Skip to main content
Erschienen in: European Radiology 9/2022

08.04.2022 | Neuro

Arterial transit artifacts on arterial spin labeling MRI can predict cerebral hyperperfusion after carotid endarterectomy: an initial study

verfasst von: Xiaoyuan Fan, Zhentao Zuo, Tianye Lin, Zhichao Lai, Hui You, Jianxun Qu, Juan Wei, Bao Liu, Feng Feng

Erschienen in: European Radiology | Ausgabe 9/2022

Einloggen, um Zugang zu erhalten

Abstract

Objectives

To investigate whether preoperative arterial spin labeling (ASL) MRI can predict cerebral hyperperfusion after carotid endarterectomy (CEA) in patients with carotid stenosis.

Methods

Consecutive patients with carotid stenosis who underwent CEA between May 2015 and July 2021 were included. For each patient, a cerebral blood flow ratio (rCBF) map was obtained by dividing postoperative CBF with preoperative CBF images from two pseudo-continuous ASL scans. Hyperperfusion regions with rCBF > 2 were extracted and weighted with rCBF to calculate the hyperperfusion index. According to the distribution of the hyperperfusion index, patients were divided into hyperperfusion and non-hyperperfusion groups. Preoperative ASL images were scored based on the presence of arterial transit artifacts (ATAs) in 10 regions of interest corresponding to the Alberta Stroke Programme Early Computed Tomography Score methodology. The degree of stenosis and primary and secondary collaterals were evaluated to correlate with the ASL score. Logistic regression and receiver operating characteristic curve analyses were performed to assess the predictive ability of the ASL score for cerebral hyperperfusion.

Results

Of 86 patients included, cerebral hyperperfusion was present in 17 (19.8%) patients. Carotid near occlusion, opening of posterior communicating arteries with incomplete anterior semicircle, and leptomeningeal collaterals were associated with lower ASL scores (p < 0.05). The preoperative ASL score was an independent predictor of cerebral hyperperfusion (OR = 0.48 [95% CI [0.33–0.71]], p < 0.001) with the optimal cutoff value of 25 points (AUC = 0.98, 94.1% sensitivity, 88.4% specificity).

Conclusions

Based on the presence of ATAs, ASL can non-invasively predict cerebral hyperperfusion after CEA in patients with carotid stenosis.

