Skip to main content
Top
Published in: Neuroradiology 4/2016

01-04-2016 | Interventional Neuroradiology

Testing flow diversion in animal models: a systematic review

Authors: Robert Fahed, Jean Raymond, Célina Ducroux, Jean-Christophe Gentric, Igor Salazkin, Daniela Ziegler, Guylaine Gevry, Tim E. Darsaut

Published in: Neuroradiology | Issue 4/2016

Login to get access

Abstract

Introduction

Flow diversion (FD) is increasingly used to treat intracranial aneurysms. We sought to systematically review published studies to assess the quality of reporting and summarize the results of FD in various animal models.

Methods

Databases were searched to retrieve all animal studies on FD from 2000 to 2015. Extracted data included species and aneurysm models, aneurysm and neck dimensions, type of flow diverter, occlusion rates, and complications. Articles were evaluated using a checklist derived from the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines.

Results

Forty-two articles reporting the results of FD in nine different aneurysm models were included. The rabbit elastase-induced aneurysm model was the most commonly used, with 3-month occlusion rates of 73.5 %, (95 %CI [61.9–82.6 %]). FD of surgical sidewall aneurysms, constructed in rabbits or canines, resulted in high occlusion rates (100 % [65.5–100 %]). FD resulted in modest occlusion rates (15.4 % [8.9–25.1 %]) when tested in six complex canine aneurysm models designed to reproduce more difficult clinical contexts (large necks, bifurcation, or fusiform aneurysms). Adverse events, including branch occlusion, were rarely reported. There were no hemorrhagic complications. Articles complied with 20.8 ± 3.9 of 41 ARRIVE items; only a small number used randomization (3/42 articles [7.1 %]) or a control group (13/42 articles [30.9 %]).

