4. Cerebral Collateral Circulation - alternative or indirect arterial
pathways that provide blood flow when an artery that normally
supplies an area of brain tissue is occluded
Structural Classification
▪ Circle of Willis
▪ Microvascular intracranial
collaterals (arterioles)
▪ Leptomeningeal (pial)
▪ Subcortical collaterals
▪ Extracranial sources of collateral
circulation
Functional Classification
▪ Primary- permanently functioning
- immediately reroute flow
▪ Secondary- pre-existing conduits that can
be recruited
- recruitment takes 12 sec in rats
▪ Tertiary- formation of new blood vessels
or the maturation of pre-existent vessels
Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
8. LEPTOMENINGEAL (PIAL) COLLATERAL SYSTEM
▪ Arteriolo-arteriolar connections (50-400 microns)
▪ Seen at the distalmost branches of large cerebral and cerebellar
vessels
▪ Variable configurations: end-to-end and end-to-side anastomoses
▪ Bidirectional flow governed by hemodynamic and metabolic needs
of the territories they connect
▪ Formation during the embryonic period (collaterogenesis)
Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
9. LEPTOMENINGEAL (PIAL) COLLATERAL SYSTEM
Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
PIAL
COLLATERAL
RECRUITMENT
PRESSURE GRADIENT >
NITRIC OXIDE >
DILATATION
NEURAL REGULATION
EXTRINSIC INNVERVATIONS
VIA PNS > VESSELS ON
THE BRAIN SURFACE
NEURAL REGULATION
INTRINSIC INNERVATIONS VIA
THE CNS (MAINLY VIA THE
BRAINSTEM) >
PARENCHYMAL VESSELS
10. OTHER FACTORS THAT MODIFY THE COLLATERAL SYSTEM
▪ Aging – decrease in number and diameter
▪ Vascular risk factors – HPN, CCA occlusion, DM > impaired
recruitment
▪ Smoking – Positive correlation in CAD(?) due to ischemic
preconditioning; Positive correlation in ischemic stroke
▪ Physical exercise – increased blood flow stimulates endothelial
mechanisms for maintenance, defense and repair > improved
collateral circulation and capacity to vasodilate
▪ Statin use – enhancement of arteriogenesis and eNOS-mediated
vasodilatation
▪ Extracranial ICA stenosis - >75% stenosis=good collaterals
Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
14. ▪ Collaterals are the key element setting the pace of the ischemic
process
▪ Temporal growth of ischemic core is modulated by collateral blood
flow
▪ Fast progressors – failing collaterals, rapid infarct growth; large
ischemic core despite presenting early (6 hrs of stroke onset)
▪ Slow progressors - good collaterals, small ischemic core and large
penumbra beyond 6 hrs and up to several days after stroke onset
- raises possibility for EVT beyond conventional time windows
(<6hrs) for acute reperfusion therapies
15.
16.
17. SIGNIFICANCE OF GRADING THE COLLATERALS
Collateral Scoring may be used as a tool to:
▪ Distinguish fast and slow progressors – identify patients that may
benefit from EVT beyond the conventional time window
▪ Predict infarct size – NECT + CTA vs NECT + CTA + CTP/MRP
▪ Help neurologic outcome prognosis
▪ Predict recanalization and reperfusion after IV rTPA and EVT –
incorporation to guidelines for AIS treatment beyond the conventional
time window?
