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An Intraoperative Look at Failure of Flow Diversion: When Additional or Alternative Treatments Should Be Considered
Case Report
An Intraoperative Look at Failure of Flow Diversion: When Additional or Alternative Treatments Should Be Considered Loyola V. Gressot1, Akash J. Patel1, Visish M. Srinivasan1, Adam Arthur2, Peter Kan1, Edward A.M. Duckworth1,2
Key words Aneurysm - Endovascular - Flow diverter - Microsurgery - Pipeline embolization device -
Abbreviations and Acronyms ACoA: Anterior communicating artery ICA: Internal carotid artery PCoA: Posterior communicating artery PED: Pipeline embolization device From the 1Department of Neurosurgery, Baylor College of Medicine, Houston, Texas; and 2SemmeseMurphey Neurologic and Spine Institute, Department of Neurosurgery, University of Tennessee, Memphis, Tennessee, USA To whom correspondence should be addressed: Edward A.M. Duckworth, M.D., M.S. [E-mail: [email protected]] Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.06.131 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
INTRODUCTION The best treatment for many internal carotid artery (ICA) aneurysms remains a debated topic. Available treatment options can be divided into microsurgical or endovascular therapies, including clip-reconstruction, trapping/ bypass, coil embolization with or without a stent, and more recently, flow diversion. Globally and nationally, treatment has shifted toward endovascular therapies, but such therapies are challenged by large, wide-necked, or fusiform-shaped aneurysms. Simple coil embolization for aneurysms with these characteristics has been reported to have a high rate of recurrence.1 In 2011, the U.S. Food and Drug Administration approved use of the Pipeline embolization device (PED) (ev3, Irvine, California, USA) for large or giant, wide-necked intracranial aneurysms of the petrous to ophthalmic segments of the ICA, up to the origin of the superior
- BACKGROUND:
The pipeline embolization device (PED) is a flow-diverting stent that provides an additional treatment modality in the management of intracranial aneurysms. An aneurysm treated with a flow diverter is expected to involute over time, contrary to the immediate obliteration expected by surgical clipping or coiling. Yet, which aneurysms will respond to PED therapy and the time frame to expect full obliteration remain unclear.
- CASE
DESCRIPTION: We report the unusual case of a 50-year-old woman with multiple (4 total) intracranial aneurysms who underwent multimodality treatment. Two aneurysms were treated with PEDs. Nine months later, the patient underwent a craniotomy for treatment of an additional aneurysm; at the time of surgery, one of the PED-treated aneurysms was noted to be clearly obliterated, and the other was visualized to be filling. The ophthalmic artery arose from the persistently filling aneurysm. The aneurysm was treated by clip ligation without incident.
- CONCLUSIONS:
The rate of PED aneurysm obliteration increases with longer follow-up; however, the time frame for observing a persistently filling aneurysm before additional treatment is considered remains unknown. Some aneurysms may never close even after discontinuation of dual antiplatelet therapy. Ophthalmic artery aneurysms have been noted to fail treatment with PED based on the anatomic relationship of the aneurysm to the ophthalmic artery. This case provokes us to consider factors that may affect the latency to aneurysm obliteration, including aneurysm size, aneurysm morphology, patient gender, failure of previous aneurysm treatment, and duration of time from initial endovascular treatment.
hypophyseal artery (Premarket Approval Number P100018). The PED is a flexible, metallic stentlike construct with fundamentally novel design features: a 48-strand braided design and a degree of metal coverage 3e5 times higher than previous intracranial stents, designed to allow for reconstruction of the parent vessel by reducing or eliminating flow to the aneurysm and to maintain flow to jailed, perforating, or side branches. It is the first device designed to affect a long sought after goal in cerebral aneurysm treatment: endoluminal reconstruction. Several studies have reported successful aneurysm obliteration of lesions in both the anterior and posterior circulation using the PED.2-9 Yet, early enthusiasm has been tempered by
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reports of complications, including incomplete obliteration, aneurysm rupture, thromboembolic phenomena, and anatomically remote intraparenchymal hemorrhages.10,11 We report the case of a 50-year-old woman with multiple intracranial aneurysms treated with different modalities, including bilateral placement of PEDs, one of which had persistent patency that required a secondary clip ligation procedure. This case shows, in a single patient, several of the existing issues and outstanding questions that are associated with flow diversion; unique intraoperative photographs of the arterial changes seen after placement of a flow-diverting stent are included.
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CASE REPORT LOYOLA V. GRESSOT ET AL.
CASE DESCRIPTION A 50-year-old woman with a history of hypothyroidism and hyperlipidemia presented with recurrent headaches. She had no neurologic deficit on initial evaluation and did not have a subarachnoid hemorrhage. An angiogram showed 4 aneurysms: a 4.1-mm wide-necked, right ophthalmic segment aneurysm, a 5.7-mm anterior communicating artery (ACoA) aneurysm, a 2.3-mm left posterior communicating artery (PCoA) aneurysm, and a 2.6-mm left carotid terminus aneurysm (Figure 1A, B). The patient was previously treated by another physician with stent-assisted coiling of the ACoA aneurysm using a 4.5-mm 20-mm Neuroform stent, and placement of a 4-mm 14-mm PED across the left PCoA aneurysm. One month later, she had a 3.75-mm 14-mm PED placed across the right ophthalmic segment aneurysm, which was complicated by a retroperitoneal hematoma and managed conservatively. A follow-up angiogram 7 months after completion of endovascular therapy showed that both ACoA and the left PCoA aneurysms were obliterated. The left carotid terminus aneurysm, which was untreated, was determined to be unchanged. However, the right ophthalmic segment aneurysm, with the ophthalmic artery arising from the aneurysm, had decreased but persistent filling (Figure 2).