Key Points

• Carotid near occlusion, opening of posterior communicating arteries with incomplete anterior semicircle, and leptomeningeal collaterals were associated with lower ASL scores.
• The ASL score performed better than the degree of stenosis, type of CoW, and leptomeningeal collaterals, as well as the combination of the three factors for the prediction of cerebral hyperperfusion.
• For patients with carotid stenosis, preoperative ASL can non-invasively identify patients at high risk of cerebral hyperperfusion after carotid endarterectomy without complex post-processing steps.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Ogasawara K, Yukawa H, Kobayashi M et al (2003) Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy using single-photon emission computerized tomography scanning. J Neurosurg 99:504–510 Ogasawara K, Yukawa H, Kobayashi M et al (2003) Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy using single-photon emission computerized tomography scanning. J Neurosurg 99:504–510
2.
Zurück zum Zitat van Mook WN, Rennenberg RJ, Schurink GW et al (2005) Cerebral hyperperfusion syndrome. Lancet Neurol 4:877–888 van Mook WN, Rennenberg RJ, Schurink GW et al (2005) Cerebral hyperperfusion syndrome. Lancet Neurol 4:877–888
3.
Zurück zum Zitat Komoribayashi N, Ogasawara K, Kobayashi M et al (2006) Cerebral hyperperfusion after carotid endarterectomy is associated with preoperative hemodynamic impairment and intraoperative cerebral ischemia. J Cereb Blood Flow Metab 26:878–884 Komoribayashi N, Ogasawara K, Kobayashi M et al (2006) Cerebral hyperperfusion after carotid endarterectomy is associated with preoperative hemodynamic impairment and intraoperative cerebral ischemia. J Cereb Blood Flow Metab 26:878–884
4.
Zurück zum Zitat Hosoda K, Kawaguchi T, Shibata Y et al (2001) Cerebral vasoreactivity and internal carotid artery flow help to identify patients at risk for hyperperfusion after carotid endarterectomy. Stroke 32:1567–1573 Hosoda K, Kawaguchi T, Shibata Y et al (2001) Cerebral vasoreactivity and internal carotid artery flow help to identify patients at risk for hyperperfusion after carotid endarterectomy. Stroke 32:1567–1573
5.
Zurück zum Zitat Spano VR, Mandell DM, Poublanc J et al (2013) CO2 blood oxygen level-dependent MR mapping of cerebrovascular reserve in a clinical population: safety, tolerability, and technical feasibility. Radiology 266:592–598 Spano VR, Mandell DM, Poublanc J et al (2013) CO2 blood oxygen level-dependent MR mapping of cerebrovascular reserve in a clinical population: safety, tolerability, and technical feasibility. Radiology 266:592–598
6.
Zurück zum Zitat Saito H, Ogasawara K, Suzuki T, Kuroda H, Kobayashi M, Yoshida K et al (2011) Adverse effects of intravenous acetazolamide administration for evaluation of cerebrovascular reactivity using brain perfusion single-photon emission computed tomography in patients with major cerebral artery steno-occlusive diseases. Neurol Med Chir 51:479–483 Saito H, Ogasawara K, Suzuki T, Kuroda H, Kobayashi M, Yoshida K et al (2011) Adverse effects of intravenous acetazolamide administration for evaluation of cerebrovascular reactivity using brain perfusion single-photon emission computed tomography in patients with major cerebral artery steno-occlusive diseases. Neurol Med Chir 51:479–483
7.
Zurück zum Zitat Fassaert LMM, Immink RV, van Vriesland DJ et al (2019) Transcranial Doppler 24 hours after carotid endarterectomy accurately identifies patients not at risk of cerebral hyperperfusion syndrome. Eur J Vasc Endovasc Surg 58:320–327 Fassaert LMM, Immink RV, van Vriesland DJ et al (2019) Transcranial Doppler 24 hours after carotid endarterectomy accurately identifies patients not at risk of cerebral hyperperfusion syndrome. Eur J Vasc Endovasc Surg 58:320–327
8.
Zurück zum Zitat Yamauchi K, Enomoto Y, Otani K, Egashira Y, Iwama T (2018) Prediction of hyperperfusion phenomenon after carotid artery stenting and carotid angioplasty using quantitative DSA with cerebral circulation time imaging. J Neurointerv Surg 10:576–579CrossRef Yamauchi K, Enomoto Y, Otani K, Egashira Y, Iwama T (2018) Prediction of hyperperfusion phenomenon after carotid artery stenting and carotid angioplasty using quantitative DSA with cerebral circulation time imaging. J Neurointerv Surg 10:576–579CrossRef
