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Balloon Test Occlusion of the Internal Carotid Artery with Stump Pressure Ratio and Venous Phase Delay Technique
Balloon Test Occlusion of the Internal Carotid Artery with Stump Pressure Ratio and Venous Phase Delay Technique Alvin Yi-Chou Wang, MD, Ching-Chang Chen, MD, Hung-Yi Lai, MD, and Shih-Tseng Lee, MD
Balloon test occlusion (BTO) is crucial before sacrificing parent arteries. We proposed a simple paradigm combining clinical tolerance with venous phase technique and stump pressure ratio as a criterion for sufficient collateral flow. Internal carotid artery (ICA) occlusion was considered safe for asymptomatic patients who exhibited less than 2 seconds of venous phase delay or had a stump pressure ratio greater than 60%. A total of 37 BTO procedures were performed on 31 patients. Twenty-three patients were monitored clinically and 3 were symptomatic. Venous phase comparison was performed on 27 patients, and 5 failed the test. The stump pressure was measured in all patients, and 7 patients failed the test. In summary, 7 patients failed the BTO, of which 6 received high-flow bypass and 1 of these 6 were symptomatic and exhibited stump pressure ratios less than 60% in the second BTO procedure. Occlusion of the ICA was performed on 29 patients. Only 1 patient developed delayed vasospasm and brain infarction. Adequate collateral flow may be indicated by a stump ratio of 60% or greater with or without a high-flow bypass. Combined with clinical assessment and venous phase technique, ICA occlusion may be a safe option that does not result in delayed ischemic complications. Key Words: Aneurysmal subarachnoid hemorrhage—balloon occlusion—cerebral aneurysm— internal carotid artery—therapeutic embolization. Ó 2013 by National Stroke Association
The primary goal in the treatment of a cerebral aneurysm is to attain complete occlusion of the aneurysm while preserving the parent artery and all its branches. This goal can be difficult to achieve depending on the size, configuration, or location of the aneurysm. For difficult cases, therapeutic occlusion of the parent artery From the Department of Neurosurgery, Chang Gung University and Chang Gung Memorial Hospital, Taoyuan, Taiwan, Republic of China. Received March 19, 2013; revision received May 13, 2013; accepted May 30, 2013. Declaration of interest: This article has not been funded by any organization. The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article. Address correspondence to Alvin Yi-Chou Wang, MD, Department of Neurosurgery, Chang Gung University and Chang Gung Memorial Hospital, No. 5 Fu-Hsing Street, Kweishan, Taoyuan, Taiwan, Republic of China. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2013 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2013.05.036
may represent the next best treatment option. However, 26% of patients who underwent a nonselective and abrupt sacrifice of the carotid artery experienced infarction; of these infarctions, 46% were fatal.1 The angiographic balloon test occlusion (BTO) frequently is performed in combination with clinical surveillance to identify patients at risk for acute stroke after permanent occlusion of the parent artery. The results of test occlusion in a conscious patient may predict the risk of acute ischemia; however, prediction of delayed ischemia after permanent occlusion is more difficult. A number of adjunctive direct or indirect blood flow measurements have been proposed as tools for predicting stroke in these patients. Clinical assessment remains the basis for all BTO paradigms. The venous phase technique and stump pressure measurement have been proposed to increase the sensitivity of the BTO clinical assessment.2-5 Here, we review our institutional experience with this simple paradigm that combines clinical tolerance with both the venous phase technique and ratio of stump to systemic
Journal of Stroke and Cerebrovascular Diseases, Vol. 22, No. 8 (November), 2013: pp e533-e540
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pressures as the major criterion for determining whether to occlude the internal carotid artery (ICA).
Methods Patient Characteristics This was a retrospective study reviewed by our institutional ethics committee. Between January 2007 and August 2012, test occlusion of the ICA was performed on 31 patients—15 men and 16 women; mean age, 45.6 years; median age, 49 years; range, 14-74 years. Each patient signed an informed consent and was informed about the potential risks. We considered performing carotid occlusion on patients with carotid aneurysms (n 5 25) and traumatic carotid cavernous fistulae (n 5 6). Among the 25 aneurysm patients, 14 presented with subarachnoid hemorrhage (SAH) and 11 with symptoms of mass effect. In patients presented with SAH, 9 patients had dorsal wall blister aneurysms and 5 patients had fusiform aneurysms. Almost all these blister and fusiform aneurysm were located at the paraclinoid ICA. For all these patients, test occlusion was performed early in the treatment regimen, and patients who passed the test received occlusion of the carotid artery.
BTO Methods Systemic arterial pressure was measured continuously by an indwelling cannula in the radial artery. Specifically, sheath introducers were placed bilaterally in the common femoral arteries. A 6-F guiding catheter was positioned in the ICA intended for occlusion. A 5-F diagnostic catheter was positioned in the contralateral ICA or vertebral artery. Each patient received 6000 U heparin. A nondetachable silicone balloon was positioned in the petrous ICA. A microcatheter was introduced distal to the balloon catheter. On occlusion of the parent artery by balloon inflation, the mean stump pressure distal to the occluded ICA was monitored and recorded for a minimum of 6 minutes until it stabilized. Because changes in systemic pressure influence stump pressure, the stump pressure ratio was calculated by comparing the ratio of mean stump pressure to the mean systemic pressure during the ICA occlusion procedure. Conscious patients were monitored neurologically for at least 30 minutes during the BTO process. A resident asked the patient simple questions and tested the motor function of the extremities at short intervals. Patients were instructed to report any changes in sensory function, such as paresthesia or dizziness. If any neurological deficits were detected during balloon occlusion, the balloon catheter was immediately deflated. After the first global neurologic assessment, anteroposterior angiography was performed on the entire skull at 2 frames per second. A fixed volume (9 mL) of contrast material was injected into the contralateral ICA for a period of 1.5 seconds, and anteroposterior and lateral vertebral angiography was performed. The length of time to
attain opacification of the first cortical veins was compared between the territory of the occluded hemisphere and the examined hemisphere. The test occlusion was considered negative when the delay between the venous drainage of the injected and the occluded hemisphere was no more than 2 seconds.
BTO for Patients Receiving High-Flow Bypass For patients who did not pass the BTO procedure, a great saphenous venous graft was used to perform a high-flow bypass from the common carotid artery (CCA) to the middle cerebral artery (MCA). After the bypass procedure, a second BTO procedure was performed a few days later to test the patency and efficacy of the high-flow bypass. For this BTO, a 6-F guiding catheter was positioned on the lesion side of the CCA. The patency of the bypass graft was demonstrated by contrast injection through the CCA. The silicone balloon was positioned in the petrous ICA, and a microcatheter was introduced distal to the balloon catheter. Following the occlusion of the parent artery by balloon inflation, the mean stump pressure distal to the occluded ICA was monitored and recorded for a minimum of 6 minutes. The patient was monitored for neurological symptoms for 30 minutes.
Occlusion or Trapping of the ICA For safety purposes, parent artery ligation or occlusion was performed only in asymptomatic patients who either exhibited less than 2 seconds of venous phase lag between the occluded and injected territories or a pressure ratio of greater than 60%.3,6 If endovascular occlusion was indicated, the target vessel was occluded immediately after the BTO procedure; if surgical ligation was indicated, the target vessel was ligated within 2 days.
