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(Stroke. 1995;26:1603-1606.)
© 1995 American Heart Association, Inc.

Articles

Middle Cerebral Artery Blood Flow Velocity and Stable Xenon-Enhanced Computed Tomographic Blood Flow During Balloon Test Occlusion of the Internal Carotid Artery

W. Andrew Kofke, MD; Patric Brauer, MD; Raymond Policare, MPH; Susan Penthany, RN, PA-C; David Barker, BS Joseph Horton, MD

From the Departments of Anesthesiology/Critical Care Medicine (W.A.K., R.P.) and Neurological Surgery (W.A.K.), University of Pittsburgh (Pa) School of Medicine (D.B.); Department of Anesthesiology, University Hospital Eppendorf, Hamburg, Germany (P.B.); Department of Radiology, Division of Neuroradiology, University of Pittsburgh (Pa) Medical Center (S.P.); and Department of Radiology, Medical University of South Carolina, Charleston (J.H.).

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Transcranial Doppler ultrasonography has been reported to reflect changes in cerebral blood flow (CBF) with the use of radioactive tracer techniques, which are weighted to measure primarily cortical structures. We tested the hypothesis that changes in transcranial Doppler ultrasonography would reflect changes in CBF in the middle cerebral artery vascular territory with the use of stable xenon-enhanced CT to assess CBF during carotid occlusion.

Methods Thirty-one conscious patients underwent balloon test occlusion of the internal carotid artery and transcranial Doppler ultrasonography and xenon-enhanced CT assessment of blood flow velocity and CBF, respectively, of the middle cerebral artery and its distribution during balloon test occlusion.

Results A significant correlation was seen between the change in CBF and the change in blood flow velocity for both brain levels at which CBF was determined (P<.0001). The average change in blood flow velocity was -13.4%, and the change in CBF was -15.1% and -17.7% at the two anatomic levels examined.

Conclusions The data indicate that changes in blood flow velocity generally reflect changes in CBF throughout the middle cerebral artery vascular territory with abrupt occlusion of the internal carotid artery in unanesthetized humans.

Key Words: cerebral blood flow • cerebral ischemia • tomography, emission-computed • ultrasonics

	Introduction

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Blood flow velocity in major human basal cerebral arteries can be measured noninvasively and continuously by TCD. Recent studies suggest that changes in TCD MCA blood flow velocity during carotid endarterectomy may reflect changes in CBF.^{1 2} These studies, however, were done in anesthetized humans with rCBF assessed by radioactive xenon injection. The purpose of this investigation was to determine the relationship between MCA blood flow velocity and CT assessment of CBF in the MCA distribution during acute carotid occlusion in conscious humans.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
After Institutional Review Board approval and informed consent were obtained, 38 adult patients were enrolled in the study. All patients were scheduled for an elective balloon test occlusion to assess the effects of carotid occlusion on neurological examination and CBF before planned surgical occlusion of the carotid artery.^{3 4} MCA blood flow velocity was detected at the ipsilateral temporal window at depths of 45 to 60 mm with a pulsed-wave, range-gated TCD instrument (Transpect, Medsonics) with the use of a 2-MHz probe secured with a head harness and was recorded by means of a video thermal graphic printer. Blood flow velocity was recorded immediately before and continuously during balloon inflation and immediately after balloon deflation.

Balloon Test Occlusion Method
A complete balloon test occlusion examination was performed as described previously.³ After baseline neurological examination, a four-vessel angiogram was performed, and a double lumen catheter was introduced (Swan-Ganz, Edward Laboratories) into the femoral artery. The catheter was advanced within the ICA to the level of the first or second cervical vertebral body. The patient was given 5000 to 7000 U IV of heparin during the procedure. While continuously measuring blood pressure through the angiographic catheter in the distal ICA and intermittently measuring systemic blood pressure using an automatic dynamometer (Critikon Dynamap), we inflated the intra-arterial balloon with radiographic contrast material until distal pressure fell and balloon deformation consistent with the vessel was observed. Intracarotid occlusion was further confirmed by injecting a small amount of radiographic contrast material distal to the balloon and observing a stagnant column of intracarotid radiopaque material. A continuous neurological examination was performed for 5 minutes and subsequently at 4- to 5-minute intervals. The balloon remained inflated for a 15-minute period but was immediately deflated if the patient showed any neurological alteration. If no neurological alteration was seen, the patient was transferred to the CT suite with the balloon deflated but still in place. After transfer to the CT suite, a lateral scout image was acquired to verify that the balloon was at the same location as it was in the fluoroscopy suite. We performed xenon-enhanced CT CBF studies with the balloon deflated and during a second 5-minute period of balloon reinflation using an identical balloon inflation volume and being careful to minimize any movement of the angiographic catheter. If there was any question about maintenance of an occlusive position of the inflated balloon while the patient was undergoing CT, a small amount of radiographic contrast was injected to confirm the presence of a stagnant column of intracarotid radiopaque material.

