Operative Technique
The Anterior Temporal Approach for Microsurgical Thromboembolectomy of an Acute Proximal Posterior Cerebral Artery Occlusion BACKGROUND: In a short window of time, intravenous and intra-arterial thrombolysis is the first treatment option for patients with an acute ischemic stroke caused by the occlusion of one of the major brain vessels. Endovascular treatment techniques provide additional treatment options. In selected cases, high revascularization rates following microsurgical thromboembolectomy in the anterior circulation were reported. A technical note on successful thromboembolectomy of the proximal posterior cerebral artery has not yet been published. OBJECTIVE: To describe the technique of microsurgical thromboembolectomy of an acute proximal posterior cerebral artery occlusion and the brainstem perforators via the anterior temporal approach. METHODS: The authors present a technical report of a successful thromboembolectomy in the proximal posterior cerebral artery. The 64-year-old male patient had an acute partial P1 thromboembolic occlusion, with contraindications for intravenous recombinant tissue plasminogen activator. The patient underwent an urgent microsurgical thromboembolectomy after a frontotemporal craniotomy. RESULTS: The postoperative computerized tomography angiography showed complete recanalization of the P1 segment and its perforators, which were previously occluded. The early outcome after 1 month and 1 year follow-ups showed improvement from modified Rankin scale 4 to modified Rankin scale 1. CONCLUSION: Microsurgical thromboembolectomy can be an effective treatment option for proximal occlusion of the posterior cerebral artery in selected cases and experienced hands. Compared with endovascular treatment, direct visual control of brainstem perforators is possible.
Felix Goehre, MD* Hiroyasu Kamiyama, MD‡ Akira Kosaka, MD‡ Toshiyuki Tsuboi, MD‡ Shiro Miyata, MD‡ Kosumo Noda, MD‡ Behnam Rezai Jahromi, MB§ Nakao Ohta, MD‡ Sadahisa Tokuda, MD‡ Juha Hernesniemi, MD, PhD§ Rokuya Tanikawa, MD‡ *Department of Neurosurgery, Stroke Center, Bergmannstrost Hospital Halle, Halle, Germany; ‡Department of Neurosurgery, Stroke Center, Sapporo Teishinkai Hospital, Sapporo, Japan; §Department of Neurosurgery, Helsinki University Central Hospital, Helsinki, Finland Correspondence: Felix Goehre, MD, Department of Neurosurgery, Stroke Center, Bergmannstrost Hospital Halle, Merseburger Straße 165, 06112 Halle, Germany. E-mail: [email protected]
KEY WORDS: Anterior temporal approach, Microsurgical technique, P1, Posterior cerebral artery, Thromboembolectomy Operative Neurosurgery 10:174–178, 2014
Received, September 9, 2013. Accepted, December 20, 2013. Published Online, December 30, 2013. Copyright © 2013 by the Congress of Neurological Surgeons.
F
or the treatment of acute ischemic stroke presenting within a 3-hour time window, the intravenous application of recombinant tissue plasminogen activator (r-tPA) is a level IA recommendation and has been included in the treatment guidelines of several countries.1-4 Occlusions of proximal intracra-
ABBREVIATIONS: ICG, indocyanine green; mRS, modified Rankin scale; P1, precommunicating segment of posterior cerebral artery; PCA, posterior cerebral artery; r-tPA, recombinant tissue plasminogen activator
174 | VOLUME 10 | NUMBER 2 | JUNE 2014
DOI: 10.1227/NEU.0000000000000284
nial vessels do not respond well to systemic intravenous thrombolysis.5 As a result, endovascular therapies for these proximal cerebral vessel occlusions have evolved over the past few years. These newer therapies include intraarterial drug-related thrombolysis, stenting, and mechanical thromboembolectomy or embolectomy.6-12 The first surgical thromboembolectomy of an intracranial vessel was reported by Welch in 1956.13 Since then, there have been several promising reports of successful microsurgical embolectomies in the anterior cerebral circulation.14-18 As a result of their deep anatomic
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
P1 EMBOLECTOMY
location, the main trunks of the vertebrobasilar system, including the posterior cerebral artery (PCA), are more difficult to approach surgically.19-22 To date, there have been no detailed reports in the literature of a successful embolectomy of the PCA. The preservation of midbrain and perforating branches to the brainstem from the P1 segment (the precommunicating segment of PCA) is critical for the revascularization of the proximal PCA.21 The objective of this technical report is to present the microsurgical technique for a thromboembolectomy of a rightsided P1 segment of the PCA under direct visual control of the perforating branches via the anterior temporal approach.
ILLUSTRATIVE CASE History and Examination A 64-year-old man became suddenly unconscious while watching television, and was immediately transferred to our hospital. On arrival he was comatose, and National Institutes of Health stroke scale score was 40. He had been taking warfarin for 5 years for atrial fibrillation, and was found to have an international normalized ratio of 2.5. The warfarin effect was slowly reversed with vitamin K. The magnetic resonance angiography reconstruction displayed a flow reduction in P1 segment (Figure 1A), the diffusion weight image indicated no pathological changes (Figure 1B), and, in axial magnetic resonance angiography, an embolus short before the P1/2 junction was visible (Figure 1C). Single photon emission computed tomography was not performed. Shortly before the patient arrived at our hospital, an endovascular procedure for another patient had begun in our angiography room; consequently, there were no immediate facilities to perform a further endovascular revascularization procedure. Therefore, the decision was made to perform a microsurgical embolectomy.
