Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Hemorrhagic stroke
ORIGINAL RESEARCH
Leptomeningeal collateral vessels are a major risk factor for intracranial hemorrhage after carotid stenting in patients with carotid atherosclerotic plaque Kang Ji Lee, Hyo Sung Kwak, Gyung Ho Chung, Ji Soo Song, Seung Bae Hwang Radiology and Research Institute of Clinical Medicine of Chonbuk National UniversityBiomedical Research Institute of Chonbuk National University Hospital, Jeonju-shi, South Korea Correspondence to Professor Hyo Sung Kwak, Radiology and Research Institute of Clinical Medicine of Chonbuk National UniversityBiomedical Research Institute of Chonbuk National University Hospital, 634-18, KeumamDong, Jeonju-shi, Jeonbuk 561-712, South Korea; [email protected] Received 31 December 2014 Revised 25 February 2015 Accepted 15 March 2015
ABSTRACT Aim To evaluate the relationship between leptomeningeal collaterals and intracranial hemorrhage (ICH) after carotid artery stenting (CAS). Methods A retrospective study was undertaken of 228 patients (median age 75 years (range 44–90); 187 men and 41 women) who underwent CAS due to unilateral carotid atherosclerotic plaque from January 2009 to December 2013. Cerebral angiographic findings were classified into three patterns: type I, normal visualization of the anterior and middle cerebral arteries without leptomeningeal collaterals; type II, visualization of the middle cerebral artery only without leptomeningeal collaterals; and type III, visualization of leptomeningeal collateral flow. Results For all cerebral angiographic findings, 146 (64.0%) were type I, 61 (26.8%) were type II, and 21 (9.2%) were type III. Four patients (1.8%) died with fatal ICH after CAS and had type III angiographic findings (19%). The prevalence of ICH in patients with leptomeningeal collateral vessels was significantly higher than in patients without leptomeningeal collateral vessels (19% vs 0%, p50% and in asymptomatic patients with carotid artery stenosis >70%. The degree of stenosis was calculated from digital subtraction angiography images using the North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria. HPS with ICH was defined by CT evidence of punctate or confluent hyperdensities consistent with blood within the parenchyma of the cerebral hemisphere after CAS.
CAS procedure The CAS procedures were performed by one interventional neuroradiologist with 10 years of experience in neurovascular intervention. All patients were examined by a stroke neurologist before and after the procedure to document cerebrovascular symptom status and to record any new neurologic deficits. For at least 3 days before the CAS, each patient received oral antiplatelet treatment consisting of aspirin (100 mg/day) and clopidogrel (75 mg/day). At the beginning of the procedure, heparin was given intravenously as a 3000 IU bolus. All procedures were performed using a femoral approach. After placement of the 8 F long sheath, diagnostic cerebral angiography using a 5 F catheter was performed to evaluate the severity of
Lee KJ, et al. J NeuroIntervent Surg 2015;0:1–6. doi:10.1136/neurintsurg-2014-011634
1
Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Hemorrhagic stroke Table 1 Cerebral angiographic findings with carotid atherosclerotic plaque Type I IA IB Type II IIA IIB Type III IIIA IIIB IIIC
Normal visualization of the ACA and MCA branches without leptomeningeal collaterals Normal continuous ACA visualization Compromised ACA flow, but visualization of the A1 and A2 Only visualization of MCA flow without leptomeningeal collaterals on ipsilateral cerebral angiography Collateral MCA flow due to Acom or Pcom No visualization of Acom or Pcom flow Visualization of leptomeningeal collateral flow with/without ACA flow ACA leptomeningeal collateral flow PCA leptomeningeal collateral flow ACA and PCA leptomeningeal collateral flow
ACA, anterior cerebral artery; Acom, anterior communicating artery; MCA, middle cerebral artery; PCA, posterior cerebral artery; Pcom, posterior communicating artery.
