Skip to main content

Advertisement

Log in

Hemodynamic differences of posterior communicating artery aneurysms between adult and fetal types of posterior cerebral artery

  • Original Article
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

The recanalization of posterior communicating artery (PCoA) aneurysms after endovascular treatment has been analyzed by various factors. However, the differences between adult and fetal types of posterior cerebral artery (PCA) have not been fully investigated. The main aim of this study was to investigate hemodynamic differences of PCoA aneurysms between adult and fetal types using computational fluid dynamics (CFD).

Methods

Fifty-five PCoA aneurysms were evaluated by 3D CT angiography and divided into unruptured aneurysms with adult-type or fetal-type PCAs (19 cases, UA group; 9 cases, UF group) and ruptured aneurysms with adult-type or fetal-type PCAs (17 cases, RA group; 10 cases, RF group). These native aneurysms were analyzed by CFD regarding morphological and hemodynamic characteristics. To evaluate simulated endovascular treatment of aneurysms, CFD was performed using porous media modeling.

Results

Morphologically, the RA group had significantly smaller parent artery diameter (2.91 mm vs. 3.49 mm, p=0.005) and higher size ratio (2.54 vs. 1.78, p=0.023) than the RF group. CFD revealed that the UA group had significantly lower oscillatory shear index (OSI) (0.0032 vs. 0.0078, p=0.004) than the UF group and that the RA group had lower WSS (3.09 vs. 11.10, p=0.001) and higher OSI (0.014 vs. 0.006, p=0.031) than the RF group, while the RF group presented significantly higher intra-aneurysmal flow velocity (0.19 m/s vs. 0.061 m/s, p=0.002) than the RA group. Porous media modeling of simulated treatment revealed higher residual flow volume in the fetal-type groups.

Conclusions

These results suggested that PCoA aneurysms with fetal-type PCAs had different morphological features and hemodynamic characteristics compared with those with adult-type PCAs, leading to high risks of recanalization.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All data relevant to the study are included in the article or uploaded as supplementary information.

Code availability

Not applicable.

References

  1. Abdehkakha A, Hammond AL, Patel TR, Siddiqui AH, Dargush GF, Meng H (2021) Cerebral aneurysm flow diverter modeled as a thin inhomogeneous porous medium in hemodynamic simulations. Comput Biol Med. 139:104988. https://doi.org/10.1016/j.compbiomed.2021.104988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Akgiray Ö, Saatçı AM (2001) A new look at filter backwash hydraulics. Water Supply 1(2):65–72. https://doi.org/10.2166/ws.2001.0022

    Article  CAS  Google Scholar 

  3. Augsburger L, Reymond P, Rufenacht DA, Stergiopulos N (2011) Intracranial stents being modeled as a porous medium: flow simulation in stented cerebral aneurysms. Ann Biomed Eng 39(2):850–863. https://doi.org/10.1007/s10439-010-0200-6

    Article  CAS  PubMed  Google Scholar 

  4. Beppu M, Tsuji M, Ishida F, Shirakawa M, Suzuki H, Yoshimura S (2020) Computational fluid dynamics using a porous media setting predicts outcome after flow-diverter treatment. AJNR Am J Neuroradiol. 41:2107–2113. https://doi.org/10.3174/ajnr.A6766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne JV (2007) Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the international subarachnoid aneurysm trial (ISAT). Stroke 38:1538–1544. https://doi.org/10.1161/STROKEAHA.106.466987

    Article  PubMed  Google Scholar 

  6. Can A, Ho AL, Emmer BJ, Dammers R, Dirven CM, Du R (2015) Association between vascular anatomy and posterior communicating artery aneurysms. World Neurosurg 84(5):1251–1255. https://doi.org/10.1016/j.wneu.2015.05.078

    Article  PubMed  Google Scholar 

  7. Cho YD, Lee WJ, Kim KM, Kang HS, Kim JE, Han MH (2013) Stent-assisted coil embolization of posterior communicating artery aneurysms. AJNR 34(11):2171–2176. https://doi.org/10.3174/ajnr.A3541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Choi HH, Cho YD, Yoo DH, Lee HS, Kim SH, Jang D, Lee SH, Cho WS, Kang HS, Kim JE (2020) Impact of fetal-type posterior cerebral artery on recanalization of posterior communicating artery aneurysms after coil embolization: matched-pair case–control study. J Neurointerv Surg 12(8):783–787. https://doi.org/10.1136/neurintsurg-2019-015531

