Urgent cerebral revascularization bypass surgery for iatrogenic skull base internal carotid artery injury.

COMPLICATION

Urgent Cerebral Revascularization Bypass Surgery for Iatrogenic Skull Base Internal Carotid Artery Injury Leonardo Rangel-Castilla, MD Cameron G. McDougall, MD Robert F. Spetzler, MD Peter Nakaji, MD Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona Correspondence: Peter Nakaji, MD, c/o Neuroscience Publications, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W Thomas Rd, Phoenix, AZ 85013. E-mail: [email protected] Received, April 25, 2014. Accepted, August 4, 2014. Published Online, August 29, 2014. Copyright © 2014 by the Congress of Neurological Surgeons.

BACKGROUND: When feasible, the management of iatrogenic internal carotid artery (ICA) injury during skull base surgery is mainly endovascular. OBJECTIVE: To propose a cerebral revascularization procedure as a rescue option when endovascular treatment is not feasible. METHODS: We retrospectively reviewed all extracranial-intracranial (EC-IC) bypass procedures performed between July 2007 and January 2014. RESULTS: From 235 procedures, we identified 8 consecutive patients with iatrogenic ICA injury managed with an EC-IC bypass. Injury to the ICA occurred during an endoscopic transsphenoidal surgery (n = 3), endoscopic transfacial-transmaxillary surgery (n = 1), myringotomy (n = 1), cavernous sinus meningioma resection (n = 1), posterior communicating artery aneurysm clipping (n = 1), and cavernous ICA aneurysm coiling (n = 1). Endovascular management was considered first-line treatment but was not successful. All patients received a high-flow EC-IC bypass. At a mean clinical/radiographic follow-up of 19 months (range, 3-36 months), all patients had a modified Rankin Scale score of 0 or 1. All bypasses remained patent. CONCLUSION: Iatrogenic injury of the skull base ICA is uncommon but can lead to lethal consequences. Many injuries can be treated with endovascular techniques. However, certain cases may still require a cerebral revascularization procedure. KEY WORDS: Bypass, Cerebral revascularization, Endovascular, Extracranial-to-intracranial, Internal carotid artery injury, Skull base surgery Operative Neurosurgery 10:640–648, 2014

C

erebral revascularization via extracranialintracranial (EC-IC) bypass surgery has been described predominantly for the treatment of atherosclerotic disease, moyamoya, complex intracranial aneurysms, and skull base tumors.1-5 Cerebral revascularization procedures are complex, require adequate preparation, and therefore most of the time are done electively. There are recent reports of EC-IC low-flow bypass procedures performed in emergency

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ABBREVIATIONS: EC-IC, extracranial-intracranial; ICA, internal carotid artery; IST, in-stent thrombosis; MCA, middle cerebral artery; RAG, radial artery graft Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.neurosurgery-online.com).

640 | VOLUME 10 | NUMBER 4 | DECEMBER 2014

DOI: 10.1227/NEU.0000000000000529

situations for acute ischemic stroke secondary to atherosclerosis or acute nontraumatic dissection.2,6,7 Reports of EC-IC high-flow bypass for acute internal carotid artery (ICA) injury are scant. We describe a unique experience with cerebral revascularization surgery performed in an urgent fashion for patients with iatrogenic injury of the ICA at the skull base.

METHODS We retrospectively reviewed the records of all patients undergoing EC-IC bypass procedures performed at Barrow Neurological Institute between July 2007 and January 2014. Of the 235 procedures, we identified 8 patients who underwent urgent cerebral revascularization to treat iatrogenic injury of the ICA at the skull base. There were 5 male and 3 female patients; their mean age was 41.3 years (range, 10-65 years). Clinically significant ICA injury was defined as an injury caused by direct trauma (perforation) or luminal

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BYPASS FOR IATROGENIC ICA INJURY

