Skip to main content

Advertisement

Log in

Collaterals and Elusive Ischemic Penumbra

  • Review
  • Published:
Translational Stroke Research Aims and scope Submit manuscript

Abstract

As alternative blood supply routes, collateral blood vessels can play a crucial role in determining patient outcomes in acute and chronic intracranial occlusive diseases. Studies have shown that increased collateral circulation can improve functional outcomes and reduce mortality, particularly in those who are not eligible for reperfusion therapy. This article aims to discuss the anatomy and physiology of collateral circulation, describe current imaging tools used to measure collateral circulation, and identify the factors that influence collateral status.

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
Fig. 4

Similar content being viewed by others

Data Availability

Not applicable.

References

  1. Liebeskind DS. Collateral Circulation. Stroke. 2003;34:2279–84. https://doi.org/10.1161/01.STR.0000086465.41263.06.

    Article  Google Scholar 

  2. Vasquez HE, Murlimanju BV, Shrivastava A, Durango-Espinosa YA, Joaquim AF, Garcia-Ballestas E, Moscote-Salazar LR, Agrawal A. Intracranial collateral circulation and its role in neurovascular pathology. Egypt J Neurosurg. 2021;36:2. https://doi.org/10.1186/s41984-020-00095-6.

    Article  Google Scholar 

  3. Bang OY, Goyal M, Liebeskind DS. Collateral Circulation in Ischemic Stroke. Stroke. 2015;46:3302–9. https://doi.org/10.1161/STROKEAHA.115.010508.

    Article  Google Scholar 

  4. Gunnal SA, Farooqui MS, Wabale RN. Anatomical variations of the circulus arteriosus in cadaveric human brains. Neurol Res Int. 2014;2014:687281. https://doi.org/10.1155/2014/687281.

    Article  CAS  Google Scholar 

  5. Faber JE, Chilian WM, Deindl E, van Royen N, Simons M. A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol. 2014;34:1854–9. https://doi.org/10.1161/atvbaha.114.303929.

    Article  CAS  Google Scholar 

  6. Malhotra K, Liebeskind DS. Collaterals in ischemic stroke. Brain Hemorrhages. 2020;1:6–12. https://doi.org/10.1016/j.hest.2019.12.003.

    Article  Google Scholar 

  7. Bang OY, Saver JL, Kim SJ, Kim G-M, Chung C-S, Ovbiagele B, Lee KH, Liebeskind DS. Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke. Stroke. 2011;42:2235–9. https://doi.org/10.1161/STROKEAHA.110.604603.

    Article  Google Scholar 

  8. Liebeskind DS, Saber H, Xiang B, Jadhav AP, Jovin TG, Haussen DC, Budzik RF, Bonafe A, Bhuva P, Yavagal DR, Hanel RA, Ribo M, Cognard C, Sila C, Hassan AE, Smith WS, Saver JL, Nogueira RG. Collateral circulation in thrombectomy for stroke after 6 to 24 hours in the DAWN trial. Stroke. 0:STROKEAHA.121.034471. https://doi.org/10.1161/STROKEAHA.121.034471

  9. Fiehler J, Remmele C, Kucinski T, Rosenkranz M, Thomalla G, Weiller C, Zeumer H, Röther J. Reperfusion after severe local perfusion deficit precedes hemorrhagic transformation: an MRI study in acute stroke patients. Cerebrovasc Dis (Basel Switzerland). 2005;19:117–24. https://doi.org/10.1159/000083180.

    Article  Google Scholar 

  10. Bang OY, Saver JL, Kim SJ, Kim G-M, Chung C-S, Ovbiagele B, Lee KH, Liebeskind DS. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke. 2011;42:693–9. https://doi.org/10.1161/strokeaha.110.595256.

    Article  Google Scholar 

  11. Souza LC, Yoo AJ, Chaudhry ZA, Payabvash S, Kemmling A, Schaefer PW, Hirsch JA, Furie KL, González RG, Nogueira RG, Lev MH. Malignant CTA collateral profile is highly specific for large admission DWI infarct core and poor outcome in acute stroke. AJNR Am J Neuroradiol. 2012;33:1331–6. https://doi.org/10.3174/ajnr.A2985.

