RESEARCH—HUMAN—CLINICAL STUDIES RESEARCH—HUMAN—CLINICAL STUDIES

Intracranial Blood Flow Changes After Extracranial Carotid Artery Stenting Sophia F. Shakur, MD Sepideh Amin-Hanjani, MD Caroline Bednarski, BS Xinjian Du, MD Victor A. Aletich, MD Fady T. Charbel, MD Ali Alaraj, MD Department of Neurosurgery, University of Illinois at Chicago, Chicago, Illinois Correspondence: Ali Alaraj, MD, Department of Neurosurgery, University of Illinois at Chicago, 912 S Wood St, MC-799, Chicago, IL 60612. E-mail: [email protected] Received, July 1, 2014. Accepted, October 31, 2014. Published Online, January 16, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.

BACKGROUND: Carotid artery stenting is an endovascular treatment option for patients with extracranial carotid stenosis. However, intracranial blood flow changes following stenting have not been established. OBJECTIVE: To determine the effects of stenting on intracranial blood flow. METHODS: Records of patients who underwent stenting at our institution between 2004 and 2012 and had flow rates obtained pre- and poststenting by the use of quantitative magnetic resonance angiography were retrospectively reviewed. Percentage stenosis, stenosis length, and minimum vessel diameter were measured from cerebral angiography images. RESULTS: Eighteen patients were included. Mean age was 65 years with 67% presenting with symptomatic stenosis. Degree of stenosis ranged from 60% to 90%. Internal carotid artery (ICA) mean flow improved significantly poststenting from 174.9 6 83.6 mL/min to 250.7 6 91.2 mL/min (P = .011). Ipsilateral middle cerebral artery (MCA) flow, however, was not significantly altered poststenting (107.8 6 41.6 mL/min vs 114.3 6 36.3 mL/min; P = .28). Univariate analysis revealed that improved minimum vessel diameter after stenting, but not percentage stenosis (P = .18) or stenosis length (P = .45), is significantly associated with increased ICA flow (P = .02). However, improved percentage stenosis, stenosis length, minimum vessel diameter, and ICA flow poststenting were not significantly associated with increased MCA flow (P = .64, .38, .13, .37, respectively). CONCLUSION: ICA flow was compromised at baseline, improving 43% on average poststenting. Increased minimum vessel diameter was the factor most significantly associated with increased flow. Conversely, MCA flow was not significantly compromised at baseline nor altered after stenting, suggesting compensatory intracranial collateral supply prestenting that redistributes following ICA revascularization. KEY WORDS: Carotid, Flow, Intracranial, Magnetic resonance angiography, Stenosis, Stent Neurosurgery 76:330–336, 2015

DOI: 10.1227/NEU.0000000000000618

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xtracranial carotid artery stenosis is an important etiology of ischemic stroke, accounting for approximately 20% of such events in the United States.1 The primary pathogenesis of cerebral ischemia in the setting of ipsilateral carotid stenosis is postulated to be thromboembolic, although hemodynamically consequential narrowing of the vessel lumen can also lead to hypoperfusion and may even potentiate the effects of distal embolization.2-4 ABBREVIATIONS: CAS, carotid angioplasty and stenting; QMRA, quantitative magnetic resonance angiography; SPECT, single-photon emission computed tomography

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Carotid revascularization with stenting was approved by the US Food and Drug Administration for selected patients in 2004 based on the results from several randomized controlled trials, including the Stenting and Angioplasty with Protection in Patients at High Risk for Endarterectomy (SAPPHIRE) trial and the Carotid and Vertebral Artery Transluminal Angioplasty study (CAVATAS).5,6 Although stroke risk reduction has been demonstrated, the intracranial blood flow changes following carotid stenting have not been clearly delineated.7 In this study, we aimed to determine the cerebral hemodynamic changes that occur after carotid stenting by using quantitative magnetic resonance angiography (QMRA). We reviewed

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INTRACRANIAL FLOW AFTER CAROTID STENTING

patients who underwent carotid angioplasty and stenting (CAS) and had intra- and extracranial flow rates measured before and after stenting. The relationship between changes in flow and carotid disease features—namely, degree of stenosis, stenosis length, and minimum vessel diameter derived from cerebral angiographic images—was also examined.

