Ann Thorac Surg 2008;86:448-451. doi:10.1016/j.athoracsur.2008.04.024
© 2008 The Society of Thoracic Surgeons
Original Articles: Adult Cardiac
Transcranial Doppler Study to Assess Intracranial Arterial Communication Before Aortic Arch Operation
Shigeki Morita, MD, PhDa,d,*,
Masahiro Yasaka, MD, PhDb,d,
Kotaro Yasumori, MD, PhDc,
Yasuhisa Oishi, MD, PhDa,
Toru Takaseya, MD, PhDa,
Hiromichi Sonoda, MD, PhDa,
Takemi Kawara, MD, PhDa
a Department of Cardiovascular Surgery, National Hospital Organization of Japan, Fukuoka, Japan
b Department of Cerebrovascular Disease, National Hospital Organization of Japan, Fukuoka, Japan
c Department of Radiology, National Hospital Organization of Japan, Fukuoka, Japan
d Clinical Research Institute, Kyushu Medical Center, National Hospital Organization of Japan, Fukuoka, Japan
Accepted for publication April 8, 2008.
* Address correspondence to Dr Morita, Department of Cardiovascular Surgery, Kyushu Medical Center, National Hospital Organization of Japan, 1-8-1 Jigyohama, Chuo-ku, Fukuoka 810-8563, Japan (Email: morita{at}kyumed.jp).
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Abstract
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Background: The assessment of intracranial arterial communication is important to prevent a stroke from occurring during an aortic arch operation. Bilateral axillary artery perfusion was used with the left common carotid artery perfusion for selective cerebral perfusion. A preoperative left carotid artery compression test with measurement of the left middle cerebral artery (LMCA) flow was performed to determine how safe it was to interrupt the perfusion to the left common carotid artery.
Methods: Eighteen patients who were scheduled for an aortic arch operation underwent the test. Before surgery, the LMCA flow was detected using transcranial Doppler ultrasonography. During manual compression of the left carotid artery, the flow velocity of the LMCA was measured and expressed as a percent in comparison to the precompression value.
Results: During carotid artery compression, flow velocity of the LMCA was reduced to 56% ± 36% (median, 63%; range, 0% to 100%) of the precompression value. The communication to the LMCA assessed with magnetic resonance angiography showed a weak relationship to the functional flow reserve of the LMCA based on a transcranial Doppler study. The results indicated that morphologic observation with magnetic resonance angiography did not reflect the dynamic nature of the intracranial collaterals.
Conclusions: A preoperative left carotid artery compression test with a measurement of the flow of the LMCA is useful to assess the feasibility of interrupting perfusion to the left carotid artery during aortic arch surgery with bilateral axillary artery perfusion.
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Introduction
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Brain protection during aortic arch surgery remains a major issue. Deep hypothermic circulatory arrest has been the standard technique for brain protection [1, 2]. The prolonged use of this technique has been questioned, however, owing to an increase in morbidity of neurologic complications [2, 3]. Antegrade selective cerebral perfusion effectively improves the safety margin during the procedure and has become a popular technique for brain protection [4]. Bilateral axillary artery perfusion with selective perfusion of the left common carotid artery has been introduced for selective cerebral perfusion to circumvent the complexity and encumbrance of the operative field, as described by Kurisu and colleagues [5] (Fig 1). It is sometimes necessary to interrupt the perfusion to the left carotid artery transiently because of the surgical procedure, or permanently owing to an underlying pathology. The question remains, however, whether it is safe to interrupt the perfusion to the left carotid artery.

