Abstract
The progressive establishment of endovascular management in treating intracranial aneurysms had lead to continuous technique advancements and development of innovative technologies. Flow diverters are “stent-like” devices currently used for complex unruptured aneurysms allowing endoluminal reconstruction of the parent artery and occlusion of the aneurysm sac. In the present article, we review the development of flow diversion devices through in vitro and in vivo studies to clinical practice and summarize recent clinical data.
About the authors
Alice Venier took her high school diploma in humanistic studies with high honors in 2008. She graduated in Medicine and Surgery at Vita-Salute San Raffaele University (Milan, Italy) in July 2014 with Summa cum Laude and distinction. She spent 2 months as a research attendee in the Neurologic Surgery Department at Mayo Clinic Hospital in Rochester, MN, USA.
Beatrice Gardenghi took her high school diploma in scientific studies with laude in 2008. She graduated in Medicine and Surgery at Alma Mater Studiorum of Bologna (Italy) in June 2014 with Summa cum Laude. She spent three months as a research attendee in the Neurologic Surgery Department at Mayo Clinic Hospital in Rochester, MN, USA.
Giuseppe Lanzino graduated summa cum laude from the University of Bologna Medical School. Dr. Lanzino specializes in the endovascular and surgical treatment of patients with cerebrovascular disorders. He completed his neurosurgical training at the University of Virginia in Charlottesville, VA, USA. In addition, he has completed subspecialized training in neuroendovascular surgery at the State University of Buffalo, NY, USA and cerebrovascular and skull-based surgery fellowship at the Barrow Neurological Institute in Phoenix, AZ, USA. He has authored or coauthored more than 100 peer review publications, and he is the author of two textbooks.
Stylianos K. Rammos is a neurosurgeon currently practicing at the Arkansas Neuroscience Institute in Little Rock, AR, USA. Dr. Rammos completed his residency at the University of Illinois College of Medicine at Peoria, IL, USA. He completed fellowships in open cerebrovascular and endovascular neurosurgery at the Arkansas Neuroscience Institute under Ali Krisht, MD and at the University of Illinois at Chicago, IL, USA, respectively.
Conflict of interest statement: Authors state Dr. Lanzino is the Consultant for Covidien. All authors have read the journal’s publication ethics and publication malpractice statement available at the journal’s website and hereby confirm that they comply with all its parts applicable to the present scientific work.
References
[1] Alderazi YJ, Shastri D, Kass-Hout T, Prestigiacomo CJ, Gandhi CD. Flow diverters for intracranial aneurysms. Stroke Res Treat. 2014;2014:415653.10.1155/2014/415653Search in Google Scholar PubMed PubMed Central
[2] Alshafai N, Cusimano MD, Falenchuk O. Global differences in the present and future management of cerebral aneurysms. World Neurosurg. 2013;80:717−22.10.1016/j.wneu.2013.01.092Search in Google Scholar PubMed
[3] Arrese I, Sarabia R, Pintado R, Delgado-Rodriguez M. Flow-diverter devices for intracranial aneurysms: systematic review and meta-analysis. Neurosurgery. 2013;73:193−9; discussion 9–200.10.1227/01.neu.0000430297.17961.f1Search in Google Scholar PubMed
[4] Augsburger L, Farhat M, Reymond P, Fonck E, Kulcsar Z, Stergiopulos N, et al. Effect of flow diverter porosity on intraaneurysmal blood flow. Klin Neuroradiol. 2009;19:204−14.10.1007/s00062-009-9005-0Search in Google Scholar PubMed
[5] 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. 2013;267:858−68.10.1148/radiol.13120099Search in Google Scholar PubMed
[6] 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. Am J Neuroradiol. 2012;33:1150−5.10.3174/ajnr.A2907Search in Google Scholar PubMed PubMed Central