Results Table 1 lists clinical characteristics, BTO results, and treatment outcomes. Table 2 provides the patient results from the first and second BTO for each modality. Table 3 provides detailed patient information for patients who either failed the BTO or developed symptoms after ICA occlusion.
Neurological Monitoring Neurological function was monitored in 23 patients (74.2%), and the remaining 8 patients were placed under general anesthesia. Aphasia and hemiparesis were observed in 3 patients. Two patients (patients 7 and 25) were asymptomatic during the BTO but did not tolerate the injection of contrast agent and became irritable during the study. With stump pressure ratios of 52% and 50%, patients 7 and 25 exhibited results inconsistent with those observed in the clinical assessment and stump pressure ratio studies.
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Table 1. Clinical characteristics, balloon test occlusion results, and treatment outcomes for all 26 patients
from the A-com artery in 14 patients, the P-com artery in 9 patients, and from both arteries in 6 patients. Four patients did not tolerate the increased dose of contrast injection and move during study. After lowering the dose of contrast agent, the draining veins of the occluded hemisphere were too faint for reliable detection. Two of these 4 patients were asymptomatic and had stump pressures more than 60% and were considered passed the BTO studies. Another 2 patients were also asymptomatic but had stump pressures less than 60% and were considered failed the BTO studies. Among the 25 patients with collateral flow who tolerated the procedure, 3 showed a venous phase delay of more than 4 seconds and the remaining 22 showed a delay of less than 2 seconds. A total of 5 patients failed the angiography and venous delay BTO protocol.
Gender Male Female Type of ICA lesion Dorsal wall or blister Giant Fusiform Traumatic CCF Symptoms SAH Mass effect Traumatic CCF Clinical monitor Symptomatic General anesthesia Collateral flow Major A-com artery Major P-com artery A-com, P-com No collateral Venous phase delay 0-1 s 1-2 s 2-4 s .4 s No collateral Contrast injection not tolerated Stump pressure .60 mm Hg ,60 mm Hg Stump pressure ratio .60% ,60% Second BTO Symptomatic Stump pressure ratio , 60% Pass Final treatment No treatment Proximal ligation or occlusion Endovascular trapping Proximal occlusion after bypass Coiling of aneurysm Outcome in 29 patients that tolerated first or second BTO Fair Vasospasm and infarction
15 16 9 11 5 6 14 11 6 23/31 (74.2%) 3 8 14 9 6 2 27/31 (87.1%) 14 8 0 3 2 4 31/31 (100%) 22 9 31/31 (100%) 24 7 6 1 1 5 1 18 6 5 1
28 1
Abbreviations: A-com, anterior communicating; BTO, balloon test occlusion; CCF, carotid cavernous fistulae; ICA, internal carotid artery; P-com, posterior communicating; SAH, subarachnoid hemorrhage.
Angiographic Findings Angiographic studies were performed on all patients. Two patients displayed no collateral flow from either the posterior communicating (P-com) or anterior communicating (A-com) artery. The major collateral flow came
Carotid Stump Pressure The mean stump pressure was measured in all patients. However, 2 patients were unable to tolerate even brief occlusion of the ICA, and their mean stump pressure was acquired during the initial 30 seconds. Mean systemic pressures ranged from 63 to 131 mm Hg. Postocclusion mean ICA stump pressure ranged from 20 to 131 mm Hg (mean: 72.3 6 18.7 mm Hg) and the pressure ratio ranged from 28% to 98% (mean: 73.9% 6 26.6%). Nine patients exhibited a mean stump pressure of less than 60 mm Hg; 2 of these 9 patients tolerated permanent carotid artery occlusion without any problems (stump pressure of 40 mm Hg [stump pressure ratio, 62%] and 46 mm Hg [stump pressure ratio, 65%]). Seven patients showed pressure ratios of less than 60%; of these patients, 1 had a stump pressure of 60 mm Hg (stump pressure ratio 52%). Patients with stump pressure ratios greater than 60% were divided into 2 groups based on the anesthesia they received: general or local. For general anesthesia patients, the mean systemic pressure was 92 mm Hg. For local anesthesia patients, the mean was 102 mm Hg. The mean stump pressure was 74 mm Hg for general anesthesia patients and 81 mm Hg for local anesthesia patients. The mean stump pressure ratio was 80% for general anesthesia patients and 78.7% for local anesthesia patients. The hypotensive effect of general anesthesia lowered the stump pressure and systemic pressure but did not affect the stump pressure ratio.
Summary of BTO Results The BTO results are summarized in Table 2. Among the total 31 patients, only 19 (61.3%) were able to accept all 3 modalities. Neurological monitoring was performed on 23 of the 31 patients (74.2%). Three patients did not tolerate the BTO procedure and exhibited symptoms. Angiographic studies and the venous delay protocol were performed on 27 of the 31 patients (87.1%); of these patients, 5 patients failed the venous delay protocol.
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Table 2. Clinical monitoring, venous phase delay, and stump pressure ratio results during balloon test occlusion in all 31 patients
The stump pressure ratio was obtained for all patients (100%). Seven patients exhibited stump pressure ratios of less than 60%. Two patients (patients 7 and 25) displayed inconsistent results among the different modalities. These patients were asymptomatic during the BTO but demonstrated a stump pressure ratio of 52% and 50%. The venous phase could not be demonstrated clearly in these patients because the high dose of contrast injection was not tolerated. In conclusion, 3 patients failed all BTO modalities (patients 1, 9, and 10), 2 patients under general anesthesia did not pass the venous phase protocol and the stump pressure ratio measurement (patients 22 and 30), and 2 patients did not pass stump pressure ratio measurement (patients 7 and 25). Of these 7 patients, 6 underwent a high-flow bypass procedure. One of the 6 patients failed the second BTO (patient 1). The other 5 patients remained clinically asymptomatic and showed stump pressure ratios of 64%, 69%, 74%, 72%, and 93%. We conducted proximal ligation, occlusion, or trapping on all patients who passed either the first or second BTO procedure (29 of the 31 patients). None of the patients demonstrated permanent or transient ischemic events immediately after the ICA occlusion. However, 1 patient experienced a major stroke a week following the occlusion procedure; follow-up computed tomography (CT) angiography demonstrated severe vasospasm. The other 28 patients demonstrated no clinically significant events for at least 6 months after the diseased ICA was occluded. Regarding the 2 patients who did not undergo proximal ligation or occlusion, patient 1 (carotid blister aneurysm) failed the extracranial-intracranial (EC–IC) bypass procedure and underwent aneurysm embolization with coils. Patient 7 failed the BTO and was not treated.