INTRAOPERATIVE LOOK AT FAILURE OF FLOW DIVERSION
The patient was taken to the operating room for surgical clipping of the 2 remaining aneurysms, 9 months after the last of the endovascular therapies. A left minipterional craniotomy was performed to expose the left carotid terminus aneurysm, which was noted to be thin walled (Figure 3A), and the aneurysm was clipped successfully with patency of the parent arteries shown by indocyanine green videoangiography. The craniotomy exposure provided an advantageous visual of the PED-treated ICA, which showed that the vessel had a devitalized appearance, and the distal tines of the PED were visibly protruding through the adventitia of the artery with an obvious transition from healthy-appearing artery to diseased artery at the margin of the PED (Figure 3B). The previously treated left PCoA aneurysm was found to be completely obliterated and shrivelled (Figure 3C). Attention then turned to the medially projecting right ophthalmic segment aneurysm, which was optimally visualized from the left pterional craniotomy. The PED was noted to be spanning the neck of the aneurysm, but it did not divert flow away from the aneurysm, which continued to fill (Figure 3D). The neck of the aneurysm was noted to be close to the ophthalmic artery. The aneurysm was successfully clipped with a 5-mm straight miniclip. Intraoperative indocyanine green
Figure 2. Three-dimensional reconstruction of angiogram showing the ophthalmic artery arising from persistently filling ophthalmic segment aneurysm.
angiography confirmed patency of the afferent and efferent vessels and obliteration of the aneurysm. Postoperatively, the patient remained neurologically intact. She was admitted to the intensive care unit and transferred to the floor on postoperative day 1. A completion angiogram showed obliteration of both clipped aneurysms and no untoward findings (Figure 4A, B). The patient was discharged home on postoperative day 4 in good condition. The patient did well clinically, reporting no new problems during long-term outpatient follow-up. DISCUSSION
Figure 1. Digital subtraction angiography anteroposterior view of (A) right and (B) left internal carotid injections showing anterior communicating, right ophthalmic segment, left posterior communicating, and left carotid terminus aneurysms.
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Flow diversion has emerged as an important treatment for a variety of intracranial aneurysms. Although Food and Drug Administrationeapproved for large and giant wide-necked aneurysms of the cavernous and proximal supraclinoid ICA, flow diverters are also being used off label to treat aneurysms of various sizes and in various anatomic locations.12,13 Many large studies have been published evaluating the use of the PED for the treatment of intracranial aneurysms, but several questions remain as experience increases and applications expand. What are the risk factors for failure of PED therapy? Are coils necessary, in larger or symptomatic aneurysms, to prevent the rare but devastating complication of induced aneurysmal rupture? What is the risk of jailing larger branch arteries with
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CASE REPORT LOYOLA V. GRESSOT ET AL.
INTRAOPERATIVE LOOK AT FAILURE OF FLOW DIVERSION
Figure 3. Intraoperative photograph of left minipterional craniotomy showing (A) left ophthalmic segment aneurysm with weak, thin wall (arrow), (B) right internal carotid with previously deployed Pipeline embolization device with irregular appearing walls and visible tines and obvious transition (arrow) to
PED? When does one consider a persistently filling aneurysm to have failed PED treatment? What is the timeline for considering retreatment? Predicting the latency to complete aneurysm obliteration after PED treatment for different aneurysms is difficult. In our patient, the PCoA aneurysm (the smallest) was angiographically confirmed to be obliterated 8 months after placement of the PED. However, the ophthalmic segment aneurysm remained patent at 7 months and was directly visualized intraoperatively at 9 months after PED placement. Failure of PED in Ophthalmic Segment Aneurysms Many investigators have commented on the unique physiology of the ophthalmic artery and PED treatment of ophthalmic segment aneurysms, noting that the
healthy-appearing vessel at the end of Pipeline embolization device, (C) obliterated left posterior communicating artery aneurysm (arrow), and (D) persistently filling of right ophthalmic segment aneurysm with pipeline stent visible across neck (arrow).
ophthalmic segment aneurysms can be successfully obliterated with PED therapy, maintaining patency of the ophthalmic artery.14-17 Even when the aneurysm occludes, it is frequently asymptomatic.18 However, we hypothesize that the involvement of the origin of the ophthalmic artery in our case was the cause of the PED therapy failure (Figure 2). The PED functions by slowing and enlarging aneurysm inflow, with compensatory reduction in outflow, which leads to stasis within the aneurysm and thrombosis.19 It is believed that the endothelium grows across the porous stent and occludes the aneurysm.20 The inclusion of the ophthalmic artery in this aneurysm likely acted as a sump, drawing away blood flow and preventing this stasis, unlike the contralateral aneurysm on the PCoA, which did not
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incorporate a branch artery and responded well to PED therapy. Furthermore, another patient in our series has a similar ophthalmic segment aneurysm that also incorporates the ophthalmic artery, and it continues to show persistent filling 2.5 years after PED placement. Griessenhauer et al.21 noted that the close association of the ophthalmic artery with the aneurysm neck may be a significant risk factor for PED failure. Such end-vessel arteries have been associated with PED treatment failure for other locations as well.22 Variable Response to PED Treatment in a Single Patient Few reports exist regarding multiple aneurysms showing different responses to PED treatment in an individual patient. Kuzmik et al.23 documented 2 patients
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CASE REPORT LOYOLA V. GRESSOT ET AL.
