Skip to main content
SpringerLink
Log in

Progressive Occlusion of Small Saccular Aneurysms Incompletely Occluded After Stent-Assisted Coil Embolization

Analysis of Related Factors and Long-Term Outcomes

  • Original Article
  • Published:
Clinical Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Incompletely occluded aneurysms after coil embolization are subject to recanalization but occasionally progress to a totally occluded state. Deployed stents may actually promote thrombosis of coiled aneurysms. We evaluated outcomes of small aneurysms (<10 mm) wherein saccular filling with contrast medium was evident after stent-assisted coiling, assessing factors implicated in subsequent progressive occlusion.

Methods

Between September 2012 and June 2016, a total of 463 intracranial aneurysms were treated by stent-assisted coil embolization. Of these, 132 small saccular aneurysms displayed saccular filling with contrast medium in the immediate aftermath of coiling. Progressive thrombosis was defined as complete aneurysmal occlusion at the 6‑month follow-up point. Rates of progressive occlusion and factors predisposing to this were analyzed via binary logistic regression.

Results

In 101 (76.5%) of the 132 intracranial aneurysms, complete occlusion was observed in follow-up imaging studies at 6 months. Binary logistic regression analysis indicated that progressive occlusion was linked to smaller neck diameter (odds ratio [OR] = 1.533; p = 0.003), hyperlipidemia (OR = 3.329; p = 0.036) and stent type (p = 0.031). The LVIS stent is especially susceptible to progressive thrombosis, more so than Neuroform (OR = 0.098; p = 0.008) or Enterprise (OR = 0.317; p = 0.098) stents. In 57 instances of progressive thrombosis, followed for ≥12 months (mean 25.0 ± 10.7 months), 56 (98.2%) were stable, with minor recanalization noted once (1.8%) and no major recanalization.

Conclusion

Aneurysms associated with smaller diameter necks, hyperlipidemic states and LVIS stent deployment may be inclined to possible thrombosis, if occlusion immediately after stent-assisted coil embolization is incomplete. In such instances, excellent long-term durability is anticipated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Cho YD, Jeon JP, Rhim JK, Park JJ, Yoo RE, Kang HS, Kim JE, Cho WS, Han MH. Progressive thrombosis of small saccular aneurysms filled with contrast immediately after coil embolization: analysis of related factors and long-term follow-up. Neuroradiology. 2015;57:615–23.

    Article  Google Scholar 

  2. Park W, Song Y, Park KJ, Koo HW, Yang K, Suh DC. Hemodynamic characteristics regarding recanalization of completely coiled aneurysms: computational fluid dynamic analysis using virtual models comparison. Neurointervention. 2016;11(1):30–6.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Spiotta AM, Miranpuri A, Chaudry MI, Turner RD 4th, Turk AS. Combined balloon stent technique with the Scepter C balloon and low-profile visualized intraluminal stent for the treatment of intracranial aneurysms. J Neurointerv Surg. 2013;5(Suppl 3):iii82–iii79.

    Article  Google Scholar 

  4. Wanke I, Forsting M. Stents for intracranial wide-necked aneurysms: more than mechanical protection. Neuroradiology. 2008;50:991–8.

    Article  Google Scholar 

  5. Aenis M, Stancampiano AP, Wakhloo AK, Lieber BB. Modeling of flow in a straight stented and nonstented side wall aneurysm model. J Biomech Eng. 1997;119:206–12.

    Article  CAS  Google Scholar 

  6. Phatouros CC, Sasaki TY, Higashida RT, Malek AM, Meyers PM, Dowd CF, Halbach VV. Stent-supported coil embolization: the treatment of fusiform and wide-neck aneurysms and pseudoaneurysms. Neurosurgery. 2000;47:107–13.

    CAS  PubMed  Google Scholar 

  7. Park KY, Kim BM, Kim DJ. Comparison between balloon-assisted and stent-assisted technique for treatment of unruptured internal carotid artery aneurysms. Neurointervention. 2016;11:99–104.

    Article  Google Scholar 

  8. Liu H, Choe J, Jung SC, Song Y, Yang KH, Park KJ, Goo HW, Park WH, Suh DC. Does a low-wall coverage stent have a flow diverting effect in small aneurysms? Neurointervention. 2015;10:89–93.