9.
Zurück zum Zitat Iwata T, Mori T, Tanno Y, Kasakura S, Yoshioka K (2018) Measurement of oxygen extraction fraction by blood sampling to estimate severe cerebral hemodynamic failure and anticipate cerebral hyperperfusion syndrome following carotid artery stenting. J Neurointerv Surg 10:1063–1066CrossRef Iwata T, Mori T, Tanno Y, Kasakura S, Yoshioka K (2018) Measurement of oxygen extraction fraction by blood sampling to estimate severe cerebral hemodynamic failure and anticipate cerebral hyperperfusion syndrome following carotid artery stenting. J Neurointerv Surg 10:1063–1066CrossRef
10.
Zurück zum Zitat Nakagawa I, Yokoyama S, Wajima D et al (2019) Hyperventilation and breath-holding test with indocyanine green kinetics predicts cerebral hyperperfusion after carotid artery stenting. J Cereb Blood Flow Metab 39:901–912 Nakagawa I, Yokoyama S, Wajima D et al (2019) Hyperventilation and breath-holding test with indocyanine green kinetics predicts cerebral hyperperfusion after carotid artery stenting. J Cereb Blood Flow Metab 39:901–912
11.
Zurück zum Zitat Donahue MJ, Strother MK, Hendrikse J (2012) Novel MRI approaches for assessing cerebral hemodynamics in ischemic cerebrovascular disease. Stroke 43:903–915CrossRef Donahue MJ, Strother MK, Hendrikse J (2012) Novel MRI approaches for assessing cerebral hemodynamics in ischemic cerebrovascular disease. Stroke 43:903–915CrossRef
12.
Zurück zum Zitat Uchihashi Y, Hosoda K, Zimine I et al (2011) Clinical application of arterial spin-labeling MR imaging in patients with carotid stenosis: quantitative comparative study with single-photon emission CT. AJNR Am J Neuroradiol 32:1545–1551 Uchihashi Y, Hosoda K, Zimine I et al (2011) Clinical application of arterial spin-labeling MR imaging in patients with carotid stenosis: quantitative comparative study with single-photon emission CT. AJNR Am J Neuroradiol 32:1545–1551
13.
Zurück zum Zitat Zaharchuk G, Do HM, Marks MP, Rosenberg J, Moseley ME, Steinberg GK (2011) Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke 42:2485–2491CrossRef Zaharchuk G, Do HM, Marks MP, Rosenberg J, Moseley ME, Steinberg GK (2011) Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke 42:2485–2491CrossRef
14.
Zurück zum Zitat Bang OY, Goyal M, Liebeskind DS (2015) Collateral circulation in ischemic stroke: assessment tools and therapeutic strategies. Stroke 46:3302–3309CrossRef Bang OY, Goyal M, Liebeskind DS (2015) Collateral circulation in ischemic stroke: assessment tools and therapeutic strategies. Stroke 46:3302–3309CrossRef
15.
Zurück zum Zitat Lee S, Yun TJ, Yoo RE et al (2018) Monitoring cerebral perfusion changes after revascularization in patients with Moyamoya disease by using arterial spin-labeling MR Imaging. Radiology 288:565–572 Lee S, Yun TJ, Yoo RE et al (2018) Monitoring cerebral perfusion changes after revascularization in patients with Moyamoya disease by using arterial spin-labeling MR Imaging. Radiology 288:565–572
16.
Zurück zum Zitat Kunieda T, Miyake K, Sakamoto H et al (2017) Leptomeningeal collaterals strongly correlate with reduced cerebrovascular reactivity measured by acetazolamide-challenged single-photon emission computed tomography using a stereotactic extraction estimation analysis in patients with unilateral internal carotid artery stenosis. Intern Med 56:2857–2863 Kunieda T, Miyake K, Sakamoto H et al (2017) Leptomeningeal collaterals strongly correlate with reduced cerebrovascular reactivity measured by acetazolamide-challenged single-photon emission computed tomography using a stereotactic extraction estimation analysis in patients with unilateral internal carotid artery stenosis. Intern Med 56:2857–2863
17.
Zurück zum Zitat de Boorder MJ, van der Grond J, van Dongen AJ et al (2006) Spect measurements of regional cerebral perfusion and carbondioxide reactivity: correlation with cerebral collaterals in internal carotid artery occlusive disease. J Neurol 253:1285–1291 de Boorder MJ, van der Grond J, van Dongen AJ et al (2006) Spect measurements of regional cerebral perfusion and carbondioxide reactivity: correlation with cerebral collaterals in internal carotid artery occlusive disease. J Neurol 253:1285–1291
18.