INTRAOPERATIVE LOOK AT FAILURE OF FLOW DIVERSION
Figure 4. Digital subtraction angiography anteroposterior view of (A) right and (B) left internal carotid injections showing successful obliteration of all aneurysms.
with large, paraclinoid aneurysms, each treated with a SILK flow diverter device (Balt, Montmorency, France). One patient had complete obliteration of the aneurysm, while the other had a subarachnoid hemorrhage with partial recanalization of the aneurysm neck 1 week after the procedure. Lin et al.4 reported a case of a patient with a 5-mm cavernous sinus aneurysm and an ipsilateral 5-mm ophthalmic aneurysm simultaneously treated with PEDs. There was complete occlusion of the ophthalmic aneurysm, but residual filling of the cavernous sinus aneurysm. Moon et al.17 reported a patient with 2 ipsilateral, tandem, saccular ophthalmic segment aneurysms, each treated with PEDs. At 6-month follow-up, the distal lesion was completely obliterated, whereas the proximal lesion had a small residual. Risk Factors for PED Treatment Failure Many investigators have proposed ideas about the risk factors for failure of PED therapy, because occlusion rates reported in the literature range from 66% to 90.9%.3,4,10,17,20,23 Shapiro et al.24 reported on 100 patients with anterior circulation aneurysms treated with PED. Independent risk factors for failure were fusiform morphology, decreasing dome/neck ratio, and the presence of a preexisting lasercut stent. Jabbour et al.20 also identified
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shorter angiographic follow-up as a risk factor in their series of 109 patients with 120 aneurysms. O’Kelly et al.17 reported a series of 94 successfully deployed PEDs in unruptured aneurysms. Being female and having had previous aneurysm treatment were found to be predictors of persistent aneurysm filling on multivariate analysis. In reviewing the literature, the longer the follow-up, the higher the percentage of PED-treated aneurysms that are obliterated. However, some aneurysms obliterate faster than others, whereas others seem to not obliterate altogether. The factors that drive the different rates of involution remain poorly understood. Defining Treatment Failure and Timing of Retreatment Moreover, the question remains of how much time should be allowed for obliteration before considering the PED treatment as a failure. Most of the published series show that most aneurysms are obliterated after 6e10 months. Multiple series9,20 have shown that the rate of aneurysm obliteration increases with time from treatment; however, this must be weighed against the risk of an unsecured aneurysm. Several investigators have described the risk of delayed rupture after PED deployment, ranging from 1 week to 8 months after the procedure.9,25-27 Although the overall rate of delayed
postprocedure hemorrhage is low, and more likely in giant aneurysms, the risk remains present until the aneurysm is obliterated, and for a short time thereafter. There is no consensus regarding when to consider additional treatment of persistently filling aneurysms after PED placement. Fischer et al.3 reported a retreatment rate of 9% with a second PED as a result of a persistently filling aneurysm but did not state how and when this decision was made. Treatment with PED precludes secondary intrasaccular options, leaving 2 options: deployment of another flow diverter or surgery. In our case, surgery was required to secure the previously treated right ophthalmic segment aneurysm that was not amenable to endovascular therapy and was intraoperatively visualized to have persistent filling; it was successfully clipped. The patient described in this case had multiple (4) small aneurysms, all under 7 mm, and could have been managed conservatively. Multiple studies have shown that small aneurysm size is associated with low rates of rupture, although a PCoA aneurysm carries a higher rupture risk.28-31 Our patient was relatively young, and otherwise in good health, placing her at a higher lifetime risk of rupture.30 Females are also more likely than males to experience aneurysm rupture.30 Given this patient’s recurrent headaches, the possibility of a sentinel hemorrhage could not be excluded. The other treatment option would have been surgical clipping of all 4 aneurysms in a single craniotomy. This option would have eliminated the additional morbidity and risk of multiple procedures and use of dual antiplatelet medication. Treating multiple aneurysms through the same craniotomy in a single procedure does not summate risks in the same way as treating multiple aneurysms in repeated endovascular procedures. Because one of the aneurysms was unsuitable for endovascular therapy from the beginning, microsurgical exploration and clipping would have been a good alternative. The question then becomes, when should additional treatment be considered? If there is another reason for microsurgery, and an aneurysm previously treated with PED is still filling and safely
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CASE REPORT LOYOLA V. GRESSOT ET AL.
accessible (as in our case), there is not much of dilemma; it should be clipped. On the other hand, if a PED-treated aneurysm is radiographically followed, and shows signs of progressive involution, it seems sensible to stay the course. The decision-making challenge comes in cases that do not fall clearly into either of these categories. For those that are not responding as expected, initially discontinuing antiplatelet medications may accelerate thrombosis and involution. Additional PED placement may be considered if there is no change after discontinuation of antiplatelet medication. In some cases, branch artery morphology or other anatomic considerations may preclude aneurysm thrombosis, even with additional time, medication modification, or additional PED placement. In these cases, it is unclear whether the natural history has been significantly altered so that the aneurysm can be safely observed, or whether other treatments, namely surgery (because the aneurysm has failed endovascular therapy), should be considered.