    Article  PubMed  Google Scholar 

  9. Chung BJ, Doddasomayajula R, Mut F, Detmer F, Pritz MB, Hamzei-Sichani F, Brinjikji W, Kallmes DF, Jimenez CM, Putman CM, Cebral JR (2017) Angioarchitectures and hemodynamic characteristics of posterior communicating artery aneurysms and their association with rupture status. AJNR 38(11):2111–2118. https://doi.org/10.3174/ajnr.A5358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chung J, Cheong JH, Kim JM, Lee DH, Yi HJ, Choi KS, Ahn JS, Park JC, Park W (2023) Is fetal-type posterior cerebral artery a risk factor for recurrence in coiled internal carotid artery-incorporating posterior communicating artery aneurysms? Analysis of conventional statistics, computational fluid dynamics, and random forest with hyper-ensemble approach. Neurosurgery 93(3):611–621. https://doi.org/10.1227/neu.0000000000002458

    Article  PubMed  Google Scholar 

  11. Corns R, Zebian B, Tait MJ, Walsh D, Hampton T, Deasy N, Tolias C (2013) Prevalence of recurrence and retreatment of ruptured intracranial aneurysms treated with endovascular coil occlusion. Br J Neurosurg 27(1):30–33. https://doi.org/10.3109/02688697.2012.701676

    Article  PubMed  Google Scholar 

  12. Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ (2013) Review of 2 decades of aneurysm-recurrence literature, part 1: reducing recurrence after endovascular coiling. AJNR 34(2):266–270. https://doi.org/10.3174/ajnr.A3032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Daou B, Chalouhi N, Starke RM, Barros G, Ya'qoub L, Do J, Tjoumakaris S, Rosenwasser RH, Jabbour P (2016) Clipping of previously coiled cerebral aneurysms: efficacy, safety, and predictors in a cohort of 111 patients. J Neurosurg 125(6):1337–1343. https://doi.org/10.3171/2015.10.JNS151544

    Article  PubMed  Google Scholar 

  14. Ergun S (1952) Fluid flow through packed columns. Chem Eng Prog 48:85–94

    Google Scholar 

  15. Golshani K, Ferrell A, Zomorodi A, Smith TP, Britz GW (2010) A review of the management of posterior communicating artery aneurysms in the modern era. Surg Neurol Int 22(1):88. https://doi.org/10.4103/2152-7806.74147

    Article  Google Scholar 

  16. Hassan T, Timofeev EV, Saito T, Shimizu H, Ezura M, Matsumoto Y, Takayama K, Tominaga T, Takahashi A (2005) A proposed parent vessel geometry–based categorization of saccular intracranial aneurysms: computational flow dynamics analysis of the risk factors for lesion rupture. J Neurosurg 103(4):662–680. https://doi.org/10.3171/jns.2005.103.4.0662

    Article  PubMed  Google Scholar 

  17. He Z, Wan Y (2018) Is fetal-type posterior cerebral artery a risk factor for intracranial aneurysm as analyzed by multislice CT angiography? Exp Ther Med 15(1):838–846. https://doi.org/10.3892/etm.2017.5504

    Article  PubMed  Google Scholar 

  18. Horikoshi T, Akiyama I, Yamagata Z, Sugita M, Nukui H (2002) Magnetic resonance angiographic evidence of sex-linked variations in the circle of Willis and the occurrence of cerebral aneurysms. J Neurosurg 96(4):697–703. https://doi.org/10.3171/jns.2002.96.4.0697

    Article  PubMed  Google Scholar 

  19. Ishida F, Tsuji M, Tanioka S, Tanaka K, Yoshimura S, Suzuki H, Esposito G, Regli L, Cenzato M, Kaku Y, Tanaka M, Tsukahara T (2021) Computational fluid dynamics for cerebral aneurysms in clinical settings. In: Trends in cerebrovascular surgery and interventions [Internet]. Springer, Cham (CH). https://doi.org/10.1007/978-3-030-63453-7_4

    Chapter  Google Scholar 

  20. Jiang Y, Ge L, Di R, Lu G, Huang L, Li G, Leng X, Zhang S, Wan H, Geng D, Xiang J, Zhang XJ (2019) Differences in hemodynamic characteristics under high packing density between the porous media model and finite element analysis in computational fluid dynamics of intracranial aneurysm virtual treatment. Neurointerv Surg. 11(8):853–858. https://doi.org/10.1136/neurintsurg-2018-014218