carotid stenosis according to the NASCET criteria and the collateral flow of the ipsilateral cerebral hemisphere. An 8 F guiding catheter was introduced into the common carotid artery. The stenotic lesion was crossed with the guidewire using a distal embolic protection system (FilterWireEz; Boston Scientific, Natick, Massachusetts, USA or SpiderRx; ev3, Plymouth, Minnesota, USA or Emboshield; Abbott, Santa Clara, California, USA). In most cases the lesion was predilated with a 4 mm or 5 mm×40 mm percutaneous transluminal angioplasty balloon (Symmetry; Boston Scientific) inflated at 6 atm. A self-expandable stent (RX Acculink; Abbott, Santa Clara, California, USA or PRECISE; Cordis, Miami, Florida, USA) was then placed over the lesion. Post-dilation was performed with a percutaneous transluminal angioplasty balloon in patients with >30% residual stenosis by the NASCET criteria. After the CAS was completed, the filter was captured and retrieved by the delivery catheter, followed by completion of
the angiography. Procedural success was defined as a complete angiography showing 75 years), history of stroke, long-standing hypertension, severe stenosis, contralateral stenosis, and poor collateralization.4 7 20–22 In our study, patients with HPS and ICH had significant severe stenosis but age, hypertension, history of stroke, and contralateral stenosis were not significantly different between patients with HPS and ICH and patients without ICH. Leptomeningeal collaterals are anastomotic vessels providing alternative routes for blood flow during a stroke.23 The leptomeningeal vessels are not newly formed but are merely dilated pre-existing vessels.24 25 Kono et al24 performed histopathologic and morphometric studies of leptomeningeal vessels in Moyamoya disease. All patients showed dilatory changes of both arteries and veins. Attenuation or disruption of the internal elastic lamina and fibrous intimal thickening were more prominent in patients who had had Moyamoya disease. This structural alteration of the vascular walls suggests their adaptability for participation in the collateral circulation at the cerebral surface. In chronic hypoperfusion due to severe carotid stenosis or occlusion, flow via the leptomeningeal vessels can maintain cerebral blood flow when primary collateral flow (via the arterial segments of the circle of Willis) is insufficient.26–28 In our study, 21 patients (9.2%) had leptomeningeal collateral flow. Of these patients, four had a massive ICH and died within 1 week of the CAS procedure. All patients without leptomeningeal collateral flow did not develop ICH. This finding suggests that patients with carotid stenosis and leptomeningeal collateral flow had chronic hypoperfusion in the ipsilateral cerebral hemisphere and insufficient primary collateral flow via the segments of the circle of Willis. In addition, leptomeningeal collateral vessels had an ultrastructural deformity, such as disruption of the internal elastic lamina and fibrotic change of the intima, compared with normal cerebral arteries. HPS with ICH is associated with an extremely poor prognosis, as shown in our study; thus, prevention is critical. The most important perioperative management is vigilant monitoring and control of systemic blood pressure. Recently, Egashira et al29 performed a two-stage recanalization by CEA after balloon angioplasty for symptomatic severe carotid artery stenosis to avoid HPS. However, it is a difficult two-stage recanalization because of variable risk factors for developing HPS following CEA or CAS, and it is costly. We therefore performed two-stage recanalization in patients with high-grade stenosis and leptomeningeal collateral flow due to chronic hypoperfusion.
CONCLUSIONS Leptomeningeal collateral vessels and severe carotid stenosis is a major risk factor of HPS with ICH after CAS in patients with carotid atherosclerotic plaque. Patients with leptomeningeal collateral vessels and severe carotid stenosis should undergo a twostage operation, vigilant monitoring, and control of systemic blood pressure for treatment of carotid atherosclerotic plaque. Contributors KJL: wrote the manuscript; HSK: director; GHC, SBH, JSS: reviewed the manuscript. Funding This paper was supported by research funds from Chonbuk National University in 2014. Competing interests None.
0.000
HPS, hyperperfusion syndrome; ICH, intracranial hemorrhage; NASCET, North American Symptomatic Carotid Endarterectomy Trial.