SURGICAL TECHNIQUE Positioning and Craniotomy The patient was placed in the supine position with the head rotated 30° to the left using a Mayfield clamp. The head was slightly elevated above the heart level. A fast 1-layer skin-muscle flap followed by a regular frontotemporal craniotomy was performed. Intracranial Dissection The proximal portion of the sylvian fissure was carefully dissected. The M1 portion of the right middle cerebral artery was exposed with respect to the letriculostriatal perforators. The temporal uncus was then retracted posteriorly via an anterior temporal approach. The oculomotor nerve and the posterior communicating artery were visible in the carotid-oculomotortriangle (Figure 2, Figure 3A). Indocyanine green (ICG) videoangiography was performed for the distal segments of PCA filling via posterior communicating artery. A thrombus was found to occlude the P1 segment of the PCA, where no intraluminal flow was visible inside the affected segment (Figure 3B). One dominant perforating branch of the P1 segment was filled. Arteriotomy and Embolectomy Under direct visual control, temporary microclips can be placed on the PCA for the distal and proximal occlusion of the affected P1 segment. The arteriotomy was performed in the transverse direction (Figure 3C). The thrombus material was carefully removed from the vessel lumen (Figure 3D), and the exposed P1 segment inside was irrigated. Afterward, the distal temporary clip, followed by the proximal temporary clip, was partially opened in order to wash out the remaining intraluminal thrombi through the arteriotomy. The arteriotomy was closed with 3 interrupted sutures using 10-0 microthread (Figure 3E).
FIGURE 1. A, the preoperative MRA reconstruction (reveals a flow reduction to the right proximal posterior cerebral artery (arrows). B, the preoperative diffusion-weighted image indicates no pathological changes. C, the embolus (arrow) is visible short before the right P1/2 junction in axial MRA. MRA, magnetic resonance angiography.
OPERATIVE NEUROSURGERY
VOLUME 10 | NUMBER 2 | JUNE 2014 | 175
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
GOEHRE ET AL
Postoperative Course The patient was woken just after the surgery. The postoperative computerized tomography angiography show a reconstructed PCA angioarchitecture (Figure 4). Although the diffusion weight image revealed a small high-signal area in the right thalamus, no additional ischemic lesions had appeared. The patient was discharged 1 month later after the onset prognosis with a modified Rankin scale (mRS) of 4. After 1 year of rehabilitation, he made a good recovery, improving to mRS 1.
DISCUSSION FIGURE 2. Schematic drawing of the PCoA complex showing the transverse arteriotomy for the microsurgical P1 segment thromboembolectomy. A1, anterior cerebral artery A1 segment; E, embolus occlusion; ICA, internal carotid artery; M1, middle cerebral artery; P, midbrain perforating branches; P1, posterior cerebral artery P1 segment; P2, posterior cerebral artery P2 segment; PCoA, posterior communicating artery; TC, temporary clip; arrow, transverse arteriotomy.
Intraoperative ICG Videoangiography Postembolectomy ICG videoangiography provided real-time images of the blood flow inside the recanalized P1 segment (Figure 3F). All midbrain-perforating branches were preserved. Operation Time The operation began 3.5 hours after the onset of symptoms. The right PCA was recanalized (Figure 3F, Figure 4) after 30 minutes, and the entire surgery was finished in 70 minutes.
Ischemic stroke is now a leading cause of death and disability.23,24 The development of medical imaging and physiological investigations during the last century have led to a better understanding of the pathophysiology of the underlying causal diseases.25,26 In addition, effective treatment and prevention strategies have been developed. More recently, cardiac arrhythmias and coagulopathic diseases can be effectively treated to prevent the event of a stroke.27 Acute stroke is an emergency requiring a thorough knowledge of the duration of symptoms, a short rescue time, and prompt inhospital treatment, the treatment goal being to prevent secondary and continuous brain damage.28 The required logistic for the preand in-hospital rescue management, which is necessary for the stroke management method that we have described, is the limiting factor in many regions worldwide. Various studies have demonstrated the benefits of intravenous application of r-tPA in a 3-hour window in acute stroke therapy.1-4 Subsequently, the use of systemic r-tPA, when strict suitability criteria are fulfilled, became a level IA recommendation for the
FIGURE 3. After dissecting the proximal PCA (A) an ICG videoangiography shows a distal P1 segment occlusion (B) A transverse arteriotomy is performed (C) and the embolus is removed (D) from the vessel lumen. The arteriotomy is closed with interrupted sutures (E). The second ICG videoangiography (F) demonstrates open perforators from the initial occluded distal P1 segment. ICG, indocyanine green; PCA, posterior cerebral artery.
176 | VOLUME 10 | NUMBER 2 | JUNE 2014
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
P1 EMBOLECTOMY
techniques, this approach has become a relatively safe procedure in experienced hands.36,37 The microsurgical intracranial dissection is performed through the subarachnoid space, almost without affecting the neural tissue. Intraoperative ICG videoangiography provides real-time images of blood flow and allows an immediate evaluation of recanalization.38 As a result, in our case, the thromboembolus was removed from the vessel lumen without any technical problem. In addition, the arteriotomy was closed by interrupted sutures without constringence of the vessel lumen. A complete revascularization of the affected PCA was achieved, and no perioperative complications were observed.
CONCLUSION
FIGURE 4. The postoperative computerized tomography angiography shows a reconstructed angioarchitecture of the right posterior cerebral artery (arrows).