METHODS Patient Selection Clinical data for all patients (n = 28) who underwent CAS for extracranial carotid stenosis at our institution between 2004 and 2012 were collected and reviewed. Of these 28 patients, 18 patients with digital subtraction angiography and flow rates obtained pre- and poststenting using QMRA were included.

Blood Flow Measurements All patients in this study underwent quantitative flow measurements of the extracranial and intracranial arteries using QMRA before and 3 to 6 months after carotid stenting. This technique of blood flow quantification by QMRA has been described previously by Zhao et al.8 The technique is currently used in the clinical setting with commercially available software called the NOVA (Noninvasive Optimal Vessel Analysis) system (VasSol, Inc, River Forest, Illinois). Flow ratios (ipsilateral/contralateral vessel flow) were also generated for the internal carotid artery (ICA) and middle cerebral artery (MCA) to provide an internal control. Flow ratios were not obtained if the contralateral carotid stenosis was greater than 50%. All 18 patients included in the study had ipsilateral ICA flow measurements before and after stenting. Contralateral ICA flow before stenting was not measured in 6 patients and so ICA flow ratios were not calculated in these patients. ICA flow ratios were also not calculated in 2 other patients because contralateral stenosis was greater than 50%. A total of 7 patients had ICA flow ratios before and after stenting. Seventeen patients had ipsilateral MCA flow measurements before stenting, and all 18 patients had ipsilateral MCA flows after stenting. Contralateral MCA flow before stenting was measured in 17 patients. MCA flow ratios were not calculated in 8 patients because of the lack of MCA flow measurement or contralateral stenosis greater than 50%. A total of 7 patients had MCA flow ratios before and after stenting.

Blood Vessel Measurements Measurements of degree of stenosis, stenosis length, and minimum vessel diameter were made from digital subtraction angiography images. Minimum vessel diameter was measured at the point of maximal stenosis. Degree of stenosis was determined by using the North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria.9

Statistical Analysis Mean flows and mean flow ratios before and after stenting were compared by using the paired 2-tailed Student t test. Univariate analysis to assess the relationship between change in flow and change in degree of stenosis, stenosis length, and minimum vessel diameter was performed with linear regression. All analyses were performed with SPSS (Version 21; IBM, Inc).

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RESULTS Patient Characteristics Twenty-eight patients underwent CAS for carotid atherosclerotic disease at our institution between 2004 and 2012. Eighteen patients with complete anatomic and flow data were included. Mean age was 65 years. Degree of stenosis ranged from 60% to 90%, and 67% of patients presented with symptomatic stenosis. Mean degree of stenosis was 81% and the median was 85%. Blood flow and vessel measurements are outlined in Table. ICA Flow Before and After Stenting The mean ICA flow among all 18 patients in this study was 174.9 6 83.6 mL/min before stenting and 250.7 6 91.2 mL/min after stenting (P = .011) (Figure 1). The mean ratio of ipsilateral to contralateral ICA flow also increased from 0.52 6 0.14 at baseline to 0.73 6 0.30 after stenting, but not reaching statistical significance (P = .58, n = 7) (Figure 2). MCA Flow Before and After Stenting One patient did not have ipsilateral MCA flow measured; among the 17 remaining patients, the mean MCA flow was not significantly altered poststenting (107.8 6 41.6 mL/min before stenting vs 114.3 6 36.3 mL/min after stenting, P = .28) (Figure 3). Similarly, there was no significant difference (P = .12, n = 7) between the mean ratio of ipsilateral to contralateral MCA flow at baseline (1.04 6 0.52) and after stenting (0.95 6 0.29); however, mean MCA flow ratios were assessed in only 7 patients (Figure 4). Relationship Between Change in Flow and Change in Degree of Stenosis, Stenosis Length, and Minimum Vessel Diameter With the use of a univariate linear regression analysis, the effect of a change in degree of stenosis, stenosis length, and minimum vessel diameter on change in absolute ipsilateral ICA and MCA flow was evaluated. We found that the improvement in minimum vessel diameter after stenting, but not in percentage stenosis (P = .18) or in stenosis length (P = .45), is significantly associated with a change in ipsilateral ICA flow (P = .02) (Figure 5). On the other hand, neither improvement in the degree of stenosis, stenosis length, minimum vessel diameter, nor ICA flow poststenting were significantly associated with a change in ipsilateral MCA flow (P = .64, .38, .13, .37, respectively).

