Collateral blood vessels in acute ischemic stroke: a physiological window to predict future outcomes

ABSTRACT

Collateral circulation is a physiologic pathway that protects the brain against ischemic injury and can potentially bypass the effect of a blocked artery, thereby influencing ischemic lesion size and growth. Several recent stroke trials have provided information about the role of collaterals in stroke pathophysiology, and collateral perfusion has been recognized to influence arterial recanalization, reperfusion, hemorrhagic transformation, and neurological outcomes after stroke. Our current aim is to summarize the anatomy and physiology of the collateral circulation and to present and discuss a comprehensible review of the related knowledge, particularly the effects of collateral circulation on the time course of ischemic injury and stroke severity, as well as imaging findings and therapeutic implications.

RESUMO

A circulação colateral é um circuito fisiológico de proteção contra alterações isquêmicas que, potencialmente, evita os efeitos de uma oclusão arterial e com isso pode influenciar nas dimensões e no crescimento de uma lesão isquêmica. Vários estudos recentes forneceram informações a respeito do papel das colaterais na fisiopatologia do acidente vascular encefálico isquêmico e demonstraram a capacidade da circulação colateral de influenciar as taxas de reperfusão, recanalização, transformação hemorrágica e com isso desfecho clínico dos pacientes. O objetivo desta revisão é sintetizar a anatomia e a fisiologia da circulação colateral encefálica, apresentando e discutindo, o que se conhece atualmente acerca do seu efeito na cronologia e gravidade da lesão isquêmica, além dos achados de imagens e implicações terapêuticas.

stroke - brain schemia - collateral circulation - tomography - angiography - perfusion

acidente vascular cerebral - isquemia encefálica - circulação colateral - tomografia - angiografia - perfusão

