Surgical Iatrogenic Internal Carotid Artery Injury Treated with Pipeline Embolization Device: Case Report and Review of the Literature

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1 Journal of Neuroendovascular Therapy 2017; 11: Online August 22, 2017 DOI: /jnet.cr Surgical Iatrogenic Internal Carotid Artery Injury Treated with Pipeline Embolization Device: Case Report and Review of the Literature Takamitsu Tamura, David E. Rex, Ajit S. Puri, and Ajay K. Wakhloo Objective: Case reports in regard of using Pipeline Embolization Devices (PED): endoluminal reconstruction device for treatment of iatrogenic internal carotid artery (ICA) injury is still rare. We describe a successfully treated case of surgical iatrogenic ICA injury by double overlapped PEDs placement. Case Presentation: A 79-year-old female underwent endoscopic trans-nasal aspiration for chronic sphenoid and ethmoid sinusitis. This surgery was complicated by brisk arterial bleeding developed along the right lateral wall in the sphenoid sinus. There was a concern that the bleed could related to a tear in the segment of the right ICA. Immediate angiogram showed a small pseudo-aneurysm appearance, corresponding with the injured site. The pseudoaneurysm spontaneously disappeared, however, owing to recurrence of arterial nasal bleeding of upon nasal packing removal, double overlapped PEDs were successfully placed in the right ICA /supraclinoid segment. Immediate cessation of bleeding was achieved and packing could be removed. Conclusion: The use of PED for surgical iatrogenic ICA injury appears to be a rational therapeutic alternative with preservation of the parent artery blood flow. Keywords surgical iatrogenic internal carotid artery injury, pseudo-aneurysm, parent artery preservation, flow diverter, neurosurgery Introduction Although parent artery occlusion with intracranial bypass, if needed, was generally long considered standard treatment for traumatic cerebrovascular injury (TCI), ideally the goal of therapy is to achieve complete repair with parent artery preservation. Along with recent remarkable Division of Neuroimaging and Intervention and New England Center for Stroke Research, Department of Radiology, University of Massachusetts Medical School, Worcester, MA, USA Received: May 12, 2017; Accepted: July 14, 2017 Corresponding author: Takamitsu Tamura. Division of Neuroimaging and Intervention and New England Center for Stroke Research, Department of Radiology, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA 01655, USA Takamitsu.Tamura@umassmed.edu This work is licensed under a Creative Commons Attribution-NonCommercial- NoDerivatives International License The Japanese Society for Neuroendovascular Therapy advances of neuro-interventional devices, treatment with preservation of the parent artery is now often possible. Some authors have studied using Pipeline Embolization Devices (PED; Medtronic/Covidien, Irvine CA, USA) for treatment of TCI, and acceptable safety and efficacy are suggested. However, case reports in regard of using this endoluminal reconstruction device for treatment of surgical iatrogenic internal carotid artery (ICA) injury are still rare. In this injury circumstance, because multiple factors including vascular anatomy, injury characteristics, and risk of dual-antiplatelet therapy (DAPT) appear to affect outcome, more study is needed to elucidate the full safety and effectiveness of such treatment. We describe a successfully treated case of iatrogenic ICA injury by double overlapped PED placement. Case Report History A 79-year-old female underwent endoscopic trans-nasal aspiration for chronic sphenoid and ethmoid sinusitis. 640