Discussion The treatment of giant or dissection aneurysms is the main reason for performing ICA ligation. During the inflation of the balloon in ICA, neurological monitoring is an essential component to the BTO procedure. Sudhakar et al7 reported no complications after ICA occlusion in
24 patients who were asymptomatic during BTO. However, most researchers have reported relatively high rates of complication.8,9 Niimi et al10 reported a 16% complication rate with the use of neurological monitoring alone. Numerous tests, including measurement of carotid stump pressure, electroencephalographic (EEG) monitoring, hypotensive challenge, angiographic cross filling, and cerebral blood flow (CBF) measurements, have been employed in conjunction with neurological monitoring to determine which patients can tolerate carotid ligation safely and to reduce the incidence of ischemic complications. Several investigators have reported a simple, quick, and reliable angiographic criterion using the BTO technique, known as the venous phase BTO, which increases the positive predictive value of BTO to 98%-100%.2,3 Venous phase BTO stratifies patient risk of parent artery sacrifice based on the angiographically measured time lag between the hemispheric cortical draining veins during BTO. A delay of 2 seconds or greater in the venous phase between the occluded and injected territories was considered a failed test.3 Although venous BTO requires additional catheter placement in the contralateral ICA, this BTO technique is considered safe and reliable when performed under general anesthesia. Abud et al3 stated that general anesthesia induces significant reduction in mean blood pressure (26% on average compared with baseline pre-anesthetic levels), which is comparable with a hypotensive challenge test during BTO. However, some patients receiving venous phase BTO under local anesthesia may not tolerate the higher dose of contrast agent and may move during the injection. In our study, 4 patients moved during contrast injection, which rendered the subtracted image unreadable. Also, patients who failed the first BTO, and thus received a high-flow bypass graft for ICA lesions, required synchronous injection of contrast agent from 2 injectors into both carotid arteries to allow for comparison of the venous phase in both hemispheres. This technique compromised the simplicity and safety of the method. Therefore, we did not include the venous phase technique
Case no.
Age
Pass BTO
11
59
Yes
ICA blister aneurysm
A-com
1-2 s
1
47
7
50
No No No
ICA blister aneurysm Post bypass second BTO ICA fusiform aneurysm
A-com A-com P-com
9
58
10
51
22
43
25
50
No Yes No Yes No Yes No
ICA fusiform aneurysm Post bypass second BTO Giant ICA aneurysm Post bypass second BTO ICA fusiform aneurysm Post bypass second BTO ICA giant aneurysm
No Bypass graft No Bypass graft A-com Bypass graft A-com
30
64
Yes No Yes
Post bypass second BTO ICA fusiform aneurysm Post bypass second BTO
Bypass graft A-com Bypass graft
5s Poor bypass flow Not tolerate contrast injection No collateral — No collateral — 4s — Not tolerate contrast injection — .4 s —
Diagnosis
Major collateral
Stump/systemic pressure (pressure ratio)
Treatment
Outcome
No
81/106 (76%)
Proximal occlusion
Aphasia, hemiparesis Hemiparesis No
58/119 (48%) 48/116 (41%) 60/115 (52%)
Bypass Coiling No
Vasospasm 1 wk later Fair
Hemiparesis No Aphasia, hemiparesis No Anesthesia No No
35/94 (37%) 70/109 (64%) 20/72 (28%) 61/88 (69%) 40/115 (35%) 68/92 (74%) 55/110 (50%)
Bypass Proximal occlusion Bypass Proximal occlusion Bypass Proximal occlusion Bypass
No Anesthesia Anesthesia
75/10 (72%) 40/110 (36%) 64/69 (93%)
Proximal occlusion Bypass Proximal occlusion
Venous phase delay
Symptom
—
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Table 3. Detailed patient information for those who failed BTO or developed symptom after proximal occlusion of the ICA
Fair Fair Fair Fair
Fair
Abbreviations: A-com, anterior communicating; BTO, balloon test occlusion; ICA, internal carotid artery; P-com, posterior communicating. The bold terms and values were to emphasize the reason for failed BTO in each modalities.
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in the secondary BTO on patients receiving high-flow bypass. The venous delay BTO protocol also is limited because only the primary collaterals (A-com and P-com arteries) can be evaluated. Although the secondary and tertiary collaterals (leptomeningeal collaterals and external carotid feeders) can be demonstrated by angiography, they cannot be measured and evaluated quantitatively. We did not encounter this situation, but its occurrence would certainly underestimate the collateral flow in patients. With these limitations, we decided the safest option was to add the stump pressure measurement as a third criterion to evaluate collateral flow during BTO.
Stump Pressure Measurement Many studies have investigated the efficacy of stump pressure as a guide for assessing the risk of cerebral ischemia during carotid endarterectomy. The optimal carotid stump pressure that determines which patients require shunting is controversial; systolic stump pressures of less than 60 mm Hg,11 less than 50 mm Hg,12 less than 45 mm Hg,13 and less than 40 mm Hg14 all have been suggested. The measurement of stump pressure during BTO of the ICA has been proposed as a method to predict the likelihood of ischemia after permanent occlusion.6,15-18 Most studies have compared stump pressure with cerebral vascular reserve by using Xenon CT or singlephoton emission computed tomography (SPECT).4-6,16-21 They compared CBF with mean or minimal stump pressure,16,18,20,21 the ratios between stump and systemic pressures,4-6 or the ratios between stump and preocclusion carotid arterial pressures.17 Seed et al18 and Okudaira et al20 noted the correlation between mean stump pressure and Xenon CT CBF mapping but noted that the wide range of values (low sensitivity) precludes its use as an absolute predictor of adequate CBF after carotid occlusion. In our study, 2 of the patients with a mean stump pressure less than 50 mm Hg tolerated the ICA occlusion without any ischemic events. To use the ratios between stump pressure and preocclusion, carotid arterial pressures will face the problem of using the pressure measurement of 2 different time points. As Barker et al19 observed an initial drop in stump pressure on occlusion, followed by a gradual increase in the stump pressure during the first 6 minutes after occlusion, most researchers wait for at least 5-6 minutes to acquire a stable mean stump pressure after clamping or occlusion of the ICA which may further make the comparison more difficult.6,16-18 Therefore, we chose to compare the stump pressure over the systemic radial artery pressure that can be measured at the same time. Also using the ratio of stump to systematic pressures to determine patient suitability for carotid ligation has yielded more positive results than the use of stump
4-6,17
pressure alone. In the present study, we found general anesthesia to have a negative effect on the stump and systemic pressures. However, the stump pressure ratio can abolish the negative effect of this hypotensive challenge. Morishima et al17 used SPECT to measure changes in CBF on the occluded side and used this information to divide patients into high-, moderate-, and low-risk groups. Patients in the lowrisk group had mean stump pressures 60% or greater than the mean systemic pressure, whereas none of the high- and moderate-risk group patients exhibited pressure ratios greater than 58%. Tomura et al5 also used SPECT to measure CBF and compare it with the stump pressure and the stump pressure ratio. They concluded that patients with minimal mean stump pressures of 40 mm Hg or greater and patients with pressure ratios of 50% or greater demonstrated relatively symmetric cerebral perfusion. However, ligation of the carotid artery via bypass surgery was performed in only 2 of the 27 cases, and none of these 27 patients underwent simple carotid ligation surgery, which made the results less convincing. In the present study, not all patients were able to undergo neurological monitoring or yield satisfactory images of the venous phase; only 61% of patients underwent both studies. In contrast, the stump pressure ratio could be measured in all patients, including those who received high-flow bypass. Also, 2 patients whom passed the clinical assessment have actually failed the stump pressure ratio test. The stump pressure ratio method is more reliable than the clinical assessment and yields results consistent with the venous phase BTO technique. In addition, the stump pressure ratio can be measured and integrated into BTO procedures of any vessel easily, including vertebrobasilar arteries.22,23 Although the stump pressure measurement has not been used previously as a criterion for the successful establishment of a high-flow bypass, we found that the ICA stump pressure ratio in patients who received high-flow bypass could be measured easily and correlates highly with clinical outcomes.