thrombosis secondary to a surgical or endovascular procedure with clinical and/or radiographic evidence of bleeding, dissection, or thrombosis. The nature of the ICA injuries was direct injury with or without pseudoaneurysm formation, dissection, or occlusion. All patients were evaluated by a multidisciplinary team that included specialists in interventional neuroradiology, cerebrovascular and skull base surgery, neuroradiology, and neurointensive critical care. In every case, endovascular options failed or were believed to carry a much higher risk than surgical revascularization. All patients had very poor collateral flow and failed balloon test occlusion. All patients demonstrated rapid worsening of symptoms and/or radiographic evidence of pseudoaneurysm and symptomatic ICA stenosis progression despite medical therapy that included induced hypertension and antiplatelet therapy, if indicated (Table). All patients underwent ICA-middle cerebral artery (MCA) anastomosis with a radial artery graft (RAG) within 6 to 24 hours of the diagnosis or neurological deterioration. A high-flow bypass was elected because the entire ICA territory required revascularization; a low-flow bypass would have not accomplished the objective. All patients were evaluated by the neuroendovascular team and were found not to be good candidates for endovascular treatment. During the anastomosis procedure, systolic blood pressure was maintained .120 mm Hg. Barbiturate anesthesia and burst suppression were used. Intraoperative indocyanine green angiography was used to confirm patency of the anastomosis. (See Video, Supplemental Digital Content, http://links.lww.com/NEU/A687. A 65-year-old man presented with recurrent skull base chordoma. The patient had undergone several endoscopic skull base resections and radiation therapy as a result of multiple recurrence. The most recent magnetic resonance imaging showed aggressive recurrence of the tumor invading the skull base, ethmoid sinus, cavernous sinus, and right orbit.

He underwent a radical transfacial, transmaxillary resection of the tumor and orbital content. During the procedure, the ICA was injured. Immediate cerebral angiography showed stenosis and possible dissection of the cavernous ICA but with adequate distal flow. The next day, the patient experienced progressive left hemiparesis. Repeat cerebral angiography showed worsening of the stenosis with minimal distal flow. Endovascular therapy failed. The patient did not pass the balloon test occlusion. An urgent cerebral revascularization procedure was recommended. The patient underwent a high-flow ICA-MCA bypass with an RAG. Intraoperative indocyanine green angiography showed adequate patency of the bypass. The patient remained neurologically intact. Postoperative cerebral angiography 24-48 hours after the procedure showed adequate cerebral blood flow. The arterial graft had a focal stenosis that required balloon angioplasty. Used with permission from Barrow Neurological Institute.) After surgery, all patients were maintained on aspirin therapy at a dose of 325 mg/d. An experienced vascular neurosurgeon and 2 assistants (cerebrovascular fellow and chief resident) were involved in the procedures. The occlusion time for the bypass procedure was between 25 and 35 minutes.

RESULTS Follow-up and Outcome There were no deaths. One patient with subacute ICA in-stent stenosis developed hemiparesis after the procedure that recovered within 3 to 4 weeks. The rest of the patients never showed evidence of any perioperative stroke. There were no other complications related to the procedures. Postoperative imaging (computed tomography [CT] angiography or digital subtraction angiography

TABLE. Summary of Patients Requiring Cerebral Revascularization as a Result of Iatrogenic Internal Carotid Artery Injurya Age, Patient y/Sex

a

1

10/M

2

29/F

3

45/M

4

38/M

5

65/M

6

63/F

7

58/M

8

56/F

Initial Diagnosis Chronic otitis

Initial Procedure

Myringotomy and tube placement Pituitary Endoscopic Adenoma transsphenoidal resection Pituitary Endoscopic adenoma transsphenoidal resection Rathke cleft cyst Endoscopic transsphenoidal resection Recurrent skull Endoscopic skull base base chordoma tumor resection Cavernous sinus Microsurgical tumor meningioma resection Giant Pcomm Microsurgical aneurysm aneurysm clipping Cavernous ICA Stent-assisted coiling aneurysm

Type of Injury and Location Direct injury, petrous ICA Direct injury and pseudoaneurysm, cavernous ICA Direct injury and pseudoaneurysm, cavernous ICA Direct injury and pseudoaneurysm, cavernous ICA Direct injury and dissection, cavernous ICA Direct injury, cavernous ICA Direct injury, supraclinoid ICA In-stent thrombosis, cavernous ICA

Angiographic Findings PCF

Outcome CR (Modified Rankin Procedure Scale Score) HF bypass ICA-MCA HF bypass ICA-MCA

0

PCF

HF bypass ICA-MCA

0

Large pseudoaneurysm, PCF Rapidly progressive dissection and PCF N/A

HF bypass ICA-MCA

0

HF bypass ICA-MCA HF bypass ICA-MCA N/A HF bypass ICA-MCA Subacute stenosis and HF bypass PCF ICA-MCA

1

Large pseudoaneurysm, PCF

0

1 1 1

CR, cerebral revascularization; HF, high-flow; ICA, internal carotid artery; MCA, middle cerebral artery; PCF, poor collateral flow; PComm, posterior communicating artery.

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RANGEL-CASTILLA ET AL

[DSA]) showed adequate patency of the bypass 24 to 48 hours after the procedure and follow-up period. Cerebral perfusion study is not routinely done unless clinically indicated. The mean follow-up period was 19 months (range, 3-36 months). The modified Rankin Scale score was 0 and 1 in all patients (Table).