Zurück zum Zitat Roach BA, Donahue MJ, Davis LT et al (2016) Interrogating the functional correlates of collateralization in patients with intracranial stenosis using multimodal hemodynamic imaging. AJNR Am J Neuroradiol 37:1132–1138 Roach BA, Donahue MJ, Davis LT et al (2016) Interrogating the functional correlates of collateralization in patients with intracranial stenosis using multimodal hemodynamic imaging. AJNR Am J Neuroradiol 37:1132–1138
19.
Zurück zum Zitat Liang F, Fukasaku K, Liu H, Takagi S (2011) A computational model study of the influence of the anatomy of the circle of Willis on cerebral hyperperfusion following carotid artery surgery. Biomed Eng Online 10:84CrossRef Liang F, Fukasaku K, Liu H, Takagi S (2011) A computational model study of the influence of the anatomy of the circle of Willis on cerebral hyperperfusion following carotid artery surgery. Biomed Eng Online 10:84CrossRef
20.
Zurück zum Zitat Katano H, Mase M, Sakurai K, Miyachi S, Yamada K (2012) Revaluation of collateral pathways as escape routes from hyperemia/hyperperfusion following surgical treatment for carotid stenosis. Acta Neurochir 154:2139–2148 discussion 2148-2149CrossRef Katano H, Mase M, Sakurai K, Miyachi S, Yamada K (2012) Revaluation of collateral pathways as escape routes from hyperemia/hyperperfusion following surgical treatment for carotid stenosis. Acta Neurochir 154:2139–2148 discussion 2148-2149CrossRef
21.
Zurück zum Zitat North American Symptomatic Carotid Endarterectomy Trial Collaborators, HJM B, Taylor DW et al (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445–453 North American Symptomatic Carotid Endarterectomy Trial Collaborators, HJM B, Taylor DW et al (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445–453
22.
Zurück zum Zitat Johansson E, Gu T, Aviv RI, Fox AJ (2020) Carotid near-occlusion is often overlooked when CT angiography is assessed in routine practice. Eur Radiol 30:2543–2551CrossRef Johansson E, Gu T, Aviv RI, Fox AJ (2020) Carotid near-occlusion is often overlooked when CT angiography is assessed in routine practice. Eur Radiol 30:2543–2551CrossRef
23.
Zurück zum Zitat Bartlett ES, Walters TD, Symons SP, Fox AJ (2006) Diagnosing carotid stenosis near-occlusion by using CT angiography. AJNR Am J Neuroradiol 27:632–637PubMedPubMedCentral Bartlett ES, Walters TD, Symons SP, Fox AJ (2006) Diagnosing carotid stenosis near-occlusion by using CT angiography. AJNR Am J Neuroradiol 27:632–637PubMedPubMedCentral
24.
Zurück zum Zitat Maas MB, Lev MH, Ay H et al (2009) Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke 40:3001–3005 Maas MB, Lev MH, Ay H et al (2009) Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke 40:3001–3005
25.
Zurück zum Zitat Horie N, Morikawa M, Morofuji Y et al (2014) De novo ivy sign indicates postoperative hyperperfusion in moyamoya disease. Stroke 45:1488–1491 Horie N, Morikawa M, Morofuji Y et al (2014) De novo ivy sign indicates postoperative hyperperfusion in moyamoya disease. Stroke 45:1488–1491
26.
Zurück zum Zitat Mori N, Mugikura S, Higano S et al (2009) The leptomeningeal “ivy sign” on fluid-attenuated inversion recovery MR imaging in Moyamoya disease: a sign of decreased cerebral vascular reserve? AJNR Am J Neuroradiol 30:930–935 Mori N, Mugikura S, Higano S et al (2009) The leptomeningeal “ivy sign” on fluid-attenuated inversion recovery MR imaging in Moyamoya disease: a sign of decreased cerebral vascular reserve? AJNR Am J Neuroradiol 30:930–935
27.
Zurück zum Zitat Liu W, Xu G, Yue X et al (2011) Hyperintense vessels on FLAIR: a useful non-invasive method for assessing intracerebral collaterals. Eur J Radiol 80:786–791 Liu W, Xu G, Yue X et al (2011) Hyperintense vessels on FLAIR: a useful non-invasive method for assessing intracerebral collaterals. Eur J Radiol 80:786–791
28.
Zurück zum Zitat Fahlstrom M, Lewen A, Enblad P, Larsson EM, Wikstrom J (2020) High intravascular signal arterial transit time artifacts have negligible effects on cerebral blood flow and cerebrovascular reserve capacity measurement using single postlabel delay arterial spin-labeling in patients with moyamoya disease. AJNR Am J Neuroradiol 41:430–436CrossRef Fahlstrom M, Lewen A, Enblad P, Larsson EM, Wikstrom J (2020) High intravascular signal arterial transit time artifacts have negligible effects on cerebral blood flow and cerebrovascular reserve capacity measurement using single postlabel delay arterial spin-labeling in patients with moyamoya disease. AJNR Am J Neuroradiol 41:430–436CrossRef
