J Korean Neurosurg Soc.  2020 Mar;63(2):137-152. 10.3340/jkns.2020.0034.

The Evolution of Flow-Diverting Stents for Cerebral Aneurysms; Historical Review, Modern Application, Complications, and Future Direction

• Shin DS
• Carroll CP
• Elghareeb
• Hoh BL
• Kim BT

• KMID: 2501700
• DOI: http://doi.org/10.3340/jkns.2020.0034

Abstract

In spite of the developing endovascular era, large (15–25 mm) and giant (>25 mm) wide-neck cerebral aneurysms remained technically challenging. Intracranial flow-diverting stents (FDS) were developed to address these challenges by targeting aneurysm hemodynamics to promote aneurysm occlusion. In 2011, the first FDS approved for use in the United States market. Shortly thereafter, the Pipeline of Uncoilable or Failed Aneurysms (PUFS) study was published demonstrating high efficacy and a similar complication profile to other intracranial stents. The initial FDA instructions for use (IFU) limited its use to patients 22 years old or older with wide-necked large or giant aneurysms of the internal carotid artery (ICA) from the petrous segment to superior hypophyseal artery/ophthalmic segment. Expanded IFU was tested in the Prospective Study on Embolization of Intracranial Aneurysms with PipelineTM Embolization Device (PREMIER) trial. With further post-approval clinical data, the United States FDA expanded the IFU to include patients with small or medium, wide-necked saccular or fusiform aneurysms from the petrous ICA to the ICA terminus. However, IFU is more restrictive in South Korea than in United States. Several systematic reviews and meta-analyses have sought to evaluate the overall efficacy of FDS for the treatment of cerebral aneurysms and consistently identify FDS as an effective technique for the treatment of aneurysms broadly with complication rates similar to other traditional techniques. A growing body of literature has demonstrated high efficacy of FDS for small aneurysms; distal artery aneurysms; non-saccular aneurysms posterior circulation aneurysms and complication rates similar to traditional techniques. In the short interval since the Pipeline Embolization Device was first introduced, FDS has been firmly entrenched as a powerful tool in the endovascular armamentarium. As new FDS are developed, established FDS are refined, and delivery systems are improved the uses for FDS will only expand further. Researchers continue to work to optimize the mechanical characteristics of the FDS themselves, aiming to optimize deploy ability and efficacy. With expanded use for small to medium aneurysms and posterior circulation aneurysms, FDS technology is firmly entrenched as a powerful tool to treat challenging aneurysms, both primarily and as an adjunct to coil embolization. With the aforementioned advances, the ease of FDS deployment will improve and complication rates will be further minimized. This will only further establish FDS deployment as a key strategy in the treatment of cerebral aneurysms.

Keyword

Endovascular procedure; Intracranial aneurysm; Stents

Figure

• 

  Fig. 1. Successful FDS deployment requires a balance between pushing delivery-wire and unsheathing microcatheter from the device. A : It is ideal that the proximal or “unsheathing” FDS be shaped like a wine glass. B : Insufficient forward-loading or aggressive unsheathing can result in cells expanding in the shape of a champagne flute. C : Excessive forward loading of the FDS will result in the expanding FDS cells taking the shape of a martini glass. FDS : flow-diverting stents.

• 

  Fig. 2. If insufficient apposition is identified, the repetitive push-pull technique can be used to improve deployment against the vessel wall. A : Insufficient wall apposition. B : Push technique. C : Pull technique.

• 

  Fig. 3. Conformable intracranial balloons can help to remodel the stent with good vessel apposition. A : Conform insufficient wall apposition with angiography. B : Remove micro-guide wire for flow diverter stent and set up the intracranial balloon with micro-guide wire. C : Balloon angioplasty for good vessel apposition.

Reference

References

1. Alderazi YJ, Shastri D, Kass-Hout T, Prestigiacomo CJ, Gandhi CD. Flow diverters for intracranial aneurysms. Stroke Res Treat. 2014:415653. 2014.

2. Arrese I, Sarabia R, Pintado R, Delgado-Rodriguez M. Flow-diverter devices for intracranial aneurysms: systematic review and meta-analysis. Neurosurgery. 73:193–199. discussion 199-200. 2013.

