Intraoperative idiopathic subarachnoid hemorrhage during carotid artery stenting: A case report and literature review
Interventional Neuroradiology 2015, Vol. 21(5) 592–597 ! The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1591019915594332 ine.sagepub.com
Akitake Okamura, Mitsuo Nakaoka, Naohiko Ohbayashi, Kaita Yahara and Shinya Nabika
Abstract Carotid artery stenting (CAS) has a fatal complication of intracranial hemorrhage (ICH) associated with cerebral hyperperfusion syndrome (CHS), i.e. brain hemorrhage and subarachnoid hemorrhage (SAH). Although SAH accounts for a small percentage of these patients, it is difficult to make a differential diagnosis of this syndrome from CHS without ICH because the clinical presentations resemble each other. Furthermore, not only does the cause of SAH following CAS remain unclear but also the role of controlling postoperative blood pressure is not detected in preventing ICH after CAS. Herein, we report a case of SAH following CAS and review previous literature to discuss the mechanism and the management of this fatal complication. A 78-year-old woman with a history of arteriosclerotic obliteration and myocardial infarction was referred to our department for intervention to asymptomatic severe stenosis of the right internal carotid artery. We performed CAS under local anesthesia. Although her blood pressure was controlled to normotension during the procedure, the patient complained of headache following predilation. Postoperative emergent non-contrast computed tomography revealed SAH with leakage of contrast medium occupying the right sylvian fissure. We continued strict blood pressure control, and the patient was discharged without any neurological deficit. A well-opened lumen of the stent was recognized three months later at the outpatient visit. Strict control of intraoperative and postoperative blood pressure may improve the outcome of SAH following CAS though the role in preventing ICH after CAS is unclear.
Keyword Carotid artery stenting, subarachnoid hemorrhage, complication
Introduction Carotid artery stenting (CAS) has been widely performed as an alternative to carotid endarterectomy (CEA) for carotid artery stenosis, and is rather preferred especially for patients with a history of coronary disease.1,2 Hemodynamic instability after CAS consists of hypertension, hypotension, bradycardia, and cerebral hyperperfusion syndrome (CHS). Of these complications, intracranial hemorrhage (ICH) associated with CHS has a fatal outcome though incidence is rare at 0.63 0.72%.3,4 ICH after CAS is classiﬁed into brain hemorrhage and subarachnoid hemorrhage (SAH). While brain hemorrhage accounts for more than 80% of ICH after CAS associated with CHS, SAH accounts for a small percentage of these patients.4,5 It is diﬃcult to make a diﬀerential diagnosis of SAH following CAS from CHS without ICH because SAH presents with severe headache, nausea, and vomiting but usually lacks hemiplegia, whose symptoms resemble that of CHS without ICH. Furthermore, not only the
mechanism but also the management of SAH following CAS remains unclear.5,6 Although strict control of postoperative blood pressure is proved to prevent postoperative ICH in cases of CEA, the role of strict blood pressure control is controversial in cases of CAS.4 To our best knowledge, only seven cases of SAH following CAS have been reported and the mortality rate reaches 70%.5–10 Accumulating experience about this rare syndrome will improve the understanding and the poor outcome. We report a case of SAH following CAS with good clinical outcome and review previous literature to discuss the mechanism and the management of this fatal complication.
Department of Neurosurgery, Matsue Red Cross Hospital, Japan Corresponding author: Akitake Okamura, Department of Neurosurgery, Matsue Red Cross Hospital, 200 Horomachi, Matsue-city, Shimane 690-8506, Japan. Email: [email protected]
Okamura et al.
Figure 1. Perioperative N-isopropyl-p-iodoamphetamine single-photon emission computed tomography. (a) (b) Preoperative acetazolamide-enhanced test shows poor vascular reactivity of the right hemisphere. (c) Postoperative non-enhanced test five days after CAS shows that CHS has extinguished on the right hemisphere. CAS: carotid artery stenting; CHS: cerebral hyperperfusion syndrome.