2 Surgical Iatrogenic Internal Carotid Ar tery Injury Treated with PED A B C D Fig. 1 Immediate CT after endoscopic sinus surgery shows a fluid collection in the sphenoid sinus and right ethmoid sinus. A surgical clip is present within the sphenoid sinus, indicating the site of bleeding adjacent to right carotid prominence. This surgery was complicated by brisk arterial bleeding developed along the right lateral wall in the sphenoid sinus. There was a concern that the bleed could related to a tear in the segment of the right ICA. Intraoperative hemostasis was attempted by surgical clip placement and packing with cottonoid (Fig. 1). Keeping nasal packing, immediate diagnostic cerebral angiogram did not reveal active contrast extravasation, and segment of the right ICA appeared intact (Fig. 2A: first). Consecutively, particle embolization of the right sphenopalatine artery was executed. However, when the nasal packing was removed, arterial nasal bleeding recurred. After 3 hours from the first angiogram, repeat cerebral angiogram after immediate nasal packing removal demonstrated a small pseudo-aneurysm ( mm) appearance, corresponding with the injured site, medial wall of right ICA (Fig. 2B: second). Achievement of cessation of nasal bleeding under cottonoid packing enhanced us to choose observation without any interventions, preventing devastating events, such as an intra-operative re-bleeding and thromboembolic event, which are specifically incidental in acute phase. On next day, in the third angiogram keeping nasal packing, the pseudo-aneurysm spontaneously disappeared (Fig. 2C: third). In the meanwhile of 6 days after surgical injury, a few times removal of nasal packing were attempted; Fig. 2 (A: first) Immediate angiogram, post-intraoperative hemostasis with cottonoid nasal packing: Contrast extravasation are not detected, and segment of the right ICA appears intact. (B: second) After 3 hours from the first angiogram: After immediate nasal packing removal. A small pseudo-aneurysm ( mm), corresponding with the injured site, medial wall of right ICA is demonstrated. (C: third) Next day: In the third angiogram, under keeping nasal packing, the pseudo-aneurysm is not showed. (D: fourth) At 7 days post-endoscopic sinus surgery: In the fourth angiogram, under keeping nasal packing, the pseudo-aneurysm is not detected. ICA: internal carotid artery however, arterial bleeding recurred without nasal packing. Then, nasal packing had been necessary for hemostasis. Therefore, at 7 days post-endoscopic sinus surgery, although angiogram which was evaluated under nasal packing did not reveal a reappearance of the pseudo-aneurysm and hemostasis was kept with nasal packing (Fig. 2D: fourth); subsequently, a repair of the anterior genu of the right ICA was carried out by placement of double overlapping PEDs in to the right ICA /supraclinoid segment. Treatment Under general anesthesia, through a left common femoral artery approach, a 6-French 90 cm Flexor Shuttle Guiding Sheath (Cook Medical, Bloomington, IN, USA) was placed in the proximal cervical right ICA. A total 3000 units of heparin was injected intravenously with activated clotting time of 183 seconds. Verapamil 10 mg was infused intra-arterially into the right ICA for procedural vasospasm prevention. Using tri-axial technique, a 115 cm Navien 058 guide catheter (Medtronic/Covidien) was navigated over an Excelsior XT-27 Flex microcatheter (Stryker Neurovascular, Fermont, CA, USA), into the petrous segment of the right ICA. The Excelsior XT-27 Flex microcatheter was 641

3 Tamura T, et al. Fig. 3 After 7 days from endoscopic sinus surgery, (A D) A repair of the anterior genu of the right ICA was carried out by placement of double overlapping PEDs in the right ICA / supraclinoid segment with in-stent angioplasty. (B) For the purpose of reinforcing and decreasing rupture risk, additional PED 5 mm 16 mm was placed overlapping the previously deployed PED 5 mm 18 mm. (C) To assure adequate wall apposition, a TransForm 4 mm 15 mm compliant balloon was inflated within deployed PEDs. (D) Post-procedural angiogram showed adequate PED positioning in the area adjacent to the sphenoid sinus surgical clips, demarcating the site of hemorrhage. ICA: internal carotid artery; PED: pipeline embolization device navigated over a Synchro inch microwire (Stryker Neurovascular), into the M1 segment of the right middle cerebral artery. Subsequently, a PED 5 mm 18 mm was placed in the right ICA, spanning from the to supraclinoid segment. To assure adequate wall apposition, a TransForm 4 mm 15 mm compliant balloon (Stryker Neurovascular) was inflated within the previously deployed PED. For the purpose of reinforcing and decreasing rupture risk, another PED 5 mm 16 mm was placed overlapping the previously deployed PED (Fig. 3B). Again, angioplasty with TransForm 4 mm 15 mm compliant balloon was conducted (Fig. 3C). No procedural complications were evident. Postprocedural angiogram showed adequate PED positioning in the area adjacent to the sphenoid sinus clips (Fig. 3D). Complete stent to wall apposition was confirmed. There was no evidence for thromboembolic complication. Immediately after this procedure, aspirin 650 mg and Plavix 300 mg were loaded for thromboembolic events prevention. Outcome and follow-up After PED placement, for four consecutive days, minimal continued bleeding from right nare was seen. Then, cessation Fig. 4 of bleeding was achieved and packing could be removed on post-ped day 6. The patient complained temporary right retro-orbital pain, which was medicated with nonsteroidal anti-inflammatory drugs (NSAID). DAPT; daily aspirin 81 mg for life-long and Plavix 75 mg for 6 months were scheduled. The patient has remained neurologic intact. The 6-month follow-up angiogram demonstrated suspected complete endothelialization of the right ICA PEDs, no stenosis, and no aneurysm-like appearance. The covered ophthalmic artery was patent and showed brisk antegrade flow (Fig. 4A). Then, Plavix was interrupted and aspirin was continued for expected life-long. The 1-year follow-up angiogram showed brisk antegrade flow of the covered ophthalmic artery, no stenosis of stented ICA, and no aneurysm-like appearance (Fig. 4B and 4C). Discussion (A) Six months and (B and C) 1-year follow-up angiogram are showing suspected complete endothelialization of the right ICA with PEDs. The ophthalmic artery is patent and showing a brisk antegrade flow. Neither stenosis of stented ICA nor aneurysm-like appearance are not detected at ICA. ICA: internal carotid artery; PED: pipeline embolization device In TCI, particularly pseudo-aneurysms, surgical neck clipping, and endovascular selective coil embolization tend to fail with intra-procedural rupture or recanalization, due to the complete defect of the vessel wall. Although parent artery occlusion with intracranial bypass, if needed, was generally long considered standard treatment for TCI, in this treatment, sacrifice of physiologic antegrade cerebral blood flow, which could result in possible ischemic attacks, is necessary. Additionally, bypasses can fail for multiple reasons. Therefore, ideally the goal of therapy in TCI is to achieve 642

4 Surgical Iatrogenic Internal Carotid Ar tery Injury Treated with PED complete repair of injured vessel wall with parent artery antegrade blood flow. Some authors have reported successfully treated pseudo-aneurysms by selective coil embolization; however, they suggest that favorable outcomes need to meet the conditions: 1) subacute phase, 2) bony confines around the aneurysm, 3) and a narrow neck, in order to prevent intra-procedural rupture and recanalization. 1,2) Flow diverters were developed for treatment of intracranial aneurysms. The aim of these endovascular devices is endoluminal reconstruction; therefore, they are placed within the parent artery and not targeted toward the aneurysm sac. Gradual thrombosis of the aneurysm is induced by altering the hemodynamics at the aneurysm/parent artery interface; for example, by changing in-flow and outflow jets. Subsequently, inflammatory response, healing, and endothelial proliferation reduce the aneurysm and repair the parent artery wall while predominantly keeping the patency of perforators and side branches. 