ILLUSTRATIVE CASES Case 1 Clinical Presentation A 10-year-old boy with a history of chronic middle ear infection underwent a myringotomy and ventilation tube placement in the right ear at another institution 7 weeks before the current admission (Table, patient 1). The myringotomy procedure was aborted owing to sudden arterial blood loss; the ear was packed off, and the patient was sent home. A second episode of acute bleeding occurred after the patient coughed, and he was taken to the emergency department. Neurological examination was within normal limits. CT angiography and DSA revealed a pseudoaneurysm of the petrous ICA. The patient failed balloon test occlusion. The patient was felt not to be a candidate for endovascular treatment because of the sharp angle of the ICA where the pseudoaneurysm was located (Figure 1). Intervention After discussion of alternatives, the patient’s family agreed for the patient to undergo a cerebral revascularization procedure. He underwent a right pterional craniotomy to expose the sylvian fissure and M2 and M3 branches. An RAG was harvested from the nondominant arm. Intracranially, the RAG was anastomosed end to side to a temporal M2-M3 branch and proximally to the right ICA (end to end). There were no intraoperative or postoperative complications. The patient remained neurologically intact. A DSA 48 hours after the procedure demonstrated excellent patency of the graft and adequate cerebral blood flow (Figure 1). The patient was discharged 3 days after surgery. At the 3-month clinical follow-up, the patient remained neurologically asymptomatic. Case 2 Clinical Presentation A 65-year-old man with history of a skull base chordoma who had undergone multiple endoscopic endonasal resections over the last 10 years as a result of tumor recurrence presented with progressive right eye blindness caused by tumor infiltration into the right orbit, sphenoid and ethmoidal sinuses, and clivus (Table, patient 5; Figure 2). Because of the aggressiveness of the tumor, the recommendation was to undergo an endoscopic endonasal radical resection of the tumor, paranasal sinuses, and clivus, with orbital exenteration. Toward the end of the resection, the endoscopic procedure was complicated with an iatrogenic cavernous ICA injury below the level of the ophthalmic artery as hard tumor was dissected off the vessel. The surgical cavity was


packed off, and the surgery was aborted. Immediate DSA demonstrated irregularity and stenosis of the cavernous ICA. Three days later, the patient experienced abrupt hemiparesis and was found to have complete occlusion of the carotid. Endovascular thrombectomy and balloon angioplasty provided partial flow restoration, although the lumen remained very irregular. Repeat DSA 24 hours later showed progression of the dissection and stenosis (Figure 2). We recommended that he undergo a cerebral revascularization procedure. Intervention The patient underwent a right pterional craniotomy to expose the sylvian fissure and M2 and M3 branches. Intracranially, the RAG was anastomosed (end to side) to a temporal M2 branch and proximally to the right ICA (end to end). The segment of the ICA with the dissection was isolated with a vascular clip proximally and the distal end was left unclipped. There were no intraoperative or postoperative complications. The patient remained neurologically intact. DSA 48 hours after the procedure demonstrated excellent patency of the graft and adequate cerebral blood flow (Figure 2). Case 3 Clinical Presentation A 56-year-old woman with a symptomatic left cavernous ICA aneurysm was treated with stent-assisted coiling (Table, patient 8). The endovascular procedure was uneventful, and the patient was discharged on aspirin and clopidogrel. A few days later, the patient had gradual onset of paresthesias and mild weakness of the right-side extremities. Neurological examination was relevant for right-side upper- and lower-extremity numbness and motor strength of 42/5. CT perfusion imaging showed hypoperfusion of the left cerebral hemisphere. Cerebral angiography showed near-complete occlusion of the left cavernous ICA (Figure 3). Endovascular thrombolysis and balloon angioplasty were performed but were not sufficient, and a stent was deployed. Her neurological condition continued to decline. Repeat cerebral angiography 24 hours after the endovascular procedure showed worsening of the stenosis and almost complete occlusion of the cavernous ICA. At this point, the recommendation was for the patient to undergo a cerebral revascularization procedure. Intervention She underwent a left pterional craniotomy to expose the sylvian fissure and MCA branches. An RAG was obtained from the nondominant arm. Intracranially, the RAG was anastomosed end to side to a temporal M2 branch and proximally to the left common carotid artery also in an end-to-side fashion. There were no intraoperative or postoperative complications. The patient continued to have mild right-side weakness after surgery. CT angiography 48 hours after the procedure demonstrated excellent patency of the graft and adequate cerebral blood flow. At the 2-year follow-up, the patient had normal strength, and the bypass remained patent (Figure 3).