20. IMAGING THE PIAL COLLATERAL SYSTEM
Structural studies
▪ Digital subtraction angiography
▪ Methods based on CT
▪ Single phase CTA
▪ Multiphase CTA
▪ Methods based on MR
▪ Time-of-flight MRA
▪ Contrast-enhanced MRA
▪ FLAIR
▪ Transcranial Doppler
Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
Functional studies
▪ CT Perfusion
▪ MR perfusion
▪ Positron emission
tomography CT and single-
photon emission CT
21. IMAGING THE PIAL COLLATERAL SYSTEM
DSA sCTA mCTA
Gold standard Most commonly used
Increased utilization in specialized
centers
Advantages
Dynamic evaluation
Excellent spatial and
temporal resolution
Widely available
Rapid image acquisition
Technically easier to perform and interpret
Dynamic study that allows
assessment of delay in contrast
arrival and washout
Better interrater reliability in
detecting LVO
Better association with final
infarct volume and clinical
outcomes
Disadvantag
es
Invasive
Procedural risks
Contrast administration
Static evaluation
Suboptimal in diminished ejection fraction or
extracranial carotid stenosis
sCTA in the early arterial phase –
underestimates
Slightly higher radiation dose and
takes longer to perform than sCTA
22. • 2002
• Diagnostic angiogram of 162 patients
enrolled in the PROACT II study
• Collateral score correlation with clinical
presentation and outcome
Roberts et al., 2002
Conventional angiogram (n162)
1
None (n:50)
2
Partial
- Collateral flow to parts of the vascular territory at
risk (n:100)
3
Full
- Collateral flow to the entire vascular territory at risk,
with the clot visible from the distal side (n: 11)
23. ASITN/SIR 2003 - Conventional angiogram
0 No collaterals visible to the ischemic site
1 Slow collaterals to the periphery of the ischemic site
with some persistence of some of the defect
2 Rapid collateral to the periphery of 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
▪ 2003
▪ American Society of Interventional and
Therapeutic Neuroradiology/Society of
Interventional Radiology
▪ Time of collateral filling is subjective
>determined by counting the number of
frames from opacification of petrous
carotid artery and proximal basilar
artery
▪ Slow flow – filling that is 2 sec slower
than the normal contralateral side
▪ Rapid flow – filling within 2 sec
25. ▪ 2004
▪ Roberts et al., 2002 – global scoring
system; ASITN/SIR 2003 - subjective
▪ Study assessed collateral score per region
similar to ASPECTS
Kim et al., 2004- Conventional angiogram
0 No collaterals visible to the ischemic site (absence
of any capillary blush
1 Collaterals to the periphery of the ischemic site
2 Complete irrigation of the ischemic bed via
collateral flow
3 Normal antegrade flow
26.
27. Christoforidis et al., 2005- Conventional angiogram
1 Collaterals reconstituted the distal portion of the occluded
segment (in M1 segment occlusion the M1 segment distal to
the occlusion reconstituted)
2 Collaterals reconstituted vessels in the proximal portion of the
segment adjacent to the occluded vessel (in M1 occlusion,
reconstitution to the proximal M2 segments)
3 Collaterals reconstituted vessels in the distal portion of the
segment adjacent to the occluded vessel (in M1 occlusion,
reconstitution to the distal portion of the M2 segments)
4 Collaterals reconstituted vessels two segments distal to the
occluded vessel (in M1 occlusion, reconstitution up to the M3
segment)
5 Little or no significant reconstitution of the territory of the
occluded vessel
28. Tan et al., 2007 - sCTA
0 Absent collaterals
1 Collaterals filling ≤ 50% of the occluded territory
2 Collaterals filling >50%, but <100% of the
occluded territory
3 Collaterals filling 100% of the occluded territory
▪ 2007
▪ 113 patients
▪ NCT, PCT and CTA was compared with
follow-up CT or MRI for final infarct
location and volume
29. • CTA MIPs are the most appropriate way to assess the collateral
circulation
• CTA MIPs is a predictor of the final infarct volume both in patients
with persistent arterial occlusion and in patients with recanalization
30. ▪ 2009
▪ Graded in comparison with
normal hemisphere
Maas et al., 2009 - sCTA
1 Absent
2 Probably present
3 Hairline
4 Definitely present
5 Robust
31. Miteff et al., 2009- sCTA
3 Vessels are reconstituted distal to the occlusion
