Venous Phase Timing Does Not Predict SPECT Results During Balloon Test Occlusion of the Internal Carotid Artery

Accepted Manuscript Venous Phase Timing Does Not Predict SPECT Results during Balloon Test Occlusion of the Internal Carotid Artery Brian M. Snelling, M.D., Samir Sur, M.D., Sumedh S. Shah, B.S., Racheal I. Wolfson, M.D., Sudheer Ambekar, M.D., Dileep R. Yavagal, M.D., Mohamed S. Elhammady, M.D., Eric C. Peterson, M.D., M.S. PII:

S1878-8750(17)30335-2

DOI:

10.1016/j.wneu.2017.03.023

Reference:

WNEU 5392

To appear in:

World Neurosurgery

Received Date: 14 November 2016 Revised Date:

4 March 2017

Accepted Date: 7 March 2017

Please cite this article as: Snelling BM, Sur S, Shah SS, Wolfson RI, Ambekar S, Yavagal DR, Elhammady MS, Peterson EC, Venous Phase Timing Does Not Predict SPECT Results during Balloon Test Occlusion of the Internal Carotid Artery, World Neurosurgery (2017), doi: 10.1016/ j.wneu.2017.03.023. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Venous Phase Timing Does Not Predict SPECT Results during Balloon Test

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Occlusion of the Internal Carotid Artery

Authors:

Brian M. Snelling, M.D.,a Samir Sur, M.D.,a Sumedh S. Shah, B.S.,a Racheal I. Wolfson, M.D.,a

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Sudheer Ambekar, M.D.,a Dileep R. Yavagal, M.D.,b Mohamed S. Elhammady, M.D.,a Eric C. Peterson, M.D., M.S.a

a

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Affiliations:

Department of Neurological Surgery, University of Miami Miller School of Medicine, Miami,

Florida.

Department of Neurology, University of Miami Miller School of Medicine, Miami, Florida.

Corresponding Author:

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b

Eric C. Peterson, M.D., M.S.

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Department of Neurological Surgery

University of Miami School of Medicine

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1095 NW Terrace

Miami, FL 33136

Office: (305) 355-1101; E-mail: [email protected]

Running Title: Correlation of Venous Phase Timing and SPECT during BTO of the ICA Key Words: Angiography, Aneurysm, Balloon Occlusion Test, SPECT, Internal Carotid Artery

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ABSTRACT Introduction: The purpose of this study is to evaluate the role of venous phase timing when

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compared to Technetium-99m Single Photon Emission Computed Tomography (SPECT) during angiographic balloon test occlusion of the internal carotid artery (ICA) and subsequent sacrifice of the ICA.

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Methods: Fifty-six patients underwent formal BTO from April 2008, to February 2014, at our institution. Venous phase timing was calculated for each patient. SPECT imaging for each

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patient was interpreted by the nuclear medicine radiologist. Statistical analysis between the three groups (No Hypoperfusion, Mild Hypoperfusion, Moderate/Severe Hypoperfusion) was calculated using ANOVA.

Results: Twenty-six patients showed no hypoperfusion during SPECT. The average delay of venous phase for these patients was 0.65 seconds. Eight of the 26 patients went on to have vessel

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sacrifice, with none showing evidence of infarction at the time of discharge. Six patients showed evidence of mild hypoperfusion on SPECT. None of these patients went on to have vessel

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sacrifice. The average venous delay was 0.5 seconds. Twenty-four patients were found to have moderate or severe hypoperfusion. The average venous delay was 1.08 seconds. ANOVA

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between the three groups demonstrated no significant difference (p=0.22). Conclusion: Our study demonstrated no correlation between venous phase timing and SPECT. Future studies comparing multiple tests with patients who have had vessel occlusion are necessary to determine the best adjunctive measures to predict delayed ischemia following carotid occlusion.

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INTRODUCTION Therapeutic

carotid

occlusion

is

an

important

tool

in

the

neurosurgeon’s

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armamentarium.1 Balloon test occlusion (BTO) is used to assess the adequacy of collateral circulation and predict the risk of ischemic complications from carotid occlusion. Additionally, BTO is frequently employed in combination with physiologic and imaging modalities to increase

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the sensitivity in predicting ischemia.2

Adjunctive testing results in a more complicated, expensive, and lengthier procedure, and

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none of the adjunctive modalities have proven to be able to predict delayed ischemia. At our institution, BTO is most frequently performed in combination with single-photon emission computed tomography (SPECT) in order to best determine the risk of developing ischemic complications following carotid sacrifice.