Risk of Proximal Occlusion in SAH Patients The decision to sacrifice a carotid artery in SAH must be made with extreme caution.2 Patients who tolerated BTO shortly following an aneurysm rupture may not necessarily tolerate occlusion if vasospasm develops several days later.24-26 One patient with Fisher grade 3 SAH had passed all modalities of the BTO and underwent proximal ICA occlusion without any sequelae. However, the patient developed ipsilateral infarction a week later because of severe vasospasm. Angioplasty was not possible because the route to the spastic ICA segment was occluded. Therefore, to prevent ischemic complications following severe
MULTIMODAL BTO PROTOCOLS FOR ICA LESIONS
vasospasm, we do not recommend occlusion of the carotid artery during the acute phase of aneurysmal SAH.
Limitations of the Study During our study, clinical assessment and venous phase comparison were occasionally difficult to perform simultaneously. However, stump pressure was measured in all patients and was more sensitive than the clinical assessment. It also provided consistent results with the venous phase modality. It is tempting to claim that the stump pressure ratio may be the most reliable method for detecting insufficient collateral flow and the only type of assessment needed; however, we examined too few cases to definitely support the conclusion that stump pressure ratio is the sole criterion of sufficient collateral flow. Further study is required to clarify whether the stump pressure ratio in BTO procedures can achieve higher sensitivity and specificity than other modalities.
Conclusion During test occlusion, maintenance of a mean stump pressure that is 60% or greater than the mean systemic pressure may indicate adequate CBF. Combined with clinical assessment and synchronous venous phase assessment, occlusion of the ICA is considered safe and does not present any risk of delayed ischemic complication. If patients fail one of these studies, measures to augment CBF are indicated to lessen the risk of delayed cerebral ischemia or infarction. However, patients who present with aneurysmal SAH should be considered for delayed ICA occlusion because severe vasospasm may develop.
References 1. Nishioka H. Results of the treatment of intracranial aneurysms by occlusion of the carotid artery in the neck. J Neurosurg 1966;25:660-704. 2. van Rooij WJ, Sluzewski M, Slob MJ, et al. Predictive value of angiographic testing for tolerance to therapeutic occlusion of the carotid artery. Am J Neuroradiol 2005; 26:175-178. 3. Abud DG, Spelle L, Piotin M, et al. Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice. Am J Neuroradiol 2005; 26:2602-2609. 4. Kato K, Tomura N, Takahashi S, et al. Balloon occlusion test of the internal carotid artery: correlation with stump pressure and 99mTc-HMPAO SPECT. Acta Radiol 2006; 47:1073-1078. 5. Tomura N, Omachi K, Takahashi S, et al. Comparison of technetium Tc 99m hexamethylpropyleneamine oxime single-photon emission tomograph with stump pressure during the balloon occlusion test of the internal carotid artery. Am J Neuroradiol 2005;26:1937-1942. 6. Kurata A, Miyasaka Y, Tanaka C, et al. Stump pressure as a guide to the safety of permanent occlusion of the internal carotid artery. Acta Neurochir (Wien) 1996;138: 549-554.
e539 7. Sudhakar KV, Sawlani V, Phadke RV, et al. Temporary balloon occlusion of internal carotid artery: a simple and reliable clinical test. Neurol India 2000;48:140-143. 8. Yang H, Ling F, Wang D, et al. Balloon occlusion test and therapeutic occlusion on traumatic carotid cavernous fistulas. Chin J Traumatol 1999;2:118-121. 9. McIvor NP, Willinsky RA, TerBrugge KG, et al. Validity of test occlusion studies prior to internal carotid artery sacrifice. Head Neck 1994;16:11-16. 10. Niimi Y, Berenstein A, Setton A, et al. Occlusion of the internal carotid artery based on a simple tolerance test. Interv Neuroradiol 1996;2:289-296. 11. Modica PA, Tempelhoff R. A comparison of computerized EEG with internal carotid artery stump pressure for detection of ischemia during carotid endarterectomy. J Neurosurg Anesthesiol 1989;1:211-218. 12. Whitley D, Cherry KJ Jr. Predictive value of carotid artery stump pressures during carotid endarterectomy. Neurosurg Clin N Am 1996;7:723-732. 13. Jacob T, Hingorani A, Ascher E. Carotid artery stump pressure (CASP) in 1135 consecutive endarterectomies under general anesthesia: an old method that survived the test of times. J Cardiovasc Surg (Torino) 2007;48: 677-681. 14. Calligaro KD, Dougherty MJ. Correlation of carotid artery stump pressure and neurologic changes during 474 carotid endarterectomies performed in awake patients. J Vasc Surg 2005;42:684-689. 15. Holmes AE, James IM, Wise CC. Observations on distal intravascular pressure changes and cerebral blood flow after common carotid artery ligation in man. J Neurol Neurosurg Psychiatry 1971;34:78-81. 16. Leech PJ, Miller JD, Fitch W, et al. Cerebral blood flow, internal carotid artery pressure, and the EEG as a guide to the safety of carotid ligation. J Neurol Neurosurg Psychiatry 1974;37:854-862. 17. Morishima H, Kurata A, Miyasaka Y, et al. Efficacy of the stump pressure ratio as a guide to the safety of permanent occlusion of the internal carotid artery. Neurol Res 1998;20:732-736. 18. Steed DL, Webster MW, DeVries EJ, et al. Clinical observations on the effect of carotid artery occlusion on cerebral blood flow mapped by xenon computed tomography and its correlation with carotid artery back pressure. J Vasc Surg 1990;11:38-43. discussion 43-34. 19. Barker DW, Jungreis CA, Horton JA, et al. Balloon test occlusion of the internal carotid artery: change in stump pressure over 15 minutes and its correlation with xenon CT cerebral blood flow. Am J Neuroradiol 1993;14: 587-590. 20. Okudaira Y, Arai H, Sato K. Cerebral blood flow alteration by acetazolamide during carotid balloon occlusion: parameters reflecting cerebral perfusion pressure in the acetazolamide test. Stroke 1996;27:617-621. 21. Kaminogo M, Ochi M, Onizuka M, et al. An additional monitoring of regional cerebral oxygen saturation to HMPAO SPECT study during balloon test occlusion. Stroke 1999;30:407-413. 22. Sakamoto S, Ohba S, Shibukawa M, et al. Staged bilateral vertebral artery occlusion for ruptured dissecting aneurysms of the basilar artery: a report of 2 cases. Surg Neurol 2005;64:456-461. discussion 461. 23. Takira K, Taketomo O, Hisashi H, et al. The efficacy of coil embolization for the treatment of ruptured dissecting vertebral aneurysms [in Japanese]. Surg Cereb Stroke 2000;28:413-420.
e540 24. Elhammady MS, Wolfe SQ, Farhat H, et al. Carotid artery sacrifice for unclippable and uncoilable aneurysms: endovascular occlusion vs common carotid artery ligation. Neurosurgery 2010;67:1431-1436. discussion 1437. 25. Lesley WS, Rangaswamy R. Balloon test occlusion and endosurgical parent artery sacrifice for the evaluation
A.Y.-C. WANG ET AL. and management of complex intracranial aneurysmal disease. J Neurointervention Surg 2009;1:112-120. 26. O’Shaughnessy BA, Salehi SA, Mindea SA, et al. Selective cerebral revascularization as an adjunct in the treatment of giant anterior circulation aneurysms. Neurosurg Focus 2003;14:e4.