DISCUSSION Since carotid revascularization with CAS was approved by the US Food and Drug Administration approximately 10 years ago, the efficacy and durability of this procedure has been determined primarily through radiographic evaluation of vessel patency and subsequent stroke risk, rather than intracranial hemodynamic changes following CAS. For example, several studies, such as the SAPPHIRE trial, followed patients poststenting with Doppler

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TABLE. Summary of Patient Characteristics, Blood Flow, and Blood Vessel Measurementsa

ICA Ipsilateral Contralateral Patient Stenosis Symptomatic Stenosis, % Stenosis, %

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 a

Left Left Right Left Left Right Left Right Left Left Right Left Right Left Right Right Left Left

Yes Yes No Yes No No No Yes No Yes No Yes Yes Yes Yes Yes Yes Yes

90 90 85 70 85 85 90 75 90 90 85 70 85 65 85 75 60 75

0 100 65 0 100 100 50 75 30 0 30 100 0 0 100 90 0 0

Minimum Vessel Diameter, mm

Ipsilateral ICA Flow, mL/min

Contralateral ICA Flow, mL/min

ICA Flow Ratio

Ipsilateral ICA Flow After Stenting, mL/min

0.9 1.4 1.5 1.6 1.3 1.3 1.4 1.4 0.7 3.0 0.9 1.7 0.8 1.6 2.5 0.7 2.3 1.3

115 108 327 206 201 154 101 205 120 151 147 324 93 219 194 129 321 33

311 NM 257 317 NM NM 181 155 213 290 286 NM 261 277 NM NM 324 269

0.37 NC NC 0.65 NC NC 0.56 NC 0.56 0.52 0.51 NC 0.36 0.79 NC NC 0.99 0.12

167 390 310 200 280 324 171 208 155 145 227 346 256 295 149 471 219 199

Ipsilateral Contralateral MCA Flow, MCA Flow, mL/min mL/min

65 166 101 106 92 138 77 NM 115 118 136 147 80 105 12 84 193 98

129 NM 116 97 35 129 77 124 53 127 159 106 81 120 99 104 172 115

MCA Flow Ratio

Ipsilateral MCA Flow After Stenting, mL/min

Time Between Stenting and Flow Measurement After Stenting, months

0.50 NC NC 1.09 NC NC 1.00 NC 2.17 0.93 0.86 NC 0.99 0.88 NC NC 1.12 0.85

108 194 103 92 116 127 103 61 99 89 136 132 107 138 15 112 155 117

5.5 6 4.5 6 3 3 3 3 3 3 6 3 6 6 3 3 3 3

ICA, internal carotid artery; MCA, middle cerebral artery; NM, not measured; NC, not calculated for patients with .50% contralateral stenosis or occlusion.

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FIGURE 1. Mean ICA flow before stenting (174.9 6 83.6 mL/min), compared with after stenting (250.7 6 91.2 mL/min) (P = .011). CI, confidence interval; ICA, internal carotid artery.

FIGURE 3. Mean MCA flow before stenting (107.8 6 41.6 mL/min) compared with after stenting (114.3 6 36.3 mL/min) (P = .28). CI, confidence interval; MCA, middle cerebral artery.

ultrasound imaging and defined significant recurrent stenosis as symptomatic or $80% restenosis.5,10-12 Digital subtraction angiography was then used to confirm recurrent stenosis detected by Doppler ultrasound imaging. Similarly, the multicenter, prospective study Carotid Revascularization Using Endarterectomy or Stenting Systems (CaRESS) included rate of repeat angiography as an outcome measure.13 The intracranial hemodynamic changes occurring after extracranial carotid artery stenting, however, are not typically used in

follow-up assessments, mainly because these changes have not been clearly established. In 2005, Ko et al14 reported the cerebral blood flow (CBF) changes after extracranial carotid artery stenting using Xenon-133 single-photon emission computed tomography (SPECT).14,15 They found that CBF significantly increased by 21% 6 10% immediately after stent placement, but this elevated CBF did not necessarily occur in patients with the

FIGURE 2. Mean ICA flow ratios before stenting (0.52 6 0.14) vs after stenting (0.73 6 0.30) (P = .58). CI, confidence interval; ICA, internal carotid artery.