Conclusion

Preclinical studies on FD have shown various results. Occlusion of elastase-induced aneurysms was common after FD. The model is not challenging but standardized in many laboratories. Failures of FD can be reproduced in less standardized but more challenging surgical canine constructions. The quality of reporting could be improved.
Appendix
Available only for authorised users
Literature
1.
go back to reference Turjman F, Acevedo G, Moll T, Duquesnel J, Eloy R, Sindou M (1993) Treatment of experimental carotid aneurysms by endoprosthesis implantation: preliminary report. Neurol Res 15:181–184PubMed Turjman F, Acevedo G, Moll T, Duquesnel J, Eloy R, Sindou M (1993) Treatment of experimental carotid aneurysms by endoprosthesis implantation: preliminary report. Neurol Res 15:181–184PubMed
2.
go back to reference Geremia G, Haklin M, Brennecke L (1994) Embolization of experimentally created aneurysms with intravascular stent devices. AJNR Am J Neuroradiol 15:1223–1231PubMed Geremia G, Haklin M, Brennecke L (1994) Embolization of experimentally created aneurysms with intravascular stent devices. AJNR Am J Neuroradiol 15:1223–1231PubMed
5.
go back to reference Kulcsar Z, Houdart E, Bonafe A, Parker G, Millar J, Goddard AJ, Renowden S, Gál G, Turowski B, Mitchell K, Gray F, Rodriguez M, van den Berg R, Gruber A, Desal H, Wanke I, Rüfenacht DA (2011) Intra-aneurysmal thrombosis as a possible cause of delayed aneurysm rupture after flow-diversion treatment. AJNR Am J Neuroradiol 32:20–25. doi:10.3174/ajnr.A2370 CrossRefPubMed Kulcsar Z, Houdart E, Bonafe A, Parker G, Millar J, Goddard AJ, Renowden S, Gál G, Turowski B, Mitchell K, Gray F, Rodriguez M, van den Berg R, Gruber A, Desal H, Wanke I, Rüfenacht DA (2011) Intra-aneurysmal thrombosis as a possible cause of delayed aneurysm rupture after flow-diversion treatment. AJNR Am J Neuroradiol 32:20–25. doi:10.​3174/​ajnr.​A2370 CrossRefPubMed
6.
go back to reference Kulcsar Z, Ernemann U, Wetzel SG, Bock A, Goericke S, Panagiotopoulos V, Forsting M, Ruefenacht DA, Wanke I (2010) High-profile flow diverter (SILK) implantation in the basilar artery: efficacy in the treatment of aneurysms and the role of the perforators. Stroke 41:1690–1696. doi:10.1161/STROKEAHA.110.580308 CrossRefPubMed Kulcsar Z, Ernemann U, Wetzel SG, Bock A, Goericke S, Panagiotopoulos V, Forsting M, Ruefenacht DA, Wanke I (2010) High-profile flow diverter (SILK) implantation in the basilar artery: efficacy in the treatment of aneurysms and the role of the perforators. Stroke 41:1690–1696. doi:10.​1161/​STROKEAHA.​110.​580308 CrossRefPubMed
7.
go back to reference Turowski B, Macht S, Kulcsar Z, Hänggi D, Stummer W (2011) Early fatal hemorrhage after endovascular cerebral aneurysm treatment with a flow diverter (SILK-Stent): do we need to rethink our concepts? Neuroradiology 53:37–41. doi:10.1007/s00234-010-0676-7 CrossRefPubMed Turowski B, Macht S, Kulcsar Z, Hänggi D, Stummer W (2011) Early fatal hemorrhage after endovascular cerebral aneurysm treatment with a flow diverter (SILK-Stent): do we need to rethink our concepts? Neuroradiology 53:37–41. doi:10.​1007/​s00234-010-0676-7 CrossRefPubMed
8.
go back to reference Darsaut TE, Gentric JC, McDougall CM, Gevry G, Roy D, Weill A, Raymond J (2015) Uncertainty and agreement regarding the role of flow diversion in the management of difficult aneurysms. AJNR Am J Neuroradiol 36:930–936. doi:10.3174/ajnr.A4201 CrossRefPubMed Darsaut TE, Gentric JC, McDougall CM, Gevry G, Roy D, Weill A, Raymond J (2015) Uncertainty and agreement regarding the role of flow diversion in the management of difficult aneurysms. AJNR Am J Neuroradiol 36:930–936. doi:10.​3174/​ajnr.​A4201 CrossRefPubMed
11.
go back to reference Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefPubMed Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefPubMed
13.
14.
go back to reference Cumberland Consensus Working Group, Cheeran B, Cohen L, Dobkin B, Ford G, Greenwood R, Howard D, Husain M, Macleod M, Nudo R, Rothwell J, Rudd A, Teo J, Ward N, Wolf S (2009) The future of restorative neurosciences in stroke: driving the translational research pipeline from basic science to rehabilitation of people after stroke. Neurorehabil Neural Repair 23:97–107. doi:10.1177/1545968308326636 CrossRefPubMedCentral Cumberland Consensus Working Group, Cheeran B, Cohen L, Dobkin B, Ford G, Greenwood R, Howard D, Husain M, Macleod M, Nudo R, Rothwell J, Rudd A, Teo J, Ward N, Wolf S (2009) The future of restorative neurosciences in stroke: driving the translational research pipeline from basic science to rehabilitation of people after stroke. Neurorehabil Neural Repair 23:97–107. doi:10.​1177/​1545968308326636​ CrossRefPubMedCentral
15.
go back to reference Kaste M (2005) Use of animal models has not contributed to development of acute stroke therapies: pro. Stroke 36:2323–2324CrossRefPubMed Kaste M (2005) Use of animal models has not contributed to development of acute stroke therapies: pro. Stroke 36:2323–2324CrossRefPubMed
16.
go back to reference Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I, Reviewing Animal Trials Systematically (RATS) Group (2004) Where is the evidence that animal research benefits humans? BMJ 328:514–517CrossRefPubMedPubMedCentral Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I, Reviewing Animal Trials Systematically (RATS) Group (2004) Where is the evidence that animal research benefits humans? BMJ 328:514–517CrossRefPubMedPubMedCentral
20.