Case report A 78-year-old woman with a history of arteriosclerotic obliteration and myocardial infarction was referred to our department for intervention of asymptomatic severe stenosis of the right internal carotid artery. Cervical echo revealed 85% stenosis of North American Symptomatic Carotid Endarterectomy Trial (NASCET) with iso-echoic plaque. Computed tomography (CT) showed calciﬁcation of the anterior wall. Magnetic resonance imaging of black-blood showed high intensity of the plaque. Acetazolamideenhanced N-isopropyl-p-iodoamphetamine singlephoton emission computed tomography (SPECT) showed poor vascular reactivity of the right hemisphere (Figure 1(a), (b)).11 We performed CAS under local anesthesia. The patient had received dual antiplatelet therapy (aspirin 100 mg/day and cilostazol 200 mg/day) for arteriosclerotic obliteration and myocardial infarction. The procedure was performed under local anesthesia via a femoral artery route with a 9-F sheath (Medikit, Tokyo, Japan). A bolus infusion of 5000 IU heparin and continuous intravenous infusion of 1000 IU/h heparin were given to control activated clotting time from 250 to 300 seconds. A 9-F guiding catheter Optimo (Tokai Medical Products, Aichi, Japan) was placed into the right common carotid artery via the co-axial method using a 6-F catheter CATHEX JB2 (Gadelius Medical, Tokyo, Japan). Diagnostic study was performed and severe stenosis of the right internal carotid artery with delayed blood ﬂow was conﬁrmed (Figure 2(a)). PercuSurge GuardWire (Medtronic, Minneapolis, MN, USA) was placed into the external carotid artery. Then, PercuSurge and Optimo balloons were inﬂated and 0.014-inch Transend EX Guidewire (Boston Scientiﬁc, Natick, MA, USA) crossed the lesion. Predilation was performed with a SHIDEN PTA balloon 2.0 * 40 mm (Kaneka Medical Products, Osaka, Japan) and subsequently with a Starling PTA
balloon 3.5 mm * 40 mm (Boston Scientiﬁc, Natick, MA, USA). Blood ﬂow improved substantially (Figure 2(b)). Immediately after the dilation procedure, the patient complained of headache though wire perforation was not detected. We continued the procedure because she remained alert and no focal neurological deﬁcit was detected. Her blood pressure maintained normotension during the procedure from 100/70 to 120/80 mmHg. We attempted to insert a Protege RX 7-10 mm * 40 mm (ev3 Neurovascular, Irvine, CA, USA) but it did not cross the lesion. Accordingly, the lesion was dilated again by an Aviator Plus PTA balloon 5 * 40 mm (Cordis, Fremont, CA, USA) and a stent was placed into the lesion. Because the following angiography revealed distally shifted stent (Figure 2(c)), we planned to add another stent. We tried to insert a SMART STENT 10 * 10 mm (Cordis, Fremont, CA, USA) but it did not cross the lesion. The lesion was dilated by a Starling PTA balloon 3.5 * 40 mm and subsequently by an Aviator Plus PTA balloon 5 * 40 mm. Then, the second stent was placed appropriately. Twice postdilation for the two stents was performed by Starling PTA balloons 5.0 * 20 mm each for 30 seconds. Angiography conﬁrmed the internal carotid artery stenosis improved to 40% without dissection or thrombosis (Figure 2(d)). Immediately after the procedure, the patient complained of headache and vomited. We performed emergency non-contrast CT (NCCT) and detected SAH with leakage of contrast medium occupying the right sylvian ﬁssure (Figure 3(a), (b)). A second NCCT that was performed three hours later showed increased SAH extending to the basal cistern (Figure 3(c), (d)). A third NCCT six hours later after the CAS showed decreased SAH, which suggested the bleeding had stopped. Through the postoperative course described above, we continued strict blood pressure control but did not reverse the anticoagulant eﬀect because the patient remained alert and the SAH was not massive. Five days after the procedure, non-enhanced
Interventional Neuroradiology 21(5)
Figure 2. Intraoperative findings during CAS procedure. (a) Diagnostic study showed severe stenosis of the right carotid artery. (b) The pre-dilation improved blood flow substantially. (c) The first stent shifted distally. (d) A second stent was placed and post-dilation was performed. CAS: carotid artery stenting.
N-isopropyl-p-iodoamphetamine SPECT showed that the CHS had extinguished on the right hemisphere (Figure 1(c)), and the patient was discharged without any neurological deﬁcit. Cervical echo study showed a well-opened lumen of the stent three months later at the outpatient visit.