3. Becske T, Brinjikji W, Potts MB, Kallmes DF, Shapiro M, Moran CJ, et al. Long-term clinical and angiographic outcomes following pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the pipeline for uncoilable or failed aneurysms trial. Neurosurgery. 80:40–48. 2017.

4. Becske T, Kallmes DF, Saatci I, McDougall CG, Szikora I, Lanzino G, et al. Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology. 267:858–868. 2013.

5. Becske T, Potts MB, Shapiro M, Kallmes DF, Brinjikji W, Saatci I, et al. Pipeline for uncoilable or failed aneurysms: 3-year follow-up results. J Neurosurg. 127:81–88. 2017.

6. Bender MT, Colby GP, Jiang B, Lin LM, Campos JK, Xu R, et al. Flow diversion of posterior circulation cerebral aneurysms: a single-institution series of 59 cases. Neurosurgery. 84:206–216. 2019.

7. Bender MT, Lin LM, Colby GP, Lubelski D, Huang J, Tamargo RJ, et al. P2Y12 hyporesponse (PRU>200) is not associated with increased thromboembolic complications in anterior circulation pipeline. J Neurointerv Surg. 9:978–981. 2017.

8. Berge J, Biondi A, Machi P, Brunel H, Pierot L, Gabrillargues J, et al. Flow-diverter silk stent for the treatment of intracranial aneurysms: 1-year follow-up in a multicenter study. AJNR Am J Neuroradiol. 33:1150–1155. 2012.

9. Bhogal P, Martinez Moreno R, Ganslandt O, Bäzner H, Henkes H, Perez MA. Use of flow diverters in the treatment of unruptured saccular aneurysms of the anterior cerebral artery. J Neurointerv Surg. 9:283–289. 2017.

10. Bhogal P, Pérez MA, Ganslandt O, Bazner H, Henkes H, Fischer S. Treatment of posterior circulation non-saccular aneurysms with flow diverters: a single-center experience and review of 56 patients. J Neurointerv Surg. 9:471–481. 2017.

11. Biondi A, Janardhan V, Katz JM, Salvaggio K, Riina HA, Gobin YP. Neuroform stent-assisted coil embolization of wide-neck intracranial aneurysms: strategies in stent deployment and midterm follow-up. Neurosurgery. 61:460–468. discussion 468-469. 2007.

12. Briganti F, Leone G, Marseglia M, Mariniello G, Caranci F, Brunetti A, et al. Endovascular treatment of cerebral aneurysms using flow-diverter devices: a systematic review. Neuroradiol J. 28:365–375. 2015.

13. Brinjikji W, Lanzino G, Cloft HJ, Siddiqui AH, Boccardi E, Cekirge S, et al. Risk factors for ischemic complications following pipeline embolization device treatment of intracranial aneurysms: results from the IntrePED study. AJNR Am J Neuroradiol. 37:1673–1678. 2016.

14. Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke. 44:442–447. 2013.

15. Byrne JV, Beltechi R, Yarnold JA, Birks J, Kamran M. Early experience in the treatment of intra-cranial aneurysms by endovascular flow diversion: a multicentre prospective study. PLoS One. 5:e12492. 2010.

16. Cagnazzo F, Cappucci M, Dargazanli C, Lefevre PH, Gascou G, Riquelme C, et al. Treatment of distal anterior cerebral artery aneurysms with flow-diverter stents: a single-center experience. AJNR Am J Neuroradiol. 39:1100–1106. 2018.

17. Cebral JR, Mut F, Raschi M, Scrivano E, Ceratto R, Lylyk P, et al. Aneurysm rupture following treatment with flow-diverting stents: computational hemodynamics analysis of treatment. AJNR Am J Neuroradiol. 32:27–33. 2011.

18. 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. 45:54–58. 2014.

19. Chalouhi N, Tjoumakaris S, Phillips JL, Starke RM, Hasan D, Wu C, et al. A single pipeline embolization device is sufficient for treatment of intracranial aneurysms. AJNR Am J Neuroradiol. 35:1562–1566. 2014.

20. Chalouhi N, Tjoumakaris S, Starke RM, Gonzalez LF, Randazzo C, Hasan D, et al. Comparison of flow diversion and coiling in large unruptured intracranial saccular aneurysms. Stroke. 44:2150–2154. 2013.