Balloon test occlusion (BTO) is crucial before sacrificing parent arteries. We proposed a simple paradigm combining clinical tolerance with venous phase technique and stump pressure ratio as a criterion for sufficient collateral flow. Internal carotid artery (ICA) occlusion was considered safe for asymptomatic patients who exhibited less than 2 seconds of venous phase delay or had a stump pressure ratio greater than 60%. A total of 37 BTO procedures were performed on 31 patients. Twenty-three patients were monitored clinically and 3 were symptomatic. Venous phase comparison was performed on 27 patients, and 5 failed the test. The stump pressure was measured in all patients, and 7 patients failed the test. In summary, 7 patients failed the BTO, of which 6 received high-flow bypass and 1 of these 6 were symptomatic and exhibited stump pressure ratios less than 60% in the second BTO procedure. Occlusion of the ICA was performed on 29 patients. Only 1 patient developed delayed vasospasm and brain infarction. Adequate collateral flow may be indicated by a stump ratio of 60% or greater with or without a high-flow bypass. Combined with clinical assessment and venous phase technique, ICA occlusion may be a safe option that does not result in delayed ischemic complications. Key Words: Aneurysmal subarachnoid hemorrhage—balloon occlusion—cerebral aneurysm— internal carotid artery—therapeutic embolization. Ó 2013 by National Stroke Association
The primary goal in the treatment of a cerebral aneurysm is to attain complete occlusion of the aneurysm while preserving the parent artery and all its branches. This goal can be difficult to achieve depending on the size, configuration, or location of the aneurysm. For difficult cases, therapeutic occlusion of the parent artery From the Department of Neurosurgery, Chang Gung University and Chang Gung Memorial Hospital, Taoyuan, Taiwan, Republic of China. Received March 19, 2013; revision received May 13, 2013; accepted May 30, 2013. Declaration of interest: This article has not been funded by any organization. The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article. Address correspondence to Alvin Yi-Chou Wang, MD, Department of Neurosurgery, Chang Gung University and Chang Gung Memorial Hospital, No. 5 Fu-Hsing Street, Kweishan, Taoyuan, Taiwan, Republic of China. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2013 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2013.05.036
may represent the next best treatment option. However, 26% of patients who underwent a nonselective and abrupt sacrifice of the carotid artery experienced infarction; of these infarctions, 46% were fatal.1 The angiographic balloon test occlusion (BTO) frequently is performed in combination with clinical surveillance to identify patients at risk for acute stroke after permanent occlusion of the parent artery. The results of test occlusion in a conscious patient may predict the risk of acute ischemia; however, prediction of delayed ischemia after permanent occlusion is more difficult. A number of adjunctive direct or indirect blood flow measurements have been proposed as tools for predicting stroke in these patients. Clinical assessment remains the basis for all BTO paradigms. The venous phase technique and stump pressure measurement have been proposed to increase the sensitivity of the BTO clinical assessment.2-5 Here, we review our institutional experience with this simple paradigm that combines clinical tolerance with both the venous phase technique and ratio of stump to systemic
Journal of Stroke and Cerebrovascular Diseases, Vol. 22, No. 8 (November), 2013: pp e533-e540
e533
A.Y.-C. WANG ET AL.
e534
pressures as the major criterion for determining whether to occlude the internal carotid artery (ICA).
Methods Patient Characteristics This was a retrospective study reviewed by our institutional ethics committee. Between January 2007 and August 2012, test occlusion of the ICA was performed on 31 patients—15 men and 16 women; mean age, 45.6 years; median age, 49 years; range, 14-74 years. Each patient signed an informed consent and was informed about the potential risks. We considered performing carotid occlusion on patients with carotid aneurysms (n 5 25) and traumatic carotid cavernous fistulae (n 5 6). Among the 25 aneurysm patients, 14 presented with subarachnoid hemorrhage (SAH) and 11 with symptoms of mass effect. In patients presented with SAH, 9 patients had dorsal wall blister aneurysms and 5 patients had fusiform aneurysms. Almost all these blister and fusiform aneurysm were located at the paraclinoid ICA. For all these patients, test occlusion was performed early in the treatment regimen, and patients who passed the test received occlusion of the carotid artery.
BTO Methods Systemic arterial pressure was measured continuously by an indwelling cannula in the radial artery. Specifically, sheath introducers were placed bilaterally in the common femoral arteries. A 6-F guiding catheter was positioned in the ICA intended for occlusion. A 5-F diagnostic catheter was positioned in the contralateral ICA or vertebral artery. Each patient received 6000 U heparin. A nondetachable silicone balloon was positioned in the petrous ICA. A microcatheter was introduced distal to the balloon catheter. On occlusion of the parent artery by balloon inflation, the mean stump pressure distal to the occluded ICA was monitored and recorded for a minimum of 6 minutes until it stabilized. Because changes in systemic pressure influence stump pressure, the stump pressure ratio was calculated by comparing the ratio of mean stump pressure to the mean systemic pressure during the ICA occlusion procedure. Conscious patients were monitored neurologically for at least 30 minutes during the BTO process. A resident asked the patient simple questions and tested the motor function of the extremities at short intervals. Patients were instructed to report any changes in sensory function, such as paresthesia or dizziness. If any neurological deficits were detected during balloon occlusion, the balloon catheter was immediately deflated. After the first global neurologic assessment, anteroposterior angiography was performed on the entire skull at 2 frames per second. A fixed volume (9 mL) of contrast material was injected into the contralateral ICA for a period of 1.5 seconds, and anteroposterior and lateral vertebral angiography was performed. The length of time to
attain opacification of the first cortical veins was compared between the territory of the occluded hemisphere and the examined hemisphere. The test occlusion was considered negative when the delay between the venous drainage of the injected and the occluded hemisphere was no more than 2 seconds.
BTO for Patients Receiving High-Flow Bypass For patients who did not pass the BTO procedure, a great saphenous venous graft was used to perform a high-flow bypass from the common carotid artery (CCA) to the middle cerebral artery (MCA). After the bypass procedure, a second BTO procedure was performed a few days later to test the patency and efficacy of the high-flow bypass. For this BTO, a 6-F guiding catheter was positioned on the lesion side of the CCA. The patency of the bypass graft was demonstrated by contrast injection through the CCA. The silicone balloon was positioned in the petrous ICA, and a microcatheter was introduced distal to the balloon catheter. Following the occlusion of the parent artery by balloon inflation, the mean stump pressure distal to the occluded ICA was monitored and recorded for a minimum of 6 minutes. The patient was monitored for neurological symptoms for 30 minutes.
Occlusion or Trapping of the ICA For safety purposes, parent artery ligation or occlusion was performed only in asymptomatic patients who either exhibited less than 2 seconds of venous phase lag between the occluded and injected territories or a pressure ratio of greater than 60%.3,6 If endovascular occlusion was indicated, the target vessel was occluded immediately after the BTO procedure; if surgical ligation was indicated, the target vessel was ligated within 2 days.
Results Table 1 lists clinical characteristics, BTO results, and treatment outcomes. Table 2 provides the patient results from the first and second BTO for each modality. Table 3 provides detailed patient information for patients who either failed the BTO or developed symptoms after ICA occlusion.