3) For this reason, flow diverter placement for the repair of a parent artery wall accompanied by a pseudo-aneurysm, stenosis, and/or arteriovenous fistula caused from traumatic events is under consideration as an appropriate, if not improved, treatment. In the United States, from April 2011, the Food and Drug Administration approved PED for medical use for large or giant un-ruptured aneurysms in the ICA from the petrous to superior hypophyseal segments. Since that time, there are many case series and reports on the off-label using of PED for TCI. However, case reports in regard to use a flow diverter for treatment of surgical iatrogenic ICA injury are still rare. Our patient was treated in the United States. This case was discussed and approved for treatment in multidisciplinary conference, and off-label use of the PED and other available treatment options as well as the possibility of close surveillance without treatment were explained to our patient. A Pubmed search for flow diverter placement for treatment of surgical iatrogenic ICA injury revealed eight patients. 4 9) Including our case, seven trans-sphenoidal surgeries and two endoscopic sinus surgeries were involved. Angiographic findings include seven pseudo-aneurysms, one extravasation of contrast, and one carotid fistula (CCF) (Table 1). Follow-up period averaged 5.64 months (SD = 4.73, N = 7) and median value is 4 months. In eight of nine cases, angiographic result showed angiographic complete occlusions. In six patients of all nine patients, sole PED treatment was conducted and five patients showed complete lesion occlusion, and another one case demonstrated decreased flow, however, this case failed to do long follow-up (Case 8). Three of nine patients, in first treatment, failed to achieve an adequate angiographic result with covered-stent placement (Case 2) or coil embolizations (Cases 4 and 5). Therefore, additional PED placements were executed and all of them showed complete lesion occlusion in follow-up angiogram. The results are encouraging with good radiological outcomes. Owing to inadequate pressure gradient, less effectiveness of PED toward continuous bleeding circumstance, such as CCF, are concerned. Case 5 (CCF) was treated with additional PED in combination with coils and achieved a good outcome; however, effectiveness of sole PED is thought to be still suspicious and more clinical results evaluation is required. Achievement of hemostasis with, for example, intra-operative compression, and subacute phase in when imbalanced coagulation system would be improved, these conditions are thought to be required to enhance the effectiveness of sole PED treatment toward iatrogenic injured ICA. In our case, hemostasis had achieved under nasal packing, and in this packing condition, pseudo-aneurysm kept in disappeared on the first, third, and fourth angiograms. Only the second angiogram was evaluated under without nasal packing, and could show the small pseudo-aneurysm. Therefore, nasal packing might lead to intra-aneurysm thrombosis or compressive aneurysm disappearance resulted in hemostasis. In the meanwhile of 6 days after surgical injury, a few times removal of nasal packing were attempted; however, arterial bleeding recurred without nasal packing. Then, nasal packing had been necessary for hemostasis. At 7 days after endoscopic sinus surgery, keeping the condition of nasal packing and hemostasis, PED placement was conducted and good outcome was achieved. According to the review of literatures, a type 1 endoleak that was improved by balloon angioplasty was reported as the only intra-procedural technical complication (Case 4). Only one minor complication occurred as retro-orbital pain in our case (Table 2). Using a flow diverter requires procedural anticoagulation and periprocedural DAPT in regard to prevent thromboembolism, those managements in severe traumatic injury may be contraindicated due to the high risk for bleeding. In all reported cases but one (Case 2), intraoperative sufficient hemostasis was achieved by hemostatic soaked cottonoids packing. Interventional treatment was then delayed for management of DAPT with exception of Case 2, then, no hemorrhagic complication from DAPT was found. In our case, successfully double PEDs 643