21. Chalouhi N, Zanaty M, Whiting A, Yang S, Tjoumakaris S, Hasan D, et al. Safety and efficacy of the pipeline embolization device in 100 small intracranial aneurysms. J Neurosurg. 122:1498–1502. 2015.

22. Chitale R, Gonzalez LF, Randazzo C, Dumont AS, Tjoumakaris S, Rosenwasser R, et al. Single center experience with pipeline stent: feasibility, technique, and complications. Neurosurgery. 71:679–691. discussion 691. 2012.

23. Chiu AH, Cheung AK, Wenderoth JD, De Villiers L, Rice H, Phatouros CC, et al. Long-term follow-up results following elective treatment of unruptured intracranial aneurysms with the pipeline embolization device. AJNR Am J Neuroradiol. 36:1728–1734. 2015.

24. Chong W, Zhang Y, Qian Y, Lai L, Parker G, Mitchell K. Computational hemodynamics analysis of intracranial aneurysms treated with flow diverters: correlation with clinical outcomes. AJNR Am J Neuroradiol. 35:136–142. 2014.

25. Cohen JE, Gomori JM, Moscovici S, Leker RR, Itshayek E. Delayed complications after flow-diverter stenting: reactive in-stent stenosis and creeping stents. J Clin Neurosci. 21:1116–1122. 2014.

26. Colby GP, Bender MT, Lin LM, Beaty N, Huang J, Tamargo RJ, et al. Endovascular flow diversion for treatment of anterior communicating artery region cerebral aneurysms: a single-center cohort of 50 cases. J Neurointerv Surg. 9:679–685. 2017.

27. Colby GP, Lin LM, Caplan JM, Jiang B, Michniewicz B, Huang J, et al. Flow diversion of large internal carotid artery aneurysms with the surpass device: impressions and technical nuance from the initial North American experience. J Neurointerv Surg. 8:279–286. 2016.

28. Colby GP, Lin LM, Gomez JF, Paul AR, Huang J, Tamargo RJ, et al. Immediate procedural outcomes in 35 consecutive pipeline embolization cases: a single-center, single-user experience. J Neurointerv Surg. 5:237–246. 2013.

29. Colby GP, Lin LM, Huang J, Tamargo RJ, Coon AL. Utilization of the Navien distal intracranial catheter in 78 cases of anterior circulation aneurysm treatment with the pipeline embolization device. J Neurointerv Surg. 5 Suppl 3:iii16–iii21. 2013.

30. Colby GP, Lin LM, Nundkumar N, Jiang B, Huang J, Tamargo RJ, et al. Radiation dose analysis of large and giant internal carotid artery aneurysm treatment with the pipeline embolization device versus traditional coiling techniques. J Neurointerv Surg 7 : 380-384, 2015 31. Connolly ES Jr : International study of unruptured intracranial aneurysms. J Neurosurg. 121:1022–1023. 2014.

31. Connolly ES Jr. International study of unruptured intracranial aneurysms. J Neurosurg. 121:1022–1023. 2014.

32. Cruz JP, Chow M, O’Kelly C, Marotta B, Spears J, Montanera W, et al. Delayed ipsilateral parenchymal hemorrhage following flow diversion for the treatment of anterior circulation aneurysms. AJNR Am J Neuroradiol. 33:603–608. 2012.

33. Darsaut TE, Bing F, Salazkin I, Gevry G, Raymond J. Flow diverters can occlude aneurysms and preserve arterial branches: a new experimental model. AJNR Am J Neuroradiol. 33:2004–2009. 2012.

34. De Vries J, Boogaarts J, Van Norden A, Wakhloo AK. New generation of flow diverter (surpass) for unruptured intracranial aneurysms: a prospective single-center study in 37 patients. Stroke. 44:1567–1577. 2013.

35. Delgado Almandoz JE, Crandall BM, Scholz JM, Fease JL, Anderson RE, Kadkhodayan Y, et al. Last-recorded P2Y12 reaction units value is strongly associated with thromboembolic and hemorrhagic complications occurring up to 6 months after treatment in patients with cerebral aneurysms treated with the pipeline embolization device. AJNR Am J Neuroradiol. 35:128–135. 2014.