    Article  Google Scholar 

  9. Ingebrigtsen T, Morgan MK, Faulder K, Ingebrigtsen L, Sparr T, Schirmer H. Bifurcation geometry and the presence of cerebral artery aneurysms. J Neurosurg. 2004;101:108–13.

    Article  Google Scholar 

  10. Cho YD, Lee WJ, Kim KM, Kang HS, Kim JE, Han MH. Endovascular coil embolization of middle cerebral artery aneurysms of the proximal (M1) segment. Neuroradiology. 2013;55:1097–102.

    Article  Google Scholar 

  11. Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32:1998–2004.

    Article  CAS  Google Scholar 

  12. Gonzalez N, Murayama Y, Nien YL, Martin N, Frazee J, Duckwiler G, Jahan R, Gobin YP, Viñuela F. Treatment of unruptured aneurysms with GDCs: clinical experience with 247 aneurysms. AJNR Am J Neuroradiol. 2004;25:577–83.

    PubMed  Google Scholar 

  13. Murayama Y, Nien YL, Duckwiler G, Gobin YP, Jahan R, Frazee J, Martin N, Viñuela F. Guglielmi detachable coil embolization of cerebral aneurysms: 11 years’ experience. J Neurosurg. 2003;98:959–66.

    Article  Google Scholar 

  14. Murayama Y, Viñuela F, Tateshima S, Song JK, Gonzalez NR, Wallace MP. Bioabsorbable polymeric material coils for embolization of intracranial aneurysms: a preliminary experimental study. J Neurosurg. 2001;94:454–63.

    Article  CAS  Google Scholar 

  15. Ng P, Khangure MS, Phatouros CC, Bynevelt M, ApSimon H, McAuliffe W. Endovascular treatment of intracranial aneurysms with Guglielmi detachable coils: analysis of midterm angiographic and clinical outcomes. Stroke. 2002;33:210–7.

    Article  CAS  Google Scholar 

  16. Thornton J, Debrun GM, Aletich VA, Bashir Q, Charbel FT, Ausman J. Follow-up angiography of intracranial aneurysms treated with endovascular placement of Guglielmi detachable coils. Neurosurgery. 2002;50:239–49.

    PubMed  Google Scholar 

  17. Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, Lamoureux J, Chagnon M, Roy D. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34:1398–403.

    Article  Google Scholar 

  18. Gallas S, Pasco A, Cottier JP, Gabrillargues J, Drouineau J, Cognard C, Herbreteau D. A multicenter study of 705 ruptured intracranial aneurysms treated with Guglielmi detachable coils. AJNR Am J Neuroradiol. 2005;26:1723–31.

    PubMed  Google Scholar 

  19. Songsaeng D, Geibprasert S, ter Brugge KG, Willinsky R, Tymianski M, Krings T. Impact of individual intracranial arterial aneurysm morphology on initial obliteration and recurrence rates of endovascular treatments: a multivariate analysis. J Neurosurg. 2011;114:994–1002.

    Article  Google Scholar 

  20. Griessenauer CJ, Adeeb N, Foreman PM, Gupta R, Patel AS, Moore J, Abud TG, Thomas AJ, Ogilvy CS, Baccin CE. Impact of coil packing density and coiling technique on occlusion rates for aneurysms treated with stent-assisted coil embolization. World Neurosurg. 2016;94:157–66.

    Article  Google Scholar 

  21. Lee D, Yuki I, Murayama Y, Chiang A, Nishimura I, Vinters HV, Wang CJ, Nien YL, Ishil A, Wu BM, Viñuela F. Thrombus organization and healing in the swine experimental aneurysm model. Part I. A histological and molecular analysis. J Neurosurg. 2007;107:94–108.

    Article  CAS  Google Scholar 

  22. Clarke TA, Waskell LA. The metabolism of clopidogrel is catalyzed by human cytochrome P450 3A and is inhibited by atorvastatin. Drug Metab Dispos. 2003;31:53–9.

    Article  CAS  Google Scholar 

  23. Lau WC, Waskell LA, Watkins PB, Neer CJ, Horowitz K, Hopp AS, Tait AR, Carville DG, Guyer KE, Bates ER. Atorvastatin reduces the ability of clopidogrel to inhibit platelet aggregation: a new drug-drug interaction. Circulation. 2003;107:32–7.