FIGURE 1. A 10-year-old boy suffered an iatrogenic petrous internal carotid artery (ICA) injury during a myringotomy and ventilation tube placement procedure. The procedure was aborted because of severe arterial bleeding. The patient had multiple bleeding episodes afterward; however, he remained neurologically intact. A, computed tomography angiography showed lateral displacement of the ICA (arrow). B, lateral view of the right ICA injection demonstrating the presence of a pseudoaneurysm. C, anteroposterior view of the left ICA injection showing poor collateral circulation. The patient failed balloon test occlusion. The patient underwent a high-flow extracranial-intracranial bypass with a radial artery graft. D and E, follow-up cerebral angiography showing excellent patency of the graft and adequate cerebral perfusion. Used with permission from Barrow Neurological Institute.

Cases 4 Through 8 These 5 patients consisted of 2 women and 3 men with a mean age of 46.6 years (range, 29-63 years) with the diagnosis of pituitary adenoma in 2 patients, Rathke cleft cyst in 1 patient, cavernous sinus meningioma in 1 patient, and a giant posterior communicating artery aneurysm in 1 patient (Table, patients 2-4, 6, 7). All patients had a direct ICA injury during endoscopic or microscopic surgery. The 3 patients (Table, patients 2-4) who were undergoing endoscopic surgery had an immediate DSA demonstrating large pseudoaneurysm at the cavernous ICA that was technically challenging for endovascular treatment and poor collateral flow that prevented direct parent vessel occlusion; therefore, cerebral revascularization was recommended. The other 2 cases (Table, patients 6 and 7) had an ICA injury


during microsurgical dissection of intracranial tumor or aneurysm. The decision for cerebral revascularization was made intraoperatively and performed within the same surgical procedure. All patients underwent immediate postoperative and long-term follow-up CT angiography or DSA demonstrating adequate patency of the bypass.

DISCUSSION ICA Injury During Endonasal/Endoscopic Skull Base Surgery and Middle Ear Surgery Iatrogenic injuries to the ICA in the skull base are rare but can lead to catastrophic and potentially even lethal consequences. Because of the proximity of the cavernous ICA to the sphenoid




FIGURE 2. A 65-year-old man with recurrent skull base chordoma. The patient had undergone multiple endoscopic resections and radiation therapy. A, axial T1-weighted magnetic resonance imaging with contrast showing recurrence of the tumor invading the skull base and right orbit. The decision was made to perform a radical resection of the tumor and orbital content through a transfacial, transmaxillar endoscopic approach. Toward the end of the procedure, the internal carotid artery (ICA) was injured. B and C, immediate postoperative cerebral angiography showed stenosis and possible dissection of the cavernous ICA. At this point, the patient remained asymptomatic. Within the next 24 to 48 hours, the patient experienced progressive left hemiparesis. D and E, repeat cerebral angiography demonstrated worsening of the stenosis and a significant decrease in cerebral blood flow. At this point, the recommendation was to perform a high-flow extracranial-intracranial bypass with a radial artery graft. F through I, follow-up cerebral angiography showed adequate patency of the graft and cerebral perfusion. H and I, stenosis of the graft was treated with balloon angioplasty. The patient was kept on antiplatelet medication. Used with permission from Barrow Neurological Institute.

sinus wall and sella, the vessel is susceptible to injury during transsphenoidal procedures. Direct trauma to the carotid results in pseudoaneurysm formation and dissection. Fortunately, it is estimated to occur in just 1.1% of all cases.8-10 Anatomic variants of the sphenoid bone, tumor invasion into the cavernous sinus, tumor adhesion to the ICA, distortion of the normal anatomy, multiple transsphenoidal surgeries, and unusual tortuosities are conditions associated with increased risks.11,12 Prompt recognition and immediate treatment are essential for avoiding further complications such as pseudoaneurysm rupture and stroke.11,12 If significant bleeding occurs during or after surgery, immediate vascular imaging should be obtained. If packing was used, imaging should be repeated after the packing is removed. Pseudoaneurysms can also present in a delayed fashion (64-83 days after surgery) as


severe epistaxis. The management of ICA injury associated with transsphenoidal or endonasal endoscopic surgery is mainly endovascular stenting or balloon artery occlusion with different results.13-16 The 3 cases presented here of ICA injury during endoscopic transsphenoidal or endonasal surgery were recognized intraoperatively. All of them underwent immediate DSA showing pseudoaneurysm and/or dissection of the cavernous ICA. None of them were candidates for endovascular treatment because of complex pseudoaneurysms or their dissection/stenosis characteristics. When feasible, endovascular therapy with coils and/or stenting is always a reasonable first choice. Cerebral revascularization with an EC-IC high-flow bypass is certainly more invasive, but in these 3 cases, it was a good alternative. There were no strokes in the perioperative period with this management strategy in our series.