CONCLUSIONS We report the unusual case of a patient treated with bilateral PED placement, resulting in successful obliteration of one aneurysm yet persistent filling of the other. The involvement of the ophthalmic artery with the aneurysm neck likely created a sump phenomenon in our case, preventing involution. A review of the literature showed a lack of consensus regarding which aneurysms are expected to respond to or fail PED therapy and alternative treatment options after PED failure. Despite the burgeoning development of flow diversion for endovascular therapy, microsurgery remains a reasonable alternative treatment to PED treatment and an attractive secondary treatment for certain cases of PED treatment failure. ACKNOWLEDGMENTS Author contributions to the study and manuscript preparation include the following: conception and design: A.A., P.K., E.A.M.D.; acquisition of data: L.V.G., A.J.P.; analysis and interpretation of data: L.V.G., A.J.P., V.M.S.; drafting the
INTRAOPERATIVE LOOK AT FAILURE OF FLOW DIVERSION
article, critically revising the article, and reviewing submitted version of manuscript: all authors; approving the final version of the manuscript on behalf of all authors: L.V.G.; study supervision: E.A.M.D. REFERENCES 1. Piotin M, Blanc R, Spelle L, Mounayer C, Piantino R, Schmidt PJ, et al. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke. 41, 2010, 110e115. 2. Fiorella D, Kelly ME, Albuquerque FC, Nelson PK. Curative reconstruction of a giant midbasilar trunk aneurysm with the pipeline embolization device. Neurosurgery. 2009;64:212-217 [discussion: 217]. 3. Fischer S, Vajda Z, Aguilar Perez M, Schmid E, Hopf N, Bazner H, et al. Pipeline embolization device (PED) for neurovascular reconstruction: initial experience in the treatment of 101 intracranial aneurysms and dissections. Neuroradiology. 2012;54:369-382. 4. Lin LM, Colby GP, Kim JE, Huang J, Tamargo RJ, Coon AL. Immediate and follow-up results for 44 consecutive cases of small (<10 mm) internal carotid artery aneurysms treated with the pipeline embolization device. Surgl Neurol Int. 2013;4:114. 5. Lylyk P, Miranda C, Ceratto R, Ferrario A, Scrivano E, Luna HR, et al. Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization device: the Buenos Aires experience. Neurosurgery. 2009;64:632-642 [discussion 642-633; quiz N636]. 6. Piano M, Valvassori L, Quilici L, Pero G, Boccardi E. Midterm and long-term follow-up of cerebral aneurysms treated with flow diverter devices: a single-center experience. J Neurosurg. 2013;118:408-416. 7. Stapleton CJ, Ogilvy CS. Treatment of intracranial aneurysms with the pipeline embolization device from a U.S. multicenter experience. World Neurosurg. 2013;80:231-233. 8. Szikora I, Berentei Z, Kulcsar Z, Marosfoi M, Vajda ZS, Lee W, et al. Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest experience with the pipeline embolization device. AJNR Am J Neuroradiol. 2010;31:1139-1147. 9. Yu SC, Kwok CK, Cheng PW, Chan KY, Lau SS, Lui WM, et al. Intracranial aneurysms: midterm outcome of pipeline embolization deviceea prospective study in 143 patients with 178 aneurysms. Radiology. 2012;265:893-901. 10. Fargen KM, Velat GJ, Lawson MF, Mocco J, Hoh BL. Review of reported complications associated with the Pipeline Embolization Device. World Neurosurg. 2012;77:403-404. 11. Leung GK, Tsang AC, Lui WM. Pipeline embolization device for intracranial aneurysm: a systematic review. Clin Neuroradiol. 2012;22:295-303.
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12. Chalouhi N, Starke RM, Yang S, Bovenzi CD, Tjoumakaris S, Hasan D, et al. Extending the indications of flow diversion to small, unruptured, saccular aneurysms of the anterior circulation. Stroke. 2014;45:54-58. 13. Brouillard AM, Sun X, Siddiqui AH, Lin N. The use of flow diversion for the treatment of intracranial aneurysms: expansion of indications. Cureus. 2016;8:e472. 14. Durst CR, Starke RM, Clopton D, Hixson HR, Schmitt PJ, Gingras JM, et al. Endovascular treatment of ophthalmic artery aneurysms: ophthalmic artery patency following flow diversion versus coil embolization [e-pub ahead of print]. J Neurointerv Surg. http://dx.doi.org/10.1136/neurintsurg-2015011887. 15. Zanaty M, Chalouhi N, Barros G, Schwartz EW, Saigh MP, Starke RM, et al. Flow-diversion for ophthalmic segment aneurysms. Neurosurgery. 2015;76:286-289 [discussion: 289-290]. 16. Chalouhi N, Daou B, Kung D, Zanaty M, Phillips JL, Tjoumakaris S, et al. Fate of the ophthalmic artery after treatment with the pipeline embolization device. Neurosurgery. 2015;77: 581-584 [discussion: 584]. 17. Moon K, Albuquerque FC, Ducruet AF, Webster Crowley R, McDougall CG. Treatment of ophthalmic segment carotid aneurysms using the pipeline embolization device: clinical and angiographic follow-up. Neurol Res. 2014;36:344-350. 18. Vedantam A, Rao VY, Shaltoni HM, Mawad ME. Incidence and clinical implications of carotid branch occlusion following treatment of internal carotid artery aneurysms with the pipeline embolization device. Neurosurgery. 2015;76:173-178 [discussion: 178]. 19. Alderazi YJ, Shastri D, Kass-Hout T, Prestigiacomo CJ, Gandhi CD. Flow diverters for intracranial aneurysms. Stroke Res Treat. 2014;2014: 415653. 20. Jabbour P, Chalouhi N, Tjoumakaris S, Gonzalez LF, Dumont AS, Randazzo C, et al. The Pipeline Embolization Device: learning curve and predictors of complications and aneurysm obliteration. Neurosurgery. 2013;73:113-120 [discussion: 120]. 21. Griessenauer CJ, Ogilvy CS, Foreman PM, Chua MH, Harrigan MR, Stapleton CJ, et al. Pipeline Embolization Device for small paraophthalmic artery aneurysms with an emphasis on the anatomical relationship of ophthalmic artery origin and aneurysm [e-pub ahead of print]. J Neurosurg. http://dx.doi.org/10.3171/2015.12. JNS152499. 22. Srinivasan V, Kan P, Mbabuike N, Tawk RG, Ban VS, Welch BG, et al. Oral Presentations 2016 AANS Annual Scientific Meeting Chicago, IL, April 30-May 4, 2016. J Neurosurg. 2016;124: A1146-A1209. 23. Kuzmik GA, Williamson T, Ediriwickrema A, Andeejani A, Bulsara KR. Flow diverters and a tale of two aneurysms. J Neurointerv Surg. 2013;5:e23. 24. Shapiro M, Becske T, Nelson PK. Learning from failure: persistence of aneurysms following
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pipeline embolization [e-pub ahead of print]. J Neurosurg. http://dx.doi.org/10.3171/2015.12. JNS152065. 25. O’Kelly CJ, Spears J, Chow M, Wong J, Boulton M, Weill A, et al. Canadian experience with the pipeline embolization device for repair of unruptured intracranial aneurysms. AJNR Am J Neuroradiol. 2013;34:381-387. 26. Chow M, McDougall C, O’Kelly C, Ashforth R, Johnson E, Fiorella D. Delayed spontaneous rupture of a posterior inferior cerebellar artery aneurysm following treatment with flow diversion: a clinicopathologic study. AJNR Am J Neuroradiol. 2012;33:E46-E51. 27. Kan P, Siddiqui AH, Veznedaroglu E, Liebman KM, Binning MJ, Dumont TM, et al.