Xenon CT CBF Measurement
CBF studies were performed with the xenon CT CBF system, including software and hardware adapted to our scanner (GE 9800, General Electric Medical Systems). During the CBF studies, the patients inhaled a gas mixture of 33% xenon/67% oxygen (Xe SCAN, Linde Medical Gases). After two baseline scans per brain level, the xenon enhancement was monitored with six scans per brain level during a 5-minute gas inhalation period.⁵ The radiodensity enhancement of brain tissue caused by the inhalation of stable xenon was used in a modified Kety equation⁶ to calculate CBF.

For the first carotid occlusion, TCD monitoring was performed through the ipsilateral temporal window with isonation adjusted to the MCA. This artery was monitored continuously before, during, and after balloon occlusion. Subsequently, each patient underwent xenon CT CBF with the balloon deflated, followed by a repeat CBF study with the balloon inflated.

For each subject the MCA distribution on CT was manually determined post hoc, and the average CBF within this territory was calculated^{7 8} and correlated with MCA blood flow velocity.

Statistical Analysis
Repeated mean blood flow velocity and physiological data were analyzed by ANOVA and protected t tests. CBF data underwent paired t tests, and correlations were determined with Pearson's correlation coefficient. SPSS software was used for statistical procedures (SPSS, Inc).

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
CBF and TCD data are shown in Fig 1. Of the 38 patients enrolled, 31 underwent both TCD and CBF assessment. The average baseline MCA blood flow velocity was 58.3 cm/s, decreasing to a low of 49.1 cm/s with balloon test occlusion and increasing to 59.7 cm/s on reinflation. Regional MCA CBF was 53.0 and 53.8 mL/100 g per minute at the two anatomic levels measured at preinflation and declined to 45.0 and 43.1 mL/100 g per minute with inflation. The average change from baseline blood flow velocity was -13.4%, and the changes for the two CBF anatomic levels were -15.1% and -17.7% (P<.05). Fig 2 shows the correlation between changes in MCA velocity and changes in CBF within the MCA territory. The TCD recordings from one patient are depicted in Fig 3.

View larger version (23K): [in this window] [in a new window]   Figure 1. Graph shows MCA blood flow velocity (MCABFV) and distribution of CBF before, during, and after endovascular occlusion of the ICA in awake humans. *P<.05.

View larger version (14K): [in this window] [in a new window]   Figure 2. Scatterplots show change in MCA blood flow velocity (MCABFV) as a function of change in MCA distribution of CBF during balloon test occlusion. In level 1 (top), r2=.73 (P<.0001); in level 2 (bottom), r2=.43 (P<.0001).

View larger version (45K): [in this window] [in a new window]   Figure 3. TCD recordings for one patient before (top left), during (top right, middle left), and after (middle right, bottom left) endovascular occlusion of the carotid artery. LMCA indicates left MCA.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Endovascular balloon test occlusion of the carotid artery, with assessment of neurological function and CBF, is often used to determine the safety of sacrificing the ICA during some neurosurgical procedures. Moreover, it can provide justification for an intraoperative revascularization procedure with carotid artery resection.⁹ Previous studies have assessed the blood flow map on endovascular balloon inflation in the carotid artery.^{3 4} When the xenon CT CBF study with endovascular ICA balloon occlusion is compared with the baseline, patients generally fall into one of four groups: (1) CBF unchanged; (2) a mild global decrease in CBF; (3) an asymmetrical decrease in CBF, with CBF lower on the side of the occlusion; or (4) a transient neurological deficit with the balloon occlusion, presumably due to ischemia. Patients in the last group do not have xenon CBF measurements taken. Patients in groups 1 and 2 are considered to be at low risk for stroke after ICA resection or occlusion, whereas patients in groups 3 and 4 are at high risk for stroke.