The aim of our study is to assess the correlation between angiographic findings on BTO,

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namely the delay in venous phase onset between hemispheres, and the results of SPECT

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imaging.

MATERIALS AND METHODS

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Following approval from our Institutional Review Board, a retrospective review of all patients undergoing BTO at our institution from April 2008, to February 2014, was conducted. Balloon Test Occlusion

Each procedure was performed with local anesthesia and minimal intravenous conscious

sedation, ensuring that the patient could be examined neurologically during the test occlusion. A 5 French (F) or 6F sheath was placed into the right common femoral artery and a 5F sheath was 3

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placed into the left common femoral artery. Intravenous heparin was administered to maintain the activated clotting time between 250-300 seconds for the duration of the procedure.

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Angiography of both internal carotid arteries (ICA) and one vertebral artery was performed using a 5F diagnostic catheter, including specific magnified and three-dimensional views to better assess the lesion in question. The catheter was then placed into ICA contralateral to the side of

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test occlusion. A 5F or 6F guide catheter (Envoy; Codman, Raynnam, MA) was subsequently placed into the ICA to be tested.

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An occlusion balloon (Hyperform 7 x 7 mm; ev3/Covidien, Irvine, CA) was then advanced through the guide catheter and inflated under roadmap guidance in the ICA at the location of possible occlusion. Confirmation of occlusion was obtained by injection through the guide catheter. Angiography of the contralateral ICA and vertebral artery was then performed with the diagnostic catheter. The procedure was terminated if the patient developed any clinical

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signs of ischemia. In cases of clinical failure, venous phase delay was not typically recorded. The diagnostic catheter was removed and the sheath connected to a blood pressure

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monitor. Following ten minutes of occlusion, hemodynamic challenge using a sodium nitroprusside intravenous drip was started and titrated to reduce the mean arterial pressure to 2/3

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of baseline. Serial neurological examinations of the patient were performed every two minutes for the duration of test occlusion. Once the hypotensive blood pressure goal was maintained for a period of fifteen minutes, Technetium Tc-99m Bicisate was injected intravenously. The balloon was then deflated under fluoroscopy. Follow-up cervical and cerebral ICA angiography through the guide catheter was performed to rule out vessel dissection at the site of balloon inflation or intracranial vessel cut-off. The guide catheter was removed and closure devices were applied to 4

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both femoral puncture sites (Angioseal; Saint Jude Medical, St. Paul, MN). The patient was then taken for SPECT imaging. All SPECT studies were deemed technically adequate by the

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reviewing radiologist. Selection Criteria

Patients were excluded from the study for any of the following reasons: failure to tolerate

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the BTO clinically prior to radio-isotope injection, balloon placement in a vessel other than the ICA, no hemodynamic challenge performed, collateral circulation not evaluated during the BTO,

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or SPECT imaging not obtained following BTO. Study Definitions

Venous phase timing was calculated as the difference in seconds between the onsets of cortical vein filling of the two cerebral hemispheres during BTO. The venous delay was calculated independently by two authors (BS and SA) to improve accuracy. In cases with

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discordance, the senior author (EP) was consulted to determine the venous delay accurately. SPECT imaging for each patient was designated into one of three categories: No Hypoperfusion,

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Mild Hypoperfusion, or Moderate/Severe Hypoperfusion. This designation is based on the qualitative interpretation from the attending nuclear medicine radiologist.

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Data Analysis

Statistical analysis of the designated SPECT groups was calculated using an analysis of

variance (ANOVA).

RESULTS Patient Demographics 5

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Sixty-eight patients underwent formal BTO of the ICA during this time period. Twelve patients demonstrated clinical ischemia, and the exam was terminated prior to SPECT imaging.

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Thus, 56 patients underwent BTO of the ICA followed by SPECT imaging in anticipation of possible parent vessel. No procedural complications were noted. Forty were female and 16 patients were male. Average age of included patients was 55 years (range = 27 – 82 years).

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Twenty-five patients had cervical or intracranial tumors, while 31 harbored ICA aneurysms (Table 1).