[7] Briganti F, Napoli M, Leone G, Marseglia M, Mariniello G, Gabrillargues J, et al. Treatment of intracranial aneurysms by flow diverter devices: long-term results from a single center. Eur J Radiol. 2014;83:1683−90.10.1016/j.ejrad.2014.05.029Search in Google Scholar PubMed
[8] Briganti F, Napoli M, Tortora F, Solari D, Bergui M, Boccardi E, et al. Italian multicenter experience with flow-diverter devices for intracranial unruptured aneurysm treatment with periprocedural complications–a retrospective data analysis. Neuroradiol. 2012;54:1145−52.10.1007/s00234-012-1071-3Search in Google Scholar
[9] Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke. 2013;44:442−7.10.1161/STROKEAHA.112.678151Search in Google Scholar PubMed
[10] Burrows AM, Cloft H, Kallmes DF, Lanzino G. Periprocedural and mid-term technical and clinical events after flow diversion for intracranial aneurysms. J Neurointerv Surg. 2015;7:646−51.10.1136/neurintsurg-2014-011184Search in Google Scholar PubMed
[11] 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. 2010;5:pii: e12492.10.1371/journal.pone.0012492Search in Google Scholar PubMed PubMed Central
[12] Chalouhi N, Starke RM, Koltz MT, Jabbour PM, Tjoumakaris SI, Dumont AS, et al. Stent-assisted coiling versus balloon remodeling of wide-neck aneurysms: comparison of angiographic outcomes. Am J Neuroradiol. 2013;34:1987−92.10.3174/ajnr.A3538Search in Google Scholar PubMed PubMed Central
[13] 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;45:54−8.10.1161/STROKEAHA.113.003038Search in Google Scholar PubMed
[14] Chitale R, Chalouhi N, Theofanis T, Starke RM, Amenta P, Jabbour P, et al. Treatment of ruptured intracranial aneurysms: comparison of stenting and balloon remodeling. Neurosurgery. 2013;72:953−9.10.1227/NEU.0b013e31828ecf69Search in Google Scholar PubMed
[15] Chung B, Mut F, Kadirvel R, Lingineni R, Kallmes DF, Cebral JR. Hemodynamic analysis of fast and slow aneurysm occlusions by flow diversion in rabbits. J Neurointervent Surg. 2014. pii: neurintsurg-2014-011412. Doi: 10.1136/neurintsurg-2014-011412. [Epub ahead of print].10.1136/neurintsurg-2014-011412Search in Google Scholar PubMed PubMed Central
[16] Cinar C, Bozkaya H, Oran I. Endovascular treatment of cranial aneurysms with the pipeline flow-diverting stent: preliminary mid-term results. Diagn Intervent Radiol. 2013;19:154−64.10.4261/1305-3825.DIR.6111-12.1Search in Google Scholar PubMed
[17] Clarencon F, Di Maria F, Biondi A, Chiras J, Sourour NA. Distant and delayed (>7 days) hemorrhage after treatment by flow-diverter stents in intracranial aneurysms: a rare but potentially serious complication. Am J Neuroradiol. 2013;34:E81−2.10.3174/ajnr.A3597Search in Google Scholar PubMed PubMed Central
[18] Colby GP, Lin LM, Coon AL. Revisiting the risk of intraparenchymal hemorrhage following aneurysm treatment by flow diversion. Am J Neuroradiol. 2012;33:E107; author reply E8.10.3174/ajnr.A3201Search in Google Scholar PubMed PubMed Central
[19] 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 Neurointervent Surg. 2013;5:237−46.10.1136/neurintsurg-2012-010299Search in Google Scholar PubMed
[20] Consoli A, Vignoli C, Renieri L, Rosi A, Chiarotti I, Nappini S, et al. Assisted coiling of saccular wide-necked unruptured intracranial aneurysms: stent versus balloon. J Neurointervent Surg. 2014.10.1136/neurintsurg-2014-011466Search in Google Scholar PubMed
[21] 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. Am J Neuroradiol. 2012;33:603−8.10.3174/ajnr.A3065Search in Google Scholar PubMed PubMed Central
[22] D’Urso PI, Lanzino G, Cloft HJ, Kallmes DF. Flow diversion for intracranial aneurysms: a review. Stroke. 2011;42:2363−8.10.1161/STROKEAHA.111.620328Search in Google Scholar PubMed
[23] Darsaut TE, Bing F, Makoyeva A, Gevry G, Salazkin I, Raymond J. Flow diversion to treat aneurysms: the free segment of stent. J Neurointervent Surg. 2013;5:452−7.10.1136/neurintsurg-2012-010451Search in Google Scholar PubMed