    Article  CAS  Google Scholar 

  12. Tong E, Patrie J, Tong S, Evans A, Michel P, Eskandari A, Wintermark M. Time-resolved CT assessment of collaterals as imaging biomarkers to predict clinical outcomes in acute ischemic stroke. Neuroradiology. 2017;59:1101–9. https://doi.org/10.1007/s00234-017-1914-z.

    Article  Google Scholar 

  13. Choi JY, Kim EJ, Hong JM, Lee SE, Lee JS, Lim YC, Kim HS. Conventional enhancement CT: a valuable tool for evaluating pial collateral flow in acute ischemic stroke. Cerebrovasc Dis. 2011;31:346–52. https://doi.org/10.1159/000322602.

    Article  Google Scholar 

  14. Bhatia R, Bal SS, Shobha N, Menon BK, Tymchuk S, Puetz V, Dzialowski I, Coutts SB, Goyal M, Barber PA, Watson T, Smith EE, Demchuk AM. CT Angiographic source images predict outcome and final infarct volume better than noncontrast CT in proximal vascular occlusions. Stroke. 2011;42:1575–80. https://doi.org/10.1161/STROKEAHA.110.603936.

    Article  Google Scholar 

  15. Schramm P, Schellinger PD, Klotz E, Kallenberg K, Fiebach JB, Külkens S, Heiland S, Knauth M, Sartor K. Comparison of perfusion computed tomography and computed tomography angiography source images with perfusion-weighted imaging and diffusion-weighted imaging in patients with acute stroke of less than 6 hours’ duration. Stroke. 2004;35:1652–8. https://doi.org/10.1161/01.STR.0000131271.54098.22.

    Article  Google Scholar 

  16. Lee KH, Lee SJ, Cho SJ, Na DG, Byun HS, Kim YB, Song HJ, Jin IS, Chung CS. Usefulness of triphasic perfusion computed tomography for intravenous thrombolysis with tissue-type plasminogen activator in acute ischemic stroke. Arch Neurol. 2000;57:1000–8. https://doi.org/10.1001/archneur.57.7.1000.

    Article  CAS  Google Scholar 

  17. Dundamadappa S, Iyer K, Agrawal A, Choi DJ. Multiphase CT Angiography: A useful technique in acute stroke imaging—collaterals and beyond. Am J Neuroradiol. 2020. https://doi.org/10.3174/ajnr.A6889.

    Article  Google Scholar 

  18. Lee SJ, Lee KH, Na DG, Byun HS, Kim YB, Shon YM, Cho SJ, Lee J, Chung CS, Hong SC. Multiphasic helical computed tomography predicts subsequent development of severe brain edema in acute ischemic stroke. Arch Neurol. 2004;61:505–9. https://doi.org/10.1001/archneur.61.4.505.

    Article  Google Scholar 

  19. Menon BK, d’Esterre CD, Qazi EM, Almekhlafi M, Hahn L, Demchuk AM, Goyal M. Multiphase CT Angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology. 2015;275:510–20. https://doi.org/10.1148/radiol.15142256.

    Article  Google Scholar 

  20. Albers GW, Marks MP, Kemp S, Christensen S, Tsai JP, Ortega-Gutierrez S, McTaggart RA, Torbey MT, Kim-Tenser M, Leslie-Mazwi T, Sarraj A, Kasner SE, Ansari SA, Yeatts SD, Hamilton S, Mlynash M, Heit JJ, Zaharchuk G, Kim S, Carrozzella J, Palesch YY, Demchuk AM, Bammer R, Lavori PW, Broderick JP, Lansberg MG. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med. 2018;378:708–18. https://doi.org/10.1056/NEJMoa1713973.