FIGURE 3. A 56-year-old woman with a symptomatic left cavernous internal carotid artery (ICA; A) treated endovascularly with stent-assisted coiling (B). A few days later, the patient presented to the emergency department with right progressive hemiparesis. C, computed tomography (CT) perfusion imaging showed diminished blood flow to the left hemisphere. D, cerebral angiography showed complete occlusion of the left ICA. E and F, mechanical thrombectomy and the stent-in-stent technique were attempted but not successful. The patient underwent a high-flow extracranial-intracranial bypass with a radial artery graft. Her right hemiparesis recovered within the next 3 to 4 weeks. G through I, follow-up CT angiography at 2 years demonstrated adequate patency of the graft. Used with permission from Barrow Neurological Institute.

Injury to the petrous ICA during a myringotomy procedure has been reported previously.17,18 Developmental anomalies of the temporal bone and/or ICA are sometimes associated with this complication.17-20 In normal circumstances, the ICA passes through the bony petrous ridge and is separated from the middle ear cavity by the tympanic plate. This 0.5-mm-thick plate may be disrupted secondary to trauma, invasive tumor, or cholesteatoma. The ICA may be seen through the tympanic membrane where it may be mistaken for a tumor. Embryologically, displacement of the ICA secondary to malformation of the first and second branchial arches prevents the development of the tympanic plate, resulting in congenital dehiscence of the artery.21-23 Different strategies for management for this kind of ICA injury have been reported, including direct ICA ligation through the middle ear, endovascular balloon occlusion of the ICA, or stent-assisted coiling of the pseudoaneurysm.21-26 In the current case of a 10year-old boy with iatrogenic petrous ICA injury, parent artery balloon occlusion was not an option because of the poor collateral flow. Endovascular stent placement was considered; however, the fact that the injury was located at the tight bend of the artery made stent deployment technically challenging. Therefore,


a high-flow EC-IC bypass with isolation of the diseased ICA segment was indicated. Acute/Subacute Carotid Stent Thrombosis In general, in-stent thrombosis (IST) occurs in approximately 30% of patients with intracranial stents after delivery, although many of them remain asymptomatic. Acute and subacute ISTs range from 10% to 14.6%.27,28 Platelet activation is the primary mediator in acute thrombosis.29 IST is associated with aspirin and clopidogrel resistance and occurs in approximately 17% of patient undergoing coronary stent.30 Balloon angioplasty may result in endothelial injury or exposure of atheromatous plaque material and contribute to in-stent thrombus formation. The situation is very similar for stent-assisted coiling of intracranial aneurysms. Differences in stent strut designs and potential prolapse of coil segments into the parent artery likely strongly influence the risk of thrombosis. Riedel et al28 reported IST in 8.8% of patients (3 of 34 patients) with aneurysms treated with stent-assisted coiling. Of these 3 patients with IST, 2 of them still suffered a stroke after thrombolysis.28 The management of IST includes systemic or local administration of glycoprotein




IIb/IIIa receptor antagonist with or without angioplasty.27,28,31 The stent-in-stent technique is another option in acute and chronic in-stent restenosis.32 The present case of IST occurred a few days after the endovascular procedure, probably related to aspirin or clopidogrel resistance. The patient became rapidly symptomatic, and endovascular treatment (balloon angioplasty and placement of multiple stents) was not successful. Therefore, cerebral revascularization with a high-flow EC-IC bypass was indicated. Urgent Cerebral Revascularization Cerebral revascularization is indicated in the management of complex aneurysms, skull base tumors, and intracranial stenosis, including moyamoya angiopathy.1,3-5,33 The majority of these procedures are performed electively. The experience with urgent EC-IC bypass is minimal and is focused mainly on patients with acute stroke secondary to atherosclerosis.2,6,7 Nussbaum et al7 reported a group of 13 patients with progressive, refractory symptoms with enlarging areas of infarction on diffusionweighted magnetic resonance imaging despite maximal medical therapy. All patients had radiographic evidence of petrous or supraclinoid ICA dissection and underwent superficial temporal artery–MCA bypass. In every case, the bypass prevented further stroke progression. At the 3-month follow-up, the modified Rankin Scale score was 0 to 2. This strategy and the results are similar to those in some of our patients. In a larger series, Horiuchi et al6 reported their experience with 58 consecutive patients who underwent urgent EC-IC (superficial temporal artery–MCA) bypass for symptomatic ICA or MCA occlusion caused by atherosclerosis or embolism. All patients were refractory to medical treatment. The majority of the patients underwent bypass surgery on day 0; the rest of patients, no later than day 2. Sixty-nine percent of patients showed improvement in neurological function after surgery, and 74.1% had favorable outcomes. Hwang et al2 reported 9 patients with acute stroke who either had symptom aggravation despite medical treatment or were ineligible for intra-arterial thrombolysis and underwent emergent superficial temporal artery–MCA bypass 24 hours within the aggravation of symptoms. Six of the 9 achieved good functional outcome at 3 months. We present 8 cases of iatrogenic ICA injury in which endovascular treatment failed or was thought to be unsuccessful. In these selected cases, cerebral revascularization with a high-flow EC-IC bypass served as a good alternative to prevent otherwise potentially devastating consequences. A high-flow EC-IC bypass may not be performed safely in an emergent situation at some centers. Therefore, the results here may not be generalizable.