[24] Darsaut TE, Jack AS, Kerr RS, Raymond J. International Subarachnoid Aneurysm Trial -– ISAT part II: study protocol for a randomized controlled trial. Trials. 2013;14:156.10.1186/1745-6215-14-156Search in Google Scholar PubMed PubMed Central
[25] 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. 2013;44:1567−77.10.1161/STROKEAHA.111.000434Search in Google Scholar PubMed
[26] Deutschmann HA, Wehrschuetz M, Augustin M, Niederkorn K, Klein GE. Long-term follow-up after treatment of intracranial aneurysms with the pipeline embolization device: results from a single center. Am J Neuroradiol. 2012;33:481−6.10.3174/ajnr.A2790Search in Google Scholar PubMed PubMed Central
[27] Fargen KM, Hoh BL. Flow diversion technologies in evolution: a review of the first 4 generations of flow diversion devices. World Neurosurg. 2014;81:452−3.10.1016/j.wneu.2014.01.008Search in Google Scholar PubMed
[28] Fargen KM, Velat GJ, Lawson MF, Mocco J, Hoh BL. Review of reported complications associated with the pipeline embolization device. World Neurosurg. 2012;77:403−4.10.1016/j.wneu.2012.02.038Search in Google Scholar PubMed
[29] Farzin B, Brosseau L, Jamali S, Salazkin I, Jack A, Darsaut TE, et al. Flow diverters: inter and intra-rater reliability of porosity and pore density measurements. J Neurointerv Surg. 2015;7:734−9.10.1136/neurintsurg-2014-011240Search in Google Scholar PubMed
[30] Fischer S, Vajda Z, Aguilar Perez M, Schmid E, Hopf N, Bäzner H, et al. Pipeline embolization device (PED) for neurovascular reconstruction: initial experience in the treatment of 101 intracranial aneurysms and dissections. Neuroradiology. 2012;54:369−82.10.1007/s00234-011-0948-xSearch in Google Scholar PubMed PubMed Central
[31] Gentric JC, Darsaut TE, Makoyeva A, Salazkin I, Raymond J. The success of flow diversion in large and giant sidewall aneurysms may depend on the size of the defect in the parent artery. Am J Neuroradiol. 2014;35:2119−24.10.3174/ajnr.A4010Search in Google Scholar PubMed PubMed Central
[32] Gross BA, Frerichs KU. Stent usage in the treatment of intracranial aneurysms: past, present and future. J Neurol Neurosurg Psychiatry. 2013;84:244−53.10.1136/jnnp-2011-302007Search in Google Scholar PubMed
[33] Hodis S, Ding YH, Dai D, Lingineni R, Mut F, Cebral J, et al. Relationship between aneurysm occlusion and flow diverting device oversizing in a rabbit model. J Neurointerv Surg. 2014. Doi: 10.1136/neurintsurg-2014-011487.10.1136/neurintsurg-2014-011487Search in Google Scholar PubMed PubMed Central
[34] Hu YC, Deshmukh VR, Albuquerque FC, Fiorella D, Nixon RR, Heck DV, et al. Histopathological assessment of fatal ipsilateral intraparenchymal hemorrhages after the treatment of supraclinoid aneurysms with the Pipeline Embolization Device. J Neurosurg. 2014;120:365−74.10.3171/2013.11.JNS131599Search in Google Scholar PubMed
[35] Kim M, Taulbee DB, Tremmel M, Meng H. Comparison of two stents in modifying cerebral aneurysm hemodynamics. Ann Biomed Eng. 2008;36:726−41.10.1007/s10439-008-9449-4Search in Google Scholar PubMed PubMed Central
[36] Kim YH, Xu X, Lee JS. The effect of stent porosity and strut shape on saccular aneurysm and its numerical analysis with lattice Boltzmann method. Ann Biomed Eng. 2010;38:2274−92.10.1007/s10439-010-9994-5Search in Google Scholar PubMed
[37] Kocer N, Islak C, Kizilkilic O, Kocak B, Saglam M, Tureci E. Flow re-direction endoluminal device in treatment of cerebral aneurysms: initial experience with short-term follow-up results. J Neurosurg. 2014;120:1158−71.10.3171/2014.1.JNS131442Search in Google Scholar PubMed
[38] Lanzino G, Kanaan Y, Perrini P, Dayoub H, Fraser K. Emerging concepts in the treatment of intracranial aneurysms: stents, coated coils, and liquid embolic agents. Neurosurgery. 2005;57:449−59; discussion 59.10.1227/01.NEU.0000170538.74899.7FSearch in Google Scholar