36. Delgado Almandoz JE, Kadkhodayan Y, Crandall BM, Scholz JM, Fease JL, Tubman DE. Variability in initial response to standard clopidogrel therapy, delayed conversion to clopidogrel hyper-response, and associated thromboembolic and hemorrhagic complications in patients undergoing endovascular treatment of unruptured cerebral aneurysms. J Neurointerv Surg. 6:767–773. 2014.

37. Di Maria F, Pistocchi S, Clarençon F, Bartolini B, Blanc R, Biondi A, et al. Flow diversion versus standard endovascular techniques for the treatment of unruptured carotid-ophthalmic aneurysms. AJNR Am J Neuroradiol. 36:2325–2330. 2015.

38. Diaz O, Gist TL, Manjarez G, Orozco F, Almeida R. Treatment of 14 intracranial aneurysms with the FRED system. J Neurointerv Surg. 6:614–617. 2014.

39. Ferns SP, Sprengers ME, van Rooij WJ, Rinkel GJ, van Rijn JC, Bipat S, et al. Coiling of intracranial aneurysms: a systematic review on initial occlusion and reopening and retreatment rates. Stroke. 40:e523–e529. 2009.

40. Fifi JT, Brockington C, Narang J, Leesch W, Ewing SL, Bennet H, et al. Clopidogrel resistance is associated with thromboembolic complications in patients undergoing neurovascular stenting. AJNR Am J Neuroradiol. 34:716–720. 2013.

41. Fiorella D, Hsu D, Woo HH, Tarr RW, Nelson PK. Very late thrombosis of a pipeline embolization device construct: case report. Neurosurgery. 67(3 Suppl Operative):onsE313-onsE314; discussion onsE314. 2013.

42. Fiorella D, Lylyk P, Szikora I, Kelly ME, Albuquerque FC, McDougall CG, et al. Curative cerebrovascular reconstruction with the pipeline embolization device: the emergence of definitive endovascular therapy for intracranial aneurysms. J Neurointerv Surg. 1:56–65. 2009.

43. Fiorella D, Woo HH, Albuquerque FC, Nelson PK. Definitive reconstruction of circumferential, fusiform intracranial aneurysms with the pipeline embolization device. Neurosurgery. 62:1115–1120. discussion 1120-1121. 2008.

44. Girdhar G, Andersen A, Pangerl E, Jahanbekam R, Ubl S, Nguyen K, et al. Thrombogenicity assessment of pipeline flex, pipeline shield, and FRED flow diverters in an in vitro human blood physiological flow loop model. J Biomed Mater Res A. 106:3195–3202. 2018.

45. Goh C, Churilov L, Mitchell P, Dowling R, Yan B. Clopidogrel hyperresponse and bleeding risk in neurointerventional procedures. AJNR Am J Neuroradiol. 34:721–726. 2013.

46. Gonzalez NR, Duckwiler G, Jahan R, Murayama Y, Vinuela F. Challenges in the endovascular treatment of giant intracranial aneurysms. Neurosurgery. 62:1324–1335. 2008.

47. 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. J Neurosurg. 125:1352–1359. 2016.

48. Gruber A, Killer M, Bavinzski G, Richling B. Clinical and angiographic results of endosaccular coiling treatment of giant and very large intracranial aneurysms: a 7-year, single-center experience. Neurosurgery. 45:793–803. discussion 803-804. 1999.

49. Guglielmi G, Viñuela F, Dion J, Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: preliminary clinical experience. J Neurosurg. 75:8–14. 1991.

50. Guglielmi G, Viñuela F, Duckwiler G, Dion J, Lylyk P, Berenstein A, et al. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg. 77:515–524. 1992.

51. Guglielmi G, Viñuela F, Sepetka I, Macellari V. Electrothrombosis of saccular aneurysms via endovascular approach. Part 1: electrochemical basis, technique, and experimental results. J Neurosurg. 75:1–7. 1991.

52. Hagen MW, Girdhar G, Wainwright J, Hinds MT. Thrombogenicity of flow diverters in an ex vivo shunt model: effect of phosphorylcholine surface modification. J Neurointerv Surg. 9:1006–1011. 2017.