Lee KJ, et al. J NeuroIntervent Surg 2015;0:1–6. doi:10.1136/neurintsurg-2014-011634
Ethics approval Ethics approval was obtained from Chonbuk National University Hospital. Provenance and peer review Not commissioned; externally peer reviewed. Data sharing statement A technical appendix, statistical code and dataset are available from the corresponding author. Participants gave informed consent for data sharing. 5
Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Hemorrhagic stroke REFERENCES 1 2
3
4
5 6
7
8
9
10
11 12 13
6
Petty GW, Brown RD Jr, Whisnant JP, et al. Ischemic stroke subtypes: a population-based study of incidence and risk factors. Stroke 1999;30:2513–16. Ederle J, Featherstone RL, Brown MM. Percutaneous transluminal angioplasty and stenting for carotid artery stenosis. Cochrane Database Syst Rev 2007;(4): CD000515. Adams RJ, Albers G, Alberts MJ, et al. Update to the AHA/ASA recommendations for the prevention of stroke in patients with stroke and transient ischemic attack. Stroke 2008;39:1647–52. Abou-Chebl A, Yadav JS, Reginelli JP, et al. Intracranial hemorrhage and hyperperfusion syndrome following carotid artery stenting: risk factors, prevention, and treatment. J Am Coll Cardiol 2004;43:1596–601. Karapanayiotides T, Meuli R, Devuyst G, et al. Postcarotid endarterectomy hyperperfusion or reperfusion syndrome. Stroke 2005;36:21–6. Mansoor GA, White WB, Grunnet M, et al. Intracerebral hemorrhage after carotid endarterectomy associated with ipsilateral fibrinoid necrosis: a consequence of the hyperperfusion syndrome? J Vasc Surg 1996;23:147–51. Narita S, Aikawa H, Nagata S, et al. Intraprocedural prediction of hemorrhagic cerebral hyperperfusion syndrome after carotid artery stenting. J Stroke Cerebrovasc Dis 2013;22:615–19. Sbarigia E, Speziale F, Giannoni MF, et al. Post-carotid endarterectomy hyperperfusion syndrome: preliminary observations for identifying at risk patients by transcranial Doppler sonography and the acetazolamide test. Eur J Vasc Surg 1993;7:252–6. Ouriel K, Shortell CK, Illig KA, et al. Intracerebral hemorrhage after carotid endarterectomy: incidence, contribution to neurologic morbidity, and predictive factors. J Vasc Surg 1999;29:82–7. Nambiar V, Sohn SI, Almekhlafi MA, et al. CTA collateral status and response to recanalization in patients with acute ischemic stroke. AJNR Am J Neuroradiol 2014;35:884–90. van Mook WN, Rennenberg RJ, Schurink GW, et al. Cerebral hyperperfusion syndrome. Lancet Neurol 2005;4:877–88. Piepgras DG, Morgan MK, Sundt TM Jr, et al. Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 1988;68:532–6. Solomon RA, Loftus CM, Quest DO, et al. Incidence and etiology of intracerebral hemorrhage following carotid endarterectomy. J Neurosurg 1986; 64:29–34.
14 15
16
17 18
19
20 21 22
23 24 25 26 27 28 29
Schroeder T, Sillesen H, Sorensen O, et al. Cerebral hyperperfusion following carotid endarterectomy. J Neurosurg 1987;66:824–9. Meyers PM, Higashida RT, Phatouros CC, et al. Cerebral hyperperfusion syndrome after percutaneous transluminal stenting of the craniocervical arteries. Neurosurgery 2000;47:335–43. Cikrit DF, Burt RW, Dalsing MC, et al. Acetazolamide enhanced single photon emission computed tomography (SPECT) evaluation of cerebral perfusion before and after carotid endarterectomy. J Vasc Surg 1992;15:747–53. Harrison PB, Wong MJ, Belzberg A, et al. Hyperperfusion syndrome after carotid endarterectomy. CT changes. Neuroradiology 1991;33:106–10. Jansen C, Sprengers AM, Moll FL, et al. Prediction of intracerebral haemorrhage after carotid endarterectomy by clinical criteria and intraoperative transcranial Doppler monitoring. Eur J Vasc Surg 1994;8:303–8. Maas MB, Kwolek CJ, Hirsch JA, et al. Clinical risk predictors for cerebral hyperperfusion syndrome after carotid endarterectomy. J Neurol Neurosurg Psychiatry 2013;84:569–72. Medel R, Crowley RW, Dumont AS. Hyperperfusion syndrome following endovascular cerebral revascularization. Neurosurg Focus 2009;26:E4. Grunwald IQ, Politi M, Reith W, et al. Hyperperfusion syndrome after carotid stent angioplasty. Neuroradiology 2009;51:169–74. Ogasawara K, Sakai N, Kuroiwa T, et al. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J Neurosurg 2007;107:1130–6. Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 2003;34:2750–62. Kono S, Oka K, Sueishi K. Histopathologic and morphometric studies of leptomeningeal vessels in moyamoya disease. Stroke 1990;21:1044–50. Takebayashi S, Matsuo K, Kaneko M. Ultrastructural studies of cerebral arteries and collateral vessels in moyamoya disease. Stroke 1984;15:728–32. Muller M, Schimrigk K. Vasomotor reactivity and pattern of collateral blood flow in severe occlusive carotid artery disease. Stroke 1996;27:296–9. Liebeskind DS. Collateral circulation. Stroke 2003;34:2279–84. McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol 2012;33:576–82. Egashira Y, Yoshimura S, Yamada K, et al. Stepwise revascularization by carotid endarterectomy after balloon angioplasty for symptomatic severe carotid artery stenosis. Ann Vasc Surg 2012;26:e731–9.
