Skip to main navigation menu Skip to main content Skip to site footer

Original article

Vol. 154 No. 7 (2024)

Association between ischaemic stroke aetiology and leptomeningeal collateral status: a retrospective cohort study

  • Lina Sojak
  • Anna M. Toebak
  • Camilla Gallino
  • Tennessee von Streng
  • Salome Rudin
  • Lilian F. Kriemler
  • Annaelle Zietz
  • Benjamin Wagner
  • Henrik Gensicke
  • Raoul Sutter
  • Christian H. Nickel
  • Mira Katan
  • Leo H. Bonati
  • Marios Psychogios
  • Tolga D. Dittrich+
  • Gian Marco De Marchis
DOI
https://doi.org/10.57187/s.3584
Cite this as:
Swiss Med Wkly. 2024;154:3584
Published
30.07.2024

Summary

INTRODUCTION: There is limited understanding of the pathomechanistic relationship between leptomeningeal collateral formation and ischaemic stroke aetiology. We aimed to assess the association of leptomeningeal collateral status and ischaemic stroke aetiology, using the widely recognised “Trial of Org 10172 in Acute Stroke Treatment” (TOAST) classification categorising strokes into five distinct aetiologies.

METHODS: Retrospective study of consecutively admitted adult ischaemic stroke patients at a Swiss stroke centre. Leptomeningeal collateral status was assessed on admission with single-phase CT-angiographies using a validated 4-point score. Patients were categorised into large-artery atherosclerosis (LAA), cardioembolic (CE), small-vessel disease (SVD) and cryptogenic (CG) according to the TOAST classification. We performed ordinal and binary (poor [collaterals filling ≤50% of the occluded territory] vs good [collaterals filling >50% of the occluded territory] collateralisation) logistic regression to evaluate the impact of TOAST aetiology on collateral status.

RESULTS: Among 191 patients, LAA patients had better collateral status compared to non-LAA aetiology (LAA: 2 vs CE: 2 vs SVD: 3 vs CG: 2, pLAA vs non-LAA = 0.04). In weighted multivariate logistic regression, LAA and SVD independently predicted better collateral status (binary models [adjusted odds ratio; aOR]: LAA: 3.72 [1.21–11.44] and SVD: 4.19 [1.21–14.52]; ordinal models [adjusted common odds ratio; acOR]: LAA: 2.26 [95% CI: 1.23–4.15] and SVD: 1.94 [1.03–3.66]), while CE predicted worse collateral status (binary models [aOR]: CE: 0.17 [0.07–0.41]; ordinal models [acOR]: CE: 0.24 [0.11–0.51]).

CONCLUSION: The aetiology of ischaemic stroke is associated with leptomeningeal collateral status on single-phase CT-angiography, with LAA and SVD predicting better and CE predicting worse collateral status.

References

  1. McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol. 2012 Mar;33(3):576–82. 10.3174/ajnr.A2794 DOI: https://doi.org/10.3174/ajnr.A2794
  2. Lima FO, Furie KL, Silva GS, Lev MH, Camargo EC, Singhal AB, et al. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke. 2010 Oct;41(10):2316–22. 10.1161/STROKEAHA.110.592303 DOI: https://doi.org/10.1161/STROKEAHA.110.592303
  3. Berkhemer OA, Jansen IG, Beumer D, Fransen PS, van den Berg LA, Yoo AJ, et al.; MR CLEAN Investigators. Collateral Status on Baseline Computed Tomographic Angiography and Intra-Arterial Treatment Effect in Patients With Proximal Anterior Circulation Stroke. Stroke. 2016 Mar;47(3):768–76. 10.1161/STROKEAHA.115.011788
  4. Park JS, Kwak HS, Chung GH, Hwang S. The Prognostic Value of CT-Angiographic Parameters After Reperfusion Therapy in Acute Ischemic Stroke Patients With Internal Carotid Artery Terminus Occlusion: Leptomeningeal Collateral Status and Clot Burden Score. J Stroke Cerebrovasc Dis. 2018 Oct;27(10):2797–803. 10.1016/j.jstrokecerebrovasdis.2018.06.010 DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.06.010
  5. Jansen IG, Mulder MJ, Goldhoorn RB, Boers AM, van Es AC, Yo LS, et al.; MR CLEAN Registry investigators. Impact of single phase CT angiography collateral status on functional outcome over time: results from the MR CLEAN Registry. J Neurointerv Surg. 2019 Sep;11(9):866–73. 10.1136/neurintsurg-2018-014619 DOI: https://doi.org/10.1136/neurintsurg-2018-014619
  6. García-Tornel Á, Ciolli L, Rubiera M, Requena M, Muchada M, Pagola J, et al. Leptomeningeal Collateral Flow Modifies Endovascular Treatment Efficacy on Large-Vessel Occlusion Strokes. Stroke. 2021 Jan;52(1):299–303. 10.1161/STROKEAHA.120.031338 DOI: https://doi.org/10.1161/STROKEAHA.120.031338
  7. Menon BK, Smith EE, Coutts SB, Welsh DG, Faber JE, Goyal M, et al. Leptomeningeal collaterals are associated with modifiable metabolic risk factors. Annals of Neurology. 2013 2013/08/01;74(2):241-48. 10.1002/ana.23906 DOI: https://doi.org/10.1002/ana.23906
  8. Fujita K, Tanaka K, Yamagami H, Ide T, Ishiyama H, Sonoda K, et al. Detrimental Effect of Chronic Hypertension on Leptomeningeal Collateral Flow in Acute Ischemic Stroke. Stroke. 2019 2019/07/01;50(7):1751-57. 10.1161/STROKEAHA.119.025142 DOI: https://doi.org/10.1161/STROKEAHA.119.025142
  9. Hong Y, Fang J, Ma M, Su W, Zhou M, Tang L, et al. The Hyperdense middle cerebral artery sign is associated with poor leptomeningeal collaterals in acute ischemic stroke: a retrospective study. BMC Neurol. 2022 Feb;22(1):51. 10.1186/s12883-022-02566-9 DOI: https://doi.org/10.1186/s12883-022-02566-9
  10. Guglielmi V, LeCouffe NE, Zinkstok SM, Compagne KC, Eker R, Treurniet KM, et al.; MR-CLEAN Registry Investigators. Collateral Circulation and Outcome in Atherosclerotic Versus Cardioembolic Cerebral Large Vessel Occlusion. Stroke. 2019 Dec;50(12):3360–8. 10.1161/STROKEAHA.119.026299
  11. Rebello LC, Bouslama M, Haussen DC, Grossberg JA, Dehkharghani S, Anderson A, et al. Stroke etiology and collaterals: atheroembolic strokes have greater collateral recruitment than cardioembolic strokes. Eur J Neurol. 2017 Jun;24(6):762–7. 10.1111/ene.13287 DOI: https://doi.org/10.1111/ene.13287
  12. Hassler E, Kneihsl M, Deutschmann H, Hinteregger N, Magyar M, Wießpeiner U, et al. Relationship between stroke etiology and collateral status in anterior circulation large vessel occlusion. J Neurol. 2020 Nov;267(11):3362–70. 10.1007/s00415-020-10009-z DOI: https://doi.org/10.1007/s00415-020-10009-z
  13. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993 Jan;24(1):35–41. 10.1161/01.STR.24.1.35 DOI: https://doi.org/10.1161/01.STR.24.1.35
  14. Dittrich TD, Aujesky M, Rudin S, Zietz A, Wagner B, Polymeris A, et al. Apical pulmonary lesions suspected of malignancy visible on neck CT angiography performed for acute stroke: Prevalence, treatment, and clinical implications – the PLEURA study. Eur Stroke J. 2023 Jun;8(2):549-56. 23969873231151488. 10.1177/23969873231151488 DOI: https://doi.org/10.1177/23969873231151488
  15. Tan JC, Dillon WP, Liu S, Adler F, Smith WS, Wintermark M. Systematic comparison of perfusion-CT and CT-angiography in acute stroke patients. Ann Neurol. 2007 Jun;61(6):533–43. 10.1002/ana.21130 DOI: https://doi.org/10.1002/ana.21130
  16. Silimon N, Drop B, Clénin L, Nedeltchev K, Kahles T, Tarnutzer AA, et al. Ischaemic stroke despite antiplatelet therapy: causes and outcomes. Eur Stroke J. 2023 Sep;8(3):692–702. 10.1177/23969873231174942 DOI: https://doi.org/10.1177/23969873231174942
  17. Sinha A, Stanwell P, Beran RG, Calic Z, Killingsworth MC, Bhaskar SM. Stroke Aetiology and Collateral Status in Acute Ischemic Stroke Patients Receiving Reperfusion Therapy-A Meta-Analysis. Neurol Int. 2021 Nov;13(4):608–21. 10.3390/neurolint13040060 DOI: https://doi.org/10.3390/neurolint13040060
  18. Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, et al.; ESCAPE Trial Investigators. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med. 2015 Mar;372(11):1019–30. 10.1056/NEJMoa1414905
  19. Seyman E, Shaim H, Shenhar-Tsarfaty S, Jonash-Kimchi T, Bornstein NM, Hallevi H. The collateral circulation determines cortical infarct volume in anterior circulation ischemic stroke. BMC Neurol. 2016 Oct;16(1):206. 10.1186/s12883-016-0722-0 DOI: https://doi.org/10.1186/s12883-016-0722-0
  20. Al-Dasuqi K, Payabvash S, Torres-Flores GA, Strander SM, Nguyen CK, Peshwe KU, et al. Effects of Collateral Status on Infarct Distribution Following Endovascular Therapy in Large Vessel Occlusion Stroke. Stroke. 2020 Sep;51(9):e193–202. 10.1161/STROKEAHA.120.029892 DOI: https://doi.org/10.1161/STROKEAHA.120.029892
  21. Olthuis SG, Pirson FA, Pinckaers FM, Hinsenveld WH, Nieboer D, Ceulemans A, et al.; MR CLEAN-LATE investigators. Endovascular treatment versus no endovascular treatment after 6-24 h in patients with ischaemic stroke and collateral flow on CT angiography (MR CLEAN-LATE) in the Netherlands: a multicentre, open-label, blinded-endpoint, randomised, controlled, phase 3 trial. Lancet. 2023 Apr;401(10385):1371–80. 10.1016/S0140-6736(23)00575-5
  22. Seker F, Qureshi MM, Möhlenbruch MA, Nogueira RG, Abdalkader M, Ribo M, et al. Reperfusion Without Functional Independence in Late Presentation of Stroke With Large Vessel Occlusion. Stroke. 2022 2022/12/01;53(12):3594-604. 10.1161/STROKEAHA.122.039476
  23. Weyland CS, Vey JA, Mokli Y, Feisst M, Kieser M, Herweh C, et al. Full Reperfusion Without Functional Independence After Mechanical Thrombectomy in the Anterior Circulation. Clinical Neuroradiology. 2022 2022/12/01;32(4):987-95. 10.1007/s00062-022-01166-x DOI: https://doi.org/10.1007/s00062-022-01166-x
  24. Nadine Felizitas B, Mohamad El A, Chaim G, William M, Anna Maria R, Adrien B, et al. Leptomeningeal collaterals regulate reperfusion in ischemic stroke. bioRxiv. 2023:2023.02.25.529915.
  25. Helisch A, Schaper W. Arteriogenesis: the development and growth of collateral arteries. Microcirculation. 2003 Jan;10(1):83–97. 10.1080/mic.10.1.83.97 DOI: https://doi.org/10.1080/713773590

Most read articles by the same author(s)

<< < 1 2