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Venous Delay

Twenty-three patients demonstrated a synchronous venous delay (Table 2). Seventeen patients had a delay of one second or less. Ten patients had a delay of less than two seconds, but greater than one second. Five patients had a delay of less than three seconds, but greater than two

SPECT Imaging

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seconds. One patient had a delay of four seconds.

Twenty-six patients demonstrated normal SPECT imaging (‘No Hypoperfusion’). The

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mean delay of venous phase onset was 0.65 seconds, with a range of 0 to 3 seconds. Six patients were deemed to have mildly reduced perfusion on SPECT imaging (‘Mild Hypoperfusion’). The

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mean delay of venous phase onset was 0.5 seconds, with a range of 0 to 2 seconds. Twenty-four patients exhibited moderate or severe hypoperfusion (‘Moderate/Severe Hypoperfusion’) on SPECT imaging. The mean delay of venous phase onset was 1.08 seconds, with a range of 0 to 4 seconds.

ANOVA between the three groups—No Hypoperfusion, Mild Hypoperfusion, and Moderate/Severe Hypoperfusion—revealed no statistically significant difference between the 6

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groups (p = 0.22). Unpaired t-test was used to compare venous delay in patients with no hypoperfusion by SPECT with patients demonstrating any evidence of hypoperfusion and those

between groups (p=0.24 and p=0.14, respectively). Procedures Performed

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demonstrating ‘Moderate/Severe’ hypoperfusion. Again, no significant difference was found

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Eight of the 26 patients who demonstrated normal SPECT imaging (‘No Hypoperfusion’) went on to have vessel sacrifice, with none showing evidence of ischemia or infarction at the

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time of discharge. The mean delay in this subset of patients was 0.79 seconds, with a range of 01.33 seconds, and a median delay of 1 second. No procedural complications were seen. Of the 30 patients who exhibited any hypoperfusion (‘Mild or Moderate/Severe Hypoperfusion’) on SPECT imaging, 15 patients had pathology related to cervical or intracranial tumors. ICA sacrifice was performed in one patient in this category—a patient with known

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frontotemporal encephalomalacia in whom moderate hypoperfusion could not be ruled out based on SPECT scan and no evidence of venous delay in which ICA preservation could not achieved.

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Eleven patients had ICA preservation during surgery, one patient underwent an arterial bypass, and two patients underwent placement of a covered stent graft for ICA preservation. No

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procedural complications were seen.

It is important to note that our patient who underwent carotid sacrifice with

“moderate/severe hypoperfusion” on SPECT scan tolerated sacrifice well, and at the most recent follow-up (around 2.5 years post procedure), there were no clinical signs of ischemia. The findings were noted on the radiology report and including the patient in the “no hypoperfusion” category did not alter the significance of our results. 7

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Fifteen of the patients in the Mild or Moderate/Severe Hypoperfusion category had pathology related to aneurysms of the cervical, petrous, cavernous or intracranial circulation.

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Five patients underwent flow diverting stent placement, seven patients underwent coil or Onyx (ev3/Covidien, Irvine, CA) embolization with or without stent-assistance, one patient underwent trapping and bypass, while two patients had conservative management with observation. No

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procedural complications were seen. Patient Follow-Up

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Clinical follow up beyond discharge was available for 6 of 8 patients who underwent vessel sacrifice (‘No Hypoperfusion’). No patient demonstrated ischemia or infarction, which ranged from 18 to 63 months, with a mean of 38 months.

Of the 30 patients who exhibited any hypoperfusion (‘Mild or Moderate/Severe Hypoperfusion’) on SPECT imaging, follow up beyond discharge was available for 28 patients.

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The average length of follow up was 21 months, with a range of 4 to 72 months. One patient who underwent covered stent placement developed an infection of the stent, requiring prolonged

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hospitalization and multiple surgeries without vessel sacrifice. Two complications were noted in the aneurysm subgroup: one patient managed with observation developed worsening

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ophthalmoplegia from a cavernous aneurysm, while a second patient died from a subarachnoid hemorrhage following placement of a flow diverting stent that did not successfully exclude a posterior communicating artery aneurysm from circulation. Case Illustration

A 61-year-old female patient presented to our service with a right ICA aneurysm, which was found incidentally during cranial imaging. The lesion, measuring 8.0mm x 4.0mm, was 8

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located on the dorsal aspect of the right ICA, just distal to the take off of the ophthalmic artery (Figure 1a). Due to the aneurysm location and the possibility of carotid sacrifice should the need