2 Vessels can be seen at the Sylvian fissure
1 Contrast opacification is merely seen in the distal
superficial branches
▪ 2009
▪ Collateral status simply
divided into good, moderate
or poor
32. ▪ 2011
▪ Previous studies either
compare with contralateral
side (Maas and Miteff), or
assess retrograde filling
without considering regional
variability (Tan)
▪ Regional ASPECT-based CS
(rASPECTS-CS)
▪ High interrater reliability
▪ Less subjective
▪ Stronger correlation with
clinical outcomes Sylvian sulcus: 0 – not seen; 2 – less; 4 – same or more prominent
33. Souza et al., 2012 - sCTA
0 Absent collaterals in >50% of an M2 branch
territory
1 Diminished collaterals in >50% of an M2 branch
territory
2 Diminished collaterals in <50% of an M2 branch
territory
3 Collaterals equal to the contralateral
hemisphere
4 Increased collaterals
▪ 2012
▪ Modification from Tan et al., 2007
▪ Study only included terminal ICA
and MCA stem occlusion
34. ▪ 2013
▪ One of the first to assess
leptomeningeal collaterals using
mCTA
▪ Divided pial collaterals based on
origin – either from ANTERIOR (ACA
to MCA) or POSTERIOR (PCA to MCA)
circulation. Then the following three
properties were graded:
▪ Anatomic extent (graded 0 – 2)
▪ Pial prominence (0 – 2)
▪ Retrograde filling time
35. ▪ 2015
▪ Data are from the IMS III study
▪ Of 656 patients enrolled in the study, 306 patients had CTA
at baseline
36. Menon et al., 2015 - sCTA
Description ACA-MCA region PCA-MCA region
Compared with asymptomatic contralateral hemisphere, increased or
normal prominence and extent of pial vessels beyond the occluded artery
within the symptomatic hemisphere
5 5
Compared with asymptomatic contralateral hemisphere, slightly reduced
prominence and extent of pial vessels beyond the occluded artery within the
symptomatic hemisphere
4 4
Compared with asymptomatic contralateral hemisphere, there is moderately
reduced prominence and extent of pial vessels beyond the occluded artery
within the symptomatic hemisphere
3 3
Compared with asymptomatic contralateral hemisphere, there is decreased
reduced prominence and extent and regions with no vessels in some part of
the territory occluded
2 2
Compared with asymptomatic contralateral hemisphere, there is just a few
vessels visible in the occluded vascular territory
1 1
Compared with asymptomatic contralateral hemisphere, there is no vessels
visible in the occluded vascular territory
0 0
37. ▪ Menon et al., 2015
▪ University of Calgary scoring system
▪ 147 patients with NECT, sCTA, mCTA
and CTP
▪ Multiphase CTA
▪ Aortic arch to vertex (arterial phase)
▪ Skull base to vertex (peak venous
phase and late venous phase)
38.
39.
40. mCTA CTP
First phase (sCTA) - <7sec; DLP: 700-
800mGy*cm
8cm section of the brain scanned
Second scan – 3.4 sec 24 passes over 66 seconds (total scan time)
Third scan – 3.4 sec (total exposure time:
14sec)
Total exposure time 19.2 sec
80 mL of contrast at 5ml/sec followed by 50
ml saline chase at 6ml/sec
45 mL of contrast at 4.5ml/sec followed by
40 ml of saline chase at 6ml/sec
Total of 60 mGy radiation dose to the eye 200 mGy radiation dose to the eye
• mCTA and perfusion CT imaging are CONGRUENT for treatment
decision-making
41. ▪ Advantages of mCTA based on the study
▪ Minimal addition radiation (NECT + mCTA vs NECT + CTP)
▪ No additional contrast material (sCTA vs mCTA)
▪ Whole brain coverage (vs CTP)
▪ No post-processing (vs CTP)
▪ Slightly better in the prediction of clinical outcomes than NECT, sCTA
and CTP
42. Collateral scoring systems
DSA sCTA mCTA
Roberts et al., 2002 Tan et al., 2007 Menon et al., 2013
ASITN/SIR 2003 Maas et al., 2009 Menon et al., rCS, University of Calgary
scoring system, 2015
Kim et al., 2004 Miteff at al., 2009
Christoforidis et al., 2005 Menon et al., r-ASPECTS 2011
Souza et al., 2012
43. ▪ 2022, Trial investigators of ESCAPE, EXTEND-IA, SWIFT-PRIME,
REVASCAT, MR-CLEAN, PISTE, and THRACE established the HERMES
collaboration
▪ Highly Effective Reperfusion Using Multiple Endovascular Devices
(HERMES) – endovascular thrombectomy is superior to standard
medical care in AIS with proximal anterior circulation occlusion
▪ Pooled analysis of individual patient-level data - total of 1709 patients
with baseline images (CTA or MRA) were available.
