Skip to main content

Advertisement

SpringerLink
Log in

Factors associated with the new appearance of cerebral microbleeds after endovascular treatment for unruptured intracranial aneurysms

  • Interventional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Endovascular treatment of unruptured intracranial aneurysms may increase cerebral microbleeds (CMBs) in postprocedural T2*-weighted MRIs, which may be a risk for future intracerebral hemorrhage. This study examined the characteristics of postprocedural CMBs and the factors that cause their increase.

Methods

The patients who underwent endovascular treatment for unruptured intracranial aneurysms from April 2016 to February 2018 were retrospectively analyzed. Treatment techniques for endovascular treatment included simple coiling, balloon-assisted coiling, stent-assisted coiling, or flow diverter placement. To evaluate the increase in CMBs, a head MRI including diffusion-weighted imaging and T2*-weighted MRIs was performed on the preprocedural day; the first postprocedural day; and at 1, 3, and 6 months after the procedure.

Results

Among the 101 aneurysms that were analyzed, 38 (37.6%) showed the appearance of new CMBs. In the multivariate analysis examining the causes of the CMB increases, chronic kidney disease, a higher number of preprocedural CMBs, and a higher number of diffusion-weighted imaging–positive lesions on the first postprocedural day were independent risk factors. Furthermore, a greater portion of the increased CMBs was found in cortical and subcortical lesions of the treated vascular perfusion area within 1 month after the procedure.

Conclusion

In endovascular treatment for unruptured intracranial aneurysms, CMBs tended to increase in patients with small vessel disease before the procedure, and it was also implicated in hemorrhagic changes after periprocedural microinfarction.

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

Similar content being viewed by others

Data availability

The datasets during and/or analyzed during the current study available from the corresponding author on reasonable request.

References

  1. 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. https://doi.org/10.3174/ajnr.A3065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kayan Y, Delgado Almandoz JE, Fease JL, Tran K, Milner AM, Scholz JM (2016) Incidence of delayed ipsilateral intraparenchymal hemorrhage after stent-assisted coiling of intracranial aneurysms in a high-volume single center. Neuroradiology 58:261–266. https://doi.org/10.1007/s00234-015-1624-3

    Article  PubMed  Google Scholar 

  3. Sim SY, Song J, Oh SY, Kim MJ, Lim YC, Park SK, Shin YS, Chung J (2016) Incidence and characteristics of remote intracerebral hemorrhage after endovascular treatment of unruptured intracranial aneurysms. World Neurosurg 95:335–340. https://doi.org/10.1016/j.wneu.2016.08.057

    Article  PubMed  Google Scholar 

  4. Fan YH, Zhang L, Lam WW, Mok VC, Wong KS (2003) Cerebral microbleeds as a risk factor for subsequent intracerebral hemorrhages among patients with acute ischemic stroke. Stroke 34:2459–2462. https://doi.org/10.1161/01.STR.0000090841.90286.81

    Article  PubMed  Google Scholar 

  5. Bokura H, Saika R, Yamaguchi T, Nagai A, Oguro H, Kobayashi S, Yamaguchi S (2011) Microbleeds are associated with subsequent hemorrhagic and ischemic stroke in healthy elderly individuals. Stroke 42:1867–1871. https://doi.org/10.1161/STROKEAHA.110.601922

    Article  CAS  PubMed  Google Scholar 

  6. Charidimou A, Kakar P, Fox Z, Werring DJ (2013) Cerebral microbleeds and recurrent stroke risk: systematic review and meta-analysis of prospective ischemic stroke and transient ischemic attack cohorts. Stroke 44:995–1001. https://doi.org/10.1161/STROKEAHA.111.000038

    Article  PubMed  Google Scholar 

  7. Wilson D, Charidimou A, Ambler G, Fox ZV, Gregoire S, Rayson P, Imaizumi T, Fluri F, Naka H, Horstmann S, Veltkamp R, Rothwell PM, Kwa VIH, Thijs V, Lee YS, Kim YD, Huang Y, Wong KS, Jäger HR, Werring DJ (2016) Recurrent stroke risk and cerebral microbleed burden in ischemic stroke and TIA: a meta-analysis. Neurology 87:1501–1510. https://doi.org/10.1212/WNL.0000000000003183

    Article  PubMed  PubMed Central  Google Scholar 

  8. Ogawa Ito A, Shindo A, Ii Y, Matsuura K, Tabei KI, Maeda M, Umino M, Suzuki Y, Shiba M, Toma N, Suzuki H, Tomimoto H (2019) Microbleeds after carotid artery stenting: small embolism may induce cerebral microbleeds. Cerebrovasc Dis Extra 9:57–65. https://doi.org/10.1159/000500112