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Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery. 2012;71:1080-1087 [discussion: 1087-1088]. 28. Ishibashi T, Murayama Y, Urashima M, Saguchi T, Ebara M, Arakawa H, et al. Unruptured intracranial aneurysms: incidence of rupture and risk factors. Stroke. 2009;40:313-316. 29. Juvela S, Poussa K, Lehto H, Porras M. Natural history of unruptured intracranial aneurysms: a long-term follow-up study. Stroke. 2013;44: 2414-2421.
31. Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110. Conflict of interest statement: A.A. is a consultant for Covidien, Johnson and Johnson, Sequent, Siemens, Stryker, and Terumo, and has grants from Siemens and Terumo. Received 11 February 2016; accepted 30 June 2016 Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.06.131 Journal homepage: www.WORLDNEUROSURGERY.org
30. Korja M, Lehto H, Juvela S. Lifelong rupture risk of intracranial aneurysms depends on risk factors: a prospective Finnish cohort study. Stroke. 2014;45: 1958-1963.
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.06.131
An Intraoperative Look at Failure of Flow Diversion: When Additional or Alternative Treatments Should Be Considered Loyola V. Gressot1, Akash J. Patel1, Visish M. Srinivasan1, Adam Arthur2, Peter Kan1, Edward A.M. Duckworth1,2
Key words Aneurysm - Endovascular - Flow diverter - Microsurgery - Pipeline embolization device -
Abbreviations and Acronyms ACoA: Anterior communicating artery ICA: Internal carotid artery PCoA: Posterior communicating artery PED: Pipeline embolization device From the 1Department of Neurosurgery, Baylor College of Medicine, Houston, Texas; and 2SemmeseMurphey Neurologic and Spine Institute, Department of Neurosurgery, University of Tennessee, Memphis, Tennessee, USA To whom correspondence should be addressed: Edward A.M. Duckworth, M.D., M.S. [E-mail: [email protected]] Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.06.131 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
INTRODUCTION The best treatment for many internal carotid artery (ICA) aneurysms remains a debated topic. Available treatment options can be divided into microsurgical or endovascular therapies, including clip-reconstruction, trapping/ bypass, coil embolization with or without a stent, and more recently, flow diversion. Globally and nationally, treatment has shifted toward endovascular therapies, but such therapies are challenged by large, wide-necked, or fusiform-shaped aneurysms. Simple coil embolization for aneurysms with these characteristics has been reported to have a high rate of recurrence.1 In 2011, the U.S. Food and Drug Administration approved use of the Pipeline embolization device (PED) (ev3, Irvine, California, USA) for large or giant, wide-necked intracranial aneurysms of the petrous to ophthalmic segments of the ICA, up to the origin of the superior
- BACKGROUND:
The pipeline embolization device (PED) is a flow-diverting stent that provides an additional treatment modality in the management of intracranial aneurysms. An aneurysm treated with a flow diverter is expected to involute over time, contrary to the immediate obliteration expected by surgical clipping or coiling. Yet, which aneurysms will respond to PED therapy and the time frame to expect full obliteration remain unclear.
- CASE
DESCRIPTION: We report the unusual case of a 50-year-old woman with multiple (4 total) intracranial aneurysms who underwent multimodality treatment. Two aneurysms were treated with PEDs. Nine months later, the patient underwent a craniotomy for treatment of an additional aneurysm; at the time of surgery, one of the PED-treated aneurysms was noted to be clearly obliterated, and the other was visualized to be filling. The ophthalmic artery arose from the persistently filling aneurysm. The aneurysm was treated by clip ligation without incident.
