Research Article| Volume 29, ISSUE 6, 104807, June 2020

Ischemic Tolerance Evaluated by Computed Tomography Perfusion during Balloon Test Occlusion


      Objectives: Balloon test occlusion (BTO) is performed to evaluate ischemic tolerance for large and giant cerebral aneurysms and head and neck tumors that may require parent artery occlusion. However, ischemic tolerance for the temporary test occlusion does not always guarantee a tolerance for permanent occlusion. In this study, we evaluated the utility of computed tomography (CT) perfusion during BTO to quantify ischemic tolerance for detecting delayed ischemic stroke. Materials and Methods: Forty-one patients who underwent BTO for the internal carotid artery were included. The correlations between the parameters of CT perfusion and collateral angiographic appearance or stump pressure during BTO were evaluated. The cerebral blood flow (CBF), cerebral blood volume, mean transit time (MTT), and time to peak (TTP) were obtained through CT perfusion, and the asymmetry ratios were determined. Collateral angiographic appearances were categorized into 5 grades (0-4). Results: The collateral angiographic appearance showed moderate correlations with CBF, MTT, and TTP that was significant. Of these, the absolute value of the correlation coefficient was the highest for MTT. MTT also showed a moderate correlation with stump pressure. CBF and MTT were significantly different between the poor collateral group (grades 2 and 3) and the good collateral group (grade 4). Based on the MTT, the good collateral group was identified with high sensitivity (75.0%) and specificity (81.2%). Conclusions: In BTO, the MTT obtained through CT perfusion showed a correlation with collateral angiographic appearance and stump pressure. Thus, the MTT might be useful to quantify ischemic tolerance for detecting delayed ischemic stroke.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Journal of Stroke and Cerebrovascular Diseases
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Larson JJ
        • Tew Jr., JM
        • Tomsick TA
        • et al.
        Treatment of aneurysms of the internal carotid artery by intravascular balloon occlusion: long-term follow-up of 58 patients.
        Neurosurgery. 1995; 36 (discussion 30): 26-30
        • Fox AJ
        • Vinuela F
        • Pelz DM
        • et al.
        Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms.
        J Neurosurg. 1987; 66: 40-46
        • Adams GL
        • Madison M
        • Remley K
        • et al.
        Preoperative permanent balloon occlusion of internal carotid artery in patients with advanced head and neck squamous cell carcinoma.
        Laryngoscope. 1999; 109: 460-466
        • Sanna M
        • Piazza P
        • Ditrapani G
        • et al.
        Management of the internal carotid artery in tumors of the lateral skull base: preoperative permanent balloon occlusion without reconstruction.
        Otol Neurotol. 2004; 25: 998-1005
        • Serbinenko FA.
        Balloon catheterization and occlusion of major cerebral vessels.
        J Neurosurg. 1974; 41: 125-145
        • Linskey ME
        • Jungreis CA
        • Yonas H
        • et al.
        Stroke risk after abrupt internal carotid artery sacrifice: accuracy of preoperative assessment with balloon test occlusion and stable xenon-enhanced CT.
        AJNR American journal of neuroradiology. 1994; 15: 829-843
        • van der Schaaf IC
        • Brilstra EH
        • Buskens E
        • et al.
        Endovascular treatment of aneurysms in the cavernous sinus: a systematic review on balloon occlusion of the parent vessel and embolization with coils.
        Stroke. 2002; 33: 313-318
        • Vazquez Anon V
        • Aymard A
        • Gobin YP
        • et al.
        Balloon occlusion of the internal carotid artery in 40 cases of giant intracavernous aneurysm: technical aspects, cerebral monitoring, and results.
        Neuroradiology. 1992; 34: 245-251
        • Abud DG
        • Spelle L
        • Piotin M
        • et al.
        Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice.
        AJNR Am J Neuroradiol. 2005; 26: 2602-2609
        • van Rooij WJ
        • Sluzewski M
        • Slob MJ
        • et al.
        Predictive value of angiographic testing for tolerance to therapeutic occlusion of the carotid artery.
        AJNR Am J Neuroradiol. 2005; 26: 175-178
        • 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.
        AJNR Am J Neuroradiol. 2005; 26: 1937-1942
        • Takeda N
        • Fujita K
        • Katayama S
        • et al.