    Article  Google Scholar 

  21. Jou LD, Lee DH, Morsi H, Mawad ME (2008) Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 29(9):1761–1767. https://doi.org/10.3174/ajnr.A1180

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kim T, Oh CW, Bang JS, Ban SP, Lee SU, Kim YD, Kwon OK (2021) Higher oscillatory shear index is related to aneurysm recanalization after coil embolization in posterior communicating artery aneurysms. Acta Neurochir (Wien) 163(8):2327–2337. https://doi.org/10.1007/s00701-020-04607-z

    Article  PubMed  Google Scholar 

  23. Ku DN, Giddens DP, Zarins CK, Glagov S (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 5(3):293–302. https://doi.org/10.1161/01.atv.5.3.293

    Article  CAS  PubMed  Google Scholar 

  24. Luo B, Yang X, Wang S, Li H, Chen J, Yu H, Zhang Y, Zhang Y, Mu S, Liu Z, Ding G (2011) High shear stress and flow velocity in partially occluded aneurysms prone to recanalization. Stroke 42(3):745–753. https://doi.org/10.1161/STROKEAHA.110.593517

    Article  PubMed  Google Scholar 

  25. Lv N, Wang C, Karmonik C, Fang Y, Xu J, Yu Y, Cao W, Liu J, Huang Q (2016) Morphological and hemodynamic discriminators for rupture status in posterior communicating artery aneurysms. PLoS One 11(2):e0149906. https://doi.org/10.1371/journal.pone.0149906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Masanori T, Fujimaro I, Tomoyuki K, Kazuhiro F, Yoichi M, Masato S, Takanori S, Keiji F, Katsuhiro T, Hiroshi T, Yasuyuki U, Ryuta Y, Shinichi S, Hidenori S (2020) Double porous media modeling in computational fluid dynamics for hemodynamics of stent-assisted coiling of intracranial aneurysms: a technical case report. Brain Hemorrhages 1(1):85–88

    Article  Google Scholar 

  27. Masanori T, Fujimaro I, Takenori S, Kazuhiro F, Yoichi M, Ryuta Y, Yasuyuki U, Naoki T, Hidenori S (2023) Computational fluid dynamics using dual-layer porous media modeling to evaluate the hemodynamics of cerebral aneurysm treated with FRED: a technical note. Brain Hemorrhages 4(1):39–43

    Article  Google Scholar 

  28. Matthew DF, Noam A, Sung HL, David WH, David AS (2005) Characterization of volumetric flow rate waveforms in the normal internal carotid and vertebral arteries. Physiol Meas 26(4):477–488. https://doi.org/10.1088/0967-3334/26/4/013

    Article  Google Scholar 

  29. Meng H, Tutino VM, Xiang J, Siddiqui A (2017) High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol 35(7):1254–1262. https://doi.org/10.3174/ajnr.A3558

    Article  Google Scholar 

  30. Misaki K, Takao H, Suzuki T, Nishimura K, Kan I, Yuki I, Ishibashi T, Yamamoto M, Murayama Y (2017) Estimated pretreatment hemodynamic prognostic factors of aneurysm recurrence after endovascular embolization. Technol Health Care 25(5):843–850. https://doi.org/10.3233/THC-160495

    Article  PubMed  Google Scholar 

  31. Nambu I, Misaki K, Uchiyama N, Mohri M, Suzuki T, Takao H, Murayama Y, Futami K, Kawamura T, Inoguchi Y, Matsuzawa T, Nakada M (2019) High pressure in virtual postcoiling model is a predictor of internal carotid artery aneurysm recurrence after coiling. Neurosurgery 84(3):607–615. https://doi.org/10.1093/neuros/nyy073

    Article  PubMed  Google Scholar 

  32. Ojemann RG, Crowell RM (1988) Internal carotid artery aneurysms. Surgical management of cerebrovascular disease, 2nd edn. Williams and Wilkins, Baltimore, pp 179–198

    Google Scholar 

  33. Roy AK, Howard BM, Haussen DC, Osbun JW, Halani SH, Skukalek SL, Tong F, Nogueira RG, Dion JE, Cawley CM, Grossberg JA (2018) Reduced efficacy of the pipeline embolization device in the treatment of posterior communicating region aneurysms with fetal posterior cerebral artery configuration. Neurosurgery 82(5):695–700. https://doi.org/10.1093/neuros/nyx293

