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Ann Thorac Surg 2006;82:74-79
© 2006 The Society of Thoracic Surgeons

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Original article: Cardiovascular

Incomplete Circle of Willis and Right Axillary Artery Perfusion

^a Department of Thoracic and Cardiovascular Surgery, Kuopio University Hospital, Kuopio, Finland
^b Department of Neurosurgery, Kuopio University Hospital, Kuopio, Finland

Accepted for publication February 9, 2006.

^_* Address correspondence to Dr Tulla, Department of Thoracic and Cardiovascular Surgery, Department of Kuopio University Hospital, PO Box 1777, FIN-70211 Kuopio, Finland (Email: harri.tulla{at}kuh.fi).

	Abstract

Top Abstract Introduction Material and Methods Results Comment References

 
BACKGROUND: The aim of our anatomic study was to assess whether the commonly used method of perfusion through the right axillary artery is sufficient in providing uniform distribution of blood to both hemispheres of the brain in patients undergoing surgery of the aortic arch. We considered that critical arteries to examine are anterior and left posterior communicating arteries of the circle of Willis because the absence or insufficiency of either one would drastically endanger perfusion to the left hemisphere of the brain. The existence and the diameters of these arteries were studied.

METHODS: The material was collected as a part of normal forensic medicine autopsies. The anatomy of the cerebral arteries of 87 deceased individuals was assessed by angiography and permanent silicone casts. A new classification was created for this study. According to a recent observation in the literature we defined the minimum threshold of arterial diameter that allows cross flow to be 0.5 mm. We also repeated analyses using 1 mm as a threshold, which has also been recommended.

RESULTS: In our material 22% of the anterior communicating arteries and 46% of the left posterior communicating arteries were missing. In this anatomic population the perfusion to the left hemisphere might have been insufficient in 14% of the patients at a threshold of 0.5 mm and in 17% at a threshold of 1 mm.

CONCLUSIONS: When the right axillary artery is used for perfusion, the circulation to the contralateral hemisphere seems to be good for most patients undergoing operations of the aortic arch, but additional means of brain protection are still needed.

	Introduction

Top Abstract Introduction Material and Methods Results Comment References

 
Perfusion of the right axillary artery in combination with deep hypothermic circulatory arrest has become the method of choice in surgical correction of diseases of the aortic arch and has reportedly given satisfactory brain protection [1–3]. However, some patients do not fully recover postoperatively; neurologic dysfunction and even serious cerebrovascular accidents may occur [1, 4, 5]. They may be related to embolic events, and possibly caused by inadequate flow to the contralateral hemisphere [1, 4]. The perfusion used to augment brain perfusion and specifically contralateral brain flow during the interval of systemic hypothermic circulatory arrest during these operations is mainly dependent on the integrity of the circle of Willis. The minor and more difficultly assessed collateral flow is contributed by ophthalmic and leptomeningeal arteries [6]. The integrity of the circle of Willis may therefore be critical because anomalies and hypoplasia of the circle of Willis are frequent [7–12]. As an example, Figure 1 demonstrates a clinical case of a patent crossover from right to left through the anterior communicating artery (AcomA).

View larger version (167K): [in this window] [in a new window]   Fig 1. Anteroposterior view of the anterior cerebral circulation with a digital substraction angiography of the right internal carotid artery. Note the filling of the left anterior cerebral artery and middle cerebral artery through a patent anterior communicating artery (arrow).

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment References

 
The material was collected by the Department of Neurosurgery (A.O., V.S.) at the University Hospital of Kuopio from autumn 1997 to the beginning of 1999 as a part of normal forensic medicine autopsies. During this period 193 consecutive forensic medicine autopsies were carried out, of which 99 were excluded. The main reasons for exclusion were decay of or damage to the brain. Seven cases were excluded after silicon casting because of a lack of four normal afferent arteries (right and left internal carotid artery, right and left vertebral artery), leaving 87. This final sample included 58 (67%) men and 29 (33%) women. Their age ranged from 13.8 to 90.2 years with a median age of 59.3 ± 15.0 years. The median age of the men was 57.9 ± 13.5 years, and that of the women was 62.2 ± 17.5 years. By selecting forensic autopsy cases instead of medical autopsy cases, we were able to control the patient selection more easily. Indications for forensic autopsies in Finland are strictly controlled by legislation. The anatomy of the cerebral arteries was assessed after death by angiography and permanent casts, which were made by experienced autopsy technicians. The study was approved by the ethical committee of Kuopio University Hospital.