        Cerebral oximetry for the detection of cerebral ischemia during temporary carotid artery occlusion.
        Neurologia medico-chirurgica. 2000; 40 (discussion 562-553): 557-562
        • Field M
        • Jungreis CA
        • Chengelis N
        • et al.
        Symptomatic cavernous sinus aneurysms: management and outcome after carotid occlusion and selective cerebral revascularization.
        AJNR Am J Neuroradiol. 2003; 24: 1200-1207
        • Ryu YH
        • Chung TS
        • Lee JD
        • et al.
        HMPAO SPECT to assess neurologic deficits during balloon test occlusion.
        J Nucl Med. 1996; 37: 551-554
        • Kai Y
        • Hamada J
        • Morioka M
        • et al.
        Treatment strategy for giant aneurysms in the cavernous portion of the internal carotid artery.
        Surg Neurol. 2007; 67 (discussion 155): 148-155
        • Brunberg JA
        • Frey KA
        • Horton JA
        • et al.
        [15O]H2O positron emission tomography determination of cerebral blood flow during balloon test occlusion of the internal carotid artery.
        AJNR Am J Neuroradiol. 1994; 15: 725-732
        • Sato K
        • Shimizu H
        • Inoue T
        • et al.
        Angiographic circulation time and cerebral blood flow during balloon test occlusion of the internal carotid artery.
        J Cereb Blood Flow Metab\. 2014; 34: 136-143
        • Higashida RT
        • Furlan AJ
        • Roberts H
        • et al.
        Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke.
        Stroke. 2003; 34: e109-e137
        • Tani S.
        • Imamura H.
        • Asai K.
        • et al.
        Comparison of practical methods in clinical sites for estimating cerebral blood flow during balloon test occlusion.
        J Neurosurg. 2019; 131: 1430-1436
        • Gibbs JM
        • Wise RJ
        • Leenders KL
        • et al.
        Evaluation of cerebral perfusion reserve in patients with carotid-artery occlusion.
        Lancet (London, England). 1984; 1: 310-314
        • Hokari M
        • Kuroda S
        • Shiga T
        • et al.
        Combination of a mean transit time measurement with an acetazolamide test increases predictive power to identify elevated oxygen extraction fraction in occlusive carotid artery diseases.
        J Nucl Med. 2008; 49: 1922-1927
        • Kuroda S
        • Houkin K
        • Kamiyama H
        • et al.
        Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it?.
        Stroke. 2001; 32: 2110-2116
        • Kamath A
        • Smith WS
        • Powers WJ
        • et al.
        Perfusion CT compared to H(2) (15)O/O (15)O PET in patients with chronic cervical carotid artery occlusion.
        Neuroradiology. 2008; 50: 745-751
        • Hashimoto A
        • Mikami T
        • Komatsu K
        • et al.
        Assessment of hemodynamic compromise using computed tomography perfusion in combination with (123)I-IMP single-photon emission computed tomography without acetazolamide challenge test.
        J Stroke Cerebrovasc Dis. 2017; 26: 627-635
        • Kim E
        • Sohn CH
        • Na DG
        • et al.
        Perfusion computed tomography evaluation of cerebral hemodynamic impairment in patients with unilateral chronic steno-occlusive disease: a comparison with the acetazolamide challenge 99mTc-hexamethylpropyleneamine oxime single-photon emission computed tomography.
        J Comput Assist Tomogr. 2009; 33: 546-551
        • Teng MM
        • Jen SL
        • Chiu FY
        • et al.
        Change in brain perfusion after extracranial-intracranial bypass surgery detected using the mean transit time of computed tomography perfusion.
        J Chin Med Assoc. 2012; 75: 649-653
        • Takahashi S
        • Tanizaki Y
        • Kimura H
        • et al.
        Prediction of cerebrovascular reserve capacity by computed tomography perfusion using 320-row computed tomography.
        J Strok Cerebrovasc Dis. 2015; 24: 939-945
        • Kudo K
        • Sasaki M
        • Yamada K
        • et al.
        Differences in CT perfusion maps generated by different commercial software: quantitative analysis by using identical source data of acute stroke patients.
        Radiology. 2010; 254: 200-209