Neurological Monitoring Neurological function was monitored in 23 patients (74.2%), and the remaining 8 patients were placed under general anesthesia. Aphasia and hemiparesis were observed in 3 patients. Two patients (patients 7 and 25) were asymptomatic during the BTO but did not tolerate the injection of contrast agent and became irritable during the study. With stump pressure ratios of 52% and 50%, patients 7 and 25 exhibited results inconsistent with those observed in the clinical assessment and stump pressure ratio studies.
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Table 1. Clinical characteristics, balloon test occlusion results, and treatment outcomes for all 26 patients
from the A-com artery in 14 patients, the P-com artery in 9 patients, and from both arteries in 6 patients. Four patients did not tolerate the increased dose of contrast injection and move during study. After lowering the dose of contrast agent, the draining veins of the occluded hemisphere were too faint for reliable detection. Two of these 4 patients were asymptomatic and had stump pressures more than 60% and were considered passed the BTO studies. Another 2 patients were also asymptomatic but had stump pressures less than 60% and were considered failed the BTO studies. Among the 25 patients with collateral flow who tolerated the procedure, 3 showed a venous phase delay of more than 4 seconds and the remaining 22 showed a delay of less than 2 seconds. A total of 5 patients failed the angiography and venous delay BTO protocol.
Gender Male Female Type of ICA lesion Dorsal wall or blister Giant Fusiform Traumatic CCF Symptoms SAH Mass effect Traumatic CCF Clinical monitor Symptomatic General anesthesia Collateral flow Major A-com artery Major P-com artery A-com, P-com No collateral Venous phase delay 0-1 s 1-2 s 2-4 s .4 s No collateral Contrast injection not tolerated Stump pressure .60 mm Hg ,60 mm Hg Stump pressure ratio .60% ,60% Second BTO Symptomatic Stump pressure ratio , 60% Pass Final treatment No treatment Proximal ligation or occlusion Endovascular trapping Proximal occlusion after bypass Coiling of aneurysm Outcome in 29 patients that tolerated first or second BTO Fair Vasospasm and infarction
15 16 9 11 5 6 14 11 6 23/31 (74.2%) 3 8 14 9 6 2 27/31 (87.1%) 14 8 0 3 2 4 31/31 (100%) 22 9 31/31 (100%) 24 7 6 1 1 5 1 18 6 5 1
28 1
Abbreviations: A-com, anterior communicating; BTO, balloon test occlusion; CCF, carotid cavernous fistulae; ICA, internal carotid artery; P-com, posterior communicating; SAH, subarachnoid hemorrhage.
Angiographic Findings Angiographic studies were performed on all patients. Two patients displayed no collateral flow from either the posterior communicating (P-com) or anterior communicating (A-com) artery. The major collateral flow came
Carotid Stump Pressure The mean stump pressure was measured in all patients. However, 2 patients were unable to tolerate even brief occlusion of the ICA, and their mean stump pressure was acquired during the initial 30 seconds. Mean systemic pressures ranged from 63 to 131 mm Hg. Postocclusion mean ICA stump pressure ranged from 20 to 131 mm Hg (mean: 72.3 6 18.7 mm Hg) and the pressure ratio ranged from 28% to 98% (mean: 73.9% 6 26.6%). Nine patients exhibited a mean stump pressure of less than 60 mm Hg; 2 of these 9 patients tolerated permanent carotid artery occlusion without any problems (stump pressure of 40 mm Hg [stump pressure ratio, 62%] and 46 mm Hg [stump pressure ratio, 65%]). Seven patients showed pressure ratios of less than 60%; of these patients, 1 had a stump pressure of 60 mm Hg (stump pressure ratio 52%). Patients with stump pressure ratios greater than 60% were divided into 2 groups based on the anesthesia they received: general or local. For general anesthesia patients, the mean systemic pressure was 92 mm Hg. For local anesthesia patients, the mean was 102 mm Hg. The mean stump pressure was 74 mm Hg for general anesthesia patients and 81 mm Hg for local anesthesia patients. The mean stump pressure ratio was 80% for general anesthesia patients and 78.7% for local anesthesia patients. The hypotensive effect of general anesthesia lowered the stump pressure and systemic pressure but did not affect the stump pressure ratio.
Summary of BTO Results The BTO results are summarized in Table 2. Among the total 31 patients, only 19 (61.3%) were able to accept all 3 modalities. Neurological monitoring was performed on 23 of the 31 patients (74.2%). Three patients did not tolerate the BTO procedure and exhibited symptoms. Angiographic studies and the venous delay protocol were performed on 27 of the 31 patients (87.1%); of these patients, 5 patients failed the venous delay protocol.
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Table 2. Clinical monitoring, venous phase delay, and stump pressure ratio results during balloon test occlusion in all 31 patients
The stump pressure ratio was obtained for all patients (100%). Seven patients exhibited stump pressure ratios of less than 60%. Two patients (patients 7 and 25) displayed inconsistent results among the different modalities. These patients were asymptomatic during the BTO but demonstrated a stump pressure ratio of 52% and 50%. The venous phase could not be demonstrated clearly in these patients because the high dose of contrast injection was not tolerated. In conclusion, 3 patients failed all BTO modalities (patients 1, 9, and 10), 2 patients under general anesthesia did not pass the venous phase protocol and the stump pressure ratio measurement (patients 22 and 30), and 2 patients did not pass stump pressure ratio measurement (patients 7 and 25). Of these 7 patients, 6 underwent a high-flow bypass procedure. One of the 6 patients failed the second BTO (patient 1). The other 5 patients remained clinically asymptomatic and showed stump pressure ratios of 64%, 69%, 74%, 72%, and 93%. We conducted proximal ligation, occlusion, or trapping on all patients who passed either the first or second BTO procedure (29 of the 31 patients). None of the patients demonstrated permanent or transient ischemic events immediately after the ICA occlusion. However, 1 patient experienced a major stroke a week following the occlusion procedure; follow-up computed tomography (CT) angiography demonstrated severe vasospasm. The other 28 patients demonstrated no clinically significant events for at least 6 months after the diseased ICA was occluded. Regarding the 2 patients who did not undergo proximal ligation or occlusion, patient 1 (carotid blister aneurysm) failed the extracranial-intracranial (EC–IC) bypass procedure and underwent aneurysm embolization with coils. Patient 7 failed the BTO and was not treated.