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arise, our patient underwent right carotid BTO, along with SPECT radiography. The BTO of the right ICA was well tolerated by the patient, and induced hypotension to 90mmHg (systolic) progressed without incident. We recorded a venous delay of 0 seconds with our patient (Figure

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1b and 1c). However, SPECT scanning revealed evidence of decreased flow in the right middle cerebral artery territory involving the right frontal, temporal, and parietal lobes. Analysis of the

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left hemisphere though showed normal radionuclide blood flow activity (Figure 1d). Ultimately, the patient underwent successful stent-assisted coiling of her aneurysm with no evidence of recanalization at two-year follow-up.

Venous delay did not predict SPECT results in this example, as was the case elucidated

DISCUSSION

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through our analysis.

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Therapeutic ICA sacrifice remains an important treatment modality for certain intracranial aneurysms, neoplastic disease of the brain and head and neck, carotid-cavernous

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fistulas, and other traumatic and infectious etiologies. Given the significant ischemic risks associated with ICA occlusion, careful patient selection is paramount. Mathis et al. (1995) found that temporary balloon occlusion of the ICA can be performed to identify patients at risk for stroke after carotid sacrifice.3 BTO has thus become an important screening test and venous phase timing has shown promise in reliably predicting ischemic complications from carotid occlusion.4,5 However, there is no consensus as to what maximal venous phase delay can safely 9

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tolerate carotid occlusion. Furthermore, these measurements are often made from BTO performed under general anesthesia, which may limit the application of these results in patients

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in whom BTO is performed under conscious sedation.5,6 Clinical evaluation, including hemodynamic challenge, has been shown to reduce morbidity associated with vessel sacrifice by improving our ability to exclude patients with a

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high probability of having ischemic complications. However, delayed failure to tolerate ICA occlusion is well documented in patients who initially pass clinical BTO examination.7,8

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Various adjunctive tests in addition to clinical exam and venous timing have been proposed in an effort to better identify this group. Unfortunately, these additional tests often lead to increased expenses and testing times, further complexity, and theoretical increased risk for the patient without yet demonstrating reproducible and accurate prediction of failure to tolerate carotid occlusion in the long term.9,10

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Of several adjunctive tests used to evaluate cerebral perfusion in the setting of BTO, SPECT has been frequently applied and is part of our institutional protocol for BTO. This test is

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based on the expectation that the radio-isotope injected during balloon occlusion of the ICA will have a high first-pass extraction rate in brain tissue and a delayed washout, thereby enabling

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accurate recording of cerebral perfusion during carotid occlusion when imaging is performed after completion of the angiographic portion of the test. Prior studies evaluating the role of SPECT in BTO have used semi-quantitative radioactivity count ratios between the test-occluded and contralateral hemispheres (L/N ratio), and these ratios correlate well with radiologist interpretation.11 Additionally, recent attempts at quantifying SPECT data and correlating this

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data with angiographic findings in the patients under general anesthesia have been met with some success.6

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Nonetheless, several challenges exist in applying BTO with SPECT imaging widely and accurately. The first is variability in study protocol. Many clinicians perform BTO under general anesthesia, and there are no specific or universally agreed criteria for hemodynamic challenge

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and the timing of tracer injection. It is possible that injection of the tracer under conditions of significant hypotension, even without an obvious neurological change in the patient, may affect

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uniform distribution of the tracer if cerebral perfusion is at its threshold. Second, the semiquantitative nature of SPECT results has opened this adjunct testing to criticism and has hindered the establishment of validated thresholds for predicting tolerance to BTO. Indeed, a significant number of delayed ischemic complications have been described in previous series in patients demonstrating no hypoperfusion on SPECT who undergo carotid sacrifice.12-14 Finally, SPECT

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imaging interpretation can be complicated by existing structural abnormalities or artifact from metallic implants (cranioplasty plating/mesh e.g.).

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Despite the challenges of interpreting results of BTO with SPECT imaging, multiple modalities should be considered when patients are being evaluated for possible carotid sacrifice.

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SPECT remains a valuable instrument and could be a useful adjunct test in cases where there exists a high pre-test probability of inadequate collateral supply. Carotid sacrifice can be well tolerated in many patients; however, the consequences of delayed ischemia may be devastating. Therefore, at our institution we are reticent to consider carotid sacrifice in patients who demonstrate any evidence of inadequate perfusion.