Lee KJ, et al. J NeuroIntervent Surg 2015;0:1–6. doi:10.1136/neurintsurg-2014-011634
Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Leptomeningeal collateral vessels are a major risk factor for intracranial hemorrhage after carotid stenting in patients with carotid atherosclerotic plaque Kang Ji Lee, Hyo Sung Kwak, Gyung Ho Chung, Ji Soo Song and Seung Bae Hwang J NeuroIntervent Surg published online April 3, 2015
Updated information and services can be found at: http://jnis.bmj.com/content/early/2015/04/03/neurintsurg-2014-01163 4
These include:
References Email alerting service
Topic Collections
This article cites 28 articles, 11 of which you can access for free at: http://jnis.bmj.com/content/early/2015/04/03/neurintsurg-2014-01163 4#BIBL Receive free email alerts when new articles cite this article. Sign up in the box at the top right corner of the online article.
Articles on similar topics can be found in the following collections Hemorrhagic stroke (237)
Notes
To request permissions go to: http://group.bmj.com/group/rights-licensing/permissions To order reprints go to: http://journals.bmj.com/cgi/reprintform To subscribe to BMJ go to: http://group.bmj.com/subscribe/
Hemorrhagic stroke
ORIGINAL RESEARCH
Leptomeningeal collateral vessels are a major risk factor for intracranial hemorrhage after carotid stenting in patients with carotid atherosclerotic plaque Kang Ji Lee, Hyo Sung Kwak, Gyung Ho Chung, Ji Soo Song, Seung Bae Hwang Radiology and Research Institute of Clinical Medicine of Chonbuk National UniversityBiomedical Research Institute of Chonbuk National University Hospital, Jeonju-shi, South Korea Correspondence to Professor Hyo Sung Kwak, Radiology and Research Institute of Clinical Medicine of Chonbuk National UniversityBiomedical Research Institute of Chonbuk National University Hospital, 634-18, KeumamDong, Jeonju-shi, Jeonbuk 561-712, South Korea; [email protected] Received 31 December 2014 Revised 25 February 2015 Accepted 15 March 2015
ABSTRACT Aim To evaluate the relationship between leptomeningeal collaterals and intracranial hemorrhage (ICH) after carotid artery stenting (CAS). Methods A retrospective study was undertaken of 228 patients (median age 75 years (range 44–90); 187 men and 41 women) who underwent CAS due to unilateral carotid atherosclerotic plaque from January 2009 to December 2013. Cerebral angiographic findings were classified into three patterns: type I, normal visualization of the anterior and middle cerebral arteries without leptomeningeal collaterals; type II, visualization of the middle cerebral artery only without leptomeningeal collaterals; and type III, visualization of leptomeningeal collateral flow. Results For all cerebral angiographic findings, 146 (64.0%) were type I, 61 (26.8%) were type II, and 21 (9.2%) were type III. Four patients (1.8%) died with fatal ICH after CAS and had type III angiographic findings (19%). The prevalence of ICH in patients with leptomeningeal collateral vessels was significantly higher than in patients without leptomeningeal collateral vessels (19% vs 0%, p50% and in asymptomatic patients with carotid artery stenosis >70%. The degree of stenosis was calculated from digital subtraction angiography images using the North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria. HPS with ICH was defined by CT evidence of punctate or confluent hyperdensities consistent with blood within the parenchyma of the cerebral hemisphere after CAS.