Microsurgical thromboembolectomy is a viable treatment option for the recanalization of the proximal PCA in experienced hands. With the use of modern microsurgical techniques, a safe approach is possible. Compared with endovascular treatment, the important perforating branches can be preserved under direct visual control. A critical preoperative decision-making process is needed based on various factors such as vessel occlusion time, collateral flow, anatomic characteristics of the PCA, and microsurgical skills. Disclosure
29
treatment of acute strokes in several countries. The occlusion of larger proximal intracranial vessels does not respond well to systemic intravenous thrombolysis.5 This has led to further development of endovascular methods for these proximal cerebral vessel occlusions, including intra-arterial drug-related thrombolysis, stenting, and mechanical thromboembolectomy or embolectomy.6-12 Several reports on successful microsurgical embolectomies in the anterior cerebral circulation have been published, with the first by Welch in 1956.13 A high recanalization rate of up to 100% was reported in a few case series.17,30 Over the following years, microsurgical revascularization procedures were extensively tested in laboratory and animal trials.31,32 As a result, new revascularization techniques were established.18 The outcome was not only related to recanalization, but also to other factors such as timing of surgery, localization of the vessel occlusion, and collateral flow having a high impact.30 The following complications were reported: obstruction of the vessel, cortical, subcortical cerebral infarction, hemorrhagic transformation of infarction area, uncal herniation, and lack of symptomatic improvement.17 Open microsurgical thromboembolectomy of the upper posterior circulation is a challenging surgical procedure.33 The preservation of all midbrain and brainstem perforating branches of the P1 segment is critical for the revascularization of the proximal PCA. The surgical field has to be approached through a deep, narrowed corridor surrounded by several sensitive structures.21,22,34,35 This approach provides enough work space for fine instrument movements and microsutures without intense brain tissue retraction.36,37 Because of modern microsurgical
OPERATIVE NEUROSURGERY
The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. Adams HP Jr, Brott TG, Furlan AJ, et al. Guidelines for thrombolytic therapy for acute stroke: a supplement to the guidelines for the management of patients with acute ischemic stroke. Circulation. 1996;94(5):1167-1174. 2. Albers GW, Bates VE, Clark WM, Bell R, Verro P, Hamilton SA. Intravenous tissue-type plasminogen activator for treatment of acute stroke: the Standard Treatment with Alteplase to Reverse Stroke (STARS) study. JAMA. 2000;283(9): 1145-1150. 3. Hacke W, Donnan G, Fieschi C, et al. Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet. 2004;363(9411):768-774. 4. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and stroke rt-PA Stroke Study Group. N Engl J Med. 1995; 333(24):1581-1587. 5. Tomsick T, Brott T, Barsan W, et al. Prognostic value of the hyperdense middle cerebral artery sign and stroke scale score before ultraearly thrombolytic therapy. AJNR Am J Neuroradiol. 1996;17(1):79-85. 6. Bose A, Henkes H, Alfke K, et al. The Penumbra system: a mechanical device for the treatment of acute stroke due to thromboembolism. AJNR Am J Neuroradiol. 2008;29(7):1409-1413. 7. Broderick JP, Palesch YY, Demchuk AM, et al; for the Interventional Management of Stroke (IMS) III Investigators. Endovasculartherapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368(10):893-903. 8. Ciccone A, Valvassori L, Nichelatti M, et al; for the SYNTHESIS Expansion Investigators. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013;368(10):904-913. 9. Furlan A, Higashida R, Wechsler L, et al. Intra-arterial prourokinase for acute ischemic stroke. The PROACT II study: a randomized controlled trial. Prolyse in acute cerebral thromboembolism. JAMA. 1999;282(21):2003-2011. 10. Levy EI, Siddiqui AH, Crumlish A, et al. First food and drug administrationapproved prospective trial of primary intracranial stenting for acute stroke: SARIS (stent-assisted recanalization in acute ischemic stroke). Stroke. 2009;40(11):35523556.
VOLUME 10 | NUMBER 2 | JUNE 2014 | 177
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
GOEHRE ET AL
11. Ogawa A, Mori E, Minematsu K, et al. Randomized trial of intraarterial infusion of urokinase within 6 hours of middle cerebral artery stroke: the middle cerebral artery embolism local fibrinolytic intervention trial (MELT) Japan. Stroke. 2007; 38(10):2633-2639. 12. Smith WS, Sung G, Starkman S, et al. Safety and efficacy of mechanical embolectomy in acute ischemic stroke: results of the MERCI trial. Stroke. 2005;36 (7):1432-1438. 13. Welch K. Excision of occlusive lesions of the middle cerebral artery. J Neurosurg. 1956;13(1):73-80. 14. Inoue T, Tamura A, Tsutsumi K, Saito I, Saito N. Surgical embolectomy for large vessel occlusion of anterior circulation. Br J Neurosurg. 2013;27(6):783-790 [Epub ahead of print]. 15. Kim DW, Jang SJ, Kang SD. Emergency microsurgical embolectomy for the treatment of acute intracranial artery occlusion: report of two cases. J Clin Neurol. 2011;7(3):159-163. 16. Sekhar LN, Iwai Y, Wright DC, Bloom M. Vein graft replacement of the middle cerebral artery after unsuccessful embolectomy: case report. Neurosurgery. 1993;33 (4):723-726. 17. Touho H, Morisako T, Hashimoto Y, Karasawa J. Embolectomy for acute embolic occlusion of the internal carotid artery bifurcation. Surg Neurol. 1999; 51(3):313-320. 18. Yasargil MG. Microsurgery. Applied to Neurosurgery. Stuttgart, Germany: Georg Thieme-Verlag; 1969. 19. Lawton MT, Daspit CP, Spetzler RF. Technical aspects and recent trends in the management of large and giant midbasilar artery aneurysms. Neurosurgery. 1997; 41(3):513-521. 20. Terasaka S, Sawamura Y, Kamiyama H, Fukushima T. Surgical approaches for the treatment of aneurysms on the P2 segment of the posterior cerebral artery. Neurosurgery. 2000;47(2):359-364. 21. Yasargil MG. Microsurgery. In: Yasargil MG, ed. Clinical Considerations, Surgery of the Intracranial Aneurysms and Results. 2 Vol. Stuttgart, Germany: Georg ThiemeVerlag; 1984. 22. Yonekawa Y, Roth P, Fandino J, Landolt H. Aneurysms of the posterior cerebral artery and approach selection in their microsurgical treatment: emphasis on the approaches: SAHEA and SCTTA. Acta Neurochir Suppl. 2011;112:85-92. 23. Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics— 2012 update: a report from the American Heart Association. Circulation. 2012; 125(1):e2-e220. 24. Sarti C, Rastenyte D, Cepaitis Z, Tuomilehto J. International trends in mortality from stroke, 1968 to 1994. Stroke. 2000;31(7):1588-1601. 