ICA, ACA, PCA, and BA in males were significantly larger than in females, while the average diameter of the PCOA was almost equal in males and females. In previous studies the average diameter of the ICA, ACA, PCA and BA were slightly larger in males than in females, except in the study conducted by Chen et al. [17]. In their study the average diameter of the ICA and the ACA were equal in males and females, while the average diameter of the PCA was larger in females than in males. These authors did not prove significant gender-related difference in vessel diameter. The average diameter of the PCOA tended to be larger in females than in males, in this as well as in all previous studies [17, 19, 20, 22]. In the present study, as well as in the study by Voljevica et al. [20], the greatest variations were seen in the values of the ICA, which in the present study was 0.26 mm larger in males than in females.

Age-related differences in artery diameter

Chen et al. did not find in their study any significant difference in artery diameters between groups younger and older than 40, except that the older subjects had smaller caliber in the left ACA than younger [17]. Maaly and Ismail showed statistically significant age related differences in the cases of the ICA, BA, ACA, and the PCOA [18]. These arteries had smaller mean diameters in subjects older than 40. Stefani et al. found significantly larger diameters of the PCA and the BA in individuals older than 40 years, while the diameter of the ACA was equal in both groups [23]. In one of the recent studies, which observed 100 angiograms of the carotid system shown on serial angiography by Seldinger, the authors found larger diameters of the blood vessels of the CW in the younger subjects (25 to 34 years) compared to those older than 60, except the diameter of the ICA, which was about 0.2 to 0.3 mm larger in the older subjects [20]. In the present study there was a weak negative age-diameter correlation in the case of the ACA in the group comprising all examinees, as well as in males and females. In the case of the ICA in females, a weak positive age-diameter correlation was shown. This result partly corresponds to the result of Voljevica et al. [20]. In the case of other arteries of the CW, no statistically significant correlation has been proven between age and the diameters of the arteries. The results of the present study mostly agree with the results of Chen et al. [17], bearing in mind that the authors investigated the influence of age on the value of diameters of ACI, but only in the group comprising all examinees, so our results cannot be fully compared with the results of previous studies.

CONCLUSION

Our study included 1000 examinees. The examination of the early literature on the same topic showed that this study seems to be the largest MR angiography study. In the study, the average diameters of the ICA, ACA, PCA, and BA were significantly larger in males than in females, while we did not find any statistically significant correlation between age and the diameters of the arteries, except in the case of the ACA, which decreased with age in all examinees, and in the case of the ICA, which increased with age in females.

References

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