• the efficiency of collateral cerebral circulation can be indirectly assessed by evaluating perfusion distal to the occlusion/stenosis
    • in the setting of an acute stroke (⇒ estimation of prognosis and usefulness of thrombectomy, especially when CTP is not available)
    • in chronic steno-occlusive diseases of extracranial arteries (⇒ can help to decide, whether revascularization procedure should be performed)
  • for occlusions at the level of the circle of Willis and distally, leptomeningeal anastomoses (LMA) are mainly engaged
  • DSA, CT/MR angiography, CT/MR perfusion, and neurosonology can be used for evaluation
    • in clinical trials, DSA and CTA are imaging modalities most commonly used

Collateral circulation assessment on DSA

  • DSA allows assessment of collateral circulation dynamics, the disadvantage is invasiveness and necessity of examination of all 4 main arteries
  • it can be used during the endovascular procedure e.g. to assess collateral flow through the ACA in case of M1 occlusion
  • it is neccessary to assess the venous phase as well
 Collateral Grading System [Higashida,2003]
Grade Angiographic collaterals
0 no collaterals visible to the ischemic site
1 slow collaterals to the periphery of the ischemic site with persistence of some of the defect
2 rapid collaterals to the periphery of the ischemic site with persistence of some of the defect and to only a portion of the ischemic territory
3 collaterals with slow but complete angiographic blood flow of the ischemic bed by the late venous phase
4 complete and rapid collateral blood flow to the vascular bed in the entire ischemic territory by retrograde perfusion
Collateral grading score - left ACA occlusion with complete and fast ACA filling via right ICA and AcoA (grade 4)
Pial Collateral Score [Christoforidis et al,2005]
Pial collateral score 5
Collaterals from ACA to occluded MCA territory (Pial collateral score 1)
Pial collateral score

Collateral circulation assessment on CTA

  • in addition to the occlusion detection, CTA also enables the analysis of collateral circulation – the presence of good collateral circulation correlates with a smaller infarct and predicts a better clinical outcome during reperfusion therapy
  • for evaluation, we can use a simple Collateral Score (CS) – a semi-quantitative quick comparison of collateral vessel filling in the territory of the occluded artery compared to the contralateral hemisphere. There is an individual score for a single- and multiphase CTA (mCTA)
  • the disadvantage of the conventional (single-phase) CTA is the static display acquired during only a short interval in the arterial phase, which can lead to an underestimation of collateral circulation due to its late filling
  • information on dynamics is provided by multiphase CTA (MP-CTA, mCTA)
    • a total of 3-4 phases of intracranial CTA is performed (with a reduced dose of X-rays)
    • mCTA can distinguish the absence of collateral from their delayed filling Multifazická CTA - odlišení chybějících kolaterál (horní řádek) od zpomaleného průtoku (dolní řádek) [Yang, 2008]
    • mCTA can distinguish minimal anterograde flow from retrograde collateral flow [Fröhlich, 2012]
A - standard CTA, B - multiphase CTA

Evaluation of CTA source images (CTA-SI):

  • check the circle of Willis – presence and quality of communicants, presence of hypo/aplasia, etc.
  • detect arterial occlusion, try to assess its extent (thrombus length – CBS)
  • compare filling of artery branches on both sides
  • evaluate the level of the retrograde filling (in optimal scenario, the contrast agent reaches the distal part of the thrombus)

Collateral score in the anterior circulation (typically MCA)

Collateral Score (CS) on single-phase CTA [Tan, 2009]
Based on single-phase CTA in patients with unilateral anterior circulation infarct
Score collaterals on CTA
0 absent collateral supply to the occluded MCA territory
1 collateral supply filling ≤50% but >0% of the occluded MCA territory
2 collateral supply filling >50% but <100% of the occluded MCA territory
3 100% collateral supply of the occluded MCA territory
Higher grades are associated with better CT perfusion parameters (MTT, CBF, and CBV), smaller final infarct volume, smaller thrombus extent, and improved outcome
Collateral Score (CS) assessed on CT angiography source images

CTA collateral score 2

Collateral Score (CS) on multi-phase CTA [Menon, 2015]
Score Collaterals on CTA
0 no vessels visible in the affected hemisphere in any phase
1 only a few vessels are visible in the affected hemisphere in any phase
2 a filling delay of two phases in the affected hemisphere with a significantly reduced number of vessels in the ischemic territory, or one phase delay showing regions without visible vessels
3 a filling delay of two phases in the affected hemisphere, or a delay of one phase with a significantly reduced number of vessels in the ischemic territory
4
a filling delay of one phase in the affected hemisphere, but the extent and prominence of pial vessels is the same
5
no filling delay compared to the asymptomatic contralateral hemisphere, normal pial vessels in the affected hemisphere
A score of ≤ 3 indicates a poor prognosis

Case series of mCTA can be seen here

mCTA showing poor collaterals in patient with left MCA occlusion
mCTA showing good collaterals in patient with left MCA occlusion

Basilar Artery on Computed Tomography Angiography (BATMAN) score

  • BATMAN score is a 10-point CTA–based grading system that incorporates thrombus burden and the presence of collaterals
  • the posterior circulation is divided into 6 segments
    • vertebral arteries (VA) – considered as 1 segment = 1 point
    • posterior cerebral artery (PCA) – assessed separately, each 1 point
    • posterior communicant artery (PCom) – assessed separately, each 2 points (or 3 points for fetal PCoA)
    • 3 segments of the basilar artery (BA) – each 1 point
  • patients with a lower BATMAN score were more likely to have a poor outcome – the absence of PCoA (bilateral or unilateral) was the strongest predictor of poor clinical outcome (OR of 6.8) [Alemseged, 2017]
BATMAN score

Posterior circulation CTA score

  • 0 –  no posterior communicating artery (PCoA, PCom, PCOM)
  • 1 –  unilateral PCoA
  • 2 –  bilateral PCoA
  • the presence of bilateral PCoA on CTA was associated with more favorable outcomes in BAO treated with mechanical thrombectomy [Goyal, 2016]
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