    Article  Google Scholar 

  21. Nogueira RG, Jadhav AP, Haussen DC, Bonafe A, Budzik RF, Bhuva P, Yavagal DR, Ribo M, Cognard C, Hanel RA, Sila CA, Hassan AE, Millan M, Levy EI, Mitchell P, Chen M, English JD, Shah QA, Silver FL, Pereira VM, Mehta BP, Baxter BW, Abraham MG, Cardona P, Veznedaroglu E, Hellinger FR, Feng L, Kirmani JF, Lopes DK, Jankowitz BT, Frankel MR, Costalat V, Vora NA, Yoo AJ, Malik AM, Furlan AJ, Rubiera M, Aghaebrahim A, Olivot J-M, Tekle WG, Shields R, Graves T, Lewis RJ, Smith WS, Liebeskind DS, Saver JL, Jovin TG. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med. 2017;378:11–21. https://doi.org/10.1056/NEJMoa1706442.

    Article  Google Scholar 

  22. Ma H, Campbell BCV, Parsons MW, Churilov L, Levi CR, Hsu C, Kleinig TJ, Wijeratne T, Curtze S, Dewey HM, Miteff F, Tsai C-H, Lee J-T, Phan TG, Mahant N, Sun M-C, Krause M, Sturm J, Grimley R, Chen C-H, Hu C-J, Wong AA, Field D, Sun Y, Barber PA, Sabet A, Jannes J, Jeng J-S, Clissold B, Markus R, Lin C-H, Lien L-M, Bladin CF, Christensen S, Yassi N, Sharma G, Bivard A, Desmond PM, Yan B, Mitchell PJ, Thijs V, Carey L, Meretoja A, Davis SM, Donnan GA. Thrombolysis guided by perfusion imaging up to 9 hours after onset of stroke. N Engl J Med. 2019;380:1795–803. https://doi.org/10.1056/NEJMoa1813046.

    Article  Google Scholar 

  23. Demeestere J, Wouters A, Christensen S, Lemmens R, Lansberg MG. Review of perfusion imaging in acute ischemic stroke. Stroke. 2020;51:1017–24. https://doi.org/10.1161/STROKEAHA.119.028337.

    Article  Google Scholar 

  24. 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;61:533–43. https://doi.org/10.1002/ana.21130.

    Article  Google Scholar 

  25. Lin L, Chen C, Tian H, Bivard A, Spratt N, Levi CR, Parsons MW. Perfusion computed tomography accurately quantifies collateral flow after acute ischemic stroke. Stroke. 2020;51:1006–9. https://doi.org/10.1161/STROKEAHA.119.028284.

    Article  Google Scholar 

  26. Nael K, Sakai Y, Larson J, Goldstein J, Deutsch J, Awad AJ, Pawha P, Aggarwal A, Fifi J, Deleacy R, Yaniv G, Wintermark M, Liebeskind DS, Shoirah H, Mocco J. CT perfusion collateral index in assessment of collaterals in acute ischemic stroke with delayed presentation: comparison to single phase CTA. J Neuroradiol = J Neuroradiol. 2021; https://doi.org/10.1016/j.neurad.2021.11.002.

  27. Olivot JM, Mlynash M, Inoue M, Marks MP, Wheeler HM, Kemp S, Straka M, Zaharchuk G, Bammer R, Lansberg MG, Albers GW. Hypoperfusion intensity ratio predicts infarct progression and functional outcome in the DEFUSE 2 cohort. Stroke. 2014;45:1018–23. https://doi.org/10.1161/STROKEAHA.113.003857.

    Article  Google Scholar 

  28. Nomani AZ, KamtchumTatuene J, Rempel JL, Jeerakathil T, Winship IR, Khan KA, Buck BH, Shuaib A, Jickling GC. Association of CT-based hypoperfusion index with ischemic core enlargement in patients with medium and large vessel stroke. Neurology. 2021;97:e2079–87. https://doi.org/10.1212/wnl.0000000000012855.