CAS procedure The CAS procedures were performed by one interventional neuroradiologist with 10 years of experience in neurovascular intervention. All patients were examined by a stroke neurologist before and after the procedure to document cerebrovascular symptom status and to record any new neurologic deficits. For at least 3 days before the CAS, each patient received oral antiplatelet treatment consisting of aspirin (100 mg/day) and clopidogrel (75 mg/day). At the beginning of the procedure, heparin was given intravenously as a 3000 IU bolus. All procedures were performed using a femoral approach. After placement of the 8 F long sheath, diagnostic cerebral angiography using a 5 F catheter was performed to evaluate the severity of
Lee KJ, et al. J NeuroIntervent Surg 2015;0:1–6. doi:10.1136/neurintsurg-2014-011634
1
Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Hemorrhagic stroke Table 1 Cerebral angiographic findings with carotid atherosclerotic plaque Type I IA IB Type II IIA IIB Type III IIIA IIIB IIIC
Normal visualization of the ACA and MCA branches without leptomeningeal collaterals Normal continuous ACA visualization Compromised ACA flow, but visualization of the A1 and A2 Only visualization of MCA flow without leptomeningeal collaterals on ipsilateral cerebral angiography Collateral MCA flow due to Acom or Pcom No visualization of Acom or Pcom flow Visualization of leptomeningeal collateral flow with/without ACA flow ACA leptomeningeal collateral flow PCA leptomeningeal collateral flow ACA and PCA leptomeningeal collateral flow
ACA, anterior cerebral artery; Acom, anterior communicating artery; MCA, middle cerebral artery; PCA, posterior cerebral artery; Pcom, posterior communicating artery.
carotid stenosis according to the NASCET criteria and the collateral flow of the ipsilateral cerebral hemisphere. An 8 F guiding catheter was introduced into the common carotid artery. The stenotic lesion was crossed with the guidewire using a distal embolic protection system (FilterWireEz; Boston Scientific, Natick, Massachusetts, USA or SpiderRx; ev3, Plymouth, Minnesota, USA or Emboshield; Abbott, Santa Clara, California, USA). In most cases the lesion was predilated with a 4 mm or 5 mm×40 mm percutaneous transluminal angioplasty balloon (Symmetry; Boston Scientific) inflated at 6 atm. A self-expandable stent (RX Acculink; Abbott, Santa Clara, California, USA or PRECISE; Cordis, Miami, Florida, USA) was then placed over the lesion. Post-dilation was performed with a percutaneous transluminal angioplasty balloon in patients with >30% residual stenosis by the NASCET criteria. After the CAS was completed, the filter was captured and retrieved by the delivery catheter, followed by completion of
the angiography. Procedural success was defined as a complete angiography showing 75 years), history of stroke, long-standing hypertension, severe stenosis, contralateral stenosis, and poor collateralization.4 7 20–22 In our study, patients with HPS and ICH had significant severe stenosis but age, hypertension, history of stroke, and contralateral stenosis were not significantly different between patients with HPS and ICH and patients without ICH. Leptomeningeal collaterals are anastomotic vessels providing alternative routes for blood flow during a stroke.23 The leptomeningeal vessels are not newly formed but are merely dilated pre-existing vessels.24 25 Kono et al24 performed histopathologic and morphometric studies of leptomeningeal vessels in Moyamoya disease. All patients showed dilatory changes of both arteries and veins. Attenuation or disruption of the internal elastic lamina and fibrous intimal thickening were more prominent in patients who had had Moyamoya disease. This structural alteration of the vascular walls suggests their adaptability for participation in the collateral circulation at the cerebral surface. In chronic hypoperfusion due to severe carotid stenosis or occlusion, flow via the leptomeningeal vessels can maintain cerebral blood flow when primary collateral flow (via the arterial segments of the circle of Willis) is insufficient.26–28 In our study, 21 patients (9.2%) had leptomeningeal collateral flow. Of these patients, four had a massive ICH and died within 1 week of the CAS procedure. All patients without leptomeningeal collateral flow did not develop ICH. This finding suggests that patients with carotid stenosis and leptomeningeal collateral flow had chronic hypoperfusion in the ipsilateral cerebral hemisphere and insufficient primary collateral flow via the segments of the circle of Willis. In addition, leptomeningeal collateral vessels had an ultrastructural deformity, such as disruption of the internal elastic lamina and fibrotic change of the intima, compared with normal cerebral arteries. HPS with ICH is associated with an extremely poor prognosis, as shown in our study; thus, prevention is critical. The most important perioperative management is vigilant monitoring and control of systemic blood pressure. Recently, Egashira et al29 performed a two-stage recanalization by CEA after balloon angioplasty for symptomatic severe carotid artery stenosis to avoid HPS. However, it is a difficult two-stage recanalization because of variable risk factors for developing HPS following CEA or CAS, and it is costly. We therefore performed two-stage recanalization in patients with high-grade stenosis and leptomeningeal collateral flow due to chronic hypoperfusion.