[39] Lanzino G, Wakhloo AK, Fessler RD, Hartney ML, Guterman LR, Hopkins LN. Efficacy and current limitations of intravascular stents for intracranial internal carotid, vertebral, and basilar artery aneurysms. J Neurosurg. 1999;91:538−46.10.3171/jns.1999.91.4.0538Search in Google Scholar PubMed
[40] Lieber BB, Livescu V, Hopkins LN, Wakhloo AK. Particle image velocimetry assessment of stent design influence on intra-aneurysmal flow. Ann Biomed Eng. 2002;30:768−77.10.1114/1.1495867Search in Google Scholar PubMed
[41] Lieber BB, Stancampiano AP, Wakhloo AK. Alteration of hemodynamics in aneurysm models by stenting: influence of stent porosity. Ann Biomed Eng. 1997;25:460−9.10.1007/BF02684187Search in Google Scholar PubMed
[42] 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 Neurointervent Surg. 2014.10.1136/neurintsurg-2014-011320Search in Google Scholar PubMed
[43] Liou TM, Liou SN, Chu KL. Intra-aneurysmal flow with helix and mesh stent placement across side-wall aneurysm pore of a straight parent vessel. J Biomech Eng. 2004;126:36−43.10.1115/1.1644566Search in Google Scholar PubMed
[44] Lubicz B, Collignon L, Raphaeli G, De Witte O. Pipeline flow-diverter stent for endovascular treatment of intracranial aneurysms: preliminary experience in 20 patients with 27 aneurysms. World Neurosurg. 2011;76:114−19.10.1016/j.wneu.2011.02.015Search in Google Scholar PubMed
[45] Lubicz B, Collignon L, Raphaeli G, Pruvo JP, Bruneau M, De Witte O, et al. Flow-diverter stent for the endovascular treatment of intracranial aneurysms: a prospective study in 29 patients with 34 aneurysms. Stroke. 2010;41:2247−53.10.1161/STROKEAHA.110.589911Search in Google Scholar PubMed
[46] Martinez-Galdamez M, Gil A, Caniego JL, Gonzalez E, Barcena E, Perez S, et al. Preliminary experience with the pipeline flex embolization device: technical note. J Neurointerv Surg. 2015;7:748−51.10.1136/neurintsurg-2014-011385Search in Google Scholar PubMed
[47] Martinez-Galdamez M, Romance A, Vega P, Vega A, Caniego JL, Paul L, et al. Pipeline endovascular device for the treatment of intracranial aneurysms at the level of the circle of Willis and beyond: multicenter experience. J Neurointerv Surg. 2015;7:816−23.10.1136/neurintsurg-2014-011355Search in Google Scholar PubMed
[48] Matouk CC, Kaderali Z, terBrugge KG, Willinsky RA. Long-term clinical and imaging follow-up of complex intracranial aneurysms treated by endovascular parent vessel occlusion. Am J Neuroradiol. 2012;33:1991−7.10.3174/ajnr.A3079Search in Google Scholar PubMed PubMed Central
[49] Meng H, Wang Z, Kim M, Ecker RD, Hopkins LN. Saccular aneurysms on straight and curved vessels are subject to different hemodynamics: implications of intravascular stenting. Am J Neuroradiol. 2006;27:1861−5.Search in Google Scholar
[50] Murthy SB, Shah S, Shastri A, Venkatasubba Rao CP, Bershad EM, Suarez JI. The SILK flow diverter in the treatment of intracranial aneurysms. J Clin Neurosci. 2014;21:203−6.10.1016/j.jocn.2013.07.006Search in Google Scholar PubMed
[51] Murthy SB, Shah S, Venkatasubba Rao CP, Bershad EM, Suarez JI. Treatment of unruptured intracranial aneurysms with the pipeline embolization device. J Clin Neurosci. 2014;21:6−11.10.1016/j.jocn.2013.03.014Search in Google Scholar PubMed
[52] Naggara ON, Lecler A, Oppenheim C, Meder JF, Raymond J. Endovascular treatment of intracranial unruptured aneurysms: a systematic review of the literature on safety with emphasis on subgroup analyses. Radiology. 2012;263:828−35.10.1148/radiol.12112114Search in Google Scholar PubMed
[53] Nelson PK, Lylyk P, Szikora I, Wetzel SG, Wanke I, Fiorella D. The pipeline embolization device for the intracranial treatment of aneurysms trial. Am J Neuroradiol. 2011;32:34−40.10.3174/ajnr.A2421Search in Google Scholar PubMed PubMed Central