FIGURE 4. Mean MCA flow ratios before stenting (1.04 6 0.52) vs after stenting (0.95 6 0.29) (P = .12). CI, confidence interval; MCA, middle cerebral artery.

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FIGURE 5. Relationship between percentage change in ICA flow and percentage change in minimum vessel diameter after stenting. A larger increase in minimum vessel diameter is associated with a greater increase in ICA flow (P = .02, correlation coefficient r = 0.534). ICA, internal carotid artery.

most severe stenosis, demonstrating compensatory intracranial collateral supply before stenting in some patients. Although SPECT allows quantitative measurements of blood flow, it has poor spatial resolution and anatomic localization compared with magnetic resonance imaging (MRI) with perfusion or functional MRI.15,16 Consequently, Chang et al16 used blood oxygen leveldependent MRI to determine cerebral vasoreactivity and perfusion MRI to ascertain changes in CBF before and soon after stenting. This study revealed that a greater increase in CBF after stenting is significantly associated with more severe impairment in cerebral vasoreactivity at baseline (P = .026). As a result of better localization techniques with MRI in comparison with SPECT, CBF changes in this study specifically demonstrated perfusion changes within the MCA territory. More recently, Yun et al7 evaluated the effect of carotid artery stenting on CBF by using arterial spin labeling as opposed to a dynamic susceptibility contrast technique. They reported that CBF in the ipsilateral ICA and MCA territories was significantly increased after stenting (P , .05 in both). In all of these studies, however, CBF changes were assessed in the period immediately following stenting, when hyperperfusion can be encountered, and no delayed assessments were performed.14 Additionally, CBF changes were not analyzed in relationship to changes in vessel stenosis or luminal diameter after stenting. Thus, our current understanding of intracranial blood flow changes after carotid artery stenting is limited. Our study is the first to report the effects of extracranial CAS on intracranial blood flow by using QMRA, a technique that has been validated with the use of in vitro and in vivo models, and has demonstrated utility in the hemodynamic evaluation of basilar and

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vertebral artery angioplasty, as well as following stenting for intracranial stenosis.8,17-20 Our patients underwent intracranial blood flow measurements 3 to 6 months after stenting rather than in the immediate postprocedure period, thus avoiding the period at risk for postprocedural hyperperfusion as well as allowing a period of several months for restoration of cerebral autoregulation and stabilization of cerebral perfusion. We found that, on average, ipsilateral ICA flow compromise was evident in the setting of carotid stenosis, which improved by 43% on average poststenting. However, on average, ipsilateral MCA flow was not impaired at baseline, and we were unable to detect a significant difference (P = .12, n = 7) between the mean ratio of ipsilateral to contralateral MCA flow before and after stenting. Given the limitations of this retrospective study that was not powered beforehand to necessarily ascertain a difference in MCA flow before and after stenting, no conclusions can be made. Nonetheless, if accurate, this finding supports the presence of compensatory intracranial collateral supply prestenting and validates the previously described study that used SPECT scanning.14 Our results differ from the MRI studies formerly referenced that reported increased CBF within the MCA territory poststenting, but this may be attributable to the timing of the assessment with fluctuation in intracranial flow during the immediate vs late postprocedure periods, a discrepancy in flow measurement techniques, or perhaps more robust baseline collateral supply among the patients in our cohort.7,15,16 Our results, however, are corroborated by a recent study that used the optical flow method with digital subtraction angiography immediately after stenting and found significant improvement in ICA flow and nonsignificant augmentation of MCA flow.21 We also examined the relationship between change in flow and change in degree of stenosis, stenosis length, and minimum vessel diameter. Univariate linear regression analysis demonstrated that improvement in minimum vessel diameter after stenting, but not in percentage stenosis (P = .18) or in stenosis length (P = .45), is significantly associated with a larger increase in ipsilateral ICA flow (P = .02). Because improvement in minimum vessel diameter at the site of stenosis was the factor most significantly associated with increased flow, this parameter may be the best indicator of a hemodynamically successful intervention. On the other hand, improved degree of stenosis, stenosis length, minimum vessel diameter, and even ICA flow poststenting were not significantly associated with increase in ipsilateral MCA flow, suggesting that compensatory intracranial collateral supply at baseline prestenting likely redistributes once the ipsilateral ICA is recanalized. These results of MCA flow before and after stenting reiterate the seminal findings of Powers et al,22 which posited that the presence or severity of a cervical carotid lesion by itself cannot be used to extrapolate the hemodynamic status of the intracranial circulation. Rather, the primary determinant of cerebral perfusion in the setting of carotid artery disease is adequacy of collateral pathways. In other words, because MCA flow in most of our patients was neither compromised at baseline nor augmented after stenting, thromboembolism may play the more prominent