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In our series of consecutive patients undergoing BTO, we find no correlation between the onset of the venous phase in each hemisphere and SPECT results. Thirty patients exhibited any

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hypoperfusion—Mild or Moderate/Severe—on SPECT imaging; however, 14 of these patients also had synchronous venous phases (venous delay = 0 seconds). Of the 24 patients who exhibited moderate to severe hypoperfusion on SPECT, 10 patients had no venous delay and

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three patients had venous delay less than 1 second.

These findings underscore the difficulty in assessing these patients and accurately

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determining the risk of ischemic events. Given the relative strength of data supporting venous phase timing as a predictor of tolerance to carotid sacrifice, perhaps the utility of SPECT should be re-evaluated. Conversely, despite the lack of correlation between angiographic and SPECT results in our series, there is potential benefit in using multiple, sensitive modalities to identify patients at risk of developing ischemic complications.

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While utilization of both angiographic and adjunct modalities allow for increasing sensitivity, it is prudent to recognize that subsequent complex management decisions may be

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associated with high morbidity. That is to say, excluding patients from carotid sacrifice to prevent exposure to risk of ischemic complication, may paradoxically increase their exposure to

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morbidity by recommending more complex intervention. Thus, while it is clear that further studies are needed to determine the utility of adjunct

testing in BTO; perhaps a broader view is also required: to properly evaluate BTO, we must investigate not only the risk of ischemic complication following sacrifice of the ICA, but also the morbidity of excluding patients from this more traditional therapy in favor of complex, carotidsparing strategies. 12

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Limitations There are several limitations to our study. We excluded patients who did not undergo

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formal BTO. Only eight of 26 patients who passed formal BTO and demonstrated no hypoperfusion on SPECT underwent ICA occlusion. One patient who demonstrated asymmetry on SPECT due to an existing structural lesion underwent vessel sacrifice; however, repeating

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statistical analysis of our cohort excluding this patient did not change our results. More significance could be interpreted from our findings had patients across a range of SPECT results

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undergone carotid occlusion. In addition, our SPECT results are only qualitative. This has been a frequent criticism of the modality that creates difficulty in interpreting results. Finally, no baseline SPECT imaging was performed. Thus, patients with pre-existing hemispheric hypoperfusion may have exhibited falsely negative SPECT imaging. Despite these limitations, our study provides valuable data as all the procedures were

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CONCLUSION

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performed using the same protocol.

Our study demonstrated no correlation between venous phase timing and SPECT. Future

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studies comparing multiple tests with patients who have had vessel occlusion are necessary to determine the best adjunctive measures to predict delayed ischemia following carotid occlusion. We recommend a patient-specific approach to diagnostic evaluation and management in patients harboring diseases of the head and neck in whom carotid sacrifice is considered. This includes the use of SPECT as an adjunct to the traditional angiographic and clinical BTO in cases where

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there is significant pretest concern for the development of ischemic complication. In patients

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where such a risk is low, perhaps more judicious use of adjunct testing in BTO is warranted.

CONFLICT OF INTEREST

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None.

FUNDING

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This research did not receive any specific grant from funding agencies in the public, commercial,

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EP

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or not-for-profit sectors.

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FIGURE LEGEND Figure 1. 1A and 1B. Radiographic findings of a patient with a right ICA aneurysm distal

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(asterisks). Analysis of the BTO of the right ICA during the mid-arterial phase (1C) and the early venous phase (1D) indicated a venous delay of 0 seconds. SPECT scanning (1E), however,

showed evidence of decreased flow in the right MCA territory involving the frontal, temporal

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and parietal lobes (arrowheads).

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REFERENCES 1. Elhammady MS, Wolfe SQ, Farhat H, Ali Aziz-Sultan M, Heros RC. Carotid artery sacrifice

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for unclippable and uncoilable aneurysms: endovascular occlusion vs common carotid artery ligation. Neurosurgery 67(5):1431-7, 2010

2. Linskey ME, Jungreis CA, Yonas H, Hirsch WL Jr, Sekhar LN, Horton JA, et al. Stroke risk

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after abrupt internal carotid artery sacrifice: accuracy of preoperative assessment with balloon test occlusion and stable xenon-enhanced CT. AJNR Am J Neuroradiol 15(5):829-