Publikationsverlauf

Eingereicht: 31. Dezember 2015

Angenommen: 08. Februar 2016

Artikel online veröffentlicht:
06. September 2023

• References

• 1 World Health Organization. Global burden of Stroke. Geneva: World Health Organization; 2012 [cited 2015 May 4]. Available from: http://www.who.int/mediacentre/factsheets/fs310/en/
• 2 Truelsen T, Piechowski-Jóźwiak B, Bonita R, Mathers C, Bogousslavsky J, Boysen G. Stroke incidence and prevalence in Europe: a review of available data. Eur J Neurol. 2006;13(6):581-98. doi:10.1111/j.1468-1331.2006.01138.x
• 3 Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med. 2015;372(11):1019-30. doi:10.1056/NEJMoa1414905
• 4 Jauch EC, Saver JL, Adams HP Jr, Bruno A, Connors JJ, Demaerschalk BM et al. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013;44(3):870-947. doi:10.1161/STR.0b013e318284056a
• 5 Martins SC, Freitas GR, Pontes-Neto OM, Pieri A, Moro CH, Jesus PA et al. Guidelines for acute ischemic stroke treatment: part II: stroke treatment. Arq Neuropsiquiatr. 2012;70(11):885-93. doi:10.1590/S0004-282X2012001100012
• 6 Berkhemer OA, Fransen PS, Beumer D, Berg LA, Lingsma HF, Yoo AJ et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med. 2015;372(1):11-20. doi:10.1056/NEJMoa1411587
• 7 Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372(11):1009-18. doi:10.1056/NEJMoa1414792
• 8 Saver JL, Goyal M, Bonafe A, Diener HC, Levy EI, Pereira VM et al. Solitaire with the Intention for Thrombectomy as Primary Endovascular Treatment for Acute Ischemic Stroke (SWIFT PRIME) trial: protocol for a randomized, controlled, multicenter study comparing the Solitaire revascularization device with IV tPA with IV tPA alone in acute ischemic stroke. Int J Stroke. 2015;10(3):439-48. doi:10.1111/ijs.12459
• 9 Leng X, Fang H, Leung TW, Mao C, Miao Z, Liu L et al. Impact of collaterals on the efficacy and safety of endovascular treatment in acute ischaemic stroke: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2015;pii: jnnp-2015-310965. doi:10.1136/jnnp-2015-310965
• 10 Liebeskind DS, Tomsick TA, Foster LD, Yeatts SD, Carrozzella J, Demchuk AM et al. Collaterals at angiography and outcomes in the Interventional Management of Stroke (IMS) III trial. Stroke. 2014;45(3):759-64. doi:10.1161/STROKEAHA.113.004072
• 11 Liebeskind DS, Jahan R, Nogueira RG, Zaidat OO, Saver JL, Investigators S. Impact of collaterals on successful revascularization in Solitaire FR with the intention for thrombectomy. Stroke. 2014;45(7):2036-40. doi:10.1161/STROKEAHA.114.00478
• 12 Faber JE, Chilian WM, Deindl E, Royen N, Simons M. A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol. 2014;34(9):1854-9. doi:10.1161/ATVBAHA.114.303929
• 13 Verma RK, Gralla J, Klinger-Gratz PP, Schankath A, Jung S, Mordasini P et al. Infarction Distribution pattern in acute stroke may predict the extent of leptomeningeal collaterals. PLoS One. 2015;10(9):e0137292. doi:10.1371/journal.pone.0137292
• 14 Jung S, Gilgen M, Slotboom J, El-Koussy M, Zubler C, Kiefer C et al. Factors that determine penumbral tissue loss in acute ischaemic stroke. Brain. 2013;136(12):3554-60. doi:10.1093/brain/awt246
• 15 Liebeskind DS. Collateral circulation. Stroke. 2003;34(9):2279-84. doi:10.1161/01.STR.0000086465.41263.06
• 16 Krishnaswamy A, Klein JP, Kapadia SR. Clinical cerebrovascular anatomy. Catheter Cardiovasc Interv 2010;75(4):530-9. doi:10.1002/ccd.22299
• 17 Sheth SA, Liebeskind DS. Imaging evaluation of collaterals in the brain: physiology and clinical translation. Curr Radiol Rep. 2014;2(1):29. doi:10.1007/s40134-013-0029-5
• 18 Brozici M, Zwan A, Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke. 2003;34(11):2750-62. doi:10.1161/01.STR.0000095791.85737.65
• 19 Shuaib A, Butcher K, Mohammad AA, Saqqur M, Liebeskind DS. Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. Lancet Neurol. 2011;10(10):909-21. doi:10.1016/S1474-4422(11)70195-8