Permanent Casts
The permanent casts of cerebral arteries were performed before the autopsy, and 210 g of lead oxide (Pb₃O₄) was used per kilogram of liquid silicone rubber. The mixture was divided into 120-g batches; just before usage 2 mL of solidifier was added. The deceased's aortic arch and the arteries branching from it (brachiocephalic trunk, left common carotid artery, and left subclavian artery) were exposed for a range of 3 cm. A plastic Y-shaped tube was connected so that one arm of the tube was fastened to the brachiocephalic trunk and the other to the left carotid artery. Then the right and left subclavian arteries were exposed and clamped. A 50-cm-long plastic tube was connected to the Y-shaped tube, through which the mixture was introduced into the cerebral arteries using a portable perfusion device at a pressure of 120 to 180 mbar. The process lasted 1 to 2 hours. The mixture solidifies into a permanent cast within 3 to 5 hours [13].

For this study cerebral arteries were prepared and put in peroxide (20%) for a period of 1 to 2 weeks to dissolve all organic tissue from them. The outcome was an exact permanent cast of the deceased's cerebral arteries. Each of the permanent casts was prepared with extreme care, especially with regard to the circle of Willis, and then fastened on a cardboard plate. From each permanent cast the existence, shape, symmetry, and possible aneurysms of 22 arteries were assessed. The length and diameter of the arteries were also measured with a gauge (Martin 17-409-01 mm scale, Tuttlingen, Germany).

Angiography
Because lead oxide is used as the contrast medium, liquefied silicone rubber is radiopaque. After the solidification of the silicone rubber, anterior and lateral roentgenograms were taken. This made the cervical and cerebral arteries visible. The brain was removed and placed on a plate with the base upward. Two roentgenograms were taken from above. The x-ray machine was moved to form an angle of 5 degrees between the pictures. This enabled the formation of a stereoscopic view of the angiographies. The pictures were placed on the x-ray board next to each other and were examined with an optical tool that created a three-dimensional view of the cerebral arteries. The existence, visibility, and symmetry of the arteries were assessed from the pictures.

Classification
A new clinical classification was created to estimate the sufficiency of blood distribution to the left hemisphere of the brain. Our classification is based on the observation by Hoksbergen and colleagues [14], who determined the collateral artery threshold diameters for supplying collateral flow. They concluded that the threshold diameter allowing for cross-flow through the primary collateral arteries of the circle of Willis is between 0.4 and 0.6 mm [14]. Based on this study, we defined the threshold in our material to be 0.5 mm. In addition, we considered that critical arteries to examine are the AcomA and the left communicating posterior artery (AcomP sin), because the absence or limitation of either one would drastically endanger perfusion to the left hemisphere of the brain (Fig 2). This is because the AcomA transports blood through the anterior circulation of the circle of Willis to the left hemisphere and the AcomP sin establishes communication between the anterior and the posterior circulation.

View larger version (33K): [in this window] [in a new window]   Fig 2. The principle of the right axillary artery perfusion during the repair of the aortic arch. Anonymous artery is clamped. (1 = right vertebral artery; 2 = left vertebral artery; 3 = basilar artery; 4 = right posterior communicating artery; 5 = left posterior communicating artery; 6 = right internal carotid artery; 7 = left internal carotid artery; 8 = left anterior cerebral artery; 9 = anterior communicating artery; 10 = anonymous artery; 11 = perfusion line; 12 = clamp.)

The principle of our new classification is illustrated in Table 1. The diameters of AcomAs and AcomPs were the principles according to which the groups were formed in the present classification. The artery was defined as normal if its diameter was at least 0.5 mm. The artery was defined as compromised if its diameter was less than 0.5 mm. The artery was defined as missing if it was not present in either the permanent cast or the angiography.

We also took into consideration how the results would differ if the threshold of the critical arteries were changed to 1 mm. The basis of forming groups was similar as when using a threshold of 0.5 mm.