53. Hanel RA, Kallmes DF, Lopes DK, Nelson PK, Siddiqui A, Jabbour P, et al. Prospective study on embolization of intracranial aneurysms with the pipeline device: the PREMIER study 1 year results. J Neurointerv Surg. 12:62–66. 2020.

54. Health Insurance Review & Assessment Service; Notification of Ministtry of health and welfare. Flow diverter stent embolization device (No. 2014-191). Available at : http://www.hira.or.kr/bbsDummy.do?brdBltNo=5482&brdScnBltNo=5484&pgmid=HIRAA020002000100.

55. International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms--risk of rupture and risks of surgical intervention. N Engl J Med. 339:1725–1733. 1998.

56. Jo KI, Yang NR, Jeon P, Kim KH, Hong SC, Kim JS. Treatment outcomes with selective coil embolization for large or giant aneurysms : prognostic implications of incomplete occlusion. J Korean Neurosurg Soc. 61:19–27. 2018.

57. Kabbasch C, Mpotsaris A, Behme D, Dorn F, Stavrinou P, Liebig T. Pipeline embolization device for treatment of intracranial aneurysms-the more, the better? A single-center retrospective observational study. J Vasc Interv Neurol. 9:14–20. 2016.

58. Kallmes DF, Hanel R, Lopes D, Boccardi E, Bonafé A, Cekirge S, et al. International retrospective study of the pipeline embolization device: a multicenter aneurysm treatment study. AJNR Am J Neuroradiol. 36:108–115. 2015.

59. Karsy M, Guan J, Brock AA, Amin A, Park MS. Emerging technologies in flow diverters and stents for cerebrovascular diseases. Curr Neurol Neurosci Rep. 17:96. 2017.

60. Kim BM, Shin YS, Baik MW, Lee DH, Jeon P, Baik SK, et al. Pipeline embolization device for large/giant or fusiform aneurysms: an initial multicenter experience in Korea. Neurointervention. 11:10–17. 2016.

61. Kim LJ, Tariq F, Levitt M, Barber J, Ghodke B, Hallam DK, et al. Multimodality treatment of complex unruptured cavernous and paraclinoid aneurysms. Neurosurgery. 74:51–61. discussion 61; quiz 61. 2014.

62. Kim TG, Kwon O, Shin YS, Sung JH, Koh JS, Kim BT. Endovascular treatments performed collaboratively by the Society of Korean Endovascular Neurosurgeons members : a nationwide multicenter survey. J Korean Neurosurg Soc. 62:502–518. 2019.

63. Klisch J, Turk A, Turner R, Woo HH, Fiorella D. Very late thrombosis of flow-diverting constructs after the treatment of large fusiform posterior circulation aneurysms. AJNR Am J Neuroradiol. 32:627–632. 2011.

64. Kocer N, Islak C, Kizilkilic O, Kocak B, Saglam M, Tureci E. Flow redirection endoluminal Device in treatment of cerebral aneurysms: initial experience with short-term follow-up results. J Neurosurg. 120:1158–1171. 2014.

65. Kulcsár Z, Houdart E, Bonafé A, Parker G, Millar J, Goddard AJ, et al. Intra-aneurysmal thrombosis as a possible cause of delayed aneurysm rupture after flow-diversion treatment. AJNR Am J Neuroradiol. 32:20–25. 2011.

66. Lanzino G, Crobeddu E, Cloft HJ, Hanel R, Kallmes DF. Efficacy and safety of flow diversion for paraclinoid aneurysms: a matched-pair analysis compared with standard endovascular approaches. AJNR Am J Neuroradiol. 33:2158–2161. 2012.

67. Le Quellec S, Bordet JC, Negrier C, Dargaud Y. Comparison of current platelet functional tests for the assessment of aspirin and clopidogrel response. A review of the literature. Thromb Haemost. 116:638–650. 2016.

68. Lee JY, Cho YD, Kang HS, Han MH. Healing of aneurysm after treatment using flow diverter stent : histopathological study in experimental canine carotid side wall aneurysm. J Korean Neurosurg Soc. 63:34–44. 2020.

69. Lin LM, Colby GP, Huang J, Tamargo RJ, Coon AL. Ultra-distal largebore intracranial access using the hyperflexible Navien distal intracranial catheter for the treatment of cerebrovascular pathologies: a technical note. J Neurointerv Surg. 6:301–307. 2014.