▪ Only patients with intracranial internal carotid artery and/or M1 MCA
segment were included.
44.
45.
46. Association of each Collateral Score with mRS at 3 mo
▪ Primary outcome – functional independence at 3mo defined by a
mRS of 0-2
▪ Secondary outcome – ordinal mRS score (0-6) at 3 mo
47. ▪ RESULTS
▪ rCS – most strongly associated with mRS at 3mo (primary and
secondary outcome)
▪ On sCTA, the rCS and the rASPECT-CS performed significantly better in
predicting 3-month functional (primary) outcome than the Tan CS
▪ On mCTA or dCTA, no statistically significant differences were noted in
predicting 3-month functional (primary) outcome between the 3 CSs
▪ In practice, the choice of CS type might be of greater relevance when
using sCTA compared with mCTA
48. Status of the COLLATERAL SCORE at present
Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
▪ No concensus on the more accurate non-invasive imaging
technique or scoring system for collateral circulation assessment
▪ Role of collateral circulation status in the selection of patient for
endovascular treatment or the role of potential modifying
therapies to enhance collateral flow in AIS is unknown
49. Sources
▪ http://aspectsinstroke.com/collateral-scoring
▪ https://www.youtube.com/watch?v=9T0bxrDjSUE
▪ Collateral Circulation in Ischemic Stroke: An Updated Review, Maguida and Shuaib, 2022
▪ Collateral Circulation, Liebeskind, 2003
▪ Collaterals at Angiography and Outcomes in the Interventional Management of Stroke (IMS) III Trial,
Liebeskind et al., 2014
▪ Collateral Circulation in Thrombectomy for Stroke After 6 to 24 Hours in the DAWN Trial, Liebeskind et al.,
2022
▪ Computed Tomographic Findings in Patients Undergoing Intra-arterial Thrombolysis for Acute Ischemic
Stroke due to Middle Cerebral Artery Occlusion Results From the PROACT II Trial, Roberts et al., 2002
▪ Trial Design and Reporting Standards for Intra-Arterial Cerebral Thrombolysis for Acute Ischemic Stroke,
Higashida et al., 2003
▪ Regional Angiographic Grading System for Collateral Flow Correlation With Cerebral Infarction in Patients
With Middle Cerebral Artery Occlusion, Kim et al., 2004
50. Sources
▪ Angiographic Assessment of Pial Collaterals as a Prognostic Indicator Following Intra-arterial
Thrombolysis for Acute Ischemic Stroke, Christoforidis et al., 2005
▪ Systematic Comparison of Perfusion-CT and CT-Angiography in Acute Stroke Patients, Tan et
al., 2007
▪ The independent predictive utility of computed tomography angiographic collateral status in
acute ischaemic stroke, Miteff et al., 2009
▪ Collateral Vessels on CTA Predict Outcome in Acute Ischemic Stroke, Maas et al., 2009
▪ Regional Leptomeningeal Score on CT Angiography Predicts Clinical and Imaging Outcomes in
Patients with Acute Anterior Circulation Occlusions, Menon et al., 2011
▪ Malignant CTA Collateral Profile Is Highly Specific for Large Admission DWI Infarct Core and
Poor Outcome in Acute Stroke, Souza et al., 2012
▪ Multiphase CT Angiography: A New Tool for the Imaging Triage of Patients with Acute Ischemic
Stroke, Menon et al., 2015
▪ Comparison of Three Scores of Collateral Status for Their Association With Clinical Outcome:
The HERMES Collaboration, Gensicke et al., 2022
52. MODIFIED ASITN/SIR FOR mCTA
0 Non-existent or barely visible pial
collateral on the ischemic site
during any point of time
1 Partial collateralization of the
ischemic site until the late venous
phase
2 Partial collateralization of the
ischemic site before the venous
phase
3 Complete collateralization of the
ischemic site by the late venous