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role in cerebral ischemia in the majority of our patients as others have suggested; however, if collateral formation in a given individual is inadequate and leads to MCA flow impairment, the patient is also vulnerable to ischemia from hemodynamic compromise.4 Thus, our study documents the intracranial hemodynamic changes that occur following CAS and demonstrates the clinical utility of QMRA in quantitatively assessing patients before and after CAS. Indeed, prestenting flow rates may help to indicate critical thresholds that could predict high risk of symptoms or reveal evidence of paucity of collateral pathways that can be used to guide recommendations for revascularization. Poststenting flow rates obtained after stenting can provide an objective assessment of the hemodynamic efficacy of the procedure. Here, we also identified improvement in minimum vessel diameter as the benchmark of a hemodynamically successful intervention. Poststenting flow rates attained over a longer follow-up period can be used to evaluate the durability of the procedure and possibly even detect recurrent stenosis. The utility of QMRA in detecting intracranial in-stent restenosis, in fact, has previously been published.19 The authors found that .25% reduction in flow was indicative of angiographic in-stent restenosis, and more severe decrement in flow .50% resulted in symptomatic presentation and stroke. QMRA may then prove advantageous compared with existing modalities as a practical, noninvasive method to identify patients who can benefit the most from CAS and to detect restenosis in the future. Limitations The interpretation of our data is limited by the inherent biases of its retrospective design. Although blood flow and blood vessel measurements were not ascertained by using a blinded protocol, they were made by a multidisciplinary group using standard methods. Blood flow measurements poststenting were also not obtained at uniform times but rather at varying time intervals 3 to 6 months after stenting. Another possible pitfall of this study is its small sample size. The potential variability in the data underlies the fact that blood flow is a physiological parameter potentially influenced by factors such as age, heart rate, and blood pressure. Flow ratios were used in this study where possible in an attempt to control for these confounders.

CONCLUSION ICA flow compromise was evident in the setting of carotid stenosis, which improved by 43% on average poststenting. Improvement in minimum vessel diameter at the site of stenosis was the factor most significantly associated with increased flow, indicating that this parameter is the best indicator of a hemodynamically successful intervention. Within the limitations of this retrospective study, intracranial flow measured in the MCA was not significantly compromised at baseline compared with the contralateral hemisphere, nor significantly altered after stenting. This finding reflects compensatory intracranial collateral supply

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prestenting, which is presumed to redistribute once the ipsilateral ICA is revascularized. Disclosures Ali Alaraj, MD, research grant from NIH; consultant for Cordis-Codman. Victor A. Aletich, MD, research grant from Micrus; consultant for CordisCodman. Sepideh Amin-Hanjani, MD, research grant from NIH; research support (no direct funds) from GE Healthcare, VasSol Inc. Fady T. Charbel, MD, ownership interest in VasSol Inc; consultant for Transonic. The other authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