CONCLUSION Iatrogenic injury of the skull base ICA is uncommon but can lead to lethal consequences. Many injuries can be treated with endovascular techniques. However, certain cases may still require a cerebral revascularization procedure.


Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

REFERENCES 1. Abla AA, Gandhoke G, Clark JC, et al. Surgical outcomes for moyamoya angiopathy at Barrow Neurological Institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-tomiddle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery. 2013;73(3):430-439. 2. Hwang G, Oh CW, Bang JS, et al. Superficial temporal artery to middle cerebral artery bypass in acute ischemic stroke and stroke in progress. Neurosurgery. 2011; 68(3):723-729. 3. Kalani MY, Ramey W, Albuquerque FC, et al. Revascularization and aneurysm surgery: techniques, indications and outcomes in the endovascular era. Neurosurgery. 2014;74(5):482-497. 4. Quinones-Hinojosa A, Lawton MT. In situ bypass in the management of complex intracranial aneurysms: technique application in 13 patients. Neurosurgery. 2005; 57(1 suppl):140-145. 5. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery. 2012;70(6):1442-1457. 6. Horiuchi T, Nitta J, Ishizaka S, Kanaya K, Yanagawa T, Hongo K. Emergency EC-IC bypass for symptomatic atherosclerotic ischemic stroke. Neurosurg Rev. 2013;36(4):559-564. 7. Nussbaum ES, Janjua TM, Defillo A, Lowary JL, Nussbaum LA. Emergency extracranial-intracranial bypass surgery for acute ischemic stroke. J Neurosurg. 2010;112(3):666-673. 8. Cappabianca P, Cavallo LM, Colao A, de Divitiis E. Surgical complications associated with the endoscopic endonasal transsphenoidal approach for pituitary adenomas. J Neurosurg. 2002;97(2):293-298. 9. Ciric I, Ragin A, Baumgartner C, Pierce D. Complications of transsphenoidal surgery: results of a national survey, review of the literature, and personal experience. Neurosurgery. 1997;40(2):225-236. 10. Laws ER Jr. Vascular complications of transsphenoidal surgery. Pituitary. 1999;2 (2):163-170. 11. Buerke B, Tombach B, Stoll W, Heindel W, Niederstadt T. Magnetic resonance angiography follow-up examinations to detect iatrogenic pseudoaneurysms following otorhinolaryngological surgery. J Laryngol Otol. 2007;121(7):698-701. 12. Pozzati E, Giuliani G, Poppi M, Faenza A. Blunt traumatic carotid dissection with delayed symptoms. Stroke. 1989;20(3):412-416. 13. Berker M, Hazer DB, Yücel T, et al. Complications of endoscopic surgery of the pituitary adenomas: analysis of 570 patients and review of the literature. Pituitary. 2012;15(3):288-300. 14. Gondim JA, Almeida JP, Albuquerque LA, et al. Endoscopic endonasal approach for pituitary adenoma: surgical complications in 301 patients. Pituitary. 2011;14 (2):174-183. 15. Park YS, Jung JY, Ahn JY, Kim DJ, Kim SH. Emergency endovascular stent graft and coil placement for internal carotid artery injury during transsphenoidal surgery. Surg Neurol. 2009;72(6):741-746. 16. Reich O, Ringel K, Stoeter P, Maurer J. Injury of ICA during endonasal sinus surgery and management by endovascular stent application [in German]. Laryngorhinootologie. 2009;88(5):322-326. 17. Goodman RS, Cohen NL. Aberrant internal carotid artery in the middle ear. Ann Otol Rhinol Laryngol. 1981;90(1 pt 1):67-69. 18. Reilly JJ Jr, Caparosa RJ, Latchaw RE, Sheptak PE. Aberrant carotid artery injured at myringotomy: control of hemorrhage by a balloon catheter. JAMA. 1983;249 (11):1473-1475. 19. Eryilmaz A, Dagli M, Cayonu M, Dursun E, Gocer C. An aberrant internal carotid artery in the temporal bone presenting as a middle-ear mass: a case report. J Laryngol Otol. 2008;122(9):983-985. 20. Lin YY, Wang CH, Liu SC, Chen HC. Aberrant internal carotid artery in the middle ear with dehiscent high jugular bulb. J Laryngol Otol. 2012;126(6):645647. 21. Glasscock ME III, Dickins JR, Jackson CG, Wiet RJ. Vascular anomalies of the middle ear. Laryngoscope. 1980;90(1):77-88.