- CONCLUSIONS:
The rate of PED aneurysm obliteration increases with longer follow-up; however, the time frame for observing a persistently filling aneurysm before additional treatment is considered remains unknown. Some aneurysms may never close even after discontinuation of dual antiplatelet therapy. Ophthalmic artery aneurysms have been noted to fail treatment with PED based on the anatomic relationship of the aneurysm to the ophthalmic artery. This case provokes us to consider factors that may affect the latency to aneurysm obliteration, including aneurysm size, aneurysm morphology, patient gender, failure of previous aneurysm treatment, and duration of time from initial endovascular treatment.
hypophyseal artery (Premarket Approval Number P100018). The PED is a flexible, metallic stentlike construct with fundamentally novel design features: a 48-strand braided design and a degree of metal coverage 3e5 times higher than previous intracranial stents, designed to allow for reconstruction of the parent vessel by reducing or eliminating flow to the aneurysm and to maintain flow to jailed, perforating, or side branches. It is the first device designed to affect a long sought after goal in cerebral aneurysm treatment: endoluminal reconstruction. Several studies have reported successful aneurysm obliteration of lesions in both the anterior and posterior circulation using the PED.2-9 Yet, early enthusiasm has been tempered by
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reports of complications, including incomplete obliteration, aneurysm rupture, thromboembolic phenomena, and anatomically remote intraparenchymal hemorrhages.10,11 We report the case of a 50-year-old woman with multiple intracranial aneurysms treated with different modalities, including bilateral placement of PEDs, one of which had persistent patency that required a secondary clip ligation procedure. This case shows, in a single patient, several of the existing issues and outstanding questions that are associated with flow diversion; unique intraoperative photographs of the arterial changes seen after placement of a flow-diverting stent are included.
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CASE REPORT LOYOLA V. GRESSOT ET AL.
CASE DESCRIPTION A 50-year-old woman with a history of hypothyroidism and hyperlipidemia presented with recurrent headaches. She had no neurologic deficit on initial evaluation and did not have a subarachnoid hemorrhage. An angiogram showed 4 aneurysms: a 4.1-mm wide-necked, right ophthalmic segment aneurysm, a 5.7-mm anterior communicating artery (ACoA) aneurysm, a 2.3-mm left posterior communicating artery (PCoA) aneurysm, and a 2.6-mm left carotid terminus aneurysm (Figure 1A, B). The patient was previously treated by another physician with stent-assisted coiling of the ACoA aneurysm using a 4.5-mm 20-mm Neuroform stent, and placement of a 4-mm 14-mm PED across the left PCoA aneurysm. One month later, she had a 3.75-mm 14-mm PED placed across the right ophthalmic segment aneurysm, which was complicated by a retroperitoneal hematoma and managed conservatively. A follow-up angiogram 7 months after completion of endovascular therapy showed that both ACoA and the left PCoA aneurysms were obliterated. The left carotid terminus aneurysm, which was untreated, was determined to be unchanged. However, the right ophthalmic segment aneurysm, with the ophthalmic artery arising from the aneurysm, had decreased but persistent filling (Figure 2).
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The patient was taken to the operating room for surgical clipping of the 2 remaining aneurysms, 9 months after the last of the endovascular therapies. A left minipterional craniotomy was performed to expose the left carotid terminus aneurysm, which was noted to be thin walled (Figure 3A), and the aneurysm was clipped successfully with patency of the parent arteries shown by indocyanine green videoangiography. The craniotomy exposure provided an advantageous visual of the PED-treated ICA, which showed that the vessel had a devitalized appearance, and the distal tines of the PED were visibly protruding through the adventitia of the artery with an obvious transition from healthy-appearing artery to diseased artery at the margin of the PED (Figure 3B). The previously treated left PCoA aneurysm was found to be completely obliterated and shrivelled (Figure 3C). Attention then turned to the medially projecting right ophthalmic segment aneurysm, which was optimally visualized from the left pterional craniotomy. The PED was noted to be spanning the neck of the aneurysm, but it did not divert flow away from the aneurysm, which continued to fill (Figure 3D). The neck of the aneurysm was noted to be close to the ophthalmic artery. The aneurysm was successfully clipped with a 5-mm straight miniclip. Intraoperative indocyanine green
Figure 2. Three-dimensional reconstruction of angiogram showing the ophthalmic artery arising from persistently filling ophthalmic segment aneurysm.
angiography confirmed patency of the afferent and efferent vessels and obliteration of the aneurysm. Postoperatively, the patient remained neurologically intact. She was admitted to the intensive care unit and transferred to the floor on postoperative day 1. A completion angiogram showed obliteration of both clipped aneurysms and no untoward findings (Figure 4A, B). The patient was discharged home on postoperative day 4 in good condition. The patient did well clinically, reporting no new problems during long-term outpatient follow-up. DISCUSSION
Figure 1. Digital subtraction angiography anteroposterior view of (A) right and (B) left internal carotid injections showing anterior communicating, right ophthalmic segment, left posterior communicating, and left carotid terminus aneurysms.
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Flow diversion has emerged as an important treatment for a variety of intracranial aneurysms. Although Food and Drug Administrationeapproved for large and giant wide-necked aneurysms of the cavernous and proximal supraclinoid ICA, flow diverters are also being used off label to treat aneurysms of various sizes and in various anatomic locations.12,13 Many large studies have been published evaluating the use of the PED for the treatment of intracranial aneurysms, but several questions remain as experience increases and applications expand. What are the risk factors for failure of PED therapy? Are coils necessary, in larger or symptomatic aneurysms, to prevent the rare but devastating complication of induced aneurysmal rupture? What is the risk of jailing larger branch arteries with
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Figure 3. Intraoperative photograph of left minipterional craniotomy showing (A) left ophthalmic segment aneurysm with weak, thin wall (arrow), (B) right internal carotid with previously deployed Pipeline embolization device with irregular appearing walls and visible tines and obvious transition (arrow) to
PED? When does one consider a persistently filling aneurysm to have failed PED treatment? What is the timeline for considering retreatment? Predicting the latency to complete aneurysm obliteration after PED treatment for different aneurysms is difficult. In our patient, the PCoA aneurysm (the smallest) was angiographically confirmed to be obliterated 8 months after placement of the PED. However, the ophthalmic segment aneurysm remained patent at 7 months and was directly visualized intraoperatively at 9 months after PED placement. Failure of PED in Ophthalmic Segment Aneurysms Many investigators have commented on the unique physiology of the ophthalmic artery and PED treatment of ophthalmic segment aneurysms, noting that the
healthy-appearing vessel at the end of Pipeline embolization device, (C) obliterated left posterior communicating artery aneurysm (arrow), and (D) persistently filling of right ophthalmic segment aneurysm with pipeline stent visible across neck (arrow).