	Results

Top Abstract Introduction Material and Methods Results Comment References

 
The AcomA and AcomP arteries were assessable in 45% to 70% of the permanent casts. In 22% of cases, the AComA was missing and in 46% of cases the AcomP sin was missing. The mean, minimum, and maximum diameters of the arteries are presented in Figure 3.

View larger version (79K): [in this window] [in a new window]   Fig 3. Examples from the permanent cast (A) and postmortem angiography (B) from the circle of Willis. (1 = right vertebral artery, mean 2.97 mm [range, 1.50–5.00 mm]; 2 = left vertebral artery, mean 3.07 mm [range, 1.20–5.00 mm]; 3 = basilar artery, mean 3.72 mm [range, 2.00–7.00 mm]; 4 = right posterior communicating artery, mean 1.57 mm [range, 0.40–3.00 mm]; 5 = left posterior communicating artery, mean 1.59 mm [range, 0.80–2.50 mm]; 6 = right internal carotid artery, mean 3.97 mm [range, 2.70–5.50 mm]; 7 = left internal carotid artery, mean 3.92 mm [range, 2.40–5.50 mm]; 8 = left anterior cerebral artery, mean 2.41 mm [range, 0.70–3.60 mm]; 9 = anterior communicating artery, mean 1.57 mm [range, 0.50–3.00 mm].)

	Comment

Top Abstract Introduction Material and Methods Results Comment References

Circle of Willis
The perfusion to the contralateral hemisphere mainly depends on the status of the circle of Willis during the right unilateral perfusion technique. However, anatomic variations of the circle of Willis are common [15, 16]. Macchi and associates [7] demonstrated by magnetic resonance angiography that the circle of Willis has a complete configuration only in 47% of subjects. A complete configuration of its anterior part was present in 90% and of its posterior part, in 49%. In healthy volunteers studied by magnetic resonance angiography, Krabbe-Hartkamp and coworkers [9] reported an entirely complete circle of Willis in 42%, a complete anterior circulation in 74%, and a complete posterior circulation in 52% of cases. According to the study by Kim and colleagues [15], the AcomP may be hypoplastic or absent on one or both sides of the brain in about 25% to 30% of patients and the AcomA in about 10%, and hypoplasia of the anterior cerebral artery segment can be seen in about 25%. Hoksbergen and associates [17] reported that the cross flow through the anterior circulation and posterior circulation was insufficient in 5% and 45% of cases, respectively. In our study, the anterior circulation was more often insufficient (22%), but our findings on the posterior circulation were consistent with those of others. Strikingly smaller number of anomalies has also been reported [12]. The reason for dissimilarities in the anterior circulation cannot fully be explained by different study populations or different methods. It is possible that noninvasive studies, eg, by magnetic resonance angiography, cannot detect very small collaterals, with a diameter less than 0.8 mm [18].

Classification and the Methodology
The current classification is based on research by Hoksbergen and colleagues [14] on the thresholds of the primary collaterals. Up to now, a threshold of 1 mm to define hypoplasia or inadequacy of collateral arteries has been widely used in anatomic studies [19, 20]. However, according to Hoksbergen and coworkers [14], the median AcomA diameter in patients with a nonfunctional anterior collateral pathway was 0.4 mm or less, and the median AcomA diameter of patients with a functional anterior collateral pathway was 1.1 mm. The diameter of a functional AcomP was 0.9 mm versus 0.6 mm in a nonfunctional AcomP [14]. Based on this, they specified the threshold to be 0.4 to 0.6 mm. Their results indicate that in practice, communicating arteries with a diameter less than 0.5 mm should be labeled hypoplastic [14]. Based on these results, we chose a threshold of 0.5 mm.

The permanent cast method is well known [13], and it enables visualization of small cerebral arteries, but has its weaknesses: eg, despite cautious handling of the material, damage to small vessels may occur during different stages of the process, and absence of very small vessels may be caused by a possible lack of the silicone mixture in the artery.

The idea that the critical arteries to examine are the AcomA and AcomP sin has a solid anatomic basis (Fig 2). Accordingly, the only combination that would carry a potential for poor contralateral circulation would be the absence or hypoplasia of both anterior and left posterior communicating arteries, and consequently the frontal and temporal parts of the left hemisphere would be affected.