5 Tamura T, et al. Table 1 Patient features, lesion characteristics, and type of intervention Authors and year Patients no. Age, Sex Amenta et al., Case ) 64, F Shakir et al., Case ) 61, F Nerva et al., Case ) 20s, N/A Case 4 60s, N/A Iancu et al., Case ) 47, F Zanaty et al., Case ) 55, M Sylvester et al., Case ) 21, M Case 8 78, F Current case Case 9 79, F Primary lesion Chronic sinusitis Clival chordoma Sellar lesion Sellar lesion Pituitary adenoma Pituitary adenoma Pituitary adenoma Surgery type sinus surgery Location Rt ICA vertical petrous Rt ICA supraclinoidal Rt ICA N/A Rt ICA Chronic sinusitis sinus surgery Rt ICA Angiographic finding Pseuso-aneurysm 2.8 mm Extravasation of contrast mm mm Interval between injury and Tx At least 7 days Flow diverter Angioplasty Heparinization Initiation of DAPT (mg) 2PED overlapped No N/A Loading Plavix 600, ASA 325 prior to PED Immediate Failed Covered stent (Type1 endoleak), Additional 1PED No N/A Loading Prasugrel 60, ASA 600 prior to PED 15 days 2PED overlapped No ACT 250 s Loading Plavix 75, ASA h prior to PED 4 days Failed coils Additional 1PED CCF, Rt ICA, SOV 5 days Failed coils Additional 1Silk mm 2 mm 5 mm mm Yes (Type 1 endoleak) ACT 250 s Loading Plavix 75, ASA h prior to PED Yes N/A Loading Plavix 150, ASA 650 prior to PED 10 days 1PED No N/A N/A 15 days 1PED No N/A N/A 20 years 3PED No N/A N/A 7 days 2PED overlapped Yes ACT = 183 s Loading Plavix 300, ASA 650 prior to PED ACT: activated clotting time; ASA: aspirin; CCF: carotid sinus fistula; DAPT: dual-antiplatelet therapy; ICA: internal carotid artery; N/A: not available; PED: pipeline embolization device; SOV: superior ophthalmic vein; : trans-sphenoidal surgery; Tx: treatment 644

6 Surgical Iatrogenic Internal Carotid Ar tery Injury Treated with PED Table 2 Results Authors and year Patients Follow-up periods Obliteration Complication Clinical outcome Amenta et al., ) Case 1 4 months Complete No Good Shakir et al., ) Case 2 1 month Complete No Good Nerva et al., ) Case 3 4 months Complete No mrs 0 Case 4 2 weeks Complete No mrs 6 (unrelated to neurologic disease) Iancu et al., ) Case 5 12 months Complete No Good Zanaty et al., ) Case 6 Immediate Complete No Good Sylvester et al., ) Case 7 6 months Complete No Good Case 8 Immediate Decreased No N/A flow Current case Case 9 12 months Complete Retro-orbital pain Good mrs: modified Rankin scale; N/A: not available placement and keeping nasal packing were thought to be enough effective in prevention of nasal bleeding recurrence; therefore, DAPT was conducted after immediate PED placement. Flow diverter placement is not expected to produce immediate occlusion of the injured vessel hemorrhage sites and needs DAPT. For these reasons, post-operatively, rupture risk likely remains, up to achievement of endothelialization of the device. In reviewed cases, including our case, five of nine cases underwent two or three PEDs placement to reinforce and decrease this rupture risk. In one case, follow-up angiography showed mild in-stent stenosis without flow limitation (Case 3). In-stent stenosis, parent artery thrombosis, perforator occlusion, and thromboembolic events should be minded in regard to placement of additional overlapped stents. In our case, for the purpose of reinforcement at vessel wall injured site and reducing re-rupture risk that are expected from increased metalsurface covered ratio, double PEDs were placed in overlapping. The slight atherosclerotic wall dilatation at horizontal segment of ICA, which was detected pre-stenting angiogram (Fig. 3A), changed to smooth wall appearance due to suspected intimal hyperplasia after PED placement (Fig. 4A and 4B). Fortunately, this intimal hyperplasia is stable, not progressive and presenting no stenosis in the follow-up angiography. As a minor complication, in our case, post-procedural temporary retro-orbital pain occurred. Therefore, there is a concern that double PEDs deployed at ICA segment may have provided the mechanical tension stress against the ophthalmic division of the trigeminal nerve, which runs adjacent to the ICA segment. Fortunately, this pain was improved with NSAID and disappeared. In treatment of iatrogenic ICA injury, several treatments are included, such as ICA sacrifice, pseud-aneurysm embolization with or without stent-assist, and endoluminal reconstruction. Sylvester et al. 9) reviewed these endovascular treatments in 105 total cases and reported a relatively high rate of neurologic