• 20 Lucitti JL, Mackey JK, Morrison JC, Haigh JJ, Adams RH, Faber JE. Formation of the collateral circulation is regulated by vascular endothelial growth factor-A and a disintegrin and metalloprotease family members 10 and 17. Circ Res. 2012;111(12):1539-50. doi:10.1161/CIRCRESAHA.112.279109
• 21 Zhang H, Prabhakar P, Sealock R, Faber JE. Wide genetic variation in the native pial collateral circulation is a major determinant of variation in severity of stroke. J Cereb Blood Flow Metab. 2010;30(5):923-34. doi:10.1038/jcbfm.2010.10
• 22 Sealock R, Zhang H, Lucitti JL, Moore SM, Faber JE. Congenic fine-mapping identifies a major causal locus for variation in the native collateral circulation and ischemic injury in brain and lower extremity. Circ Res. 2014;114(4):660-71. doi:10.1161/CIRCRESAHA.114.302931
• 23 Arsava EM, Vural A, Akpinar E, Gocmen R, Akcalar S, Oguz KK et al. The detrimental effect of aging on leptomeningeal collaterals in ischemic stroke. J Stroke Cerebrovasc Dis. 2014;23(3):421-6. doi:10.1016/j.jstrokecerebrovasdis.2013.03.014
• 24 Menon BK, Smith EE, Coutts SB, Welsh DG, Faber JE, Goyal M et al. Leptomeningeal collaterals are associated with modifiable metabolic risk factors. Ann Neurol. 2013;74(2):241-8. doi:10.1002/ana.23906
• 25 Malik N, Hou Q, Vagal A, Patrie J, Xin W, Michel P et al. Demographic and clinical predictors of leptomeningeal collaterals in stroke patients. J Stroke Cerebrovasc Dis. 2014;23(8):2018-22. doi:10.1016/j.jstrokecerebrovasdis.2014.02.018
• 26 Sporns O, Tononi G, Kötter R. The human connectome: A structural description of the human brain. PLoS Comput Biol. 2005;1(4):e42. doi:10.1371/journal.pcbi.0010042
• 27 Liebeskind DS. Imaging the collaterome: a stroke renaissance. Curr Opin Neurol. 2015;28(1):1-3. doi:10.1097/WCO.20160050201600500171
• 28 Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature. 2010;468(7321):232-43. doi:10.1038/nature09613
• 29 Astrup J, Siesjö BK, Symon L. Thresholds in cerebral ischemia - the ischemic penumbra. Stroke. 1981;12(6):723-5. doi:10.1161/01.STR.12.6.723
• 30 Sakoh M, Ostergaard L, Gjedde A, Røhl L, Vestergaard-Poulsen P, Smith DF et al. Prediction of tissue survival after middle cerebral artery occlusion based on changes in the apparent diffusion of water. J Neurosurg. 2001;95(3):450-8. doi:10.3171/jns.2001.95.3.0450
• 31 Sobesky J, Zaro Weber O, Lehnhardt FG, Hesselmann V, Thiel A, Dohmen C et al. Which time-to-peak threshold best identifies penumbral flow? A comparison of perfusion-weighted magnetic resonance imaging and positron emission tomography in acute ischemic stroke. Stroke. 2004;35(12):2843-7. doi:10.1161/01.STR.0000147043.29399.f6
• 32 Hammer MD, Schwamm L, Starkman S, Schellinger PD, Jovin T, Nogueira R et al. Safety and feasibility of NeuroFlo use in eight- to 24-hour ischemic stroke patients. Int J Stroke. 2012;7(8):655-61. doi:10.1111/j.1747-4949.2011.00719.x
• 33 Zaharchuk G. Better late than never: the long journey for noncontrast arterial spin labeling perfusion imaging in acute stroke. Stroke. 2012;43(4):931-2. doi:10.1161/STROKEAHA.111.644344
• 34 Kamano H, Yoshiura T, Hiwatashi A, Abe K, Togao O, Yamashita K et al. Arterial spin labeling in patients with chronic cerebral artery steno-occlusive disease: correlation with (15)O-PET. Acta Radiol. 2013;54(1):99-106. doi:10.1258/ar.2012.120450
• 35 Liu LP, Xu AD, Wong LK, Wang DZ, Wang YJ. Chinese consensus statement on the evaluation and intervention of collateral circulation for ischemic stroke. CNS Neurosci Ther. 2014;20(3):202-8. doi:10.1111/cns.12226
• 36 Martinon E, Lefevre PH, Thouant P, Osseby GV, Ricolfi F, Chavent A. Collateral circulation in acute stroke: assessing methods and impact: a literature review. J Neuroradiol. 2014;41(2):97-107. doi:10.1016/j.neurad.2014.02.001