    Article  CAS  Google Scholar 

  29. Tsui B, Chen I, Qiao J, Khatibi K, Mejia LP, Liebeskind DS, Sharma LK, Tateshima S, Hosseini MB, Colby G, Nour M, Salamon N, Saver J, Jahan R, Duckwiler G, Nael K. Abstract P348: Perfusion collateral index vs. hypoperfusion intensity ratio in assessment of angiographic collateral scores in patients with acute ischemic stroke. Stroke. 2021;52:AP348–AP348. https://doi.org/10.1161/str.52.suppl_1.P348.

    Article  Google Scholar 

  30. Kim SJ, Ha YS, Ryoo S, Noh HJ, Ha S-Y, Bang OY, Kim G-M, Chung C-S, Lee KH. Sulcal effacement on fluid attenuation inversion recovery magnetic resonance imaging in hyperacute stroke. Stroke. 2012;43:386–92. https://doi.org/10.1161/STROKEAHA.111.638106.

    Article  Google Scholar 

  31. Lee KY, Latour LL, Luby M, Hsia AW, Merino JG, Warach S. Distal hyperintense vessels on FLAIR: an MRI marker for collateral circulation in acute stroke? Neurology. 2009;72:1134–9. https://doi.org/10.1212/01.wnl.0000345360.80382.69.

    Article  CAS  Google Scholar 

  32. Nael K, Khan R, Choudhary G, Meshksar A, Villablanca P, Tay J, Drake K, Coull BM, Kidwell CS. Six-minute magnetic resonance imaging protocol for evaluation of acute ischemic stroke: pushing the boundaries. Stroke. 2014;45:1985–91. https://doi.org/10.1161/strokeaha.114.005305.

    Article  Google Scholar 

  33. Bang OY, Chung J-W, Son JP, Ryu W-S, Kim D-E, Seo W-K, Kim G-M, Kim Y-C. Multimodal MRI-based triage for acute stroke therapy: challenges and progress. Front Neurol. 2018, 9. https://doi.org/10.3389/fneur.2018.00586.

  34. Lee MJ, Son JP, Kim SJ, Ryoo S, Woo S-Y, Cha J, Kim G-M, Chung C-S, Lee KH, Bang OY. Predicting collateral status with magnetic resonance perfusion parameters. Stroke. 2015;46:2800–7. https://doi.org/10.1161/STROKEAHA.115.009828.

    Article  Google Scholar 

  35. Nael K, Doshi A, De Leacy R, Puig J, Castellanos M, Bederson J, Naidich TP, Mocco J, Wintermark M. MR perfusion to determine the status of collaterals in patients with acute ischemic stroke: a look beyond time maps. Am J Neuroradiol. 2018;39:219–25. https://doi.org/10.3174/ajnr.A5454.

    Article  CAS  Google Scholar 

  36. Haller S, Zaharchuk G, Thomas DL, Lovblad KO, Barkhof F, Golay X. Arterial spin labeling perfusion of the brain: emerging clinical applications. Radiology. 2016;281:337–56. https://doi.org/10.1148/radiol.2016150789.

    Article  Google Scholar 

  37. Zaharchuk G, Do HM, Marks MP, Rosenberg J, Moseley ME, Steinberg GK. Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke. 2011;42:2485–91. https://doi.org/10.1161/STROKEAHA.111.616466.

    Article  Google Scholar 

  38. Guan J, Zhang S, Zhou Q, Li C, Lu Z. Usefulness of transcranial doppler ultrasound in evaluating cervical-cranial collateral circulations. Interv Neurol. 2013;2:8–18. https://doi.org/10.1159/000354732.

    Article  Google Scholar 

  39. Wiegers EJA, Mulder MJHL, Jansen IGH, Venema E, Compagne KCJ, Berkhemer OA, Emmer BJ, Marquering HA, Es ACGMv, Sprengers ME, Zwam WHv, Oostenbrugge RJv, Roos YBWEM, Majoie CBLM, Roozenbeek B, Lingsma HF, Dippel DWJ, Lugt Avd, Boiten J, Vos JA, Brouwer J, Hartog SJd, Hinsenveld WH, Kappelhof M, Goldhoorn R-JB, Coutinho JM, Schonewille WJ, Vos JA, Wermer MJH, Walderveen MAAv, Staals J, Hofmeijer J, Martens JM, Nijeholt GJLà, Bruijn SFd, Dijk LCv, Worp HBvd, Lo RH, Dijk EJv, Boogaarts HD, Vries Jd, Kort PLMd, Tuijl Jv, Peluso JJP, Fransen P, Berg JSPvd, Hasselt BAAMv, Aerden LAM, Dallinga RJ, Uyttenboogaart M, Eschgi O, Bokkers RPH, Schreuder THCML, Heijboer RJJ, Keizer K, Yo LSF, Hertog HMd, Sturm EJC, Brouwers P, Nijeholt GJLà, Walderveen MAAv, Jenniskens SFM, Berg Rvd, Yoo AJ, Beenen LFM, Postma AA, Roosendaal SD, Kallen BFWvd, Wijngaard IRvd, Martens JM, Yo LSF, Vos JA, Bot J, Doormaal P-Jv, Meijer A, Ghariq E, Bokkers RPH, Proosdij MPv, Krietemeijer GM, Peluso JP, Boogaarts HD, Lo R, Gerrits D, Dinkelaar W, Appelman APA, Hammer B, Pegge S, Hoorn Avd, Vinke S, Nijeholt GJLà, Boiten J, Vos JA, Schonewille WJ, Hofmeijer J, Martens JM, Worp HBvd, Lo RH, Hofmeijer J, Flach HZ, Ghannouti Ne, Sterrenberg M, Puppels C, Pellikaan W, Sprengers R, Elfrink M, Simons M, Vossers M, Meris Jd, Vermeulen T, Geerlings A, Vemde Gv, Simons T, Rijswijk Cv, Messchendorp G, Nicolaij N, Bongenaar H, Bodde K, Kleijn S, Lodico J, Droste H, Wollaert M, Verheesen S, Jeurrissen D, Bos E, Drabbe Y, Sandiman M, Elfrink M, Aaldering N, Zweedijk B, Khalilzada M, Vervoort J, Droste H, Nicolaij N, Simons M, Ponjee E, Romviel S, Kanselaar K, Bos E, Barning D, Chalos V, Geuskens RR, Straaten Tv, Ergezen S, Harmsma RRM, Muijres D, Jong Ad, Boers AMM, Huguet J, Groot PFC, Mens MA, Kranendonk KRv, Treurniet KM, Tolhuisen ML, Alves H, Weterings AJ, Kirkels ELF, Voogd EJHF, Schupp LM, Collette S, Groot AED, LeCouffe NE, Konduri PR, Prasetya H, Arrarte-Terreros N, Ramos LA. Clinical and imaging determinants of collateral status in patients with acute ischemic stroke in MR CLEAN trial and registry. Stroke. 2020, 51:1493-1502. https://doi.org/10.1161/STROKEAHA.119.027483.

  40. Broderick JP, Palesch YY, Demchuk AM, Yeatts SD, Khatri P, Hill MD, Jauch EC, Jovin TG, Yan B, Silver FL, von Kummer R, Molina CA, Demaerschalk BM, Budzik R, Clark WM, Zaidat OO, Malisch TW, Goyal M, Schonewille WJ, Mazighi M, Engelter ST, Anderson C, Spilker J, Carrozzella J, Ryckborst KJ, Janis LS, Martin RH, Foster LD, Tomsick TA. Endovascular therapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368:893–903. https://doi.org/10.1056/NEJMoa1214300.

    Article  CAS  Google Scholar 

  41. 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. 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. 2019;50:e344–418. https://doi.org/10.1161/STR.0000000000000211.