25. Sobay CG, Faraci FM, Heistad DD. Vascular biology ans atherosclerosis of cerebral arteries. In: Mohr JP, Choi DW, Grotta JC, Weir B, Wolf PA, eds. Stroke: Pathophysiology, Diagnosis, and Management. 4th ed. Philadelphia, PA: Churchill Livingstone; 2004:763-774. 26. Förster A, Griebe M, Gass A, Hennerici MG, Szabo K. Recent advances in magnetic resonance imaging in posterior circulation stroke: implications for diagnosis and prognosis. Curr Treat Options Cardiovasc Med. 2011;13(3):268-277. 27. Hirsh J, Warkentin TE, Raschke R, Granger C, Ohman EM, Dalen JE. Heparin and low-molecular-weight heparin: mechanisms of action, pharmacokinetics, dosing considerations, monitoring, efficacy, and safety. Chest. 1998;114(5 suppl):489-510. 28. Prabhakaran S, Ward E, John S, et al. Transfer delay is a major factor limiting the use of intra-arterial treatment in acute ischemic stroke. Stroke. 2011;42(6):1626-1630. 29. Kern R, Nagayama M, Toyoda K, Steiner T, Hennerici MG, Shinohara Y. Comparison of the European and Japanese guidelines for the management of ischemic stroke. Cerebrovasc Dis. 2013;35(5):402-418. 30. Horiuchi T, Nitta J, Sakai K, Tanaka Y, Hongo K. Emergency embolectomy for treatment of acute middle cerebral artery occlusion. J Neurosurg. 2007;106(2):257-262. 31. Carton CA, Kessler LA, Seidenberg B, Hurwitt ES. Experimental studies in surgery of small blood vessels. II. Patching of arteriotomy using a plastic adhesive. J Neurosurg. 1961;18:188-194. 32. Diaz FG, Mastri AR, Ausman JI, Chou SN. Acute cerebral revascularization after regional cerebral ischemia in the dog. Part 2: Clinicopathological correlation. J Neurosurg. 1979;51(5):644-653. 33. Morgan MK, Biggs MT. Direct embolectomy of the basilar artery bifurcation. Case report. J Neurosurg. 1992;77(3):463-465. 34. Surgery of vertebrobasilar aneurysms: London. In: Drake CG, Peerless SJ, Hernesniemi JA, eds. Ontario Experience on 1767 Patients. Wien, Austria: Springer-Verlag; 1996.
178 | VOLUME 10 | NUMBER 2 | JUNE 2014
35. Hernesniemi J, Ishii K, Niemelä M, Kivipelto L, Fujiki M, Shen H. Subtemporal approach to basilar bifurcation aneurysms: advanced technique and clinical experience. Acta Neurochir Suppl. 2005;94:31-38. 36. Katsuno M, Tanikawa R, Miyazaki T, et al. The limits of the anterior temporal approach for unruptured upper basilar artery aneurysms. No Shinkei Geka. 2013; 41(4):311-318. 37. Tanikawa R, Hada H, Ishizuki T, et al. Anterior temporal approach for basilar bifurcation aneurysms as a modified distal transsylvian approach. Surg Cereb Stroke (Jpn). 1998;26:259-264. 38. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52(1):132-139.
COMMENTS
T
his article reports the well-known technique of thromboembolectomy applied for the first time at the level of the P1 segment of the posterior cerebral artery. The use of intravenous systemic thrombolysis and the advent of endovascular drug and mechanical therapies will limit the application of such surgical techniques. Thromboembolectomy can nevertheless be extremely valuable in some selected indications. Michaël Bruneau Brussels, Belgium
T
he authors report on the first successful case of a surgical P1 segment embolectomy. The endovascular suite was not available, and, therefore, the patient was expeditiously taken to the operating room 3.5 hours after the ictus where a craniotomy and embolectomy were performed within 30 minutes. At 1-year follow-up the patient recovered from an mRS of 4 to an mRS of 1. They are to be commended on their surgical skills and speedy reestablishment of blood flow through that segment. As illustrated in this report, reestablishment of blood flow to the P1 segment perforators is vital to patient recovery. Direct surgical embolectomy is still a viable option, especially when endovascular intervention is not available. The administration of IV tPA could have been another option, now that the time window for IV tPA administration in an acute stroke has been extended from 3 to 4.5 hours. Jafar Jewad Jafar New York, New York
T
he authors have presented a case of posterior cerebral artery embolectomy, about 3 and 1/2 hours after the acute ictus. The authors and their operative team are to be commended for this. However, in most institutions, endovascular retrieval of clot can be done more quickly than surgical embolectomy. Just to set up the operation takes about 30 minutes, and another 30 to 60 minutes are needed in order to get down to the artery in question. Therefore, endovascular embolectomy is much more practical than surgical embolectomy. In rare situations, when the endovascular technique fails, surgery may be performed, if the patient is still in the window for revascularization, and major stroke has not occurred. Technically, it is quite easy to get down to the PCA P2 segment when the basilar artery bifurcation is in a normal position (not very high or very low). Also, embolic occlusion must be carefully distinguished from local atherosclerotic occlusion, the latter is not amenable to microsurgical or even endovascular reopening. Laligam N. Sekhar Seattle, Washington
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
The Anterior Temporal Approach for Microsurgical Thromboembolectomy of an Acute Proximal Posterior Cerebral Artery Occlusion BACKGROUND: In a short window of time, intravenous and intra-arterial thrombolysis is the first treatment option for patients with an acute ischemic stroke caused by the occlusion of one of the major brain vessels. Endovascular treatment techniques provide additional treatment options. In selected cases, high revascularization rates following microsurgical thromboembolectomy in the anterior circulation were reported. A technical note on successful thromboembolectomy of the proximal posterior cerebral artery has not yet been published. OBJECTIVE: To describe the technique of microsurgical thromboembolectomy of an acute proximal posterior cerebral artery occlusion and the brainstem perforators via the anterior temporal approach. METHODS: The authors present a technical report of a successful thromboembolectomy in the proximal posterior cerebral artery. The 64-year-old male patient had an acute partial P1 thromboembolic occlusion, with contraindications for intravenous recombinant tissue plasminogen activator. The patient underwent an urgent microsurgical thromboembolectomy after a frontotemporal craniotomy. RESULTS: The postoperative computerized tomography angiography showed complete recanalization of the P1 segment and its perforators, which were previously occluded. The early outcome after 1 month and 1 year follow-ups showed improvement from modified Rankin scale 4 to modified Rankin scale 1. CONCLUSION: Microsurgical thromboembolectomy can be an effective treatment option for proximal occlusion of the posterior cerebral artery in selected cases and experienced hands. Compared with endovascular treatment, direct visual control of brainstem perforators is possible.