    Article  PubMed  Google Scholar 

  34. Sano T, Ishida F, Tsuji M, Furukawa K, Shimosaka S, Suzuki H (2017) Hemodynamic differences between ruptured and unruptured cerebral aneurysms simultaneously existing in the same location: 2 case reports and proposal of a novel parameter oscillatory velocity index. World Neurosurg 98:868.e5–868.e10. https://doi.org/10.1016/j.wneu.2016.12.047

    Article  PubMed  Google Scholar 

  35. Shaban A, Albright KC, Boehme AK, Martin-Schild S (2013) Circle of Willis variants: fetal PCA. Stroke Res Treat 2013:105937. https://doi.org/10.1155/2013/105937

    Article  PubMed  PubMed Central  Google Scholar 

  36. Shiba M, Ishida F, Furukawa K, Tanemura H, Tsuji M, Shimosaka S, Suzuki H (2017) Relationships of morphologic parameters and hemodynamic parameters determined by computational fluid dynamics analysis with the severity of subarachnoid hemorrhage. JNET 11(10):512–519. https://doi.org/10.5797/jnet.oa.2016-0099

    Article  Google Scholar 

  37. Songsaeng D, Geibprasert S, Willinsky R, Tymianski M, TerBrugge KG, Krings T (2010) Impact of anatomical variations of the circle of Willis on the incidence of aneurysms and their recurrence rate following endovascular treatment. Clin Radiol 65(11):895–901. https://doi.org/10.1016/j.crad.2010.06.010

    Article  CAS  PubMed  Google Scholar 

  38. Songsaeng D, Geibprasert S, ter Brugge KG, Willinsky R, Tymianski M, Krings T (2011) Impact of individual intracranial arterial aneurysm morphology on initial obliteration and recurrence rates of endovascular treatments: a multivariate analysis. J Neurosurg 114(4):994–1002. https://doi.org/10.3171/2010.8.JNS10241

    Article  PubMed  Google Scholar 

  39. Tanioka S, Ishida F, Kishimoto T, Tsuji M, Tanaka K, Shimosaka S, Toyoda M, Kashiwagi N, Sano T, Suzuki H (2019) Quantification of hemodynamic irregularity using oscillatory velocity index in the associations with the rupture status of cerebral aneurysms. J Neurointerv Surg 11(6):614–617. https://doi.org/10.1136/neurintsurg-2018-014489

    Article  PubMed  Google Scholar 

  40. Tanioka S, Ishida F, Yamamoto A, Shimizu S, Sakaida H, Toyoda M, Kashiwagi N, Suzuki H (2020) Machine learning classification of cerebral aneurysm rupture status with morphologic variables and hemodynamic parameters. Radiol Artif Intell. 2(1):e190077. https://doi.org/10.1148/ryai.2019190077

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tomoaki S, Nobuyuki G, Toshiharu N, Hiroshi A (2020) Assessing the hemodynamics in residual cavities of intracranial aneurysm after coil embolization with combined computational flow dynamics and silent magnetic resonance angiography. J Stroke Cerebrovasc Dis 29(12):105290. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105290

    Article  Google Scholar 

  42. Tsuji M, Ishida F, Kishimoto T, Furukawa K, Miura Y, Shiba M, Sano T, Fukazawa K, Tanaka K, Tanemura H, Umeda Y, Yasuda R, Shimosaka S, Suzuki H (2020) Double porous media modeling in computational fluid dynamics for hemodynamics of stent-assisted coiling of intracranial aneurysms: a technical case report. Brain Hemorrhages 1(1):85–88. https://doi.org/10.1016/j.hest.2020.01.004

    Article  Google Scholar 

  43. Umeda Y, Ishida F, Tsuji M, Furukawa K, Shiba M, Yasuda R, Toma N, Sakaida H, Suzuki H (2017) Computational fluid dynamics (CFD) using porous media modeling predicts recurrence after coiling of cerebral aneurysms. PLoS One 12:e0190222. https://doi.org/10.1371/journal.pone.0190222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. van Raamt AF, Mali WP, van Laar PJ, van der Graaf Y (2006) The fetal variant of the circle of Willis and its influence on the cerebral collateral circulation. Cerebrovasc Dis 22:217–224. https://doi.org/10.1159/000094007

    Article  PubMed  Google Scholar 

  45. Wallace AN, Kayan Y, Austin MJ, Delgado Almandoz JE, Kamran M, Cross DT 3rd, Moran CJ, Osbun JW, Kansagra AP (2017) Pipeline embolization of posterior communicating artery aneurysms associated with a fetal origin posterior cerebral artery. Clin Neurol Neurosurg 160:83–87. https://doi.org/10.1016/j.clineuro.2017.06.014

    Article  PubMed  Google Scholar 

  46. Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, Siddiqui AH, Levy EI, Meng H (2011) Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 42(1):144–152. https://doi.org/10.1161/STROKEAHA.110.592923

    Article  PubMed  Google Scholar 

  47. Xiang J, Tremmel M, Kolega J, Levy EI, Natarajan SK, Meng H (2012) Newtonian viscosity model could overestimate wall shear stress in intracranial aneurysm domes and underestimate rupture risk. J Neurointerv Surg 4(5):351–357. https://doi.org/10.1136/neurintsurg-2011-010089

    Article  PubMed  Google Scholar 

  48. Yamamoto H, Yabuta T, Negi Y, Horikawa D, Kawamura K, Tamura E, Tanaka K, Ishida F (2020) Measurement of human blood viscosity a using falling needle rheometer and the correlation to the Modified Herschel-Bulkley model equation. Heliyon 6(9):e04792. https://doi.org/10.1016/j.heliyon.2020.e04792

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yasuda R, Miura Y, Suzuki Y, Tsuji M, Shiba M, Toma N, Suzuki H (2022) Posterior communicating artery-incorporated internal carotid-posterior communicating artery aneurysms prone to recur after coil embolization. World Neurosurg 162:e546e552. https://doi.org/10.1016/j.wneu.2022.03.062

    Article  Google Scholar 

  50. Yuan J, Huang C, Li Z, Jiang X, Zhao X, Lai N, Xia D, Wu D, Zhang B, Wang X, Fang X (2021) Hemodynamic characteristics associated with recurrence of middle cerebral artery bifurcation aneurysms after total embolization. Clin Interv Aging 6(16):2023–2032. https://doi.org/10.2147/CIA.S326635

    Article  Google Scholar 

  51. Yuan J, Huang C, Li Z, Jiang X, Zhao X, Wu D, Lai N, Liu J, Zhang B, Qin F, Xia D, Fang X (2021) Hemodynamic and morphological parameters of ruptured mirror posterior communicating artery aneurysms. Front Neurol 27(12):653589. https://doi.org/10.3389/fneur.2021.653589

    Article  Google Scholar 

Download references

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Katsuhiro Tanaka, Fujimaro Ishida

Data curation: Katsuhiro Tanaka, Kazuhiro Furukawa, Fujimaro Ishida

Formal analysis: Katsuhiro Tanaka, Kazuhiro Furukawa, Fujimaro Ishida

Methodology: Kazuhiro Furukawa, Fujimaro Ishida

Project administration: Katsuhiro Tanaka, Fujimaro Ishida

Software: Kazuhiro Furukawa, Fujimaro Ishida

Supervision: Fujimaro Ishida, Hidenori Suzuki

Validation: Katsuhiro Tanaka, Fujimaro Ishida

Visualization: Katsuhiro Tanaka, Fujimaro Ishida

Writing–original draft: Katsuhiro Tanaka

Writing–review and editing: Katsuhiro Tanaka, Fujimaro Ishida, Hidenori Suzuki

Corresponding author

Correspondence to Katsuhiro Tanaka.

Ethics declarations

Ethics approval

This study was conducted in accordance with the guideline and under the approval of the ethics review board of Mie Chuo Medical Center (approval number: MCERB 201820).

Consent to participate

The requirement for informed consents for participation and publication were waived.

Consent for publication

Patient records and geometric data were anonymized before the analysis.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

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

Supplementary information

ESM 1

(DOCX 13 kb)

ESM 2

(DOCX 15 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tanaka, K., Furukawa, K., Ishida, F. et al. Hemodynamic differences of posterior communicating artery aneurysms between adult and fetal types of posterior cerebral artery. Acta Neurochir 165, 3697–3706 (2023). https://doi.org/10.1007/s00701-023-05840-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-023-05840-y

Keywords

Navigation