• 37 Wintermark M, Sanelli PC, Albers GW, Bello J, Derdeyn C, Hetts SW et al. Imaging recommendations for acute stroke and transient ischemic attack patients: A joint statement by the American Society of Neuroradiology, the American College of Radiology, and the Society of NeuroInterventional Surgery. AJNR Am J Neuroradiol. 2013;34(11):E117-27. doi:10.3174/ajnr.A3690
• 38 Pulli B, Yoo AJ. CT angiography source images with modern multisection CT scanners: delay time from contrast injection to imaging determines correlation with infarct core. AJNR Am J Neuroradiol. 2012;33:E61. doi:10.3174/ajnr.A3039
• 39 Sabarudin A, Subramaniam C, Sun Z. Cerebral CT angiography and CT perfusion in acute stroke detection: a systematic review of diagnostic value. Quant Imaging Med Surg. 2014;4(4):282-90. doi:10.3978/j.issn.2223-4292.2014.07.10
• 40 Shin NY, Kim KE, Park M, Kim YD, Kim DJ, Ahn SJ et al. Dual-phase CT collateral score: a predictor of clinical outcome in patients with acute ischemic stroke. PLoS One. 2014;9(9):e107379. doi:10.1371/journal.pone.0107379
• 41 Mair G, Kummer R, Adami A, White PM, Adams ME, Yan B et al. Observer reliability of CT angiography in the assessment of acute ischaemic stroke: data from the Third International Stroke Trial. Neuroradiology. 2015;57(1):1-9. doi:10.1007/s00234-014-1441-0
• 42 Kortman HG, Smit EJ, Oei MT, Manniesing R, Prokop M, Meijer FJ. 4D-CTA in neurovascular disease: a review. AJNR Am J Neuroradiol. 2015;36(6):1026-33. doi:10.3174/ajnr.A4162
• 43 Mendrik AM, Vonken EJ, Ginneken B, Jong HW, Riordan A, Seeters T et al. TIPS bilateral noise reduction in 4D CT perfusion scans produces high-quality cerebral blood flow maps. Phys Med Biol. 2011;56(13):3857-72. doi:10.1088/0031-9155/56/13/008
• 44 Ernst M, Forkert ND, Brehmer L, Thomalla G, Siemonsen S, Fiehler J et al. Prediction of infarction and reperfusion in stroke by flow- and volume-weighted collateral signal in MR angiography. AJNR Am J Neuroradiol. 2015;36(2):275-82. doi:10.3174/ajnr.A4145
• 45 Aries MJ, Elting JW, De Keyser J, Kremer BP, Vroomen PC. Cerebral autoregulation in stroke: a review of transcranial Doppler studies. Stroke. 2010;41(11):2697-704. doi:10.1161/STROKEAHA.110.594168
• 46 Cheng-Ching E, Frontera JA, Man S, Aoki J, Tateishi Y, Hui FK et al. Degree of collaterals and not time is the determining factor of core infarct volume within 6 hours of stroke onset. AJNR Am J Neuroradiol. 2015;36(7):1272-6. doi:10.3174/ajnr.A4274
• 47 Higashida RT, Furlan AJ, Roberts H, Tomsick T, Connors B, Barr J et al. Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke. 2003;34(8):e109-37. doi:10.1161/01.STR.0000082721.62796.09
• 48 Christoforidis GA, Mohammad Y, Kehagias D, Avutu B, Slivka AP. Angiographic assessment of pial collaterals as a prognostic indicator following intra-arterial thrombolysis for acute ischemic stroke. AJNR Am J Neuroradiol. 2005;26(7):1789-97.
• 49 Liebeskind DS, Jahan R, Nogueira RG, Jovin TG, Lutsep HL, Saver JL. Early arrival at the emergency department is associated with better collaterals, smaller established infarcts and better clinical outcomes with endovascular stroke therapy: SWIFT study. J Neurointerv Surg. 2015; pii:neurintsurg-2015-011758. doi:10.1136/neurintsurg-2015-011758
• 50 Singer OC, Berkefeld J, Nolte CH, Bohner G, Reich A, Wiesmann M et al. Collateral vessels in proximal middle cerebral artery occlusion: the ENDOSTROKE study. Radiology. 2015;274(3):851-8. doi:10.1148/radiol.14140951
• 51 Hwang YH, Kang DH, Kim YW, Kim YS, Park SP, Liebeskind DS. Impact of time-to-reperfusion on outcome in patients with poor collaterals. AJNR Am J Neuroradiol. 2015;36(3):495-500. doi:10.3174/ajnr.A4151
• 52 Singer OC, Berkefeld J, Nolte CH, Bohner G, Haring HP, Trenkler J et al. Mechanical recanalization in basilar artery occlusion: the ENDOSTROKE study. Ann Neurol. 2015;77(3):415-24. doi:10.1002/ana.24336