    Article  CAS  Google Scholar 

  24. Neubauer H, Gunesdogan B, Hanefeld C, Spiecker M, Mugge A. Lipophilic statins interfere with the inhibitory effects of clopidogrel on platelet function – a flow cytometry study. Eur Heart J. 2003;24:1744–9.

    Article  CAS  Google Scholar 

  25. Mach F, Senouf D, Fontana P, Boehlen F, Reber G, Daali Y, de Moerloose P, Sigwart U. Not all statins interfere with clopidogrel during antiplatelet therapy. Eur J Clin Invest. 2005;35:476–81.

    Article  CAS  Google Scholar 

  26. Brophy JM, Babapulle MN, Costa V, Rinfret S. A pharmacoepidemiology study of the interaction between atorvastatin and clopidogrel after percutaneous coronary intervention. Am Heart J. 2006;152:263–9.

    Article  CAS  Google Scholar 

  27. Kang HS, Han MH, Kwon BJ, Jung C, Kim JE, Kwon OK, Oh CW. Is clopidogrel premedication useful to reduce thromboembolic events during coil embolization for unruptured intracranial aneurysms? Neurosurgery. 2010;67:1371–6.

    Article  Google Scholar 

  28. Saw J, Steinhubl SR, Berger PB, Kereiakes DJ, Serebruany VL, Brennan D, Topol EJ; Clopidogrel for the Reduction of Events During Observation Investigators. Lack of adverse clopidogrel-atorvastatin clinical interaction from secondary analysis of a randomized, placebo-controlled clopidogrel trial. Circulation. 2003;108:921–4.

    Article  CAS  Google Scholar 

  29. Saw J, Brennan DM, Steinhubl SR, Bhatt DL, Mak KH, Fox K, Topol EJ; CHARISMA Investigators. Lack of evidence of a clopidogrel-statin interaction in the CHARISMA trial. J Am Coll Cardiol. 2007;50:291–5.

    Article  CAS  Google Scholar 

  30. Lotfi A, Schweiger MJ, Giugliano GR, Murphy SA, Cannon CP, Investigators T. High-dose atorvastatin does not negatively influence clinical outcomes among clopidogrel treated acute coronary syndrome patients – a pravastatin or atorvastatin evaluation and infection therapy-thrombolysis in myocardial infarction 22 (PROVE IT-TIMI 22) analysis. Am Heart J. 2008;155:954–8.

    Article  CAS  Google Scholar 

  31. Phan K, Huo YR, Jia F, Phan S, Rao PJ, Mobbs RJ, Mortimer AM. Meta-analysis of stent-assisted coiling versus coiling-only for the treatment of intracranial aneurysms. J Clin Neurosci. 2016;31:15–22.

    Article  Google Scholar 

  32. Yao PF, Yu Y, Yang PF, Xu Y, Hong B, Zhao WY, Liu JM, Huang QH. Safety and long-term efficacy of endovascular treatment of small posterior communicating artery aneurysms by coiling with or without stent: a single center retrospective study. Clin Neurol Neurosurg. 2013;115:2502–7.

    Article  Google Scholar 

  33. Jeon JP, Cho YD, Rhim JK, Park JJ, Cho WS, Kang HS, Kim JE, Han MH. Effect of stenting on progressive occlusion of small unruptured saccular intracranial aneurysms with residual sac immediately after coil embolization: a propensity score analysis. J Neurointerv Surg. 2016;8:1025–9.

    Article  Google Scholar 

  34. Gu DQ, Zhang X, Luo B, Long XA, Duan CZ. The effect of Neuroform stent-assisted coil embolization of wide-necked intracranial aneurysms and clinical factors on progressive aneurysm occlusion on angiographic follow-up. J Clin Neurosci. 2013;20:244–7.

    Article  Google Scholar 

  35. Fiorella D, Albuquerque FC, Deshmukh VR, McDougall CG. Usefulness of the Neuroform stent for the treatment of cerebral aneurysms: results at initial (3–6-mo) follow-up. Neurosurgery. 2005;56:1191–201.

    Article  Google Scholar 

  36. Maldonado IL, Machi P, Costalat V, Mura T, Bonafe A. Neuroform stent-assisted coiling of unruptured intracranial aneurysms: short- and midterm results from a single-center experience with 68 patients. AJNR Am J Neuroradiol. 2011;32:131–6.