When taking into account only our static anatomic observations and neglecting dynamic flow in hypothermic settings we hypothesize that the circulation to the left hemisphere would be sufficient in the majority of patients when using a threshold of 0.5 mm. However, insufficient collateral circulation to the left hemisphere would jeopardize at least 14% of the subjects for complications. When using a diameter threshold of 1 mm, we found that the proportion of subjects belonging the high-risk group was similar (14%). In addition, 3 patients in the compromised group would be at a moderate risk, which increased the number of patients in danger of ischemia to 15 (17%).

Clinical Aspects
Despite efforts to improve brain protection in aortic arch reconstructions, a considerable number of patients are still at risk for neurologic injuries. These can be either global or focal in nature. Global insult may be reflective of generalized ischemia or attributable to inadequate or absent perfusion [21].

To improve the brain protection in patients undergoing time-consuming complex reconstructions, antegrade brain perfusion in combination with hypothermia has largely been used. Antegrade brain perfusion can be performed with separate cannulas into each of the supraaortic vessels. This technique has been used by Kazui and associates [22] and has formerly included also the use of a femoral arterial cannula. An alternative option for arterial access is use the right axillary artery with a direct cannula [23] or a vascular side prosthesis [5]. Even the right proximal brachial artery has been used [4].

A detailed and representative presentation of different perfusion methods, reconstruction techniques, and results have been given recently by Spielvogel and colleagues [21]. Despite different protocols and techniques, the number of postoperative transient neurologic dysfunction, stroke rate, and mortality are comparable: 4.2% to 16% for transient neurologic dysfunction, 0.9% to 12.7% for stroke, and 4.6% to 16.9% for perioperative mortality [21]. An advantage of the use of the right axillary artery is the minimal incidence of atherosclerotic lesions, suggesting a lower risk for embolization in comparison to that of femoral arteries [24]. Also anatomic facts favor the use of the right axillary artery as it facilitates perfusion not only to the right carotid artery but also to the right vertebral artery in patients with normal cervical vascular anatomy.

Whatever the technique to conduct aortic arch reconstruction is, periods of arrest in brain perfusion may exist, especially when using stepwise protocols for selective antegrade brain perfusion. These periods may be a risk for global insults but also focal insults inasmuch as manipulation of the proximal supraaortic vessels may contribute to debris embolization [1]. Perfusion through the right axillary artery gives a simple operative field for aortic arch reconstructions and may allow circulation also to the left hemisphere [25]. However, in this technique clamping of the innominate artery is needed and risk of embolization exists. Moreover, collateral circulation through the circle of Willis may be inadequate because of anomalies as demonstrated by our study.

In conclusion, this study confirms large anatomic variations in the circle of Willis, but also offers a tool to evaluate the intracranial vascular anatomy and possible risks for perfusion to the contralateral hemisphere of the brain. Theoretically the results of our anatomic study indicate that the circulation to the left hemisphere would be sufficient in most patients undergoing an operation of the aortic arch. In 14% of subjects at a threshold of 0.5 mm and 17% at a threshold of 1 mm the circulation would have been insufficient. Therefore, for cerebral protection deep hypothermia should always be included. If possible, eg, in elective patients, the anatomy of the cervical and cerebral arteries of the patients undergoing reconstruction of the aortic arch should be examined for better risk stratification. For example, the minimally invasive computed tomography angiogram with good illustration of the brain vascular anatomy could be used preoperatively to identify high-risk patients (Fig 4). In case of marked problems in the cervical arteries or circle of Willis, additional perfusion methods, eg, perfusion through the left carotid artery, should be considered.

View larger version (135K): [in this window] [in a new window]   Fig 4. The minimally invasive computed tomography angiogram with good illustration of the brain vascular anatomy. (1 = right vertebral artery; 2 = left vertebral artery; 3 = basilar artery; 4 = right posterior communicating artery; 5 = left posterior communicating artery; 6 = right internal carotid artery; 7 = left internal carotid artery; 8 = left anterior cerebral artery; 9 = anterior communicating artery; 10 = incidental aneurysm in the middle cerebral artery on the right.)

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Mikko Hippeläinen Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Merkkola, P. Articles by Hippeläinen, M. Search for Related Content PubMed PubMed Citation Articles by Merkkola, P. Articles by Hippeläinen, M. Related Collections Cerebral protection