29.
Zurück zum Zitat Lin T, Qu J, Zuo Z, Fan X, You H, Feng F (2020) Test-retest reliability and reproducibility of long-label pseudo-continuous arterial spin labeling. Magn Reson Imaging 73:111–117CrossRef Lin T, Qu J, Zuo Z, Fan X, You H, Feng F (2020) Test-retest reliability and reproducibility of long-label pseudo-continuous arterial spin labeling. Magn Reson Imaging 73:111–117CrossRef
30.
Zurück zum Zitat Di Napoli A, Cheng SF, Gregson J et al (2020) Arterial spin labeling MRI in carotid stenosis: arterial transit artifacts may predict symptoms. Radiology 297:652–660 Di Napoli A, Cheng SF, Gregson J et al (2020) Arterial spin labeling MRI in carotid stenosis: arterial transit artifacts may predict symptoms. Radiology 297:652–660
31.
Zurück zum Zitat Lin TY, Lai ZC, Lv YL et al (2018) Effective collateral circulation may indicate improved perfusion territory restoration after carotid endarterectomy. Eur Radiol 28:727–735 Lin TY, Lai ZC, Lv YL et al (2018) Effective collateral circulation may indicate improved perfusion territory restoration after carotid endarterectomy. Eur Radiol 28:727–735
32.
Zurück zum Zitat Zaharchuk G (2020) Arterial transit awesomeness. Radiology 297:661–662CrossRef Zaharchuk G (2020) Arterial transit awesomeness. Radiology 297:661–662CrossRef
33.
Zurück zum Zitat Alsop DC, Detre JA, Golay X et al (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116 Alsop DC, Detre JA, Golay X et al (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116
34.
Zurück zum Zitat Cay F, Cil BE, Balci S, Arsava EM, Topcuoglu MA, Arat A (2020) Relevance of distal arterial collapse in stenting of atherosclerotic near-occlusion of the carotid artery. AJNR Am J Neuroradiol 41:1054–1060CrossRef Cay F, Cil BE, Balci S, Arsava EM, Topcuoglu MA, Arat A (2020) Relevance of distal arterial collapse in stenting of atherosclerotic near-occlusion of the carotid artery. AJNR Am J Neuroradiol 41:1054–1060CrossRef
35.
Zurück zum Zitat Ohta T, Nakahara I, Matsumoto S et al (2017) Prediction of cerebral hyperperfusion after carotid artery stenting by cerebral angiography and single-photon emission computed tomography without acetazolamide challenge. Neurosurgery 81:512–519 Ohta T, Nakahara I, Matsumoto S et al (2017) Prediction of cerebral hyperperfusion after carotid artery stenting by cerebral angiography and single-photon emission computed tomography without acetazolamide challenge. Neurosurgery 81:512–519
36.
Zurück zum Zitat Markus H, Cullinane M (2001) Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 124:457–467CrossRef Markus H, Cullinane M (2001) Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 124:457–467CrossRef
37.
Zurück zum Zitat Adhiyaman V, Alexander S (2007) Cerebral hyperperfusion syndrome following carotid endarterectomy. QJM 100:239–244CrossRef Adhiyaman V, Alexander S (2007) Cerebral hyperperfusion syndrome following carotid endarterectomy. QJM 100:239–244CrossRef
38.
Zurück zum Zitat de Borst GJ, Antonopoulos CN, Meershoek AJA, Liapis CD (2020) Carotid artery near occlusion: time to rethink the management? Eur J Vasc Endovasc Surg 60:169–170CrossRef de Borst GJ, Antonopoulos CN, Meershoek AJA, Liapis CD (2020) Carotid artery near occlusion: time to rethink the management? Eur J Vasc Endovasc Surg 60:169–170CrossRef
39.
Zurück zum Zitat Iancu-Gontard D, Oppenheim C, Touzé E et al (2003) Evaluation of hyperintense vessels on FLAIR MRI for the diagnosis of multiple intracerebral arterial stenoses. Stroke 34:1886–1891 Iancu-Gontard D, Oppenheim C, Touzé E et al (2003) Evaluation of hyperintense vessels on FLAIR MRI for the diagnosis of multiple intracerebral arterial stenoses. Stroke 34:1886–1891
Metadaten
Titel
Arterial transit artifacts on arterial spin labeling MRI can predict cerebral hyperperfusion after carotid endarterectomy: an initial study
verfasst von
Xiaoyuan Fan
Zhentao Zuo
Tianye Lin
Zhichao Lai
Hui You
Jianxun Qu
Juan Wei
Bao Liu
Feng Feng
Publikationsdatum
08.04.2022
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 9/2022
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-022-08755-x

Weitere Artikel der Ausgabe 9/2022

European Radiology 9/2022 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.