Discussion The treatment of giant or dissection aneurysms is the main reason for performing ICA ligation. During the inflation of the balloon in ICA, neurological monitoring is an essential component to the BTO procedure. Sudhakar et al7 reported no complications after ICA occlusion in
24 patients who were asymptomatic during BTO. However, most researchers have reported relatively high rates of complication.8,9 Niimi et al10 reported a 16% complication rate with the use of neurological monitoring alone. Numerous tests, including measurement of carotid stump pressure, electroencephalographic (EEG) monitoring, hypotensive challenge, angiographic cross filling, and cerebral blood flow (CBF) measurements, have been employed in conjunction with neurological monitoring to determine which patients can tolerate carotid ligation safely and to reduce the incidence of ischemic complications. Several investigators have reported a simple, quick, and reliable angiographic criterion using the BTO technique, known as the venous phase BTO, which increases the positive predictive value of BTO to 98%-100%.2,3 Venous phase BTO stratifies patient risk of parent artery sacrifice based on the angiographically measured time lag between the hemispheric cortical draining veins during BTO. A delay of 2 seconds or greater in the venous phase between the occluded and injected territories was considered a failed test.3 Although venous BTO requires additional catheter placement in the contralateral ICA, this BTO technique is considered safe and reliable when performed under general anesthesia. Abud et al3 stated that general anesthesia induces significant reduction in mean blood pressure (26% on average compared with baseline pre-anesthetic levels), which is comparable with a hypotensive challenge test during BTO. However, some patients receiving venous phase BTO under local anesthesia may not tolerate the higher dose of contrast agent and may move during the injection. In our study, 4 patients moved during contrast injection, which rendered the subtracted image unreadable. Also, patients who failed the first BTO, and thus received a high-flow bypass graft for ICA lesions, required synchronous injection of contrast agent from 2 injectors into both carotid arteries to allow for comparison of the venous phase in both hemispheres. This technique compromised the simplicity and safety of the method. Therefore, we did not include the venous phase technique
Case no.
Age
Pass BTO
11
59
Yes
ICA blister aneurysm
A-com
1-2 s
1
47
7
50
No No No
ICA blister aneurysm Post bypass second BTO ICA fusiform aneurysm
A-com A-com P-com
9
58
10
51
22
43
25
50
No Yes No Yes No Yes No
ICA fusiform aneurysm Post bypass second BTO Giant ICA aneurysm Post bypass second BTO ICA fusiform aneurysm Post bypass second BTO ICA giant aneurysm
No Bypass graft No Bypass graft A-com Bypass graft A-com
30
64
Yes No Yes
Post bypass second BTO ICA fusiform aneurysm Post bypass second BTO
Bypass graft A-com Bypass graft
5s Poor bypass flow Not tolerate contrast injection No collateral — No collateral — 4s — Not tolerate contrast injection — .4 s —
Diagnosis
Major collateral
Stump/systemic pressure (pressure ratio)
Treatment
Outcome
No
81/106 (76%)
Proximal occlusion
Aphasia, hemiparesis Hemiparesis No
58/119 (48%) 48/116 (41%) 60/115 (52%)
Bypass Coiling No
Vasospasm 1 wk later Fair
Hemiparesis No Aphasia, hemiparesis No Anesthesia No No
35/94 (37%) 70/109 (64%) 20/72 (28%) 61/88 (69%) 40/115 (35%) 68/92 (74%) 55/110 (50%)
Bypass Proximal occlusion Bypass Proximal occlusion Bypass Proximal occlusion Bypass
No Anesthesia Anesthesia
75/10 (72%) 40/110 (36%) 64/69 (93%)
Proximal occlusion Bypass Proximal occlusion
Venous phase delay
Symptom
—
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Table 3. Detailed patient information for those who failed BTO or developed symptom after proximal occlusion of the ICA
Fair Fair Fair Fair
Fair
Abbreviations: A-com, anterior communicating; BTO, balloon test occlusion; ICA, internal carotid artery; P-com, posterior communicating. The bold terms and values were to emphasize the reason for failed BTO in each modalities.
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in the secondary BTO on patients receiving high-flow bypass. The venous delay BTO protocol also is limited because only the primary collaterals (A-com and P-com arteries) can be evaluated. Although the secondary and tertiary collaterals (leptomeningeal collaterals and external carotid feeders) can be demonstrated by angiography, they cannot be measured and evaluated quantitatively. We did not encounter this situation, but its occurrence would certainly underestimate the collateral flow in patients. With these limitations, we decided the safest option was to add the stump pressure measurement as a third criterion to evaluate collateral flow during BTO.
Stump Pressure Measurement Many studies have investigated the efficacy of stump pressure as a guide for assessing the risk of cerebral ischemia during carotid endarterectomy. The optimal carotid stump pressure that determines which patients require shunting is controversial; systolic stump pressures of less than 60 mm Hg,11 less than 50 mm Hg,12 less than 45 mm Hg,13 and less than 40 mm Hg14 all have been suggested. The measurement of stump pressure during BTO of the ICA has been proposed as a method to predict the likelihood of ischemia after permanent occlusion.6,15-18 Most studies have compared stump pressure with cerebral vascular reserve by using Xenon CT or singlephoton emission computed tomography (SPECT).4-6,16-21 They compared CBF with mean or minimal stump pressure,16,18,20,21 the ratios between stump and systemic pressures,4-6 or the ratios between stump and preocclusion carotid arterial pressures.17 Seed et al18 and Okudaira et al20 noted the correlation between mean stump pressure and Xenon CT CBF mapping but noted that the wide range of values (low sensitivity) precludes its use as an absolute predictor of adequate CBF after carotid occlusion. In our study, 2 of the patients with a mean stump pressure less than 50 mm Hg tolerated the ICA occlusion without any ischemic events. To use the ratios between stump pressure and preocclusion, carotid arterial pressures will face the problem of using the pressure measurement of 2 different time points. As Barker et al19 observed an initial drop in stump pressure on occlusion, followed by a gradual increase in the stump pressure during the first 6 minutes after occlusion, most researchers wait for at least 5-6 minutes to acquire a stable mean stump pressure after clamping or occlusion of the ICA which may further make the comparison more difficult.6,16-18 Therefore, we chose to compare the stump pressure over the systemic radial artery pressure that can be measured at the same time. Also using the ratio of stump to systematic pressures to determine patient suitability for carotid ligation has yielded more positive results than the use of stump
4-6,17
pressure alone. In the present study, we found general anesthesia to have a negative effect on the stump and systemic pressures. However, the stump pressure ratio can abolish the negative effect of this hypotensive challenge. Morishima et al17 used SPECT to measure changes in CBF on the occluded side and used this information to divide patients into high-, moderate-, and low-risk groups. Patients in the lowrisk group had mean stump pressures 60% or greater than the mean systemic pressure, whereas none of the high- and moderate-risk group patients exhibited pressure ratios greater than 58%. Tomura et al5 also used SPECT to measure CBF and compare it with the stump pressure and the stump pressure ratio. They concluded that patients with minimal mean stump pressures of 40 mm Hg or greater and patients with pressure ratios of 50% or greater demonstrated relatively symmetric cerebral perfusion. However, ligation of the carotid artery via bypass surgery was performed in only 2 of the 27 cases, and none of these 27 patients underwent simple carotid ligation surgery, which made the results less convincing. In the present study, not all patients were able to undergo neurological monitoring or yield satisfactory images of the venous phase; only 61% of patients underwent both studies. In contrast, the stump pressure ratio could be measured in all patients, including those who received high-flow bypass. Also, 2 patients whom passed the clinical assessment have actually failed the stump pressure ratio test. The stump pressure ratio method is more reliable than the clinical assessment and yields results consistent with the venous phase BTO technique. In addition, the stump pressure ratio can be measured and integrated into BTO procedures of any vessel easily, including vertebrobasilar arteries.22,23 Although the stump pressure measurement has not been used previously as a criterion for the successful establishment of a high-flow bypass, we found that the ICA stump pressure ratio in patients who received high-flow bypass could be measured easily and correlates highly with clinical outcomes.