70. Lin LM, Colby GP, Jiang B, Uwandu C, Huang J, Tamargo RJ, et al. Classification of cavernous internal carotid artery tortuosity: a predictor of procedural complexity in pipeline embolization. J Neurointerv Surg. 7:628–633. 2015.

71. Lin N, Brouillard AM, Keigher KM, Lopes DK, Binning MJ, Liebman KM, et al. Utilization of Pipeline embolization device for treatment of ruptured intracranial aneurysms: US multicenter experience. J Neurointerv Surg. 7:808–815. 2015.

72. Lin N, Brouillard AM, Krishna C, Mokin M, Natarajan SK, Sonig A, et al. Use of coils in conjunction with the pipeline embolization device for treatment of intracranial aneurysms. Neurosurgery. 76:142–149. 2015.

73. Lin N, Lanzino G, Lopes DK, Arthur AS, Ogilvy CS, Ecker RD, et al. Treatment of distal anterior circulation aneurysms with the pipeline embolization device: a US multicenter experience. Neurosurgery. 79:14–22. 2016.

74. 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. 64:632–642. discussion 642-643; quiz N6. 2009.

75. Mahboobani NR, Chong WH, Lam SS, Siu JC, Tan CB, Wong YC. Treatment of intracranial aneurysms with flow re-direction endoluminal device - a single centre experience with short-term follow-up results. Neurointervention. 12:11–19. 2017.

76. Martínez-Galdámez M, Gil A, Caniego JL, Gonzalez E, Bárcena E, Perez S, et al. Preliminary experience with the pipeline flex embolization device: technical note. J Neurointerv Surg. 7:748–751. 2015.

77. Martínez-Galdámez M, Lamin SM, Lagios KG, Liebig T, Ciceri EF, Chapot R, et al. Treatment of intracranial aneurysms using the pipeline flex embolization device with shield technology: angiographic and safety outcomes at 1-year follow-up. J Neurointerv Surg. 11:396–399. 2019.

78. Martínez-Galdámez M, Pérez S, Vega A, Ruiz P, Caniego JL, Bárcena E, et al. Endovascular treatment of intracranial aneurysms using the pipeline flex embolization device: a case series of 30 consecutive patients. J Neurointerv Surg. 8:396–401. 2016.

79. Meckel S, McAuliffe W, Fiorella D, Taschner CA, Phatouros C, Phillips TJ, et al. Endovascular treatment of complex aneurysms at the vertebrobasilar junction with flow-diverting stents: initial experience. Neurosurgery. 73:386–394. 2013.

80. Meyers PM, Coon AL, Kan PT, Wakhloo AK, Hanel RA. SCENT trial. Stroke. 50:1473–1479. 2019.

81. Möhlenbruch MA, Herweh C, Jestaedt L, Stampfl S, Schönenberger S, Ringleb PA, et al. The FRED flow-diverter stent for intracranial aneurysms: clinical study to assess safety and efficacy. AJNR Am J Neuroradiol. 36:1155–1161. 2015.

82. Möhlenbruch MA, Kizilkilic O, Killer-Oberpfalzer M, Baltacioglu F, Islak C, Bendszus M, et al. Multicenter experience with FRED Jr flow redirection endoluminal device for intracranial aneurysms in small arteries. AJNR Am J Neuroradiol. 38:1959–1965. 2017.

83. Moret J, Cognard C, Weill A, Castaings L, Rey A. The “remodelling technique” in the treatment of wide neck intracranial aneurysms. angiographic results and clinical follow-up in 56 cases. Interv Neuroradiol. 3:21–35. 1997.

84. Murthy SB, Shah J, Mangat HS, Stieg P. Treatment of intracranial aneurysms with pipeline embolization device: newer applications and technical advances. Curr Treat Options Neurol. 18:16. 2016.

85. Nelson PK, Lylyk P, Szikora I, Wetzel SG, Wanke I, Fiorella D. The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol. 32:34–40. 2011.

86. Nossek E, Chalif DJ, Chakraborty S, Lombardo K, Black KS, Setton A. Concurrent use of the pipeline embolization device and coils for intracranial aneurysms: technique, safety, and efficacy. J Neurosurg. 122:904–911. 2015.