complication for ICA sacrifice, 21.7%; and a major technical complication rate for pseud-aneurysm embolization with or without stent-assist, 22.2% and 31.3%, respectively. In regard to endoluminal reconstruction using covered stents was reported to have a high rate of technical complications including temporary stroke symptoms, in-stent thrombosis, and endovascular endoleak repair, 41.7%, however, they tended to resolve and led to a small percentage with major technical complications, 8.3%, including re-bleeding with ICA sacrifice and interventricular hemorrhage requiring external ventricular drain placement. However, covered stent placement has the potential risk of perforating branch and side artery occlusion with possible downstream injury. With regard to flow diverter placement, from review of the literature including our case, the results are encouraging with good radiological outcomes and only one minor complication, transient retro-orbital pain. Unfortunately, one patient died due to sepsis derived from subglottic edema requiring tracheostomy, then pneumonia, and acute respiratory distress syndrome unrelated to neurologic disease 3 months after PED placement (Case 4). Concerning with required procedural anticoagulation under inadequate hemostasis condition, balloon occlusion test of ICA was not evaluated in our case, however, under adequate lesion hemostasis, the test might be recommended for further required parent artery occlusion, against thromboembolic events. The use of flow diverters for iatrogenic ICA injury appears to be a rational therapeutic alternative with preservation of the parent artery blood flow. However, more study and long-term results are needed to fully evaluate the safety and effectiveness of such treatment. 645

7 Tamura T, et al. Disclosure Statement AKW is a consultant for Stryker Neurovascular; research grants: Philips Healthcare, Wyss Institute; speaker: Harvard Postgraduate Course, Miami Cardiovascular Institute. ASP is a consultant for Codman Neurovascular, Stryker Neurovascular, and Covidien; research grants: Stryker Neurovascular, and Covidien; speaker: Miami Cardiovascular Institute. The other two authors have no conflict of interests to be disclosure. Contributorship Statement Study design: TT, ASP, and AKW. Data acquisition: TT, ASP, and AKW. Literature research: TT and DER. Data analysis and interpretation: TT and DER. Manuscript preparation: TT and DER. Revision of manuscript for important intellectual content: TT, DER, ASP, and AKW. Approval of final version of manuscript: all authors. References 1) Lempert TE, Halbach VV, Higashida RT, et al: Endovascular treatment of pseudoaneurysms with electrolytically detachable coils. AJNR Am J Neuroradiol 1998; 19: ) Tamura T, Kishida Y, Ichikawa M, et al: Traumatic intracranial aneurysms treated by intra-aneurysmal coil embolization. JNET 2016: 10: ) Kallmes DF, Ding YH, Dai D, et al: A new endoluminal, flow-disrupting device for treatment of saccular aneurysms. Stroke 2007; 38: ) Amenta PS, Starke RM, Jabbour PM, et al: Successful treatment of a traumatic carotid pseudoaneurysm with the Pipeline stent: case report and review of the literature. Surg Neurol Int 2012; 3: ) Shakir HJ, Garson AD, Sorkin GC, et al: Combined use of covered stent and flow diversion to seal iatrogenic carotid injury with vessel preservation during transsphenoidal endoscopic resection of clival tumor. Surg Neurol Int 2014; 5: 81. 6) Nerva JD, Morton RP, Levitt MR, et al: Pipeline embolization device as primary treatment for blister aneurysms and iatrogenic pseudoaneurysms of the internal carotid artery. J Neurointerv Surg 2015; 7: ) Iancu D, Lum C, Ahmed ME, et al: Flow diversion in the treatment of carotid injury and carotid- fistula after transsphenoidal surgery. Interv Neuroradiol 2015; 21: ) Zanaty M, Chalouhi N, Jabbour P, et al: The unusual angiographic course of intracranial pseudoaneurysms. Asian J Neurosurg 2015; 10: ) Sylvester PT, Moran CJ, Derdeyn CP, et al: Endovascular management of internal carotid artery injuries secondary to endonasal surgery: case series and review of the literature. J Neurosurg 2016; 125: