Skip to main content

Advertisement

Log in

Cerebral circulation time on DSA after thrombectomy associated with hemorrhagic transformation in acute ischemic stroke

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

Abstract

Background

To investigate the association between cerebral circulation time (CCT) on digital subtraction angiography immediately after thrombectomy and hemorrhagic transformation (HT) in acute ischemic stroke (AIS).

Methods

Retrospectively enrolled consecutive AIS patients presented with large vessel occlusion who received thrombectomy and achieved successful recanalization between January 2019 and June 2021. The time interval from the beginning of the siphon segment of internal carotid artery visualization until the end of the arterial phase during cerebral angiography was calculated as CCT. The independent association of CCT with HT was evaluated using logistic regression analyses. The receiver operating characteristic curve was analyzed to evaluate the association between CCT and HT.

Results

Two hundred and twenty-four patients were included, of whom 86 (38.4%) suffered HT. Compared with patients without HT, patients with HT were of advanced age, less commonly male, had more diabetes mellitus, had higher baseline National Institutes of Health Stroke Scale score, lower Alberta Stroke Program Early Computed Tomographic Score, and shorter CCT (P < 0.05). Multivariable logistic regression suggested that CCT was independently associated with HT (adjusted odds ratio, 0.170; 95% confidence interval, 0.004–0.450; P < 0.001). According to the receiver operating characteristic curve, the optimal cut-off value for the strong correlation between CCT and HT was 1.72 s, which had 76.6% sensitivity, 81.6% specificity, and the area under the curve was 0.846.

Conclusion

Shorter post-thrombectomy CCT was independently associated with HT.

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
Fig. 3

Similar content being viewed by others

Data availability

Data can be obtained from corresponding authors upon reasonable request.

References

  1. Angermaier A, Khaw AV, Kirsch M, Kessler C, Langner S (2015) Influence of recanalization and time of cerebral ischemia on tissue outcome after endovascular stroke treatment on computed tomography perfusion. J Stroke Cerebrovasc Dis 24(10):2306–2312. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.06.025

    Article  PubMed  Google Scholar 

  2. Brown MM, Wade JP, Marshall J (1985) Fundamental importance of arterial oxygen content in the regulation of cerebral blood flow in man. Brain 108(Pt 1):81–93. https://doi.org/10.1093/brain/108.1.81

    Article  PubMed  Google Scholar 

  3. Castro P, Azevedo E, Serrador J, Rocha I, Sorond F (2017) Hemorrhagic transformation and cerebral edema in acute ischemic stroke: link to cerebral autoregulation. J Neurol Sci 372:256–261. https://doi.org/10.1016/j.jns.2016.11.065

    Article  PubMed  Google Scholar 

  4. Hong JM, Kim DS, Kim M (2021) Hemorrhagic transformation after ischemic stroke: mechanisms and management. Front Neurol 12:703258. https://doi.org/10.3389/fneur.2021.703258

    Article  PubMed  PubMed Central  Google Scholar 

  5. Huang S, Liu C, Li X, Wu Y, Liang C, Li W, Zhang M (2022) Artery diameter ratio after recanalization in endovascular therapy for acute ischemic stroke: a new predictor of clinical outcomes. Neuroradiology 64(4):785–793. https://doi.org/10.1007/s00234-021-02841-5

    Article  PubMed  Google Scholar 

  6. Immink RV, van Montfrans GA, Stam J, Karemaker JM, Diamant M, van Lieshout JJ (2005) Dynamic cerebral autoregulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke 36(12):2595–2600. https://doi.org/10.1161/01.STR.0000189624.06836.03

    Article  PubMed  Google Scholar 

  7. Jeong HG, Kim BJ, Kim H, Jung C, Han MK, Liebeskind DS, Bae HJ (2019) Blood pressure drop and penumbral tissue loss in nonrecanalized emergent large vessel occlusion. Stroke 50(10):2677–2684. https://doi.org/10.1161/STROKEAHA.119.025426

    Article  PubMed  Google Scholar 

  8. Jovin TG, Chamorro A, Cobo E, de Miquel MA, Molina CA, Rovira A, San Román L, Serena J, Abilleira S, Ribó M, Millán M, Urra X, Cardona P, López-Cancio E, Tomasello A, Castaño C, Blasco J, Aja L, Dorado L, Quesada H, Rubiera M, Hernandez-Pérez M, Goyal M, Demchuk AM, von Kummer R, Gallofré M, Dávalos A, REVASCAT Trial Investigators (2015) Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med 372(24):2296–2306. https://doi.org/10.1056/NEJMoa1503780

    Article  PubMed  CAS  Google Scholar 

  9. Kadry H, Noorani B, Cucullo L (2020) A blood-brain barrier overview on structure, function, impairment, and biomarkers of integrity. Fluids Barriers CNS 17(1):69. https://doi.org/10.1186/s12987-020-00230-3

    Article  PubMed  PubMed Central  Google Scholar 

  10. LeCouffe NE, Kappelhof M, Treurniet KM, Rinkel LA, Bruggeman AE, Berkhemer OA, Wolff L, van Voorst H, Tolhuisen ML, Dippel DWJ, van der Lugt A, van Es ACGM, Boiten J, Lycklama À, Nijeholt GJ, Keizer K, Gons RAR, Yo LSF, van Oostenbrugge RJ, van Zwam WH, Roozenbeek B, van der Worp HB, Lo RTH, van den Wijngaard IR, de Ridder IR, Costalat V, Arquizan C, Lemmens R, Demeestere J, Hofmeijer J, Martens JM, Schonewille WJ, Vos JA, Uyttenboogaart M, Bokkers RPH, van Tuijl JH, Kortman H, Schreuder FHBM, Boogaarts HD, de Laat KF, van Dijk LC, den Hertog HM, van Hasselt BAAM, Brouwers PJAM, Bulut T, Remmers MJM, van Norden A, Imani F, Rozeman AD, Elgersma OEH, Desfontaines P, Brisbois D, Samson Y, Clarençon F, Krietemeijer GM, Postma AA, van Doormaal PJ, van den Berg R, van der Hoorn A, Beenen LFM, Nieboer D, Lingsma HF, Emmer BJ, Coutinho JM, Majoie CBLM, Roos YBWEM, MR CLEAN–NO IV Investigators (2021) A randomized trial of intravenous alteplase before endovascular treatment for stroke. N Engl J Med 385(20):1833–1844. https://doi.org/10.1056/NEJMoa2107727

    Article  PubMed  CAS  Google Scholar 

  11. Lin CH, Saver JL, Ovbiagele B, Huang WY, Lee M (2022) Endovascular thrombectomy without versus with intravenous thrombolysis in acute ischemic stroke: a non-inferiority meta-analysis of randomized clinical trials. J Neurointerv Surg 14(3):227–232. https://doi.org/10.1136/neurintsurg-2021-017667

    Article  PubMed  Google Scholar 

  12. Loo JK, Hu YS, Lin TM, Lin CJ, Lirng JF, Wu HM, Yang HC, Lee CC, Luo CB, Guo WY (2022) Shortened cerebral circulation time correlates with seizures in brain arteriovenous malformation: a cross-sectional quantitative digital subtraction angiography study. Eur Radiol 32(8):5402–5412. https://doi.org/10.1007/s00330-022-08690-x

    Article  PubMed  CAS  Google Scholar 

  13. Neuberger U, Möhlenbruch MA, Herweh C, Ulfert C, Bendszus M, Pfaff J (2017) Classification of bleeding events: comparison of ECASS III (European Cooperative Acute Stroke Study) and the new Heidelberg Bleeding Classification. Stroke 48(7):1983–1985. https://doi.org/10.1161/STROKEAHA.117.016735

    Article  PubMed  Google Scholar 

  14. Ohta H, Nakano S, Yokogami K, Iseda T, Yoneyama T, Wakisaka S (2004) Appearance of early venous filling during intra-arterial reperfusion therapy for acute middle cerebral artery occlusion: a predictive sign for hemorrhagic complications. Stroke 35(4):893–898. https://doi.org/10.1161/01.STR.0000119751.92640.7F

    Article  PubMed  Google Scholar 

  15. Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, Biller J, Brown M, Demaerschalk BM, Hoh B, Jauch EC, Kidwell CS, Leslie-Mazwi TM, Ovbiagele B, Scott PA, Sheth KN, Southerland AM, Summers DV, Tirschwell DL (2019) Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 50(12):e344–e418. https://doi.org/10.1161/STR.0000000000000211

    Article  PubMed  Google Scholar 

  16. Qureshi AI (2008) Acute hypertensive response in patients with stroke: pathophysiology and management. Circulation 118(2):176–187. https://doi.org/10.1161/CIRCULATIONAHA.107.723874

    Article  PubMed  Google Scholar 

  17. Schembri M, Verbaan D, Emmer BJ, Coert BA, Majoie CBLM, Vandertop WP, van den Berg R (2021) Cerebral circulation time on DSA during endovascular treatment in WFNS grade I aneurysmal SAH patients-a predictor of DCI? Neuroradiology 63(12):2131–2138. https://doi.org/10.1007/s00234-021-02749-0

    Article  PubMed  Google Scholar 

  18. Shao Y, Xu Y, Li Y, Wen X, He X (2021) A new classification system for postinterventional cerebral hyperdensity: the influence on hemorrhagic transformation and clinical prognosis in acute stroke. Neural Plast 2021:6144304. https://doi.org/10.1155/2021/6144304

    Article  PubMed  PubMed Central  Google Scholar 

  19. Silverman A, Kodali S, Sheth KN, Petersen NH (2020) Hemodynamics and hemorrhagic transformation after endovascular therapy for ischemic stroke. Front Neurol 11:728. https://doi.org/10.3389/fneur.2020.00728

    Article  PubMed  PubMed Central  Google Scholar 

  20. Suzuki K, Matsumaru Y, Takeuchi M, Morimoto M, Kanazawa R, Takayama Y, Kamiya Y, Shigeta K, Okubo S, Hayakawa M, Ishii N, Koguchi Y, Takigawa T, Inoue M, Naito H, Ota T, Hirano T, Kato N, Ueda T, Iguchi Y, Akaji K, Tsuruta W, Miki K, Fujimoto S, Higashida T, Iwasaki M, Aoki J, Nishiyama Y, Otsuka T, Kimura K, SKIP Study Investigators (2021) Effect of mechanical thrombectomy without vs with intravenous thrombolysis on functional outcome among patients with acute ischemic stroke: the SKIP randomized clinical trial. JAMA 325(3):244–253. https://doi.org/10.1001/jama.2020.23522

    Article  PubMed  PubMed Central  Google Scholar 

  21. Van Kranendonk KR, Treurniet KM, Boers AMM, Berkhemer OA, van den Berg LA, Chalos V, Lingsma HF, van Zwam WH, van der Lugt A, van Oostenbrugge RJ, Dippel DWJ, Roos YBWEM, Marquering HA, Majoie CBLM, MR CLEAN investigators (2019) Haemorrhagic transformation is associated with poor functional outcome in patients with acute ischaemic stroke due to a large vessel occlusion. J Neurointerv Surg 11(5):464–468. https://doi.org/10.1136/neurintsurg-2018-014141

    Article  PubMed  Google Scholar 

  22. Von Kummer R, Broderick JP, Campbell BC, Demchuk A, Goyal M, Hill MD, Treurniet KM, Majoie CB, Marquering HA, Mazya MV, San Román L, Saver JL, Strbian D, Whiteley W, Hacke W (2015) The Heidelberg bleeding classification: classification of bleeding events after ischemic stroke and reperfusion therapy. Stroke 46:2981–2986. https://doi.org/10.1161/STROKEAHA.115.010049

    Article  Google Scholar 

  23. Wang JQ, Wang YJ, Qiu J, Li W, Sun XH, Zhao YG, Liu X, Zhao ZA, Liu L, Nguyen TN, Chen HS (2022) Cerebral circulation time after thrombectomy: a potential predictor of outcome after recanalization in acute stroke. J Am Heart Assoc 11(11):e025853. https://doi.org/10.1161/JAHA.122.025853

    Article  PubMed  PubMed Central  Google Scholar 

  24. Yamauchi K, Enomoto Y, Otani K, Egashira Y, Iwama T (2018) Prediction of hyperperfusion phenomenon after carotid artery stenting and carotid angioplasty using quantitative DSA with cerebral circulation time imaging. J Neurointerv Surg 10(6):576–579. https://doi.org/10.1136/neurintsurg-2017-013259

    Article  PubMed  Google Scholar 

  25. Yang P, Zhang Y, Zhang L, Zhang Y, Treurniet KM, Chen W, Peng Y, Han H, Wang J, Wang S, Yin C, Liu S, Wang P, Fang Q, Shi H, Yang J, Wen C, Li C, Jiang C, Sun J, Yue X, Lou M, Zhang M, Shu H, Sun D, Liang H, Li T, Guo F, Ke K, Yuan H, Wang G, Yang W, Shi H, Li T, Li Z, Xing P, Zhang P, Zhou Y, Wang H, Xu Y, Huang Q, Wu T, Zhao R, Li Q, Fang Y, Wang L, Lu J, Li Y, Fu J, Zhong X, Wang Y, Wang L, Goyal M, Dippel DWJ, Hong B, Deng B, Roos YBWEM, Majoie CBLM, Liu J, Investigators DIRECT-MT (2020) Endovascular thrombectomy with or without intravenous alteplase in acute stroke. N Engl J Med 382(21):1981–1993. https://doi.org/10.1056/NEJMoa2001123

    Article  PubMed  CAS  Google Scholar 

  26. Zi W, Qiu Z, Li F, Sang H, Wu D, Luo W, Liu S, Yuan J, Song J, Shi Z, Huang W, Zhang M, Liu W, Guo Z, Qiu T, Shi Q, Zhou P, Wang L, Fu X, Liu S, Yang S, Zhang S, Zhou Z, Huang X, Wang Y, Luo J, Bai Y, Zhang M, Wu Y, Zeng G, Wan Y, Wen C, Wen H, Ling W, Chen Z, Peng M, Ai Z, Guo F, Li H, Guo J, Guan H, Wang Z, Liu Y, Pu J, Wang Z, Liu H, Chen L, Huang J, Yang G, Gong Z, Shuai J, Nogueira RG, Yang Q, Trial Investigators DEVT (2021) Effect of endovascular treatment alone vs intravenous alteplase plus endovascular treatment on functional independence in patients with acute ischemic stroke: the DEVT randomized clinical trial. JAMA 325(3):234–243. https://doi.org/10.1001/jama.2020.23523

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Da-zhong Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's note

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

Supplementary Information

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

Liu, J., Gu, Y. & Zhang, Dz. Cerebral circulation time on DSA after thrombectomy associated with hemorrhagic transformation in acute ischemic stroke. Acta Neurochir 166, 64 (2024). https://doi.org/10.1007/s00701-024-05959-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00701-024-05959-6

Keywords

Navigation