phase
4 Complete collateralization of the
ischemic site before the venous
phase
53. ▪ Interterritorial leptomeningeal collaterals between the posterior
circulation and the MCA territory are functionally better than those
between the ACA and MCA territories
▪ Variability in size and retrograde filling time of pial arteries
probably related to blood flow regulation – may relate to functional
status
54. ▪ Relative advantages of rCS
▪ Assessing difference between ACA-MCA and PCA-MCA collateral status
▪ Capturing hemodynamic aspects of collateral filling (prominence of
vessels)
Editor's Notes
The collateral circulation of the brain refers to alternative or indirect arterial pathways that can provide blood flow when an artery that normally supplies an area of brain tissue is occluded.Subdivided using a structural classification and a functional classification.Under the structural classification, the collaterals are categorized into…
Under the functional classification, the collaterals are categorized into…
The primary collateral circulation corresponds to permanently functioning pathways that can immediately reroute blood flow when a blood vessel occlusion occurs. This term refers mainly to the CoW.The secondary collateral circulation refers to pre-existing arterial conduits that can instantaneously be recruited to provide an alternative pathway for blood flow. This refers mainly to the leptomeningeal collaterals. recruitment of leptomeningeal collaterals is extremely fast. For example, in rat models of ICA occlusion, it takes only 12 seconds for leptomeningeal collaterals to reach their maximal vasodilatation.The tertiary collaterals is used to refer to the formation of new blood vessels or the maturation of pre-existent vessels in ischemic areas.
Two main processes are involved. Angiogenesis is the physiologic process in which new blood vessels arise from pre-existent onesThe main stimuli for angiogenesis are ischemia and hypoxia. In contrast, arteriogenesis refers to the maturation of pre-existent arterioles into arteries. It is an important process of adaptation of blood vessels to new demands from tissue at risk after an arterial occlusion. The main stimulus for arteriogenesis is the shear stress on the endothelium, which is generated by pressure gradients
Diagram of the COW which has 10 components, namely..
Middle image is a CTA showing a complete COW, seen only in 20-25%
Left image is another CTA showing an absent left PCOM, which is the most common anatomic variant seen in ~30%
hypoplastic/absent A1 segment of ACA ~15% (range 10-15%)
absent or fenestrated ACOM ~12.5% (range 10-15%)
origin of PCA from the ICA with absent/hypoplastic P1 segment (fetal PCA) ~20% (range 17-25%)
infundibular dilatation of the PCOM origin ~10% (range 5-15%)
Diagram of the intracranial collateral circulation connecting the anterior circulation (black) and posterior circulation (gray)
Focus on the leptomeningeal anastomosis
POSTERIOR COMMUNICATING ARTERY
LEPTOMENINGEAL ANASTOMOSIS BETWEEN THE ACA AND MCA
LEPTOMENINGEAL ANASTOMOSIS BETWEEN THE MCA AND PCA
TECTAL PLEXUS BETWEEN THE PCA AND SUPERIOR CEREBELLAR ARTERIES
ANASTOMOSES OF DISTAL CEREBELLAR ARTERIES
aCOMM
Diagram of the extra-cranial collaterals that originate from the branches of the ECA
Shown are anastomoses from the facial (a), maxillary (b), and middle meningeal (c) arteries to the ophthalmic artery and dural arteriolar anastomoses from the middle meningeal artery (d) and occipital artery through the mastoid foramen (e) and parietal foramen (f).