22. Glasscock ME III, Seshul M, Seshul MB Sr. Bilateral aberrant internal carotid artery case presentation. Arch Otolaryngol Head Neck Surg. 1993;119 (3):335-339. 23. Saylam G, Tulgar M, Saatci I, Korkmaz H. Iatrogenic carotid artery pseudoaneurysm presenting with conductive hearing loss. Am J Otolaryngol. 2009;30(2): 141-144. 24. Henriksen SD, Kindt MW, Pedersen CB, Nepper-Rasmussen HJ. Pseudoaneurysm of a lateral internal carotid artery in the middle ear. Int J Pediatr Otorhinolaryngol. 2000;52(2):163-167. 25. Oates JW, McAuliffe W, Coates HL. Management of pseudo-aneurysm of a lateral aberrant internal carotid artery. Int J Pediatr Otorhinolaryngol. 1997;42(1):73-79. 26. Sauvaget E, Paris J, Kici S, et al. Aberrant internal carotid artery in the temporal bone: imaging findings and management. Arch Otolaryngol Head Neck Surg. 2006; 132(1):86-91. 27. Lawson MF, Fautheree GL, Waters MF, Decker DA, Mocco JD, Hoh BL. Acute intraprocedural thrombus formation during wingspan intracranial stent placement for intracranial atherosclerotic disease. Neurosurgery. 2010;67(3 suppl operative): ons166-ons170. 28. Riedel CH, Tietke M, Alfke K, Stingele R, Jansen O. Subacute stent thrombosis in intracranial stenting. Stroke. 2009;40(4):1310-1314. 29. Jeong MH, Owen WG, Staab ME, et al. Porcine model of stent thrombosis: platelets are the primary component of acute stent closure. Cathet Cardiovasc Diagn. 1996;38(1):38-43. 30. Grossmann R, Sokolova O, Schnurr A, et al. Variable extent of clopidogrel responsiveness in patients after coronary stenting. Thromb Haemost. 2004;92(6): 1201-1206. 31. Levy EI, Turk AS, Albuquerque FC, et al. Wingspan in-stent restenosis and thrombosis: incidence, clinical presentation, and management. Neurosurgery. 2007;61(3):644-650. 32. Lee SJ, Shin HS, Lee SH, Koh JS. Coincidental occurrence of acute in-stent thrombosis and iatrogenic vessel perforation during a Wingspan stent placement: management with a stent in-stent technique. Neurointervention. 2012;7(1):40-44. 33. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decision-making using intraoperative blood flow measurements. Acta Neurochir (Wien). 2010;152(6):1021-1032.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.neurosurgery-online.com).

COMMENTS

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his article describes a series of 8 patients who sustained iatrogenic internal carotid artery injuries near the skull base. These patients were subsequently treated with urgent (within 24 hours) high -low bypass with a radial artery interposition graft from the internal carotid artery to the middle cerebral artery. The vessel injuries included dissections, pseudoaneurysm formation, and thrombosis that led to bleeding, high-grade stenosis, or thrombosis. Each patient was considered to be a poor candidate for endovascular treatment and failed balloon test occlusion. Furthermore, each patient showed severe flow limitation and poor collateral circulation. Revascularization was performed in each case within 24 hours of initial injury. Most of the patients recovered without incident, although 1 patient with an in-stent stenosis developed a transient hemiparesis. It is unclear whether any patient sustained a true stroke based on imaging, but follow-up vascular imaging demonstrated graft patency in all patients at an average of 19 months, and all patients experienced a good outcome as judged by modified Rankin Scale score. Revascularization procedures are both technically demanding and risky and ordinarily are not ideally suited to urgent surgery. This study demonstrates the feasibility of complex revascularization in the acute setting. Iatrogenic injury to the internal carotid artery carries the potential for