go back to reference Landis SC, Amara SG, Asadullah K, Austin CP, Blumenstein R, Bradley EW, Crystal RG, Darnell RB, Ferrante RJ, Fillit H, Finkelstein R, Fisher M, Gendelman HE, Golub RM, Goudreau JL, Gross RA, Gubitz AK, Hesterlee SE, Howells DW, Huguenard J, Kelner K, Koroshetz W, Krainc D, Lazic SE, Levine MS, Macleod MR, McCall JM, Moxley RT 3rd, Narasimhan K, Noble LJ, Perrin S, Porter JD, Steward O, Unger E, Utz U, Silberberg SD (2012) A call for transparent reporting to optimize the predictive value of preclinical research. Nature 490:187–191. doi:10.1038/nature11556 CrossRefPubMedPubMedCentral Landis SC, Amara SG, Asadullah K, Austin CP, Blumenstein R, Bradley EW, Crystal RG, Darnell RB, Ferrante RJ, Fillit H, Finkelstein R, Fisher M, Gendelman HE, Golub RM, Goudreau JL, Gross RA, Gubitz AK, Hesterlee SE, Howells DW, Huguenard J, Kelner K, Koroshetz W, Krainc D, Lazic SE, Levine MS, Macleod MR, McCall JM, Moxley RT 3rd, Narasimhan K, Noble LJ, Perrin S, Porter JD, Steward O, Unger E, Utz U, Silberberg SD (2012) A call for transparent reporting to optimize the predictive value of preclinical research. Nature 490:187–191. doi:10.​1038/​nature11556 CrossRefPubMedPubMedCentral
24.
go back to reference Kallmes DF, Helm GA, Hudson SB, Altes TA, Do HM, Mandell JW, Cloft HJ (1999) Histologic evaluation of platinum coil embolization in an aneurysm model in rabbits. Radiology 213:217–222CrossRefPubMed Kallmes DF, Helm GA, Hudson SB, Altes TA, Do HM, Mandell JW, Cloft HJ (1999) Histologic evaluation of platinum coil embolization in an aneurysm model in rabbits. Radiology 213:217–222CrossRefPubMed
25.
go back to reference Ding YH, Dai D, Lewis DA, Cloft HJ, Kallmes DF (2005) Angiographic and histologic analysis of experimental aneurysms embolized with platinum coils, Matrix, and HydroCoil. AJNR Am J Neuroradiol 26:1757–1763PubMed Ding YH, Dai D, Lewis DA, Cloft HJ, Kallmes DF (2005) Angiographic and histologic analysis of experimental aneurysms embolized with platinum coils, Matrix, and HydroCoil. AJNR Am J Neuroradiol 26:1757–1763PubMed
26.
go back to reference Hans FJ, Krings T, Moller-Hartmann W, Thiex R, Pfeffer J, Scherer K, Brunn A, Dreeskamp H, Stein KP, Meetz A, Gilsbach JM, Thron A (2003) Endovascular treatment of experimentally induced aneurysms in rabbits using stents: a feasibility study. Neuroradiology 45:430–434CrossRefPubMed Hans FJ, Krings T, Moller-Hartmann W, Thiex R, Pfeffer J, Scherer K, Brunn A, Dreeskamp H, Stein KP, Meetz A, Gilsbach JM, Thron A (2003) Endovascular treatment of experimentally induced aneurysms in rabbits using stents: a feasibility study. Neuroradiology 45:430–434CrossRefPubMed
27.
go back to reference Krings T, Hans FJ, Moller-Hartmann W, Brunn A, Thiex R, Schmitz-Rode T, Verken P, Scherer K, Dreeskamp H, Stein KP, Gilsbach J, Thron A (2005) Treatment of experimentally induced aneurysms with stents. Neurosurgery 56:1347–1359, discussion 1360CrossRefPubMed Krings T, Hans FJ, Moller-Hartmann W, Brunn A, Thiex R, Schmitz-Rode T, Verken P, Scherer K, Dreeskamp H, Stein KP, Gilsbach J, Thron A (2005) Treatment of experimentally induced aneurysms with stents. Neurosurgery 56:1347–1359, discussion 1360CrossRefPubMed
29.
go back to reference Cruz JP, Chow M, O’Kelly C, Marotta B, Spears J, Montanera W, Fiorella D, Marotta T (2012) Delayed ipsilateral parenchymal hemorrhage following flow diversion for the treatment of anterior circulation aneurysms. AJNR Am J Neuroradiol 33:603–608. doi:10.3174/ajnr.A3065 CrossRefPubMed Cruz JP, Chow M, O’Kelly C, Marotta B, Spears J, Montanera W, Fiorella D, Marotta T (2012) Delayed ipsilateral parenchymal hemorrhage following flow diversion for the treatment of anterior circulation aneurysms. AJNR Am J Neuroradiol 33:603–608. doi:10.​3174/​ajnr.​A3065 CrossRefPubMed
30.
go back to reference Raymond J, Darsaut TE, Kotowski M, Makoyeva A, Gevry G, Berthelet F, Salazkin I (2013) Thrombosis heralding aneurysmal rupture: an exploration of potential mechanisms in a novel giant swine aneurysm model. AJNR Am J Neuroradiol 34:346–353. doi:10.3174/ajnr.A3407 CrossRefPubMed Raymond J, Darsaut TE, Kotowski M, Makoyeva A, Gevry G, Berthelet F, Salazkin I (2013) Thrombosis heralding aneurysmal rupture: an exploration of potential mechanisms in a novel giant swine aneurysm model. AJNR Am J Neuroradiol 34:346–353. doi:10.​3174/​ajnr.​A3407 CrossRefPubMed
31.
go back to reference Siddiqui AH, Abla AA, Kan P, Dumont TM, Jahshan S, Britz GW, Hopkins LN, Levy EI (2012) Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. J Neurosurg 116:1258–1266. doi:10.3171/2012.2.JNS111942 CrossRefPubMed Siddiqui AH, Abla AA, Kan P, Dumont TM, Jahshan S, Britz GW, Hopkins LN, Levy EI (2012) Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. J Neurosurg 116:1258–1266. doi:10.​3171/​2012.​2.​JNS111942 CrossRefPubMed
32.
go back to reference Juni P, Holenstein F, Sterne J, Bartlett C, Egger M (2002) Direction and impact of language bias in meta-analyses of controlled trials: empirical study. Int J Epidemiol 31:115–123CrossRefPubMed Juni P, Holenstein F, Sterne J, Bartlett C, Egger M (2002) Direction and impact of language bias in meta-analyses of controlled trials: empirical study. Int J Epidemiol 31:115–123CrossRefPubMed
Metadata
Title
Testing flow diversion in animal models: a systematic review
Authors
Robert Fahed
Jean Raymond
Célina Ducroux
Jean-Christophe Gentric
Igor Salazkin
Daniela Ziegler
Guylaine Gevry
Tim E. Darsaut
Publication date
01-04-2016
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology / Issue 4/2016
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-015-1635-0

Other articles of this Issue 4/2016

Neuroradiology 4/2016 Go to the issue