CONCLUSIONS Leptomeningeal collateral vessels and severe carotid stenosis is a major risk factor of HPS with ICH after CAS in patients with carotid atherosclerotic plaque. Patients with leptomeningeal collateral vessels and severe carotid stenosis should undergo a twostage operation, vigilant monitoring, and control of systemic blood pressure for treatment of carotid atherosclerotic plaque. Contributors KJL: wrote the manuscript; HSK: director; GHC, SBH, JSS: reviewed the manuscript. Funding This paper was supported by research funds from Chonbuk National University in 2014. Competing interests None.
0.000
HPS, hyperperfusion syndrome; ICH, intracranial hemorrhage; NASCET, North American Symptomatic Carotid Endarterectomy Trial.
Lee KJ, et al. J NeuroIntervent Surg 2015;0:1–6. doi:10.1136/neurintsurg-2014-011634
Ethics approval Ethics approval was obtained from Chonbuk National University Hospital. Provenance and peer review Not commissioned; externally peer reviewed. Data sharing statement A technical appendix, statistical code and dataset are available from the corresponding author. Participants gave informed consent for data sharing. 5
Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Hemorrhagic stroke REFERENCES 1 2
3
4
5 6
7
8
9
10
11 12 13
6
Petty GW, Brown RD Jr, Whisnant JP, et al. Ischemic stroke subtypes: a population-based study of incidence and risk factors. Stroke 1999;30:2513–16. Ederle J, Featherstone RL, Brown MM. Percutaneous transluminal angioplasty and stenting for carotid artery stenosis. Cochrane Database Syst Rev 2007;(4): CD000515. Adams RJ, Albers G, Alberts MJ, et al. Update to the AHA/ASA recommendations for the prevention of stroke in patients with stroke and transient ischemic attack. Stroke 2008;39:1647–52. Abou-Chebl A, Yadav JS, Reginelli JP, et al. Intracranial hemorrhage and hyperperfusion syndrome following carotid artery stenting: risk factors, prevention, and treatment. J Am Coll Cardiol 2004;43:1596–601. Karapanayiotides T, Meuli R, Devuyst G, et al. Postcarotid endarterectomy hyperperfusion or reperfusion syndrome. Stroke 2005;36:21–6. Mansoor GA, White WB, Grunnet M, et al. Intracerebral hemorrhage after carotid endarterectomy associated with ipsilateral fibrinoid necrosis: a consequence of the hyperperfusion syndrome? J Vasc Surg 1996;23:147–51. Narita S, Aikawa H, Nagata S, et al. Intraprocedural prediction of hemorrhagic cerebral hyperperfusion syndrome after carotid artery stenting. J Stroke Cerebrovasc Dis 2013;22:615–19. Sbarigia E, Speziale F, Giannoni MF, et al. Post-carotid endarterectomy hyperperfusion syndrome: preliminary observations for identifying at risk patients by transcranial Doppler sonography and the acetazolamide test. Eur J Vasc Surg 1993;7:252–6. Ouriel K, Shortell CK, Illig KA, et al. Intracerebral hemorrhage after carotid endarterectomy: incidence, contribution to neurologic morbidity, and predictive factors. J Vasc Surg 1999;29:82–7. Nambiar V, Sohn SI, Almekhlafi MA, et al. CTA collateral status and response to recanalization in patients with acute ischemic stroke. AJNR Am J Neuroradiol 2014;35:884–90. van Mook WN, Rennenberg RJ, Schurink GW, et al. Cerebral hyperperfusion syndrome. Lancet Neurol 2005;4:877–88. Piepgras DG, Morgan MK, Sundt TM Jr, et al. Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 1988;68:532–6. Solomon RA, Loftus CM, Quest DO, et al. Incidence and etiology of intracerebral hemorrhage following carotid endarterectomy. J Neurosurg 1986; 64:29–34.