    Article  CAS  Google Scholar 

  37. Yahia AM, Latorre JG, Gordon V, Whapham J, Swarnkar A, Fessler RD. Progressive occlusion of aneurysms in neuroform stent-assisted treatment of intracranial aneurysms. J Neurol Neurosurg Psychiatr. 2011;82:278–82.

    Article  CAS  Google Scholar 

  38. Lubicz B, Bandeira A, Bruneau M, Dewindt A, Baleriaux D, De Witte O. Stenting is improving and stabilizing anatomical results of coiled intracranial aneurysms. Neuroradiology. 2009;51:419–25.

    Article  Google Scholar 

  39. Cho YD, Sohn CH, Kang HS, Kim JE, Cho WS, Hwang G, Kwon OK, Ko MS, Park NM, Han MH. Coil embolization of intracranial saccular aneurysms using the Low-profile Visualized Intraluminal Support (LVIS™) device. Neuroradiology. 2014;56:543–51.

    Article  Google Scholar 

  40. Durst CR, Khan P, Gaughen J, Patrie J, Starke RM, Conant P, Liu KC, Jensen ME, Evans AJ. Direct comparison of Neuroform and Enterprise stents in the treatment of wide-necked intracranial aneurysms. Clin Radiol. 2014;69:e471–e6.

    Article  CAS  Google Scholar 

  41. Ge H, Lv X, Yang X, He H, Jin H, Li Y. LVIS stent versus enterprise stent for the treatment of unruptured intracranial aneurysms. World Neurosurg. 2016;91:365–70.

    Article  Google Scholar 

  42. Wang C, Tian Z, Liu J, Jing L, Paliwal N, Wang S, Zhang Y, Xiang J, Siddiqui AH, Meng H, Yang X. Flow diverter effect of LVIS stent on cerebral aneurysm hemodynamics: a comparison with enterprise stents and the pipeline device. J Transl Med. 2016;14:199.

    Article  Google Scholar 

  43. Jeon JP, Cho YD, Rhim JK, Yoo DH, Kang HS, Kim JE, Cho WS, Han MH. Extended monitoring of coiled aneurysms completely occluded at 6‑month follow-up: late recanalization rate and related risk factors. Eur Radiol. 2016;26(10):3319–26.

    Article  Google Scholar 

  44. Jeon JP, Cho YD, Rhim JK, Yoo DH, Cho WS, Kang HS, Kim JE, Han MH. Fate of coiled aneurysms with minor recanalization at 6 months: rate of progression to further recanalization and related risk factors. AJNR Am J Neuroradiol. 2016;37:1490–5.

    Article  CAS  Google Scholar 

  45. Nakiri GS, Santos AC, Abud TG, Aragon DC, Colli BO, Abud DG. A comparison between magnetic resonance angiography at 3 teslas (time-of-flight and contrast-enhanced) and flat-panel digital subtraction angiography in the assessment of embolized brain aneurysms. Clinics (Sao Paulo). 2011;66:641–8.

    Article  Google Scholar 

  46. Ferré JC, Carsin-Nicol B, Morandi X, Carsin M, de Kersaint-Gilly A, Gauvrit JY, Desal HA. Time-of-flight mr angiography at 3t versus digital subtraction angiography in the imaging follow-up of 51 intracranial aneurysms treated with coils. Eur Radiol. 2009;72:365–9.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Chungnam National University Hospital, Chungnam National University College of Medicine, Daejeon, Korea (Republic of)

    Jeong Wook Lim

  2. Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine, 101 Daehak-ro, 03080, Jongno-gu, Seoul, Korea (Republic of)

    Jeongjun Lee & Young Dae Cho

Authors
  1. Jeong Wook Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeongjun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Young Dae Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young Dae Cho.

Ethics declarations

Conflict of interest

J.W. Lim, J. Lee and Y.D. Cho declare that they have no competing interests.

Caption Electronic Supplementary Material

62_2017_612_MOESM1_ESM.docx

Supplemental TABLE. Logistic regression model assessing the risk of progressive thrombosis in coiled aneurysms with stent

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lim, J.W., Lee, J. & Cho, Y.D. Progressive Occlusion of Small Saccular Aneurysms Incompletely Occluded After Stent-Assisted Coil Embolization. Clin Neuroradiol 28, 569–577 (2018). https://doi.org/10.1007/s00062-017-0612-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00062-017-0612-x

Keywords

Search

Navigation