Felix Goehre, MD* Hiroyasu Kamiyama, MD‡ Akira Kosaka, MD‡ Toshiyuki Tsuboi, MD‡ Shiro Miyata, MD‡ Kosumo Noda, MD‡ Behnam Rezai Jahromi, MB§ Nakao Ohta, MD‡ Sadahisa Tokuda, MD‡ Juha Hernesniemi, MD, PhD§ Rokuya Tanikawa, MD‡ *Department of Neurosurgery, Stroke Center, Bergmannstrost Hospital Halle, Halle, Germany; ‡Department of Neurosurgery, Stroke Center, Sapporo Teishinkai Hospital, Sapporo, Japan; §Department of Neurosurgery, Helsinki University Central Hospital, Helsinki, Finland Correspondence: Felix Goehre, MD, Department of Neurosurgery, Stroke Center, Bergmannstrost Hospital Halle, Merseburger Straße 165, 06112 Halle, Germany. E-mail: [email protected]
KEY WORDS: Anterior temporal approach, Microsurgical technique, P1, Posterior cerebral artery, Thromboembolectomy Operative Neurosurgery 10:174–178, 2014
Received, September 9, 2013. Accepted, December 20, 2013. Published Online, December 30, 2013. Copyright © 2013 by the Congress of Neurological Surgeons.
F
or the treatment of acute ischemic stroke presenting within a 3-hour time window, the intravenous application of recombinant tissue plasminogen activator (r-tPA) is a level IA recommendation and has been included in the treatment guidelines of several countries.1-4 Occlusions of proximal intracra-
ABBREVIATIONS: ICG, indocyanine green; mRS, modified Rankin scale; P1, precommunicating segment of posterior cerebral artery; PCA, posterior cerebral artery; r-tPA, recombinant tissue plasminogen activator
174 | VOLUME 10 | NUMBER 2 | JUNE 2014
DOI: 10.1227/NEU.0000000000000284
nial vessels do not respond well to systemic intravenous thrombolysis.5 As a result, endovascular therapies for these proximal cerebral vessel occlusions have evolved over the past few years. These newer therapies include intraarterial drug-related thrombolysis, stenting, and mechanical thromboembolectomy or embolectomy.6-12 The first surgical thromboembolectomy of an intracranial vessel was reported by Welch in 1956.13 Since then, there have been several promising reports of successful microsurgical embolectomies in the anterior cerebral circulation.14-18 As a result of their deep anatomic
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
P1 EMBOLECTOMY
location, the main trunks of the vertebrobasilar system, including the posterior cerebral artery (PCA), are more difficult to approach surgically.19-22 To date, there have been no detailed reports in the literature of a successful embolectomy of the PCA. The preservation of midbrain and perforating branches to the brainstem from the P1 segment (the precommunicating segment of PCA) is critical for the revascularization of the proximal PCA.21 The objective of this technical report is to present the microsurgical technique for a thromboembolectomy of a rightsided P1 segment of the PCA under direct visual control of the perforating branches via the anterior temporal approach.
ILLUSTRATIVE CASE History and Examination A 64-year-old man became suddenly unconscious while watching television, and was immediately transferred to our hospital. On arrival he was comatose, and National Institutes of Health stroke scale score was 40. He had been taking warfarin for 5 years for atrial fibrillation, and was found to have an international normalized ratio of 2.5. The warfarin effect was slowly reversed with vitamin K. The magnetic resonance angiography reconstruction displayed a flow reduction in P1 segment (Figure 1A), the diffusion weight image indicated no pathological changes (Figure 1B), and, in axial magnetic resonance angiography, an embolus short before the P1/2 junction was visible (Figure 1C). Single photon emission computed tomography was not performed. Shortly before the patient arrived at our hospital, an endovascular procedure for another patient had begun in our angiography room; consequently, there were no immediate facilities to perform a further endovascular revascularization procedure. Therefore, the decision was made to perform a microsurgical embolectomy.