14 15
16
17 18
19
20 21 22
23 24 25 26 27 28 29
Schroeder T, Sillesen H, Sorensen O, et al. Cerebral hyperperfusion following carotid endarterectomy. J Neurosurg 1987;66:824–9. Meyers PM, Higashida RT, Phatouros CC, et al. Cerebral hyperperfusion syndrome after percutaneous transluminal stenting of the craniocervical arteries. Neurosurgery 2000;47:335–43. Cikrit DF, Burt RW, Dalsing MC, et al. Acetazolamide enhanced single photon emission computed tomography (SPECT) evaluation of cerebral perfusion before and after carotid endarterectomy. J Vasc Surg 1992;15:747–53. Harrison PB, Wong MJ, Belzberg A, et al. Hyperperfusion syndrome after carotid endarterectomy. CT changes. Neuroradiology 1991;33:106–10. Jansen C, Sprengers AM, Moll FL, et al. Prediction of intracerebral haemorrhage after carotid endarterectomy by clinical criteria and intraoperative transcranial Doppler monitoring. Eur J Vasc Surg 1994;8:303–8. Maas MB, Kwolek CJ, Hirsch JA, et al. Clinical risk predictors for cerebral hyperperfusion syndrome after carotid endarterectomy. J Neurol Neurosurg Psychiatry 2013;84:569–72. Medel R, Crowley RW, Dumont AS. Hyperperfusion syndrome following endovascular cerebral revascularization. Neurosurg Focus 2009;26:E4. Grunwald IQ, Politi M, Reith W, et al. Hyperperfusion syndrome after carotid stent angioplasty. Neuroradiology 2009;51:169–74. Ogasawara K, Sakai N, Kuroiwa T, et al. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J Neurosurg 2007;107:1130–6. Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 2003;34:2750–62. Kono S, Oka K, Sueishi K. Histopathologic and morphometric studies of leptomeningeal vessels in moyamoya disease. Stroke 1990;21:1044–50. Takebayashi S, Matsuo K, Kaneko M. Ultrastructural studies of cerebral arteries and collateral vessels in moyamoya disease. Stroke 1984;15:728–32. Muller M, Schimrigk K. Vasomotor reactivity and pattern of collateral blood flow in severe occlusive carotid artery disease. Stroke 1996;27:296–9. Liebeskind DS. Collateral circulation. Stroke 2003;34:2279–84. McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol 2012;33:576–82. Egashira Y, Yoshimura S, Yamada K, et al. Stepwise revascularization by carotid endarterectomy after balloon angioplasty for symptomatic severe carotid artery stenosis. Ann Vasc Surg 2012;26:e731–9.
Lee KJ, et al. J NeuroIntervent Surg 2015;0:1–6. doi:10.1136/neurintsurg-2014-011634
Downloaded from http://jnis.bmj.com/ on May 16, 2015 - Published by group.bmj.com
Leptomeningeal collateral vessels are a major risk factor for intracranial hemorrhage after carotid stenting in patients with carotid atherosclerotic plaque Kang Ji Lee, Hyo Sung Kwak, Gyung Ho Chung, Ji Soo Song and Seung Bae Hwang J NeuroIntervent Surg published online April 3, 2015
Updated information and services can be found at: http://jnis.bmj.com/content/early/2015/04/03/neurintsurg-2014-01163 4
These include:
References Email alerting service
Topic Collections
This article cites 28 articles, 11 of which you can access for free at: http://jnis.bmj.com/content/early/2015/04/03/neurintsurg-2014-01163 4#BIBL Receive free email alerts when new articles cite this article. Sign up in the box at the top right corner of the online article.
Articles on similar topics can be found in the following collections Hemorrhagic stroke (237)
Notes
To request permissions go to: http://group.bmj.com/group/rights-licensing/permissions To order reprints go to: http://journals.bmj.com/cgi/reprintform To subscribe to BMJ go to: http://group.bmj.com/subscribe/