    Article  Google Scholar 

  42. Casaubon LK, Boulanger JM, Blacquiere D, Boucher S, Brown K, Goddard T, Gordon J, Horton M, Lalonde J, LaRivière C, Lavoie P, Leslie P, McNeill J, Menon BK, Moses B, Penn M, Perry J, Snieder E, Tymianski D, Foley N, Smith EE, Gubitz G, Hill MD, Glasser E, Lindsay P. Canadian stroke best practice recommendations: hyperacute stroke care guidelines, update 2015. Int J Stroke Off J Int Stroke Soc. 2015;10:924–40. https://doi.org/10.1111/ijs.12551.

    Article  Google Scholar 

  43. Liu L, Ding J, Leng X, Pu Y, Huang L-A, Xu A, Wong KSL, Wang X, Wang Y. Guidelines for evaluation and management of cerebral collateral circulation in ischaemic stroke 2017. Stroke Vasc Neurol. 2018;3:117–30. https://doi.org/10.1136/svn-2017-000135.

    Article  Google Scholar 

  44. Parthasarathy R, Kate M, Rempel JL, Liebeskind DS, Jeerakathil T, Butcher KS, Shuaib A. Prognostic evaluation based on cortical vein score difference in stroke. Stroke. 2013;44:2748–54. https://doi.org/10.1161/strokeaha.113.001231.

    Article  Google Scholar 

  45. Parthasarathy R, Sohn S-I, Jeerakathil T, Kate MP, Mishra SM, Nambiar VK, Ahmad A, Menon BK, Shuaib A. A combined arterial and venous grading scale to predict outcome in anterior circulation ischemic stroke. J Neuroimaging. 2015;25:969–77. https://doi.org/10.1111/jon.12260.

    Article  Google Scholar 

  46. Markus HS. Cerebral perfusion and stroke. J Neurol Neurosurg Psychiatry. 2004;75:353–61. https://doi.org/10.1136/jnnp.2003.025825.

    Article  CAS  Google Scholar 

  47. Vagal A, Aviv R, Sucharew H, Reddy M, Hou Q, Michel P, Jovin T, Tomsick T, Wintermark M, Khatri P. Collateral clock is more important than time clock for tissue fate. Stroke. 2018;49:2102–7. https://doi.org/10.1161/STROKEAHA.118.021484.

    Article  Google Scholar 

  48. Schirmer SH, van Nooijen FC, Piek JJ, van Royen N. Stimulation of collateral artery growth: travelling further down the road to clinical application. Heart (British Cardiac Soc). 2009;95:191–7. https://doi.org/10.1136/hrt.2007.136119.

    Article  CAS  Google Scholar 

  49. Fujita K, Tanaka K, Yamagami H, Ide T, Ishiyama H, Sonoda K, Satow T, Takahashi JC, Ihara M, Koga M, Yokota T, Toyoda K. Detrimental effect of chronic hypertension on leptomeningeal collateral flow in acute ischemic stroke. Stroke. 2019;50:1751–7. https://doi.org/10.1161/STROKEAHA.119.025142.

    Article  CAS  Google Scholar 

  50. Cipolla MJ, Chan S-L. Impact of acute and chronic hypertension on changes in pial collateral tone in vivo during transient ischemia. Hypertension. 2020;76:1019–26. https://doi.org/10.1161/HYPERTENSIONAHA.120.15356.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Equal contribution from Patel and Liebeskind.

Corresponding author

Correspondence to Smit D. Patel.

Ethics declarations

Ethical Approval and Consent to Participate

Not applicable.

Human and Animal Ethics

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

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.

Highlights

• Anatomy of the brain’s collateral circulation.

• Vascular biology of the brain’s collateral circulation.

• Measurement of collateral flow and the ischemic penumbra.

• Clinical and imaging definitions of collateral status.

• Impact of collateral flow on evolution of the penumbra and penumbral salvage after stroke.

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

Patel, S.D., Liebeskind, D. Collaterals and Elusive Ischemic Penumbra. Transl. Stroke Res. 14, 3–12 (2023). https://doi.org/10.1007/s12975-022-01116-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12975-022-01116-2

Keywords

Navigation