several possible extra-intracranial anastomoses, which can provide blood flow in the case of a blood vessel occlusion. These extracranial sources originate from branches of the external carotid artery or from ascending and deep cerviocclusion of the internal carotid artery (ICA) before the emergence of the ophthalmic artery. If there is a complete and functional CoW, the terminal ICA may receive retrograde flow through the circle and immediately restore the anterograde flow through the ophthalmic artery. e external carotid artery, which can anastomose with branches of the ophthalmic artery and provide retrograde flow, which will ultimately reach the terminal ICA
Several neurohumoral mechanisms involved in the process of leptomeningeal collateral recruitment. The main driver of the functionality of these pathways is pressure gradients. Where increased pressure and shear stress activates nitric oxide (NO)- dependent mechanisms that lead to their dilation and improved blood flow. There is also a neural regulation of the cerebrovascular tone through intrinsic and extrinsic innervations. The intrinsic nerves originate mainly in the brainstem and are distributed predominantly in the parenchymal vessels.
Whereas the extrinsic nerves supply the vessels on the surface of the brain.
The extrinsic parasympathetic nerves, which arise from the superior salivatory nucleus and pass along cranial nerve VII to the sphenopalatine and otic ganglia, are involved in vasodilation and their stimulation has been studied as a therapeutic target
1. Aging causes a decrease in number and diameter and an increase in tortuosity of leptomeningeal collaterals, which lead to increased vascular resistance. These changes are associated with impaired endothelial NO synthase (eNOS) signaling and increased oxidative stress.
2. In animal models of chronic hypertension, induction of collateral flow during acute ischemic stroke is impaired. Similarly, murine models of common carotid artery occlusion have shown impaired collateral flow in diabetic mice.3. On patients with coronary artery disease, previous studies showed that smoking may be associated with better collaterals. The proposed mechanism is ischemic preconditioning; However, a 2021 meta-analysis of 18 studies and more than 4,000 patients did not demonstrate a positive association. In the case of ischemic stroke patients, a retrospective analysis of embolic LVO in more than 600 patients found a positive correlation between smoking (current or previous) and good collaterals.
4. Regular exercise has been shown to improve collateral circulation in patients with coronary artery disease and in animal models of stroke. Physical exercise increases blood flow and the shear stress stimulates different mechanisms in the endothelium, which lead to maintenance, defense, and repair of the vasculature. It also enhances the capacity of the vessels to vasodilate. Another more indirect effect of physical exercise is the reduction of vascular risk factors
5. Statin use and better collaterals in ischemic stroke patients. Proposed mechanisms for this effect are enhancement of arteriogenesis and eNOS-mediated vasodilation.
6. observational study of 385 patients who underwent mechanical thrombectomy for LVO, patients with an ipsilateral stenosis of the extracranial ICA of more than 75% had good collaterals
2014 331 SUBJECTS using angiography
Study aimed to establish an association between the degree of collaterals before endovascular therapy (intra-arterial t-PA and ) and the likelihood of recanalization, reperfusion, and good clinical outcome at 90 defined as mRS of 2 or less.
Their results showed that for these primary outcomes, there is positive correlation between good collaterals of grades 3 and 4, with increased likelihood of recanalization and reperfusion seen in more than 80% of cases.
Positive correlation is also noted between good collaterals and better clinical outcome at 90 days.
Other than its correlation to EVT outcome….
As discussed before, there is a concept of infarct core and ischemic penumbra, where the penumbra grows gradually if perfusion is not re-established.
A large study of 161 patients shows the correlation of collaterals with infarct size at baseline and 24 hours of onset.
Collateral scores were stratified into good, fair and poor. The study showed that good collaterals were associated with smaller core infarcts at presentation and 24 hours post-ictus.
