• collateral cerebral circulation plays a critical role in maintaining blood flow to ischemic areas in the acute, subacute, or chronic phases after ischemic stroke
    • good collateral circulation is associated with a favorable functional outcome and a lower risk of stroke recurrence
    • in occlusions at the level of the circle of Willis and distally, leptomeningeal anastomoses (LMA) are mainly engaged
  • the efficiency of collateral cerebral circulation can be assessed by evaluating perfusion distal to the occlusion/stenosis
    • in acute stroke (⇒ estimation of prognosis and usefulness of thrombectomy, especially when CTP is not available)
    • in the management of chronic extracranial steno-occlusive diseases (⇒  may help decide whether to perform revascularization)
  • imaging methods used to assess cerebral collateral circulation:
    • digital subtraction angiography (DSA)
      • gold standard; currently used as a part of endovascular procedure;  evaluation by the ASITN/SIR collateral scale helps predict the risk and benefit of acute endovascular treatment
    • CT angiography
      • traditional single-phase CTA (more reliable than MRA)
      • CTA source image
      • multiphase CTA (dynamic CTA)
    • MR angiography
      • time-of-flight MRA (TOF-MRA)
      • phase-contrast MRA
      • quantitative MRA (QMRA)
    • CT perfusion
    • MR perfusion
    • neurosonology
  • DSA is considered a gold standard; however, noninvasive imaging modalities are more commonly used
  • there is no general agreement on the optimal collateral grading system based on noninvasive imaging modalities; further research is needed
Imaging methods to assess the structure of the cerebral collateral circulation Imaging methods to assess the function of the cerebral collateral circulation
  • DSA
  • CTA (single phase)
  • TOF-MRA
  • neurosonology
  • detection of cerebrovascular reserve 
    • TCD/TCCD
    • xenon CT
    • single-photon emission CT (SPECT)
    • positron emission tomography (PET)
    • CT perfusion
    • MR perfusion
  • quantitative MRA (QMRA)
  • neurosonology

Collateral circulation assessment on DSA

  • DSA allows the assessment of collateral circulation dynamics; disadvantages are invasiveness and the need to examine all 4 main arteries
  • it can be used during the endovascular procedure, e.g., to assess the collateral flow through the ACA in the case of M1 occlusion
  • it is also necessary to assess the venous phase
The American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) grading system  [Higashida,2003]
Grade Angiographic collaterals
0 no collaterals visible in the ischemic area
1 slow collaterals to the periphery of the ischemic area with persisting defect
2 fast collaterals to the periphery of the ischemic area with some persisting defect
3 collaterals with slow but complete filling of the ischemic area in the late venous phase
4 complete and rapid blood flow to the entire ischemic territory by retrograde perfusion
Collateral grading score - left ACA occlusion with complete and rapid ACA filling via right ICA and AcoA (grade 4)
Pial Collateral Score [Christoforidis et al,2005]
  • another DSA-based collateral grading system, that is less frequently used in clinical practice
    • grade 1 – collaterals reconstitute the entire distal portion of the occluded vessel segment
    • grade 2 – collaterals reconstitute vessels in the proximal portion of the segment adjacent to the occluded vessel
    • grade 3 – collaterals reconstitute vessels in the distal portion of the segment adjacent to the occluded vessel
    • grade 4 – collaterals reconstitute vessels two segments distal to the occluded vessel
    • grade 5 – little or no significant reconstitution of the territory of the occluded vessel
  • good collateral status (grades 1 and 2) has been correlated with smaller infarct volume, lower risk of hemorrhagic transformation, and lower modified Rankin Scale (mRS) at discharge
Pial collateral score 5
Collaterals from the ACA to the occluded MCA territory (Pial collateral score 1)
Pial collateral score