SURGICAL TECHNIQUE Positioning and Craniotomy The patient was placed in the supine position with the head rotated 30° to the left using a Mayfield clamp. The head was slightly elevated above the heart level. A fast 1-layer skin-muscle flap followed by a regular frontotemporal craniotomy was performed. Intracranial Dissection The proximal portion of the sylvian fissure was carefully dissected. The M1 portion of the right middle cerebral artery was exposed with respect to the letriculostriatal perforators. The temporal uncus was then retracted posteriorly via an anterior temporal approach. The oculomotor nerve and the posterior communicating artery were visible in the carotid-oculomotortriangle (Figure 2, Figure 3A). Indocyanine green (ICG) videoangiography was performed for the distal segments of PCA filling via posterior communicating artery. A thrombus was found to occlude the P1 segment of the PCA, where no intraluminal flow was visible inside the affected segment (Figure 3B). One dominant perforating branch of the P1 segment was filled. Arteriotomy and Embolectomy Under direct visual control, temporary microclips can be placed on the PCA for the distal and proximal occlusion of the affected P1 segment. The arteriotomy was performed in the transverse direction (Figure 3C). The thrombus material was carefully removed from the vessel lumen (Figure 3D), and the exposed P1 segment inside was irrigated. Afterward, the distal temporary clip, followed by the proximal temporary clip, was partially opened in order to wash out the remaining intraluminal thrombi through the arteriotomy. The arteriotomy was closed with 3 interrupted sutures using 10-0 microthread (Figure 3E).
FIGURE 1. A, the preoperative MRA reconstruction (reveals a flow reduction to the right proximal posterior cerebral artery (arrows). B, the preoperative diffusion-weighted image indicates no pathological changes. C, the embolus (arrow) is visible short before the right P1/2 junction in axial MRA. MRA, magnetic resonance angiography.
OPERATIVE NEUROSURGERY
VOLUME 10 | NUMBER 2 | JUNE 2014 | 175
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
GOEHRE ET AL
Postoperative Course The patient was woken just after the surgery. The postoperative computerized tomography angiography show a reconstructed PCA angioarchitecture (Figure 4). Although the diffusion weight image revealed a small high-signal area in the right thalamus, no additional ischemic lesions had appeared. The patient was discharged 1 month later after the onset prognosis with a modified Rankin scale (mRS) of 4. After 1 year of rehabilitation, he made a good recovery, improving to mRS 1.
DISCUSSION FIGURE 2. Schematic drawing of the PCoA complex showing the transverse arteriotomy for the microsurgical P1 segment thromboembolectomy. A1, anterior cerebral artery A1 segment; E, embolus occlusion; ICA, internal carotid artery; M1, middle cerebral artery; P, midbrain perforating branches; P1, posterior cerebral artery P1 segment; P2, posterior cerebral artery P2 segment; PCoA, posterior communicating artery; TC, temporary clip; arrow, transverse arteriotomy.
Intraoperative ICG Videoangiography Postembolectomy ICG videoangiography provided real-time images of the blood flow inside the recanalized P1 segment (Figure 3F). All midbrain-perforating branches were preserved. Operation Time The operation began 3.5 hours after the onset of symptoms. The right PCA was recanalized (Figure 3F, Figure 4) after 30 minutes, and the entire surgery was finished in 70 minutes.
Ischemic stroke is now a leading cause of death and disability.23,24 The development of medical imaging and physiological investigations during the last century have led to a better understanding of the pathophysiology of the underlying causal diseases.25,26 In addition, effective treatment and prevention strategies have been developed. More recently, cardiac arrhythmias and coagulopathic diseases can be effectively treated to prevent the event of a stroke.27 Acute stroke is an emergency requiring a thorough knowledge of the duration of symptoms, a short rescue time, and prompt inhospital treatment, the treatment goal being to prevent secondary and continuous brain damage.28 The required logistic for the preand in-hospital rescue management, which is necessary for the stroke management method that we have described, is the limiting factor in many regions worldwide. Various studies have demonstrated the benefits of intravenous application of r-tPA in a 3-hour window in acute stroke therapy.1-4 Subsequently, the use of systemic r-tPA, when strict suitability criteria are fulfilled, became a level IA recommendation for the
FIGURE 3. After dissecting the proximal PCA (A) an ICG videoangiography shows a distal P1 segment occlusion (B) A transverse arteriotomy is performed (C) and the embolus is removed (D) from the vessel lumen. The arteriotomy is closed with interrupted sutures (E). The second ICG videoangiography (F) demonstrates open perforators from the initial occluded distal P1 segment. ICG, indocyanine green; PCA, posterior cerebral artery.
176 | VOLUME 10 | NUMBER 2 | JUNE 2014
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
P1 EMBOLECTOMY
techniques, this approach has become a relatively safe procedure in experienced hands.36,37 The microsurgical intracranial dissection is performed through the subarachnoid space, almost without affecting the neural tissue. Intraoperative ICG videoangiography provides real-time images of blood flow and allows an immediate evaluation of recanalization.38 As a result, in our case, the thromboembolus was removed from the vessel lumen without any technical problem. In addition, the arteriotomy was closed by interrupted sutures without constringence of the vessel lumen. A complete revascularization of the affected PCA was achieved, and no perioperative complications were observed.
CONCLUSION
FIGURE 4. The postoperative computerized tomography angiography shows a reconstructed angioarchitecture of the right posterior cerebral artery (arrows).