87. Park MS, Albuquerque FC, Nanaszko M, Sanborn MR, Moon K, Abla AA, et al. Critical assessment of complications associated with use of the pipeline embolization device. J Neurointerv Surg. 7:652–659. 2015.

88. Park MS, Kilburg C, Taussky P, Albuquerque FC, Kallmes DF, Levy EI, et al. Pipeline embolization device with or without adjunctive coil embolization: analysis of complications from the IntrePED registry. AJNR Am J Neuroradiol. 37:1127–1131. 2016.

89. Patel PD, Chalouhi N, Atallah E, Tjoumakaris S, Hasan D, Zarzour H, et al. Off-label uses of the Pipeline embolization device: a review of the literature. Neurosurg Focus. 42:E4. 2017.

90. Pereira VM, Kelly M, Vega P, Murias E, Yilmaz H, Erceg G, et al. New pipeline flex device: initial experience and technical nuances. J Neurointerv Surg. 7:920–925. 2015.

91. Petr O, Brinjikji W, Cloft H, Kallmes DF, Lanzino G. Current trends and results of endovascular treatment of unruptured intracranial aneurysms at a single institution in the flow-diverter era. AJNR Am J Neuroradiol. 37:1106–1113. 2016.

92. Petr O, Coufalová L, Bradáč O, Rehwald R, Glodny B, Beneš V. Safety and efficacy of surgical and endovascular treatment for distal anterior cerebral artery aneurysms: a systematic review and meta-analysis. World Neurosurg. 100:557–566. 2017.

93. Pierot L, Spelle L, Berge J, Januel AC, Herbreteau D, Aggour M, et al. Feasibility, complications, morbidity, and mortality results at 6 months for aneurysm treatment with the flow re-direction endoluminal device: report of SAFE study. J Neurointerv Surg. 10:765–770. 2018.

94. Pistocchi S, Blanc R, Bartolini B, Piotin M. Flow diverters at and beyond the level of the circle of willis for the treatment of intracranial aneurysms. Stroke. 43:1032–1038. 2012.

95. Potts MB, Shapiro M, Zumofen DW, Raz E, Nossek E, DeSousa KG, et al. Parent vessel occlusion after pipeline embolization of cerebral aneurysms of the anterior circulation. J Neurosurg. 127:1333–1341. 2017.

96. Puffer RC, Kallmes DF, Cloft HJ, Lanzino G. Patency of the ophthalmic artery after flow diversion treatment of paraclinoid aneurysms. J Neurosurg. 116:892–896. 2012.

97. Puffer RC, Piano M, Lanzino G, Valvassori L, Kallmes DF, Quilici L, et al. Treatment of cavernous sinus aneurysms with flow diversion: results in 44 patients. AJNR Am J Neuroradiol. 35:948–951. 2014.

98. Rajah G, Narayanan S, Rangel-Castilla L. Update on flow diverters for the endovascular management of cerebral aneurysms. Neurosurg Focus. 42:E2. 2017.

99. Rouchaud A, Brinjikji W, Cloft HJ, Kallmes DF. Endovascular treatment of ruptured blister-like aneurysms: a systematic review and meta-analysis with focus on deconstructive versus reconstructive and flow-diverter treatments. AJNR Am J Neuroradiol. 36:2331–2339. 2015.

100. Rouchaud A, Brinjikji W, Lanzino G, Cloft HJ, Kadirvel R, Kallmes DF. Delayed hemorrhagic complications after flow diversion for intracranial aneurysms: a literature overview. Neuroradiology. 58:171–177. 2016.

101. Saatci I, Yavuz K, Ozer C, Geyik S, Cekirge HS. Treatment of intracranial aneurysms using the pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol. 33:1436–1446. 2012.

102. Sadasivan C, Cesar L, Seong J, Rakian A, Hao Q, Tio FO, et al. An original flow diversion device for the treatment of intracranial aneurysms: evaluation in the rabbit elastase-induced model. Stroke. 40:952–958. 2009.

103. Sadasivan C, Fiorella D. Preliminary in vitro angiographic comparison of the flow diversion behavior of evolve and pipeline devices. J Neurointerv Surg. 2019; [Epub ahead of print].