Risk of Proximal Occlusion in SAH Patients The decision to sacrifice a carotid artery in SAH must be made with extreme caution.2 Patients who tolerated BTO shortly following an aneurysm rupture may not necessarily tolerate occlusion if vasospasm develops several days later.24-26 One patient with Fisher grade 3 SAH had passed all modalities of the BTO and underwent proximal ICA occlusion without any sequelae. However, the patient developed ipsilateral infarction a week later because of severe vasospasm. Angioplasty was not possible because the route to the spastic ICA segment was occluded. Therefore, to prevent ischemic complications following severe
MULTIMODAL BTO PROTOCOLS FOR ICA LESIONS
vasospasm, we do not recommend occlusion of the carotid artery during the acute phase of aneurysmal SAH.
Limitations of the Study During our study, clinical assessment and venous phase comparison were occasionally difficult to perform simultaneously. However, stump pressure was measured in all patients and was more sensitive than the clinical assessment. It also provided consistent results with the venous phase modality. It is tempting to claim that the stump pressure ratio may be the most reliable method for detecting insufficient collateral flow and the only type of assessment needed; however, we examined too few cases to definitely support the conclusion that stump pressure ratio is the sole criterion of sufficient collateral flow. Further study is required to clarify whether the stump pressure ratio in BTO procedures can achieve higher sensitivity and specificity than other modalities.
Conclusion During test occlusion, maintenance of a mean stump pressure that is 60% or greater than the mean systemic pressure may indicate adequate CBF. Combined with clinical assessment and synchronous venous phase assessment, occlusion of the ICA is considered safe and does not present any risk of delayed ischemic complication. If patients fail one of these studies, measures to augment CBF are indicated to lessen the risk of delayed cerebral ischemia or infarction. However, patients who present with aneurysmal SAH should be considered for delayed ICA occlusion because severe vasospasm may develop.
References 1. Nishioka H. Results of the treatment of intracranial aneurysms by occlusion of the carotid artery in the neck. J Neurosurg 1966;25:660-704. 2. van Rooij WJ, Sluzewski M, Slob MJ, et al. Predictive value of angiographic testing for tolerance to therapeutic occlusion of the carotid artery. Am J Neuroradiol 2005; 26:175-178. 3. Abud DG, Spelle L, Piotin M, et al. Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice. Am J Neuroradiol 2005; 26:2602-2609. 4. Kato K, Tomura N, Takahashi S, et al. Balloon occlusion test of the internal carotid artery: correlation with stump pressure and 99mTc-HMPAO SPECT. Acta Radiol 2006; 47:1073-1078. 5. Tomura N, Omachi K, Takahashi S, et al. Comparison of technetium Tc 99m hexamethylpropyleneamine oxime single-photon emission tomograph with stump pressure during the balloon occlusion test of the internal carotid artery. Am J Neuroradiol 2005;26:1937-1942. 6. Kurata A, Miyasaka Y, Tanaka C, et al. Stump pressure as a guide to the safety of permanent occlusion of the internal carotid artery. Acta Neurochir (Wien) 1996;138: 549-554.
e539 7. Sudhakar KV, Sawlani V, Phadke RV, et al. Temporary balloon occlusion of internal carotid artery: a simple and reliable clinical test. Neurol India 2000;48:140-143. 8. Yang H, Ling F, Wang D, et al. Balloon occlusion test and therapeutic occlusion on traumatic carotid cavernous fistulas. Chin J Traumatol 1999;2:118-121. 9. McIvor NP, Willinsky RA, TerBrugge KG, et al. Validity of test occlusion studies prior to internal carotid artery sacrifice. Head Neck 1994;16:11-16. 10. Niimi Y, Berenstein A, Setton A, et al. Occlusion of the internal carotid artery based on a simple tolerance test. Interv Neuroradiol 1996;2:289-296. 11. Modica PA, Tempelhoff R. A comparison of computerized EEG with internal carotid artery stump pressure for detection of ischemia during carotid endarterectomy. J Neurosurg Anesthesiol 1989;1:211-218. 12. Whitley D, Cherry KJ Jr. Predictive value of carotid artery stump pressures during carotid endarterectomy. Neurosurg Clin N Am 1996;7:723-732. 13. Jacob T, Hingorani A, Ascher E. Carotid artery stump pressure (CASP) in 1135 consecutive endarterectomies under general anesthesia: an old method that survived the test of times. J Cardiovasc Surg (Torino) 2007;48: 677-681. 14. Calligaro KD, Dougherty MJ. Correlation of carotid artery stump pressure and neurologic changes during 474 carotid endarterectomies performed in awake patients. J Vasc Surg 2005;42:684-689. 15. Holmes AE, James IM, Wise CC. Observations on distal intravascular pressure changes and cerebral blood flow after common carotid artery ligation in man. J Neurol Neurosurg Psychiatry 1971;34:78-81. 16. Leech PJ, Miller JD, Fitch W, et al. Cerebral blood flow, internal carotid artery pressure, and the EEG as a guide to the safety of carotid ligation. J Neurol Neurosurg Psychiatry 1974;37:854-862. 17. Morishima H, Kurata A, Miyasaka Y, et al. Efficacy of the stump pressure ratio as a guide to the safety of permanent occlusion of the internal carotid artery. Neurol Res 1998;20:732-736. 18. Steed DL, Webster MW, DeVries EJ, et al. Clinical observations on the effect of carotid artery occlusion on cerebral blood flow mapped by xenon computed tomography and its correlation with carotid artery back pressure. J Vasc Surg 1990;11:38-43. discussion 43-34. 19. Barker DW, Jungreis CA, Horton JA, et al. Balloon test occlusion of the internal carotid artery: change in stump pressure over 15 minutes and its correlation with xenon CT cerebral blood flow. Am J Neuroradiol 1993;14: 587-590. 20. Okudaira Y, Arai H, Sato K. Cerebral blood flow alteration by acetazolamide during carotid balloon occlusion: parameters reflecting cerebral perfusion pressure in the acetazolamide test. Stroke 1996;27:617-621. 21. Kaminogo M, Ochi M, Onizuka M, et al. An additional monitoring of regional cerebral oxygen saturation to HMPAO SPECT study during balloon test occlusion. Stroke 1999;30:407-413. 22. Sakamoto S, Ohba S, Shibukawa M, et al. Staged bilateral vertebral artery occlusion for ruptured dissecting aneurysms of the basilar artery: a report of 2 cases. Surg Neurol 2005;64:456-461. discussion 461. 23. Takira K, Taketomo O, Hisashi H, et al. The efficacy of coil embolization for the treatment of ruptured dissecting vertebral aneurysms [in Japanese]. Surg Cereb Stroke 2000;28:413-420.
e540 24. Elhammady MS, Wolfe SQ, Farhat H, et al. Carotid artery sacrifice for unclippable and uncoilable aneurysms: endovascular occlusion vs common carotid artery ligation. Neurosurgery 2010;67:1431-1436. discussion 1437. 25. Lesley WS, Rangaswamy R. Balloon test occlusion and endosurgical parent artery sacrifice for the evaluation
A.Y.-C. WANG ET AL. and management of complex intracranial aneurysmal disease. J Neurointervention Surg 2009;1:112-120. 26. O’Shaughnessy BA, Salehi SA, Mindea SA, et al. Selective cerebral revascularization as an adjunct in the treatment of giant anterior circulation aneurysms. Neurosurg Focus 2003;14:e4.