ophthalmic segment aneurysms can be successfully obliterated with PED therapy, maintaining patency of the ophthalmic artery.14-17 Even when the aneurysm occludes, it is frequently asymptomatic.18 However, we hypothesize that the involvement of the origin of the ophthalmic artery in our case was the cause of the PED therapy failure (Figure 2). The PED functions by slowing and enlarging aneurysm inflow, with compensatory reduction in outflow, which leads to stasis within the aneurysm and thrombosis.19 It is believed that the endothelium grows across the porous stent and occludes the aneurysm.20 The inclusion of the ophthalmic artery in this aneurysm likely acted as a sump, drawing away blood flow and preventing this stasis, unlike the contralateral aneurysm on the PCoA, which did not
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incorporate a branch artery and responded well to PED therapy. Furthermore, another patient in our series has a similar ophthalmic segment aneurysm that also incorporates the ophthalmic artery, and it continues to show persistent filling 2.5 years after PED placement. Griessenhauer et al.21 noted that the close association of the ophthalmic artery with the aneurysm neck may be a significant risk factor for PED failure. Such end-vessel arteries have been associated with PED treatment failure for other locations as well.22 Variable Response to PED Treatment in a Single Patient Few reports exist regarding multiple aneurysms showing different responses to PED treatment in an individual patient. Kuzmik et al.23 documented 2 patients
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Figure 4. Digital subtraction angiography anteroposterior view of (A) right and (B) left internal carotid injections showing successful obliteration of all aneurysms.
with large, paraclinoid aneurysms, each treated with a SILK flow diverter device (Balt, Montmorency, France). One patient had complete obliteration of the aneurysm, while the other had a subarachnoid hemorrhage with partial recanalization of the aneurysm neck 1 week after the procedure. Lin et al.4 reported a case of a patient with a 5-mm cavernous sinus aneurysm and an ipsilateral 5-mm ophthalmic aneurysm simultaneously treated with PEDs. There was complete occlusion of the ophthalmic aneurysm, but residual filling of the cavernous sinus aneurysm. Moon et al.17 reported a patient with 2 ipsilateral, tandem, saccular ophthalmic segment aneurysms, each treated with PEDs. At 6-month follow-up, the distal lesion was completely obliterated, whereas the proximal lesion had a small residual. Risk Factors for PED Treatment Failure Many investigators have proposed ideas about the risk factors for failure of PED therapy, because occlusion rates reported in the literature range from 66% to 90.9%.3,4,10,17,20,23 Shapiro et al.24 reported on 100 patients with anterior circulation aneurysms treated with PED. Independent risk factors for failure were fusiform morphology, decreasing dome/neck ratio, and the presence of a preexisting lasercut stent. Jabbour et al.20 also identified
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shorter angiographic follow-up as a risk factor in their series of 109 patients with 120 aneurysms. O’Kelly et al.17 reported a series of 94 successfully deployed PEDs in unruptured aneurysms. Being female and having had previous aneurysm treatment were found to be predictors of persistent aneurysm filling on multivariate analysis. In reviewing the literature, the longer the follow-up, the higher the percentage of PED-treated aneurysms that are obliterated. However, some aneurysms obliterate faster than others, whereas others seem to not obliterate altogether. The factors that drive the different rates of involution remain poorly understood. Defining Treatment Failure and Timing of Retreatment Moreover, the question remains of how much time should be allowed for obliteration before considering the PED treatment as a failure. Most of the published series show that most aneurysms are obliterated after 6e10 months. Multiple series9,20 have shown that the rate of aneurysm obliteration increases with time from treatment; however, this must be weighed against the risk of an unsecured aneurysm. Several investigators have described the risk of delayed rupture after PED deployment, ranging from 1 week to 8 months after the procedure.9,25-27 Although the overall rate of delayed
postprocedure hemorrhage is low, and more likely in giant aneurysms, the risk remains present until the aneurysm is obliterated, and for a short time thereafter. There is no consensus regarding when to consider additional treatment of persistently filling aneurysms after PED placement. Fischer et al.3 reported a retreatment rate of 9% with a second PED as a result of a persistently filling aneurysm but did not state how and when this decision was made. Treatment with PED precludes secondary intrasaccular options, leaving 2 options: deployment of another flow diverter or surgery. In our case, surgery was required to secure the previously treated right ophthalmic segment aneurysm that was not amenable to endovascular therapy and was intraoperatively visualized to have persistent filling; it was successfully clipped. The patient described in this case had multiple (4) small aneurysms, all under 7 mm, and could have been managed conservatively. Multiple studies have shown that small aneurysm size is associated with low rates of rupture, although a PCoA aneurysm carries a higher rupture risk.28-31 Our patient was relatively young, and otherwise in good health, placing her at a higher lifetime risk of rupture.30 Females are also more likely than males to experience aneurysm rupture.30 Given this patient’s recurrent headaches, the possibility of a sentinel hemorrhage could not be excluded. The other treatment option would have been surgical clipping of all 4 aneurysms in a single craniotomy. This option would have eliminated the additional morbidity and risk of multiple procedures and use of dual antiplatelet medication. Treating multiple aneurysms through the same craniotomy in a single procedure does not summate risks in the same way as treating multiple aneurysms in repeated endovascular procedures. Because one of the aneurysms was unsuitable for endovascular therapy from the beginning, microsurgical exploration and clipping would have been a good alternative. The question then becomes, when should additional treatment be considered? If there is another reason for microsurgery, and an aneurysm previously treated with PED is still filling and safely
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accessible (as in our case), there is not much of dilemma; it should be clipped. On the other hand, if a PED-treated aneurysm is radiographically followed, and shows signs of progressive involution, it seems sensible to stay the course. The decision-making challenge comes in cases that do not fall clearly into either of these categories. For those that are not responding as expected, initially discontinuing antiplatelet medications may accelerate thrombosis and involution. Additional PED placement may be considered if there is no change after discontinuation of antiplatelet medication. In some cases, branch artery morphology or other anatomic considerations may preclude aneurysm thrombosis, even with additional time, medication modification, or additional PED placement. In these cases, it is unclear whether the natural history has been significantly altered so that the aneurysm can be safely observed, or whether other treatments, namely surgery (because the aneurysm has failed endovascular therapy), should be considered.