Discussion The incidence of CHP following CAS ranges from 1.1% to 5.0%.4,12 CHP is characterized by the symptoms of ipsilateral headaches, nausea, vomiting, focal seizures, and altered mental status usually associated with elevated blood pressure.7,13 Although the incidence of SAH following CAS associated with CHP occurs only in 0.07% of patients after CAS,4 the syndrome has a fatal outcome of 70% mortality. On the other hand, it is diﬃcult to make a diﬀerential diagnosis
of SAH following CAS without imaging studies from CHS without ICH because the syndrome presents with severe headache, nausea, and vomiting but usually lacks hemiplegia, whose symptoms resemble that of CHS without ICH. However, SAH following CAS requires prompt diﬀerential diagnosis owing to the fatal outcome. Seven reported cases of SAH following CAS, and the present case, are shown in Table 1.5–10 The ages ranged from 43 to 78 years (average 61.1 years), consisting of three women (37.5%) and ﬁve men (62.5%). All cases had high-grade stenosis and most internal carotid arteries were symptomatic stenosis (87.5%). All cases were diagnosed by NCCT within at least 24 hours after CAS procedures (mean 6.9 hours). Poor outcome of death is reported in ﬁve of eight cases (62.5%). Symptoms are headache, nausea, vomiting, and disturbance of consciousness.
Okamura et al.
Figure 3. Non-contrast CT (NCCT) showing subarachnoid hemorrhage (SAH) following CAS procedure. (a)–(d): (a), (b): SAH immediate after CAS accompanied by leakage of contrast medium occupying the right sylvian fissure. (c), (d): SAH increases and extends to the basal cistern three hours later. CAS: carotid artery stenting; NCCT: non-contrast computed tomography; SAH: subarachnoid hemorrhage.
Table 1. Reported cases of idiopathic SAH following PTA and CAS. First author
Procedure Age Sex Stenosis
(1997) PTA Schoser10 7 Al-Mubarak (2001) CAS
High L Symptomatic 90% R Symptomatic
95% L Symptomatic
High R Symptomatic
(2009) CAS (2009) CAS
99% R Symptomatic 90% R Symptomatic
95% L Symptomatic
85% R Non-symptomatic Local
CT hours) Outcome
Coma, seizure 16 Headache, nausea, 1 vomiting Disturbance of 5 consciousness Headache, nausea, 2 vomiting (not described) 0.5 Disturbance of 7 consciousness Headache, vomiting, 24 dizziness Headache, nausea, 0 vomiting
Dead Dead Dead No neurological deficit Dead No neurological deficit Dead No neurological deficit
CAS: carotid artery stenting; CT: computed tomography; F: female; L: left; M: male; PTA: percutaneous transluminal angioplasty; R: right; SAH: subarachnoid hemorrhage.
596 These non-speciﬁc symptoms made diﬀerential diagnosis so diﬃcult that two cases took time until NCCT was performed.9,10 High-grade symptomatic stenosis with the aforementioned symptoms may require immediate NCCT following a CAS procedure. The contrast medium on the right sylvian ﬁssure proves that the SAH onset occurred during the procedure. The second NCCT showing increased SAH proves that the bleeding persisted for a while after the ﬁrst NCCT. The mean onset time of SAHs following CAS ranges from 6.1 hours to 1.7 days and intraoperative bleeding is not rare shown in the presented case.4,5 While SAH accounts for a small percentage in the post-CAS course, the diagnosis tends to be late owing to nonspeciﬁc symptoms. Maintaining strict intraoperative and postoperative blood pressure control is recommended for CAS patients. The mechanism of SAH following CAS is not detected, unlike aneurysmal SAH. Although the arterial wall located in the subarachnoid space distal to the circle of Willis is considered to be a rupture point,4 an autopsy report failed to detect the cause of SAH.6 Likewise, the leakage of contrast medium occupying the right sylvian ﬁssure in the present case suggests the rupture of the arterial wall distal to the circle of Willis, but the rupture point was not detected. Reportedly, prolonged hypoperfusion dilates small arterioles to supply adequate blood ﬂow and impairs autoregulation, causing a lack of reconstruction ability.6 In this case, the elevated perfusion following CAS might disrupt the arterioles in the sylvian ﬁssure to cause SAH. This idiopathic mechanism requires diﬀerential diagnosis in patients with SAH following CAS from