Microsurgical thromboembolectomy is a viable treatment option for the recanalization of the proximal PCA in experienced hands. With the use of modern microsurgical techniques, a safe approach is possible. Compared with endovascular treatment, the important perforating branches can be preserved under direct visual control. A critical preoperative decision-making process is needed based on various factors such as vessel occlusion time, collateral flow, anatomic characteristics of the PCA, and microsurgical skills. Disclosure
29
treatment of acute strokes in several countries. The occlusion of larger proximal intracranial vessels does not respond well to systemic intravenous thrombolysis.5 This has led to further development of endovascular methods for these proximal cerebral vessel occlusions, including intra-arterial drug-related thrombolysis, stenting, and mechanical thromboembolectomy or embolectomy.6-12 Several reports on successful microsurgical embolectomies in the anterior cerebral circulation have been published, with the first by Welch in 1956.13 A high recanalization rate of up to 100% was reported in a few case series.17,30 Over the following years, microsurgical revascularization procedures were extensively tested in laboratory and animal trials.31,32 As a result, new revascularization techniques were established.18 The outcome was not only related to recanalization, but also to other factors such as timing of surgery, localization of the vessel occlusion, and collateral flow having a high impact.30 The following complications were reported: obstruction of the vessel, cortical, subcortical cerebral infarction, hemorrhagic transformation of infarction area, uncal herniation, and lack of symptomatic improvement.17 Open microsurgical thromboembolectomy of the upper posterior circulation is a challenging surgical procedure.33 The preservation of all midbrain and brainstem perforating branches of the P1 segment is critical for the revascularization of the proximal PCA. The surgical field has to be approached through a deep, narrowed corridor surrounded by several sensitive structures.21,22,34,35 This approach provides enough work space for fine instrument movements and microsutures without intense brain tissue retraction.36,37 Because of modern microsurgical
OPERATIVE NEUROSURGERY
The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. Adams HP Jr, Brott TG, Furlan AJ, et al. Guidelines for thrombolytic therapy for acute stroke: a supplement to the guidelines for the management of patients with acute ischemic stroke. Circulation. 1996;94(5):1167-1174. 2. Albers GW, Bates VE, Clark WM, Bell R, Verro P, Hamilton SA. Intravenous tissue-type plasminogen activator for treatment of acute stroke: the Standard Treatment with Alteplase to Reverse Stroke (STARS) study. JAMA. 2000;283(9): 1145-1150. 3. Hacke W, Donnan G, Fieschi C, et al. Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet. 2004;363(9411):768-774. 4. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and stroke rt-PA Stroke Study Group. N Engl J Med. 1995; 333(24):1581-1587. 5. Tomsick T, Brott T, Barsan W, et al. Prognostic value of the hyperdense middle cerebral artery sign and stroke scale score before ultraearly thrombolytic therapy. AJNR Am J Neuroradiol. 1996;17(1):79-85. 6. Bose A, Henkes H, Alfke K, et al. The Penumbra system: a mechanical device for the treatment of acute stroke due to thromboembolism. AJNR Am J Neuroradiol. 2008;29(7):1409-1413. 7. Broderick JP, Palesch YY, Demchuk AM, et al; for the Interventional Management of Stroke (IMS) III Investigators. Endovasculartherapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368(10):893-903. 8. Ciccone A, Valvassori L, Nichelatti M, et al; for the SYNTHESIS Expansion Investigators. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013;368(10):904-913. 9. Furlan A, Higashida R, Wechsler L, et al. Intra-arterial prourokinase for acute ischemic stroke. The PROACT II study: a randomized controlled trial. Prolyse in acute cerebral thromboembolism. JAMA. 1999;282(21):2003-2011. 10. Levy EI, Siddiqui AH, Crumlish A, et al. First food and drug administrationapproved prospective trial of primary intracranial stenting for acute stroke: SARIS (stent-assisted recanalization in acute ischemic stroke). Stroke. 2009;40(11):35523556.
VOLUME 10 | NUMBER 2 | JUNE 2014 | 177
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
GOEHRE ET AL
11. Ogawa A, Mori E, Minematsu K, et al. Randomized trial of intraarterial infusion of urokinase within 6 hours of middle cerebral artery stroke: the middle cerebral artery embolism local fibrinolytic intervention trial (MELT) Japan. Stroke. 2007; 38(10):2633-2639. 12. Smith WS, Sung G, Starkman S, et al. Safety and efficacy of mechanical embolectomy in acute ischemic stroke: results of the MERCI trial. Stroke. 2005;36 (7):1432-1438. 13. Welch K. Excision of occlusive lesions of the middle cerebral artery. J Neurosurg. 1956;13(1):73-80. 14. Inoue T, Tamura A, Tsutsumi K, Saito I, Saito N. Surgical embolectomy for large vessel occlusion of anterior circulation. Br J Neurosurg. 2013;27(6):783-790 [Epub ahead of print]. 15. Kim DW, Jang SJ, Kang SD. Emergency microsurgical embolectomy for the treatment of acute intracranial artery occlusion: report of two cases. J Clin Neurol. 2011;7(3):159-163. 16. Sekhar LN, Iwai Y, Wright DC, Bloom M. Vein graft replacement of the middle cerebral artery after unsuccessful embolectomy: case report. Neurosurgery. 1993;33 (4):723-726. 17. Touho H, Morisako T, Hashimoto Y, Karasawa J. Embolectomy for acute embolic occlusion of the internal carotid artery bifurcation. Surg Neurol. 1999; 51(3):313-320. 18. Yasargil MG. Microsurgery. Applied to Neurosurgery. Stuttgart, Germany: Georg Thieme-Verlag; 1969. 19. Lawton MT, Daspit CP, Spetzler RF. Technical aspects and recent trends in the management of large and giant midbasilar artery aneurysms. Neurosurgery. 1997; 41(3):513-521. 