• 53 McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol. 2012;33(3):576-82. doi:10.3174/ajnr.A2794
• 54 Schramm P, Schellinger PD, Fiebach JB, Heiland S, Jansen O, Knauth M et al. Comparison of CT and CT angiography source images with diffusion-weighted imaging in patients with acute stroke within 6 hours after onset. Stroke. 2002;33(10):2426-32. doi:10.1161/01.STR.0000032244.03134.37
• 55 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(6):533-43. doi:10.1002/ana.21130
• 56 Souza LC, Yoo AJ, Chaudhry ZA, Payabvash S, Kemmling A, Schaefer PW et al. 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(7):1331-6. doi:10.3174/ajnr.A2985
• 57 Yeo LL, Paliwal P, Teoh HL, Seet RC, Chan BP, Ting E et al. Assessment of intracranial collaterals on CT angiography in anterior circulation acute ischemic stroke. AJNR Am J Neuroradiol. 2015;36(2):289-94. doi:10.3174/ajnr.A4117
• 58 Sheth SA, Liebeskind DS. Collaterals in endovascular therapy for stroke. Curr Opin Neurol. 2015;28(1):10-5. doi:10.1097/WCO.20160050201600500166
• 59 Liebeskind DS. Collateral lessons from recent acute ischemic stroke trials. Neurol Res. 2014;36(5):397-402. doi:10.1179/1743132814Y.201600500348
• 60 Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P, Parsons MW. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain. 2009;132(8):2231-8. doi:10.1093/brain/awp155
• 61 Maas MB, Lev MH, Ay H, Singhal AB, Greer DM, Smith WS et al. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke. 2009;40(9):3001-5. doi:10.1161/STROKEAHA.109.552513
• 62 Tan IY, Demchuk AM, Hopyan J, Zhang L, Gladstone D, Wong K et al. CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. AJNR Am J Neuroradiol. 2009;30(3):525-31. doi:10.3174/ajnr.A1408
• 63 Menon BK, Smith EE, Modi J, Patel SK, Bhatia R, Watson TW et al. Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. AJNR Am J Neuroradiol. 2011;32(9):1640-5. doi:10.3174/ajnr.A2564
• 64 Al-Ali F, Jefferson A, Barrow T, Cree T, Louis S, Luke K et al. The capillary index score: rethinking the acute ischemic stroke treatment algorithm. Results from the Borgess Medical Center Acute Ischemic Stroke Registry. J Neurointerv Surg. 2013;5(2):139-43. doi:10.1136/neurintsurg-2011-010146
• 65 Al-Ali F, Elias JJ, Tomsick TA, Liebeskind DS, Broderick JP. Relative Influence of Capillary Index Score, Revascularization, and Time on Stroke Outcomes From the Interventional Management of Stroke III Trial. Stroke. 2015;46L6)1590-4. doi:10.1161/STROKEAHA.115.009066
• 66 Soares BP, Chien JD, Wintermark M. MR and CT monitoring of recanalization, reperfusion, and penumbra salvage: everything that recanalizes does not necessarily reperfuse! Stroke. 2009;40(3 Suppl 1):S24-7. doi:10.1161/STROKEAHA.108.526814
• 67 Spiessberger A, Federau C, Guggenberger R, Kollias S. Influence of leptomeningeal collateral pattern on the prognostic value of mismatch in acute anterior circulation stroke. J Comput Assist Tomogr. 2015;39(2):213-6. doi:10.1097/RCT.20160050201600500204
• 68 Hom J, Dankbaar JW, Soares BP, Schneider T, Cheng SC, Bredno J et al. Blood-brain barrier permeability assessed by perfusion CT predicts symptomatic hemorrhagic transformation and malignant edema in acute ischemic stroke. AJNR Am J Neuroradiol. 2011;32(1):41-8. doi:10.3174/ajnr.A2244
• 69 Jain AR, Jain M, Kanthala AR, Damania D, Stead LG, Wang HZ et al. Association of CT perfusion parameters with hemorrhagic transformation in acute ischemic stroke. AJNR Am J Neuroradiol. 2013;34(10):1895-900. doi:10.3174/ajnr.A3502
• 70 Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B et al. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke. 2011;42(3):693-9. doi:10.1161/STROKEAHA.110.595256
• 71 Saarinen JT, Rusanen H, Sillanpää N. Collateral score complements clot location in predicting the outcome of intravenous thrombolysis. AJNR Am J Neuroradiol. 2014;35(10):1892-6. doi:10.3174/ajnr.A3983