Collateral circulation assessment on CTA

  • in addition to the detection of occlusions, CTA also enables the analysis of collateral circulation; the presence of good collateral circulation correlates with smaller infarct size and predicts a better clinical outcome during reperfusion therapy
  • a simple Collateral Score (CS) may be used for evaluation
    • a semi-quantitative rapid comparison of collateral filling in the territory of the occluded artery compared to the contralateral hemisphere
    • a single-phase and multiphase CTA (mCTA) can be used
  • a limitation of conventional (single-phase) CTA is its static presentation; it is acquired during a short interval in the arterial phase, which can lead to an underestimation of delayed collateral circulation
  • dynamic information is provided by multiphase CTA (MP-CTA / mCTA)
    • a total of 3-4 phases of intracranial CTA are performed using a reduced X-ray dose
    • mCTA can differentiate between the absence of collaterals and delayed filling  [Yang, 2008]
    • mCTA can distinguish between minimal anterograde flow and retrograde collateral flow [Fröhlich, 2012]
Multiphase CTA - distinguishing missing collaterasl from slowed flow antero- or retrograde flow
A - standard CTA, B - multiphase CTA

The evaluation of CTA source images (CTA-SI) includes the following steps:

  • check the circle of Willis for the presence and quality of communicating arteries, hypo/aplasia, etc.
  • identify arterial occlusions and try to estimate their extent (thrombus length ⇒  Clot Burden Score (CBS)
  • compare the filling of the arterial branches in both hemispheres
  • evaluate the degree of the retrograde filling (optimally, the contrast agent should reach the distal end of the thrombus)

Collateral score in the anterior circulation (typically MCA)

Miteff collateral grading on single-phase CTA (Miteff, 2009)
good major MCA branches are reconstituted distal to the occlusion
moderate some MCA branches are shown in the Sylvian fissure
poor only the distal superficial MCA branches are reconstituted
Collateral status is graded in maximum intensity projection reconstructions (MIP) of single-phase CTA in axial, coronal, and sagittal planes in patients with MCA occlusion
Collateral Score (CS) assessed on CT angiography source images
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 multiphase CTA [Menon, 2015]
Score Collaterals on CTA
0 no vessels are 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 with no 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 are 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 a patient with left MCA occlusion
mCTA showing good collaterals in patient with left MCA occlusion

Basilar Artery on Computed Tomography Angiography (BATMAN) score

  • the 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) – scored separately, 1 point each
    • posterior communicant artery (PComA) – scored separately, 2 points each (or 3 points for fetal PCA)
    • 3 segments of the basilar artery (BA) – 1 point each
  • patients with a lower BATMAN score were more likely to have a poor outcome – the absence of PComA (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 (PComA)
  • 1 –  unilateral PComA
  • 2 –  bilateral PComA
  • the presence of bilateral PComA on CTA was associated with more favorable outcomes in patients with BAO undergoing mechanical thrombectomy [Goyal, 2016]

Posterior Circulation Collateral Score (PC-CS)

  • max. 10 points (normal findings)
  • AICA, PICA, SCA – assign 1 point to each patent artery (assess bilaterally)
  • PComA – assign 1 point if PComA is smaller than the P1 segment, 2 points if larger
  • patients with higher scores have better prognosis  [Goyal, 2016]

Time of flight MRA

  • another noninvasive method commonly used to assess the structure of cerebral collateral circulation
  • assessment of leptomeningeal collaterals is limited due to relatively low spatial resolution
  • TOF-MRA is typically used to assess primary collaterals via the circle of Willis
  • sensitivity and specificity can be increased by combining the TOF-MRA with TCD/TCCD

Neurosonology

  • TCD/TCCD is a noninvasive, low-cost method reflecting real-time cerebral blood flow velocity, collateral status, and cerebrovascular reactivity
  • accuracy is highly operator-dependent
  • TCD/TCCD can asses (directly or indirectly):
    • collateral flow through AComA, PComA, ophthalmic artery, and leptomeningeal arteries
    • the flow diversion phenomenon – high-velocity and low-resistance flow in the ACA or PCA in the presence of the MCA occlusion/severe stenosis (implies leptomeningeal collateral anastomoses between the ACA/PCA and the distal MCA branches

Related Content

You cannot copy content of this page

Send this to a friend
Hi,
you may find this topic useful:

Collateral circulation assessment
link: https://www.stroke-manual.com/collateral-circulation-assessment/