    Article  PubMed  PubMed Central  Google Scholar 

  9. Shi ZS, Duckwiler GR, Jahan R, Tateshima S, Gonzalez NR, Szeder V, Saver JL, Kim D, Ali LK, Starkman S, Vespa PM, Salamon N, Villablanca JP, Viñuela F, Feng L, Loh Y, Liebeskind DS (2015) New cerebral microbleeds after mechanical thrombectomy for large-vessel occlusion strokes. Medicine 94:e2180. https://doi.org/10.1097/MD.0000000000002180

    Article  PubMed  PubMed Central  Google Scholar 

  10. Gao Y, Nie K, Duan Z, Wang S, Ma G, Zhang X, Li C, Zhang Y, Dai C, Wang L (2019) A follow-up study of cerebral microbleeds in patients who received stents for symptomatic cerebral artery stenosis. Ann Vasc Surg 58:338–346. https://doi.org/10.1016/j.avsg.2018.11.031

    Article  PubMed  Google Scholar 

  11. Nishikawa Y, Satow T, Takagi T, Murao K, Miyamoto S, Iihara K (2013) Efficacy and safety of single versus dual antiplatelet therapy for coiling of unruptured aneurysms. J Stroke Cerebrovasc Dis 22:650–655. https://doi.org/10.1016/j.jstrokecerebrovasdis.2012.02.008

    Article  PubMed  Google Scholar 

  12. Wakhloo AK, Linfante I, Silva CF, Samaniego EA, Dabus G, Etezadi V, Spilberg G, Gounis MJ (2012) Closed-cell stent for coil embolization of intracranial aneurysms: clinical and angiographic results. AJNR Am J Neuroradiol 33:1651–1656. https://doi.org/10.3174/ajnr.A3034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rossen JD, Chalouhi N, Wassef SN, Thomas J, Abel TJ, Jabbour PM, Kung DK, Hasan DM (2012) Incidence of cerebral ischemic events after discontinuation of clopidogrel in patients with intracranial aneurysms treated with stent-assisted techniques. J Neurosurg 117:929–933. https://doi.org/10.3171/2012.8.JNS12185

    Article  CAS  PubMed  Google Scholar 

  14. Becske T, Potts MB, Shapiro M, Kallmes DF, Brinjikji W, Saatci I, McDougall CG, Szikora I, Lanzino G, Moran CJ, Woo HH, Lopes DK, Berez AL, Cher DJ, Siddiqui AH, Levy EI, Albuquerque FC, Fiorella DJ, Berentei Z, Marosföi M, Cekirge SH, Nelson PK (2017) Pipeline for uncoilable or failed aneurysms: 3-year follow-up results. J Neurosurg 127:81–88. https://doi.org/10.3171/2015.6.JNS15311

    Article  PubMed  Google Scholar 

  15. Roob G, Fazekas F (2000) Magnetic resonance imaging of cerebral microbleeds. Curr Opin Neurol 13:69–73. https://doi.org/10.1097/00019052-200002000-00013

    Article  CAS  PubMed  Google Scholar 

  16. Becske T, Kallmes DF, Saatci I, McDougall CG, Szikora I, Lanzino G, Moran CJ, Woo HH, Lopes DK, Berez AL, Cher DJ, Siddiqui AH, Levy EI, Albuquerque FC, Fiorella DJ, Berentei Z, Marosfoi M, Cekirge SH, Nelson PK (2013) Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology 267:858–868. https://doi.org/10.1148/radiol.13120099

    Article  PubMed  Google Scholar 

  17. Fischer S, Vajda Z, Aguilar Perez M, Schmid E, Hopf N, Bäzner H, Henkes H (2012) Pipeline embolization device (PED) for neurovascular reconstruction: initial experience in the treatment of 101 intracranial aneurysms and dissections. Neuroradiology 54:369–382. https://doi.org/10.1007/s00234-011-0948-x

    Article  PubMed  Google Scholar 

  18. Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF (2013) Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke 44:442–447. https://doi.org/10.1161/STROKEAHA.112.678151

    Article  PubMed  Google Scholar 

  19. Sweid A, Starke RM, Herial N, Chalouhi N, Das S, Baldassari MP, Alexander TD, Tjoumakaris S, Gooch MR, Hasan D, Rosenwasser RH, Romo V, Jabbour P (2019) Predictors of complications, functional outcome, and morbidity in a large cohort treated with flow diversion. Neurosurgery. 87:730–743. https://doi.org/10.1093/neuros/nyz508