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43, 1994

3. Mathis JM, Barr JD, Jungreis CA, Yonas H, Sekhar LN, Vincent D, et al. Temporary balloon test occlusion of the internal carotid artery: experience in 500 cases. AJNR Am J Neuroradiol 16(4):749-54, 1995

4. Van Rooij WJ, Sluzewski M, Slob MJ, Rinkel GJ. Predictive value of angiographic testing

26(1):175-8, 2005

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for tolerance to therapeutic occlusion of the carotid artery. AJNR Am J Neuroradiol

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5. Abud DG, Spelle L, Piotin M, Mounayer C, Vanzin JR, Moret J. Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice. AJNR

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Am J Neuroradiol 26(10):2602-9, 2005 6. Sato K, Shimizu H, Inoue T, Fujimura M, Matsumoto Y, Kondo R, et al. Angiographic circulation time and cerebral blood flow during balloon test occlusion of the internal carotid artery. J Cereb Blood Flow Metab 34(1):136-43, 2014 7. Larson JJ, Tew JM Jr, Tomsick TA, van Loveren HR. Treatment of aneurysms of the internal carotid artery by intravascular balloon occlusion: long-term follow-up of 58 patients. 16

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Neurosurgery 36(1):26-30, 1995 8. Standard SC, Ahuja A, Guterman LR, Chavis TD, Gibbons KJ, Barth AP, et al. Balloon test

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occlusion of the internal carotid artery with hypotensive challenge. AJNR Am J Neuroradiol 16(7):1453-8, 1995

9. Allen JW, Alastra AJ, Nelson PK. Proximal intracranial internal carotid artery branches:

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prevalence and importance for balloon occlusion test. J Neurosurg 102(1):45-52, 2005

10. Chen PR, Oritz R, Page JH, Siddiqui AH, Veznedaroglu E, Rosenwasser RH. Spontaneous

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systolic blood pressure elevation during temporary balloon occlusion increases the risk of ischemic events after carotid artery occlusion. Neurosurgery 63(2):256-65, 2008 11. Sugawara Y, Kikuchi T, Ueda T, Nishizaki M, Nakata S, Mochizuki T, et al. Usefulness of brain SPECT to evaluate brain tolerance and hemodynamic changes during temporary balloon occlusion test and after permanent carotid occlusion. J Nucl Med 43(12):1616-23,

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2002

12. Lorberboym M, Pandit N, Machac J, Holan V, Sacher M, Segal D, et al. Brain perfusion

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imaging during preoperative temporary balloon occlusion of the internal carotid artery. J Nucl Med 37(3):415-9, 1996

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13. Cloughesy TF, Nuwer MR, Hoch D, Vinuela F, Duckwiler G, Martin N. Monitoring carotid test occlusions with continuous EEG and clinical examination. J Clin Neurophysiol 10(3):363-9, 1993

14. Miller JD, Jawad K, Jennett B. Safety of carotid ligation and its role in the management of intracranial aneurysms. J Neurol Neurosurg Psychiatry 40(1):64-72, 1997

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Total

Male

3

13

16

Female

28

12

40

Total

31

25

56

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Tumors

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Aneurysms

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Table 1. Patient diagnosis at time of BTO.

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Table 2. Patient results of venous delay timing and corresponding SPECT analysis of cerebral perfusion.

0 sec Delay 9

0-1 sec Delay 11

1-2 sec Delay 5

2-3 sec Delay 1

> 3 sec Delay 0

Mean Delay (s) 0.65

4

1

1

0

0

0.5

10

5

4

1

1.08

4

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Mild Hypoperfusion

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No Hypoperfusion

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Moderate/Severe Hypoperfusion

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HIGHLIGHTS Venous phase delay and SPECT results in patients with carotid BTO are compared.

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Retrospective analysis reveals no correlation between venous delay and SPECT.

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SPECT should be used with traditional angiography to determine ischemia potential.

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Future study needed to define best adjuncts to predict ischemia post ICA occlusion.

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ABBREVIATIONS ANOVA – analysis of variance

F – French ICA – internal carotid artery

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SPECT – single-photon emission computer tomography

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BTO – balloon test occlusion

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DISCLOSURE STATEMENT/CONFLICT OF INTEREST None.

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EP

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production, research, and publication of this manuscript.

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All authors of this manuscript report no conflicts of interest or relevant disclosures regarding the