devastating neurological deficits and therefore should be investigated and treated with vigilance. Typically, the decision to perform a cerebral bypass integrates not only the patient’s clinical status and vascular anatomy but also some assessment of their cerebral perfusion. Perhaps a weakness of this article is that cerebral perfusion testing was not used to characterize preoperative ischemia or postoperative response to bypass. Although none of the patients tolerated temporary balloon occlusion, it is not clear if they would have tolerated stenosis alone or stenosis with a low-flow bypass. Perfusion testing can be helpful to sort this out and to select the best revascularization technique. It is interesting that the patient in case 2 developed a complete occlusion caused by thrombosis of the internal carotid artery. Although the vessel was subsequently reopened with endovascular balloon angioplasty and thrombectomy, the vessel showed progressive stenosis. The authors state that all patients failed balloon occlusion testing, yet this patient seemed to tolerate complete occlusion before intervention. I am not convinced that this patient would not have tolerated carotid sacrifice or perhaps a low-flow bypass with a superficial temporal artery–to–middle cerebral artery bypass. Because cerebral perfusion studies were not performed, the true nature of each patient’s ischemic deficit before surgery cannot be determined, nor can the contribution of revascularization to their ultimate perfusion be assessed. The traditional axiom that loss of a large vessel demands a high-flow bypass may not apply in all cases. An superficial temporal artery–to– middle cerebral artery bypass may be sufficient in select cases (with stenosis) and may have several distinct advantages, including a shorter temporary occlusion time, a single anastomosis, a shorter graft, superficial access, and less tortuosity. These are all features that have been shown to contribute to long-term graft survival. The authors proxy the literature on emergency revascularization for evolving stroke as an indication for urgent bypass surgery in their cohort. These patients, however, typically show progressive symptoms resulting from an acute evolving stroke in the context of atherosclerotic disease. They usually have multiple medical comorbidities that would increase the risk of surgery such as hypertension, obesity, and diabetes mellitus. I am not certain that the present study reflects this type of patient, and therefore, I am not sure that the acute stroke bypass literature applies. The authors are to be commended for their technical skill. None of their patients suffered complications as a result of surgery, and all grafts remained patent at follow-up (range, 3-36 months). They report a temporary occlusion time of 25 to 35 minutes, which is truly impressive for 2 arterial anastamoses. My personal belief is that there is an important role for revascularization surgery in contemporary vascular neurosurgery. Despite the unclear and controversial literature on the subject, we have all seen patients who clearly benefit from this treatment. Refined clinical judgment and technical skill are essential to an optimal outcome; therefore, this is not a therapy that should be performed outside of highly specialized centers. The indications for this treatment continue to evolve, and this article is a meaningful contribution to the knowledge base on the subject. Joel D. MacDonald Salt Lake City, Utah

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his report presents a series of challenging vascular complications managed with remarkable outcomes. I found it interesting that half of the 8 patients with iatrogenic internal carotid artery injury experienced their injury as a result of an endoscopic procedure. With the growing interest in these less invasive approaches, we may expect to be




faced with this situation more commonly. Although the management of complex vascular neurosurgical conditions is becoming regionalized to high-volume centers and these conditions are managed by teams of interdisciplinary experts, this type of injury may occur in centers where the expertise for complex cerebral revascularization may not exist. Furthermore, the more commonly used endovascular approaches to address iatrogenic carotid injury may also be unavailable in many centers performing procedures that may be associated with these complications. The patients in this series underwent their revasculari-


zation procedures within 6 to 24 hours of the diagnosis or neurological deterioration. This underscores the importance of rapid transfer to a center with endovascular and advanced microsurgical capabilities in the event of such a complication. This article also illustrates the importance of training our next generation of neurosurgeons in complex microsurgical skills. Daniel L. Barrow Atlanta, Georgia



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A Perfusion-based Human Cadaveric Model for Management of Carotid Artery Injury during Endoscopic Endonasal Skull Base Surgery.

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Bypass surgery for complex middle cerebral artery aneurysms: an algorithmic approach to revascularization.

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STA-MCA bypass surgery for internal carotid artery occlusion--comparative follow-up study.

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Using PTFE covered stent-artery anastomosis in a new hybrid operation for giant juxta-skull internal carotid aneurysm with tortuous internal carotid artery.

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Bilateral dissecting aneurysms of the internal carotid arteries misdiagnosed as skull base tumors: A case report.

The ocular aspects of carotid artery bypass surgery.

Skull base surgery: Indian perspective.