CONCLUSIONS We report the unusual case of a patient treated with bilateral PED placement, resulting in successful obliteration of one aneurysm yet persistent filling of the other. The involvement of the ophthalmic artery with the aneurysm neck likely created a sump phenomenon in our case, preventing involution. A review of the literature showed a lack of consensus regarding which aneurysms are expected to respond to or fail PED therapy and alternative treatment options after PED failure. Despite the burgeoning development of flow diversion for endovascular therapy, microsurgery remains a reasonable alternative treatment to PED treatment and an attractive secondary treatment for certain cases of PED treatment failure. ACKNOWLEDGMENTS Author contributions to the study and manuscript preparation include the following: conception and design: A.A., P.K., E.A.M.D.; acquisition of data: L.V.G., A.J.P.; analysis and interpretation of data: L.V.G., A.J.P., V.M.S.; drafting the
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article, critically revising the article, and reviewing submitted version of manuscript: all authors; approving the final version of the manuscript on behalf of all authors: L.V.G.; study supervision: E.A.M.D. REFERENCES 1. Piotin M, Blanc R, Spelle L, Mounayer C, Piantino R, Schmidt PJ, et al. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke. 41, 2010, 110e115. 2. Fiorella D, Kelly ME, Albuquerque FC, Nelson PK. Curative reconstruction of a giant midbasilar trunk aneurysm with the pipeline embolization device. Neurosurgery. 2009;64:212-217 [discussion: 217]. 3. Fischer S, Vajda Z, Aguilar Perez M, Schmid E, Hopf N, Bazner H, et al. Pipeline embolization device (PED) for neurovascular reconstruction: initial experience in the treatment of 101 intracranial aneurysms and dissections. Neuroradiology. 2012;54:369-382. 4. Lin LM, Colby GP, Kim JE, Huang J, Tamargo RJ, Coon AL. Immediate and follow-up results for 44 consecutive cases of small (<10 mm) internal carotid artery aneurysms treated with the pipeline embolization device. Surgl Neurol Int. 2013;4:114. 5. Lylyk P, Miranda C, Ceratto R, Ferrario A, Scrivano E, Luna HR, et al. Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization device: the Buenos Aires experience. Neurosurgery. 2009;64:632-642 [discussion 642-633; quiz N636]. 6. Piano M, Valvassori L, Quilici L, Pero G, Boccardi E. Midterm and long-term follow-up of cerebral aneurysms treated with flow diverter devices: a single-center experience. J Neurosurg. 2013;118:408-416. 7. Stapleton CJ, Ogilvy CS. Treatment of intracranial aneurysms with the pipeline embolization device from a U.S. multicenter experience. World Neurosurg. 2013;80:231-233. 8. Szikora I, Berentei Z, Kulcsar Z, Marosfoi M, Vajda ZS, Lee W, et al. Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest experience with the pipeline embolization device. AJNR Am J Neuroradiol. 2010;31:1139-1147. 9. Yu SC, Kwok CK, Cheng PW, Chan KY, Lau SS, Lui WM, et al. Intracranial aneurysms: midterm outcome of pipeline embolization deviceea prospective study in 143 patients with 178 aneurysms. Radiology. 2012;265:893-901. 10. Fargen KM, Velat GJ, Lawson MF, Mocco J, Hoh BL. Review of reported complications associated with the Pipeline Embolization Device. World Neurosurg. 2012;77:403-404. 11. Leung GK, Tsang AC, Lui WM. Pipeline embolization device for intracranial aneurysm: a systematic review. Clin Neuroradiol. 2012;22:295-303.
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Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery. 2012;71:1080-1087 [discussion: 1087-1088]. 28. Ishibashi T, Murayama Y, Urashima M, Saguchi T, Ebara M, Arakawa H, et al. Unruptured intracranial aneurysms: incidence of rupture and risk factors. Stroke. 2009;40:313-316. 29. Juvela S, Poussa K, Lehto H, Porras M. Natural history of unruptured intracranial aneurysms: a long-term follow-up study. Stroke. 2013;44: 2414-2421.
31. Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110. Conflict of interest statement: A.A. is a consultant for Covidien, Johnson and Johnson, Sequent, Siemens, Stryker, and Terumo, and has grants from Siemens and Terumo. Received 11 February 2016; accepted 30 June 2016 Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.06.131 Journal homepage: www.WORLDNEUROSURGERY.org
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