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Fig 1. (A) Bilateral axillary perfusion shows the selective perfusion of the left common carotid artery during an aortic arch procedure. (B) The question remains regarding whether it is safe to interrupt the perfusion to the left common carotid artery. It is necessary to determine whether the left middle cerebral artery would be perfused through the cross-communicating arteries. Arrows indicate presence of blood flow in the arteries. Question marks indicate whether or not blood flow exists during the occlusion of the left carotid artery.
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To answer this question, transcranial Doppler ultrasonography was performed before surgery to visualize the left middle cerebral artery. The left common carotid artery was occluded with manual compression, and the changes in flow velocity of the left middle cerebral artery were measured. The results demonstrate the feasibility of the test and show the advantages of this method in comparison with preoperative magnetic resonance angiography (MRA).
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Patients and Methods
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Between March 2006 and May 2007, a total of 21 patients (15 men; median age 71 years, ranging from 52 to 88), who were electively scheduled for aortic arch surgery underwent the test preoperatively. Because of the retrospective and descriptive nature of this study, the Clinical Ethics Board of Kyushu Medical Center approved the record review and waived the need for individual informed consent.
Carotid ultrasonography (Philips iU22; Philips Medical System, Cleveland, Ohio) was first performed to check for intimal plaques in the left common carotid artery, and to confirm that it was safe to compress the artery. Next, the distal portion of the extracranial left internal carotid artery was visualized using transoral carotid ultrasonography [6]. The neck was then compressed over the left common carotid artery, and the occlusion was confirmed with transoral carotid ultrasonography. Finally, transcranial Doppler ultrasonography was used to visualize the left middle cerebral artery and measured flow velocity, before and during the left carotid artery compression (Fig 2).

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Fig 2. Two examples of the flow pattern of the left middle cerebral artery are shown. In case A, the flow of the left middle cerebral artery was maintained during the left common carotid artery compression. In case B, the left middle cerebral artery flow completely disappeared during the left common carotid artery compression. O and X indicate "good" and "poor" collateral flow to the left middle cerebral artery, respectively.
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In patients whose MRA was available, collaterals to the left middle cerebral artery were assessed by examining absence or hypoplasia of the anterior communicating artery and the left posterior communicating artery. The development of collaterals to the left middle cerebral artery was assessed as poor if both communicating arteries were absent or hypoplastic, good if both communicating arteries were intact, and fair if one of the communicating arteries was absent or hypoplastic.
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Results
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Of the 21 patients studied, the left middle cerebral artery could not be visualized with transcranial Doppler ultrasonography in 3 patients. These were a 70-year-old man, a 67-year-old woman, and an 88-year-old woman. In the remaining 18 patients, it was possible to measure the flow velocity of the left middle cerebral artery. The mean flow velocity before carotid artery compression was 55.8 ± 20.9 cm/s. It was reduced to 30.3 ± 22.8 cm/s during the left carotid artery compression. When the value was expressed as a percent in comparison to the flow velocity before compression, it was reduced to 56% ± 36%. These values were highly variable from patient to patient, ranging from 0% to 100%, with a median value of 63% (Fig 3). In 4 patients, the flow of the left middle cerebral artery completely disappeared during the compression of the left carotid artery. In the remaining patients, the flow velocity of the left middle cerebral artery was variable, which indicated that the development of intracranial arterial communication was, therefore, highly patient dependent.

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Fig 3. The left middle cerebral artery flow during the left common carotid artery compression was expressed as a percent of the precompression value (%LMCA flow) and sorted according to the value of %LMCA flow. Note that the values of %LMCA were highly variable.
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There was a very weak correlation between the age and flow velocity of the left middle cerebral artery during compression (Fig 4). The ages of the patients with no flow during the compression, were 64, 71, 84, and 85 years.

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Fig 4. The relationship between age and the left middle cerebral artery flow during the left common carotid artery compression expressed as a percent of the precompression value (%LMCA flow) flow is shown. The correlation constant between the %LMCA flow and age was weak (r = –0.43). Each circle indicates an individual patient.
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Magnetic resonance angiography was available preoperatively in 15 patients; 5 patients were identified by MRA to have poor collaterals to the left middle cerebral artery, 5 patients were identified as fair, and 5 patients as good (Fig 5).