104. Schievink WI, Wijdicks EF, Piepgras DG, Chu CP, O’Fallon WM, Whisnant JP. The poor prognosis of ruptured intracranial aneurysms of the posterior circulation. J Neurosurg. 82:791–795. 1995.

105. Shapiro M, Becske T, Sahlein D, Babb J, Nelson PK. Stent-supported aneurysm coiling: a literature survey of treatment and follow-up. AJNR Am J Neuroradiol. 33:159–163. 2012.

106. Siddiqui AH, Kan P, Abla AA, Hopkins LN, Levy EI. Complications after treatment with pipeline embolization for giant distal intracranial aneurysms with or without coil embolization. Neurosurgery. 71:E509–E513. discussion E513. 2012.

107. Sönmez Ö, Brinjikji W, Murad MH, Lanzino G. Deconstructive and reconstructive techniques in treatment of vertebrobasilar dissecting aneurysms: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 36:1293–1298. 2015.

108. Steinberg GK, Drake CG, Peerless SJ. Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms. Immediate results and long-term outcome in 201 patients. J Neurosurg. 79:161–173. 1993.

109. Sturiale CL, Brinjikji W, Murad MH, Cloft HJ, Kallmes DF, Lanzino G. Endovascular treatment of distal anterior cerebral artery aneurysms: singlecenter experience and a systematic review. AJNR Am J Neuroradiol. 34:2317–2320. 2013.

110. Tan LA, Keigher KM, Munich SA, Moftakhar R, Lopes DK. Thromboembolic complications with pipeline embolization device placement: impact of procedure time, number of stents and pre-procedure P2Y12 reaction unit (PRU) value. J Neurointerv Surg. 7:217–221. 2015.

111. Tanweer O, Raz E, Brunswick A, Zumofen D, Shapiro M, Riina HA, et al. Cavernous carotid aneurysms in the era of flow diversion: a need to revisit treatment paradigms. AJNR Am J Neuroradiol. 35:2334–2340. 2014.

112. Taschner CA, Vedantham S, de Vries J, Biondi A, Boogaarts J, Sakai N, et al. Surpass flow diverter for treatment of posterior circulation aneurysms. AJNR Am J Neuroradiol. 38:582–589. 2017.

113. Texakalidis P, Bekelis K, Atallah E, Tjoumakaris S, Rosenwasser RH, Jabbour P. Flow diversion with the pipeline embolization device for patients with intracranial aneurysms and antiplatelet therapy: a systematic literature review. Clin Neurol Neurosurg. 161:78–87. 2017.

114. U.S. Food and Drug Administration; Instructions for Use (IFU). PipelineTM Embolization Device. Available at : https://www.accessdata.fda.gov/cdrh_docs/pdf10/P100018c.pdf.

115. U.S. Food and Drug Administration. Surpass Streamline Flow Diverter - P170024. Available at : https://www.fda.gov/medical-devices/recently-approved-devices/surpass-streamline-flow-diverter-p170024.

116. U.S. Food and Drug Administration. Pipeline Flex Embolization Device - P100018/S015. Available at : https://www.fda.gov/medicaldevices/recently-approved-devices/pipeline-flex-embolization-devicep100018s015.

117. van Rooij WJ, Sluzewski M. Endovascular treatment of large and giant aneurysms. AJNR Am J Neuroradiol. 30:12–18. 2009.

118. 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. 76:173–178. discussion 178. 2015.

119. Velioglu M, Kizilkilic O, Selcuk H, Kocak B, Tureci E, Islak C, et al. Early and midterm results of complex cerebral aneurysms treated with silk stent. Neuroradiology. 54:1355–1365. 2012.

120. Yan Y, Zhu D, Tang H, Huang Q. Safety and efficacy of flow diverter treatment for aneurysm in small cerebral vessels: a systematic review and meta-analysis. World Neurosurgery. 115:54–64. 2018.

121. Yao X, Ma J, Li H, Shen H, Lu X, Chen G. Safety and efficiency of flow diverters for treating small intracranial aneurysms: a systematic review and meta-analysis. J Int Med Res. 45:11–21. 2017.

122. Zhou G, Su M, Yin YL, Li MH. Complications associated with the use of flow-diverting devices for cerebral aneurysms: a systematic review and meta-analysis. Neurosurg Focus. 42:E17. 2017.