    Article  Google Scholar 

  20. Nakae R, Nagaishi M, Kawamura Y, Tanaka Y, Hyodo A, Suzuki K (2019) Microhemorrhagic transformation of ischemic lesions on T2*-weighted magnetic resonance imaging after pipeline embolization device treatment. J Neurosurg 130:1997–2004. https://doi.org/10.3171/2017.12.JNS172480

    Article  Google Scholar 

  21. Fazekas F, Kleinert R, Roob G, Kleinert G, Kapeller P, Schmidt R, Hartung HP (1999) Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am J Neuroradiol 20:637–642

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Fisher M (2014) Cerebral microbleeds: where are we now? Neurology 83:1304–1305. https://doi.org/10.1212/WNL.0000000000000871

    Article  PubMed  Google Scholar 

  23. Kim SH, Shin DW, Yun JM, Lee JE, Lim JS, Cho BL, Kwon HM, Park JH (2017) Kidney dysfunction and cerebral microbleeds in neurologically healthy adults. PLoS One 12:e0172210. https://doi.org/10.1371/journal.pone.0172210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cho AH, Lee SB, Han SJ, Shon YM, Yang DW, Kim BS (2009) Impaired kidney function and cerebral microbleeds in patients with acute ischemic stroke. Neurology 73:1645–1648. https://doi.org/10.1212/WNL.0b013e3181c1defa

    Article  PubMed  Google Scholar 

  25. Laible M, Horstmann S, Möhlenbruch M, Wegele C, Rizos T, Schüler S, Zorn M, Veltkamp R (2015) Renal dysfunction is associated with deep cerebral microbleeds but not white matter hyperintensities in patients with acute intracerebral hemorrhage. J Neurol 262:2312–2322. https://doi.org/10.1007/s00415-015-7840-2

    Article  PubMed  Google Scholar 

  26. Lee M, Saver JL, Hong KS, Rao NM, Wu YL, Ovbiagele B (2013) Risk-benefit profile of long-term dual- versus single-antiplatelet therapy among patients with ischemic stroke: a systematic review and meta-analysis. Ann Intern Med 159:463–470. https://doi.org/10.7326/0003-4819-159-7-201310010-00006

    Article  PubMed  Google Scholar 

  27. Nishi H, Nakahara I, Matsumoto S, Hashimoto T, Ohta T, Sadamasa N, Ishibashi R, Gomi M, Saka M, Miyata H, Watanabe S, Okata T, Sonoda K, Kouge J, Ishii A, Nagata I, Kira J (2016) Platelet reactivity and hemorrhage risk in neurointerventional procedures under dual antiplatelet therapy. J Neurointerv Surg 8:949–953. https://doi.org/10.1136/neurintsurg-2015-011844

    Article  PubMed  Google Scholar 

  28. Delgado Almandoz JE, Crandall BM, Scholz JM, Fease JL, Anderson RE, Kadkhodayan Y, Tubman DE (2014) 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. https://doi.org/10.3174/ajnr.A3621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ajadi E, Kabir S, Cook A, Grupke S, Alhajeri A, Fraser JF (2019) Predictive value of platelet reactivity unit (PRU) value for thrombotic and hemorrhagic events during flow diversion procedures: a meta-analysis. J Neurointerv Surg 11:1123–1128. https://doi.org/10.1136/neurintsurg-2019-014765

    Article  PubMed  Google Scholar 

  30. Jeon SB, Kang DW (2007) Neurological Picture. Cerebral air emboli on T2-weighted gradient-echo magnetic resonance imaging. J Neurol Neurosurg Psychiatry 78:871. https://doi.org/10.1136/jnnp.2006.102954

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Stroke Center, Kokura Memorial Hospital, 3-2-1 Asano, Kokurakita-ku, Kitakyushu, Fukuoka, 802-8555, Japan

    Eiji Higashi, Taketo Hatano, Mitsushige Ando, Hideo Chihara, Takenori Ogura, Keita Suzuki, Keitaro Yamagami, Daisuke Kondo, Takahiko Kamata, Shota Sakai, Hiroki Sakamoto & Izumi Nagata

Authors
  1. Eiji Higashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Taketo Hatano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitsushige Ando
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hideo Chihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takenori Ogura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Keita Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Keitaro Yamagami
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Daisuke Kondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Takahiko Kamata
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shota Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hiroki Sakamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Izumi Nagata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eiji Higashi.

Ethics declarations

Conflict of interest

We declare that we have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Higashi, E., Hatano, T., Ando, M. et al. Factors associated with the new appearance of cerebral microbleeds after endovascular treatment for unruptured intracranial aneurysms. Neuroradiology 63, 1079–1085 (2021). https://doi.org/10.1007/s00234-020-02616-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-020-02616-4

Keywords

Search

Navigation