REFERENCES 1. Go AS, Mozaffarian D, Roger VL, et al. Heart disease and stroke statistics—2014 update: a report from the American Heart Association. Circulation. 2014;129(3): e28-e292. 2. Fisher CM. Occlusion of the internal carotid artery. Arch Neurol Psychiatry. 1951; 65(3):346-377. 3. Caplan LR, Hennerici M. Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol. 1998;55 (11):1475-1482. 4. Loftus CM, Harbaugh RE, Fleck JD, Biller J. Carotid occlusive disease: natural history and medical management. In: Winn HR, ed. Youman’s Neurological Surgery. 6th ed. Philadelphia, PA: WB Saunders; 2011:3616. 5. Yadav JS, Wholey MH, Kuntz RE, et al. Protected carotid-artery stenting versus endarterectomy in high-risk patients. N Engl J Med. 2004;351(15): 1493-1501. 6. CAVATAS investigators. Endovascular versus surgical treatment in patients with carotid stenosis in the Carotid and Vertebral Artery Transluminal Angioplasty Study (CAVATAS): a randomized trial. Lancet. 2001;357(9270):1729-1737. 7. Yun TJ, Sohn C-H, Han MH, et al. Effect of carotid artery stenting on cerebral blood flow: evaluation of hemodynamic changes using arterial spin labeling. Neuroradiology. 2013;55(3):271-281. 8. Zhao M, Charbel FT, Alperin N, Loth F, Clark ME. Improved phase-contrast flow quantification by three-dimensional vessel localization. Magn Reson Imaging. 2000;18(6):697-706. 9. The North American symptomatic carotid endarterectomy trial collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with highgrade carotid stenosis. N Engl J Med. 1991;325(7):445-453. 10. Siddiqui AH, Ecker RD, Mocco J, Snyder KV, Levy EI, Hopkins LN. Carotid artery angioplasty and stenting. In: Winn HR, ed. Youman’s Neurological Surgery. 6th ed. Philadelphia, PA: WB Saunders; 2011:3632-3640. 11. Setacci C, Pula G, Baldi I, et al. Determinants of in-stent restenosis after carotid angioplasty: a case-control study. J Endovasc Ther. 2003;10(6):1031-1038. 12. Levy EI, Hanel RA, Lau T, et al. Frequency and management of recurrent stenosis after carotid artery stent implantation. J Neurosurg. 2005;102(1):29-37. 13. CaRESS Steering Committee. Carotid Revascularization Using Endarterectomy or Stenting Systems (CaRESS) phase I clinical trial: 1-year results. J Vasc Surg. 2005; 42(2):213-219. 14. Ko N, Achrol AS, Chopra M, et al. Cerebral blood flow changes after endovascular treatment of cerebrovascular stenoses. AJNR Am J Neuroradiol. 2005;26(3): 538-542. 15. Ko N, Achrol AS, Martin AJ, et al. Magnetic resonance perfusion tracks 133Xe cerebral blood flow changes after carotid stenting. Stroke. 2005;36(3):676-678. 16. Chang TY, Liu HL, Lee TH, et al. Change in cerebral perfusion after carotid angioplasty with stenting is related to cerebral vasoreactivity: a study using dynamic susceptibility-weighted contrast-enhanced MR imaging and functional MR imaging with a breath-holding paradigm. AJNR Am J Neuroradiol. 2009;30(7): 1330-1336. 17. Amin-Hanjani S, Du X, Zhao M, Walsh K, Malisch TW, Charbel FT. Use of quantitative magnetic resonance angiography to stratify stroke risk in symptomatic vertebrobasilar disease. Stroke. 2005;36(6):1140-1145. 18. Guppy KH, Charbel FT, Corsten LA, Zhao M, Debrun G. Hemodynamic evaluation of basilar and vertebral artery angioplasty. Neurosurgery. 2002;51(2): 327-334.