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Fig 5. The patients were grouped based on the findings of magnetic resonance angiography, namely, as having good, fair, and poor cross-circulation to the left middle cerebral artery. The findings were related to the %LMCA flow. Each circle indicates an individual patient. (%LMCA = the left middle cerebral artery flow during the left common carotid artery compression expressed as a percent of the precompression value.)
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Patients who were assessed as having good collaterals by MRA showed good flow reserve during carotid artery compression. However, in patients who were assessed to have poor or fair collaterals based on MRA, 40% (4 of 10) of the patients had more than 50% of the left middle cerebral artery flow in comparison with the precompression value. Importantly, 1 patient who showed no flow of the left middle cerebral artery during carotid artery compression was assessed to have at least one communicating artery to the left middle cerebral artery by MRA. These findings implied that the morphologic observation with MRA did not reflect the functional flow reserve of the left middle cerebral artery during the left carotid artery compression.
During surgery, none of the patients required clamping of the left common carotid artery. There was 1 hospital death due to pneumonia. One patient had cerebral infarction at the right hemisphere; this patient fully recovered neurologically and was discharged.
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Comment
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Brain complications are a major cause of morbidity and mortality in aortic arch surgery. Traditionally, hypothermic circulatory arrest has been used during the manipulation of the aortic arch [1, 2]. Hypothermic circulatory arrest is a simple and reliable method of brain protection if the duration is kept shorter than 25 minutes [7]. An alarming incidence of neurologic complications has been reported when the duration of hypothermic circulatory arrest is prolonged. Selective cerebral perfusion, first reported using normothermic perfusion of the arch vessels by De Bakey and colleagues [8], was revisited by Bachet's group using cold blood as a perfusate [9]. Recently, Kazui and colleagues [4, 10] refined the technique with the introduction of selective cannulation to the brachiocephalic and left carotid artery with the left subclavian artery clamped. The concept underlying this technique is to maintain physiologic antegrade perfusion to the brain without interruption. Bilateral axillary artery perfusion was introduced because perfusing all the cerebral arteries is considered to have a protective effect on the brain (Fig 1). In the current study, we sought to investigate how safe it was to interrupt the flow to the carotid artery when other arch vessels were perfused.
Transcranial Doppler ultrasonography to visualize the flow of the left middle cerebral artery showed that, in nearly half of the patients, compression of the left carotid artery caused a significant flow reduction in the left middle cerebral artery. There have so far been few studies that elucidate intracranial artery communication to evaluate safety during the aortic arch surgery. Merkkola and colleagues [11] reported that with right unilateral perfusion through the right axillary artery, 14% to 16% of the subjects would be exposed to malperfusion of the left hemisphere owing to an incomplete Circle of Willis. They studied postmortem subjects and examined the diameter of the communicating arteries of the Circle of Willis. Their study did not include a functional assessment, such as the transcranial Doppler ultrasonography used in the current study. Our current results indicated that morphologic completeness of the Circle of Willis observed with MRA does not guarantee a functioning collateral circulation. These findings are consistent with those of Hoksbergen and associates [12] that there is a threshold diameter, which is around 0.5 mm, to allow for cross-flow through the primary collateral arteries of the Circle of Willis. With the MRA, it may not be possible to discriminate the arteries with a diameter larger or smaller than 0.5 mm.
What is the impact of current study on the practice of aortic arch surgery? With bilateral axillary artery perfusion, there is no interruption of the flow to the cerebral arteries, especially for the arteries perfused through the brachiocephalic artery and the left subclavian artery. The interruption of the flow to the left common carotid artery would occur in some occasions, such as with acute aortic dissection, which involves the left common carotid artery. On those occasions, putting a cannula into the carotid artery may not be feasible. When the test shows a good flow of the left middle cerebral artery with compression of the left carotid artery, it may be possible to interrupt the perfusion to the left common carotid artery, and reconstruct the left common carotid artery with a good safety margin.
The notable limitation of this test is that it cannot evaluate the appropriateness of the technique of only perfusing the brachiocephalic artery with [3, 4, 13] or without left common carotid artery [14, 15] perfusion. A preoperative evaluation of the intracranial circulation in the above situations with transcranial Doppler ultrasonography cannot be performed because it is not possible to interrupt the flow of the left vertebral artery. For this purpose, the assessment of the functional patency of the anterior communicating artery and both posterior communicating arteries should be performed [12]. The test requires visualization of the anterior and posterior cerebral arteries with quantitative measurement of flow velocities. These extensive evaluations were not performed because the test was beyond the scope of the clinical requirements. But if one is using only brachiocephalic artery perfusion as a technique for selective cerebral perfusion, then the assessment of the functional patency of the anterior communicating artery and both posterior communicating arteries is worth considering. The other obvious limitation of the current study is the small number of patients investigated. The collection of more extensive data is therefore warranted.
In conclusion, a functional assessment of the intracranial collaterals to the left middle cerebral artery was performed with the compression of the left common carotid artery. The test is considered to be useful to evaluate the safety of interrupting the left common carotid artery perfusion during aortic arch surgery with bilateral axillary perfusion.
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