TCD does not measure CBF but rather blood flow velocity. This velocity is affected by a number of variables including CBF, vascular caliber, hematocrit, viscosity, and insonation depth and angle.¹⁰ Sorteberg et al¹¹ examined the relationship between absolute rCBF and blood flow velocity in 17 normal subjects, observing a statistically significant correlation. However, there was wide scatter along the regression line, making blood flow velocity unsuitable to predict rCBF in a given patient. Moreover, others have reported a poor correlation between blood flow velocity and rCBF.^{12 13} These observations indicate that a one-time measurement of blood flow velocity cannot be used reliably to estimate CBF in a given subject.

Several investigations have examined the relationship between changes in rCBF and changes in blood flow velocity. Several methods have been used to induce changes in these measurements. These generally include alterations in brain tissue PCO₂ or changes in intracranial arterial pressure. Techniques of altering tissue PCO₂ include altering ventilation or inspired CO₂¹⁴ or administering acetazolamide.^{15 16} Methods of altering intracranial arterial pressure include changing blood pressure by administration of vasoactive drugs^{14 17 18} or decreasing cardiac preload^{14 18 19 20 21} or inflow interruption by occlusion of the carotid artery.^{1 2} In addition, assessment of the relationship of rCBF to blood flow velocity during exercise has also been reported.^{22 23} In all of these studies and others, conditions were further varied with respect to the presence or absence of cerebrovascular disease, use of anesthesia, and method of determining rCBF. Accordingly, the results are somewhat variable, most likely due to the disparate conditions.

There have been several case reports on the effects of carotid occlusion on blood flow velocity without rCBF assessment in unanesthetized subjects.^{24 25} In these cases a decrement in blood flow velocity resulted from carotid occlusion with a decrease in pulsatility index. Correlation of carotid occlusion–induced decrements in blood flow velocity with CBF was performed in anesthetized patients with cerebrovascular disease with the use of ¹³³Xe rCBF technology.^{1 2} Such data obtained during carotid endarterectomy suggest that blood flow velocity changes can estimate cortical CBF decreases as measured by gamma counter detection of radioactive xenon entering the brain. The correlation in that situation is strong at lower CBF. However, this technique does not assess deeper structures in the brain and can be misleading if cortical flow is low with persistent perfusion in deeper structures.²⁶ Moreover, the lack of correlation at higher rCBF may have been related to the fact that TCD measures blood flow velocity in some MCA territories not measured by ¹³³Xe rCBF. Our data provide additional information regarding the relationship between rCBF and MCA blood flow velocity in awake subjects without known arteriosclerotic disease undergoing abrupt carotid occlusion. Importantly, we provide evidence of a positive correlation between rCBF and blood flow velocity in this situation, assessing the entire MCA territory with stable xenon CT CBF.

An additional factor in evaluating data involving decrements in intracranial arterial pressure is whether the arterial pressure is below the autoregulatory threshold, since this may involve alterations in vascular caliber.²⁷ Data from studies assessing and/or correlating rCBF and blood flow velocity within the autoregulatory range indicate that CBF changes briefly until autoregulatory adjustments occur, after which it returns to its prior level. Blood flow velocity varies with changes in CBF.^{18 21} Our data and observations of Halsey et al^{1 2} and Larsen et al¹⁸ also indicate that rCBF and blood flow velocity vary proportionately when intracranial arterial pressure decreases below the lower limit of CBF autoregulation.

We observed two instances of rather poor correlation (ie, a 5% velocity increase with a 34% CBF decrease and a 25% velocity increase with a 6% CBF increase), which suggests that TCD readings may occasionally misrepresent CBF. Because we were unable to measure TCD and CBF simultaneously, it is also possible that the variability was due to the measurements being made during different balloon inflations. Nonetheless, overall the data support the theory that TCD generally reflects MCA territory CBF in situations of abrupt carotid occlusion.

	Selected Abbreviations and Acronyms

 

CBF = cerebral blood flow ICA = internal carotid artery MCA = middle cerebral artery rCBF = regional cerebral blood flow TCD = transcranial Doppler ultrasonography

	Acknowledgments

 
The authors gratefully acknowledge the assistance of Margaret Moriello and Cynthia Hladik with manuscript preparation and thank Francie Siegfried for editorial review. In addition, the authors are grateful for the review of the manuscript provided by Howard Yonas. Medsonics (Fremont, Calif) kindly loaned the TCD instrument.

	Footnotes

 
Reprint requests to W. Andrew Kofke, MD, Department of Anesthesiology/CCM, University of Pittsburgh School of Medicine, A1305 Scaife Hall, Pittsburgh, PA 15241. E-mail wak@med.pitt.edu.

Received March 21, 1995; revision received June 9, 1995; accepted June 16, 1995.

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