20. Terasaka S, Sawamura Y, Kamiyama H, Fukushima T. Surgical approaches for the treatment of aneurysms on the P2 segment of the posterior cerebral artery. Neurosurgery. 2000;47(2):359-364. 21. Yasargil MG. Microsurgery. In: Yasargil MG, ed. Clinical Considerations, Surgery of the Intracranial Aneurysms and Results. 2 Vol. Stuttgart, Germany: Georg ThiemeVerlag; 1984. 22. Yonekawa Y, Roth P, Fandino J, Landolt H. Aneurysms of the posterior cerebral artery and approach selection in their microsurgical treatment: emphasis on the approaches: SAHEA and SCTTA. Acta Neurochir Suppl. 2011;112:85-92. 23. Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics— 2012 update: a report from the American Heart Association. Circulation. 2012; 125(1):e2-e220. 24. Sarti C, Rastenyte D, Cepaitis Z, Tuomilehto J. International trends in mortality from stroke, 1968 to 1994. Stroke. 2000;31(7):1588-1601. 25. Sobay CG, Faraci FM, Heistad DD. Vascular biology ans atherosclerosis of cerebral arteries. In: Mohr JP, Choi DW, Grotta JC, Weir B, Wolf PA, eds. Stroke: Pathophysiology, Diagnosis, and Management. 4th ed. Philadelphia, PA: Churchill Livingstone; 2004:763-774. 26. Förster A, Griebe M, Gass A, Hennerici MG, Szabo K. Recent advances in magnetic resonance imaging in posterior circulation stroke: implications for diagnosis and prognosis. Curr Treat Options Cardiovasc Med. 2011;13(3):268-277. 27. Hirsh J, Warkentin TE, Raschke R, Granger C, Ohman EM, Dalen JE. Heparin and low-molecular-weight heparin: mechanisms of action, pharmacokinetics, dosing considerations, monitoring, efficacy, and safety. Chest. 1998;114(5 suppl):489-510. 28. Prabhakaran S, Ward E, John S, et al. Transfer delay is a major factor limiting the use of intra-arterial treatment in acute ischemic stroke. Stroke. 2011;42(6):1626-1630. 29. Kern R, Nagayama M, Toyoda K, Steiner T, Hennerici MG, Shinohara Y. Comparison of the European and Japanese guidelines for the management of ischemic stroke. Cerebrovasc Dis. 2013;35(5):402-418. 30. Horiuchi T, Nitta J, Sakai K, Tanaka Y, Hongo K. Emergency embolectomy for treatment of acute middle cerebral artery occlusion. J Neurosurg. 2007;106(2):257-262. 31. Carton CA, Kessler LA, Seidenberg B, Hurwitt ES. Experimental studies in surgery of small blood vessels. II. Patching of arteriotomy using a plastic adhesive. J Neurosurg. 1961;18:188-194. 32. Diaz FG, Mastri AR, Ausman JI, Chou SN. Acute cerebral revascularization after regional cerebral ischemia in the dog. Part 2: Clinicopathological correlation. J Neurosurg. 1979;51(5):644-653. 33. Morgan MK, Biggs MT. Direct embolectomy of the basilar artery bifurcation. Case report. J Neurosurg. 1992;77(3):463-465. 34. Surgery of vertebrobasilar aneurysms: London. In: Drake CG, Peerless SJ, Hernesniemi JA, eds. Ontario Experience on 1767 Patients. Wien, Austria: Springer-Verlag; 1996.
178 | VOLUME 10 | NUMBER 2 | JUNE 2014
35. Hernesniemi J, Ishii K, Niemelä M, Kivipelto L, Fujiki M, Shen H. Subtemporal approach to basilar bifurcation aneurysms: advanced technique and clinical experience. Acta Neurochir Suppl. 2005;94:31-38. 36. Katsuno M, Tanikawa R, Miyazaki T, et al. The limits of the anterior temporal approach for unruptured upper basilar artery aneurysms. No Shinkei Geka. 2013; 41(4):311-318. 37. Tanikawa R, Hada H, Ishizuki T, et al. Anterior temporal approach for basilar bifurcation aneurysms as a modified distal transsylvian approach. Surg Cereb Stroke (Jpn). 1998;26:259-264. 38. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52(1):132-139.
COMMENTS
T
his article reports the well-known technique of thromboembolectomy applied for the first time at the level of the P1 segment of the posterior cerebral artery. The use of intravenous systemic thrombolysis and the advent of endovascular drug and mechanical therapies will limit the application of such surgical techniques. Thromboembolectomy can nevertheless be extremely valuable in some selected indications. Michaël Bruneau Brussels, Belgium
T
he authors report on the first successful case of a surgical P1 segment embolectomy. The endovascular suite was not available, and, therefore, the patient was expeditiously taken to the operating room 3.5 hours after the ictus where a craniotomy and embolectomy were performed within 30 minutes. At 1-year follow-up the patient recovered from an mRS of 4 to an mRS of 1. They are to be commended on their surgical skills and speedy reestablishment of blood flow through that segment. As illustrated in this report, reestablishment of blood flow to the P1 segment perforators is vital to patient recovery. Direct surgical embolectomy is still a viable option, especially when endovascular intervention is not available. The administration of IV tPA could have been another option, now that the time window for IV tPA administration in an acute stroke has been extended from 3 to 4.5 hours. Jafar Jewad Jafar New York, New York
T
he authors have presented a case of posterior cerebral artery embolectomy, about 3 and 1/2 hours after the acute ictus. The authors and their operative team are to be commended for this. However, in most institutions, endovascular retrieval of clot can be done more quickly than surgical embolectomy. Just to set up the operation takes about 30 minutes, and another 30 to 60 minutes are needed in order to get down to the artery in question. Therefore, endovascular embolectomy is much more practical than surgical embolectomy. In rare situations, when the endovascular technique fails, surgery may be performed, if the patient is still in the window for revascularization, and major stroke has not occurred. Technically, it is quite easy to get down to the PCA P2 segment when the basilar artery bifurcation is in a normal position (not very high or very low). Also, embolic occlusion must be carefully distinguished from local atherosclerotic occlusion, the latter is not amenable to microsurgical or even endovascular reopening. Laligam N. Sekhar Seattle, Washington
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