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19. Amin-Hanjani S, Alaraj A, Calderon-Arnulphi M, Aletich VA, Thulborn KR, Charbel FT. Detection of intracranial in-stent restenosis using quantitative magnetic resonance angiography. Stroke. 2010;41(11):2534-2538. 20. Calderon-Arnulphi M, Amin-Hanjani S, Alaraj A, et al. In vivo evaluation of quantitative MR angiography in a canine carotid artery stenosis model. AJNR Am J Neuroradiol. 2011;32(8):1552-1559. 21. Wu T-H, Lin C-J, Lin Y-H, Guo W-Y, Huang T-C. Quantitative analysis of digital subtraction angiography using optical flow method on occlusive cerebrovascular disease. Comput Methods Programs Biomed. 2013;111(3): 693-700. 22. Powers WJ, Press GA, Grubb RL, Gado M, Raichle ME. The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. Ann Intern Med. 1987;106(1):27-35.

COMMENTS

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he authors retrospectively review a series of patients with MRI-based quantification of vascular flow before and after CAS. They report that revascularization results in higher flow within the internal carotid artery (ICA) but were unable to establish a similar trend for middle cerebral artery flow, ostensibly indicating collateral supply via the circle of Willis. The authors further indicate that minimum luminal diameter is superior to percent stenosis and stenosis length as an index of flow increase following revascularization. One must exercise caution with any small case series, particularly when groupwise analysis is performed in lieu of longitudinal analysis, but the results reported here comport with our existing understanding of intracranial flow dynamics (assuming that collateral routes across the circle of Willis are indeed present). More importantly, these results underscore the desirability of a perfusion-based index to replace proxy anatomic criteria (eg, percent stenosis) that are currently widely used as the basis of patient selection for intervention. However, even patients with severely compromised distal ICA flow may not benefit from treatment if robust collateral flow is present. For this reason, measurement of end-organ perfusion based on arterial spin-labeling MRI or related methods may hold even greater promise for patient selection. With any approach, one must be cognizant that the timing of blood flow changes following revascularization is complex and can evolve over many months.

precise. The methods described in this article are another attempt to address that topic. Monika Killer-Oberpfälzer Salzburg, Austria

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he authors present a series of patients who underwent carotid artery stenting (CAS) and had quantitative magnetic resonance angiography (QMRA) performed before the procedure and approximately 3 months after the procedure. Their stated goal was to “determine the cerebral hemodynamic changes that occur after carotid stenting using quantitative magnetic resonance angiography.” QMRA is an established method for quantifying flow in the intracranial circulation, and the authors apply this analysis to their patients to better understand and objectively evaluate the changes induced by CAS. The major findings are the following: internal carotid artery flow is improved by CAS; the improvement in flow is most significantly correlated with residual lumen; and middle cerebral artery flow is not altered by CAS. There are few studies that objectify the changes in the intracranial circulation after CAS. The authors reference a technique for quantitative analysis of flow using digital subtraction angiography after CAS by Wu et al1 that corroborates this article’s findings. However, QMRA has the benefit of providing a method for continued, noninvasive evaluation of the intracranial circulation postrevascularization. The main finding likely limited by small sample size is that circle of Willis collaterals are robust in most patients and significantly compensate for most proximal stenoses. The authors describe results from a small, retrospective case series, so applying their results to a broader patient population would be premature. These results do highlight the importance of developing a better collective understanding of carotid stenosis and its relationship to cerebral perfusion so that patient selection for revascularization can be further optimized. Although the article has limitations, it represents an important move toward allowing the results of CAS to be more easily quantified. This is critical as clinicians look for new ways of identifying asymptomatic carotid stenosis patients who have hypoperfusion and may be experiencing subtle cognitive consequences from proximal carotid stenosis.

Akash P. Kansagra St. Louis, Missouri

Marshall C. Cress Adnan H. Siddiqui Buffalo, New York

lthough it would be very helpful in the treatment of carotid artery stenosis if we would have the possibility to know exactly the amount and sufficiency of collaterals before treatment, all methods used so far to evaluate and interpret cerebral blood flow in this means are not very

1. Wu TH, Lin CJ, Lin YH, Guo WY, Huang TC. Quantitative analysis of digital subtraction angiography using optical flow method on occlusive cerebrovascular disease. Comput Methods Programs Biomed. 2013;111(3):693-700.

A

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Intracranial blood flow changes after extracranial carotid artery stenting.

Carotid artery stenting is an endovascular treatment option for patients with extracranial carotid stenosis. However, intracranial blood flow changes ...
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