[54] 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;118:408−16.10.3171/2012.10.JNS112222Search in Google Scholar PubMed
[55] Pierot L, Wakhloo AK. Endovascular treatment of intracranial aneurysms: current status. Stroke. 2013;44:2046−54.10.1161/STROKEAHA.113.000733Search in Google Scholar PubMed
[56] Piotin M, Blanc R. Balloons and stents in the endovascular treatment of cerebral aneurysms: vascular anatomy remodeled. Front Neurol. 2014;5:41.10.3389/fneur.2014.00041Search in Google Scholar PubMed PubMed Central
[57] Puffer RC, Kallmes DF, Cloft HJ, Lanzino G. Patency of the ophthalmic artery after flow diversion treatment of paraclinoid aneurysms. J Neurosurg. 2012;116:892−6.10.3171/2011.11.JNS111612Search in Google Scholar PubMed
[58] Raymond J, Darsaut TE, Guilbert F, Weill A, Roy D. Flow diversion in aneurysms trial: the design of the FIAT study. Intervent Neuroradiol. 2011;17:147−53.10.1177/159101991101700202Search in Google Scholar PubMed PubMed Central
[59] Ringelstein A, Schlamann M, Goericke SL, Monninghoff C, Sandalcioglu IE, El Hindy N, et al. [3-year follow-up after endovascular aneurysm treatment with Silk(R) flow diverter]. RoFo. 2013;185:328−32.10.1055/s-0032-1330353Search in Google Scholar PubMed
[60] 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. Am J Neuroradiol. 2012;33:1436−46.10.3174/ajnr.A3246Search in Google Scholar PubMed PubMed Central
[61] Shankar JJ, Vandorpe R, Pickett G, Maloney W. SILK flow diverter for treatment of intracranial aneurysms: initial experience and cost analysis. J Neurointervent Surg. 2013;5:iii11-5.10.1136/neurintsurg-2012-010590Search in Google Scholar PubMed
[62] Taussky P, Tawk RG, Miller DA, Freeman WD, Hanel RA. New therapies for unruptured intracranial aneurysms. Neurol Clin. 2013;31:737−47.10.1016/j.ncl.2013.03.011Search in Google Scholar PubMed
[63] Trager AL, Sadasivan C, Seong J, Lieber BB. Correlation between angiographic and particle image velocimetry quantifications of flow diverters in an in vitro model of elastase-induced rabbit aneurysms. J Biomech Eng. 2009;131:034506.10.1115/1.3049528Search in Google Scholar PubMed PubMed Central
[64] Turk AS, 3rd, Martin RH, Fiorella D, Mocco J, Siddiqui A, Bonafe A. Flow diversion versus traditional endovascular coiling therapy: design of the prospective LARGE aneurysm randomized trial. Am J Neuroradiol. 2014;35:1341−5.10.3174/ajnr.A3968Search in Google Scholar PubMed PubMed Central
[65] van Rooij WJ, Bechan RS, Peluso JP, Sluzewski M. Endovascular treatment of intracranial aneurysms in the flow diverter era: frequency of use and results in a consecutive series of 550 treatments in a single centre. Intervent Neuroradiol. 2014;20:428−35.10.15274/INR-2014-10047Search in Google Scholar PubMed PubMed Central
[66] Wagner A, Cortsen M, Hauerberg J, Romner B, Wagner MP. Treatment of intracranial aneurysms. Reconstruction of the parent artery with flow-diverting (Silk) stent. Neuroradiology. 2012;54:709−18.10.1007/s00234-011-0949-9Search in Google Scholar PubMed
[67] Wakhloo AK, Lylyk P, de Vries J, Taschner C, Lundquist J, Biondi A, et al. Surpass flow diverter in the treatment of intracranial aneurysms: a prospective multicenter study. Am J Neuroradiol. 2015;36:98−107.10.3174/ajnr.A4078Search in Google Scholar PubMed PubMed Central
[68] Wakhloo AK, Schellhammer F, de Vries J, Haberstroh J, Schumacher M. Self-expanding and balloon-expandable stents in the treatment of carotid aneurysms: an experimental study in a canine model. Am J Neuroradiol. 1994;15:493−502.Search in Google Scholar
[69] Wong GK, Kwan MC, Ng RY, Yu SC, Poon WS. Flow diverters for treatment of intracranial aneurysms: current status and ongoing clinical trials. J Clin Neurosci. 2011;18:737−40.10.1016/j.jocn.2010.10.011Search in Google Scholar PubMed
The authors stated that there are no conflicts of interest regarding the publication of this article.
©2015 by De Gruyter