aneurysms, dissections, arteriovenous malformations, and dural-arteriovenous ﬁstulas. Careful examination of preoperational images and intraoperational angiography to exclude a mechanical cause of SAH is required when SAH was shown to follow CAS. Neurological monitoring and strict blood pressure control are important in the prevention and treatment of ICH following CAS associated with CHS. Although strict control of postoperative blood pressure is reported to prevent ICH after CEA, the role in CAS is controversial.4 The very prompt onset of ICH after CAS, which sometimes occurs during the procedure, may account for this phenomenon. Strict blood pressure control may need to start intraoperatively. Neurological monitoring helps to diagnose CHS during the procedure. Transcranial Doppler can increase peak velocity of the middle cerebral artery, which suggests CHS.8 The risk factors for CHS include age, long-standing hypertension, high-grade stenosis, poor collateral blood ﬂow, contralateral carotid artery occlusion, pretreatment cerebral vasoreactivity, and pretreatment asymmetry of resting cerebral blood ﬂow.14 General anesthesia and staged angioplasty are considered for the patients who have several risk factors of CHS.5,11
Interventional Neuroradiology 21(5)
Conclusion SAH following CAS associated with CHP is very rare. However, the syndrome has a fatal outcome and it is diﬃcult to make a diﬀerential diagnosis without imaging studies from CHS without ICH. Strict control of intraoperative and postoperative blood pressure may improve the outcome of SAH following CAS, though the role in preventing ICH after CAS is unclear. Funding The author(s) received no ﬁnancial support for the research, authorship, and/or publication of this article.
Declaration of conflicting interests The author(s) declared no potential conﬂicts of interest with respect to the research, authorship, and/or publication of this article.
References 1. Brott TG, Hobson 2nd, RW, Howard G, et al. Stenting versus endarterectomy for treatment of carotid-artery stenosis. N Engl J Med 2010; 363: 11–23. 2. Yadav JS, Wholey MH, Kuntz RE, et al. Protected carotid-artery stenting versus endarterectomy in high-risk patients. N Engl J Med 2004; 351: 1493–1501. 3. Kang HS, Han MH, Kwon OK, et al. Intracranial hemorrhage after carotid angioplasty: A pooled analysis. J Endovasc Ther 2007; 14: 77–85. 4. 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: 1130–1136. 5. Xu Y, Wanga Y, Feng L, et al. Treatment and outcome of intracranial hemorrhage after carotid artery stenting. A ten year single center experience. Interv Neuroradiol 2009; 15: 316–324. 6. Hartmann M, Weber R, Zoubaa S, et al. Fatal subarachnoid hemorrhage after carotid stenting. J Neuroradiol 2004; 31: 63–66. 7. Al-Mubarak N, Roubin GS, Vitek JJ, et al. Subarachnoidal hemorrhage following carotid stenting with the distal-balloon protection. Catheter Cardiovasc Interv 2001; 54: 521–523. 8. Przewlocki T, Pieniazek P, Kablak-Ziembicka A, et al. Subarachnoid hemorrhage after carotid artery stenting. J Vasc Surg 2007; 45: 1072–1075. 9. Sato K, Suzuki S, Kurata A, et al. A case of subarachnoid hemorrhage and in-stent occlusion following carotid artery stenting without post balloon dilatation accompanied by hyperperfusion. JNET 2013; 7: 259–265. 10. Schoser BG, Heesen C, Eckert B, et al. Cerebral hyperperfusion injury after percutaneous transluminal angioplasty of extracranial arteries. J Neurol 1997; 244: 101–104. 11. Yoshimura S, Kitajima H, Enomoto Y, et al. Staged angioplasty for carotid artery stenosis to prevent postoperative hyperperfusion. Neurosurgery 2009; 64(3 Suppl): ons122–ons128.
Okamura et al. 12. Meyers PM, Higashida RT, Phatouros CC, et al. Cerebral hyperperfusion syndrome after percutaneous transluminal stenting of the craniocervical arteries. Neurosurgery 2000; 47: 335–343. 13. Sundt Jr, TM, Sharbrough FW, Piepgras DG, et al. Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy: With
597 results of surgery and hemodynamics of cerebral ischemia. Mayo Clin Proc 1981; 56: 533–543. 14. Kaku Y, Yoshimura S and Kokuzawa J. Factors predictive of cerebral hyperperfusion after carotid angioplasty and stent placement. AJNR Am J Neuroradiol 2004; 25: 1403–1408.