Comparing the change of infarct size with baseline and 24 hrs, there is notable slower infarct evolution in those with good collaterals
Same study also shows good correlations between clinical outcome and good collaterals
Class of recommendation Iib – weak
Level of evidence – limited data
No recommendation for any imaging study to be used for collateral circulation assessement
No recommendation on which CS system to be used
Since no recommendation was given, we will briefly discuss all CS systems, focusing on their merits and demerits
The methods to assess the collateral circulation can be broadly divided into structural and functional types
Focus on DSA and CTA, both sCTA and mCTA
e not as readily available and they are usually slower to perform. Time-of-flight MR angiography (TOF-MRA) is a T1-based sequence that does not require gadolinium injection and is used to assess the proximal intracranial vasculature.
ontrast-enhanced MR angiography (CE-MRA) is also a T1- based sequence and it requires the injection of a bolus of gadolinium. Its advantages are a high signal-to-noise ratio and a relative insensitivity to slow flow.42
hyperintensities represent a more indirect marker of leptomeningeal collaterals, but they are non-specific and their usefulness is limited. TThis non-invasive method provides real-time information about intracranial blood flow. It only allows the assessment of proximal blood vessels at the level of the CoW
there is no consensus about the more accurate noninvasive technique or scale for CC assessment. Furthermore, the role of the CC status in the selection of patient for endovascular treatment or the role of the potential modifying therapies to enhance collateral flow in acute ischemic stroke is unknown
Digital subtraction angiography (DSA) is considered the gold standard for structural assessment of the collateral circulation. It allows dynamic evaluation of blood flow with excellent spatial and temporal resolution.Its main disadvantages are its invasive nature, its associated procedural risks, the need for contrast agent administration, and its limited availability.sCTA is the most frequently used study in the assessment of the collateral circulation because of their widespread availability and rapid image acquisition. Single-phase CT angiography (sCTA), which is performed at a single time point in relation to the contrast bolus injection, has the limitation of being a static evaluation. It will provide an inexact measurement of the state of collaterals if the acquisition is not performed at the optimal time point. For example, in patients with a diminished cardiac ejection fraction or an extracranial carotid stenosis, the collaterals may be underestimated because the image acquisition will tend to be performed before the contrast agent can reach the leptomeningeal vessels. studies have suggested that collateral assessment in sCTA in the early arterial and late venous phases underestimate and overestimate the collateral status, respectively.
Multiphase CTA (mCTA) is performed in different time points and provides a better characterization of the collateral circulation than sCTA because it allows the assessment of the delay in contrast arrival and washout. This technique also has a better interrater reliability for the detection of LVO, it allows for a more precise assessment of the thrombus length, and it has a better association with final infarct volume and clinical outcomes
The first few CS systems were derived from conventional angiogram
Simplistic – more pt will be categorized under partial (2)
Collateral circulation was assessed from the baseline diagnostic angiogram in blinded fashion by the core laboratory neuroradiologist. The presence of collateral vessels was categorized as (1) none, (2) partial (collateral flow to parts of the vascular territory at risk), or (3) full (collateral flow to the entire vascular territory at risk, with the clot visible from the distal side)present report describes the CT findings in PROACT II and their correlation with clinical presentation, angiographic findings, and outcome
2002Of 162 patients (108 r-ProUK patients and 54 control patients) who actually received the treatment to which they were randomized, 50 patients had no angiographic collaterals, 100 had partial collaterals, and 11 had full collaterals (1 patient could not be assessed for collaterals).
Note that descriptors such as slow and rapid collateral is now incorporated, which makes this scoring system subjective
However, time of collateral filling might be determined by counting the number of frames from contrast-agent filling of the petrous carotid artery (from the anterior circulation) and the proximal basilar artery (in the posterior circulation) to complete collateral filling (provided that the number of frames per second is known, so that the time for collateral filling can be calculated.) This is then compared with time to normal filling of the nonoccluded hemisphere in the parenchymal phase of the angiogram. Slow collateral flow is defined, arbitrarily, as filling that is 2 seconds slower than the contralateral side. Rapid collateral flow is defined as filling that is within 2 seconds of the contralateral side.
2013
Notably the first to perform a regional scoring system
Image on the left shows ASPECTS regions, with decreased collaterals in the M1, M2 and M6 regions, correlating well with infarctions in these regions as shown in the CT scan.
Notice that there is variability in collaterals per region, which cannot be properly addressed using a global scoring system
Anteroposterior (A and C) and lateral (B and C) images from a left internal carotid artery angiogram obtained during the early (A and B) and delayed angiographic phases (C and D) in a patient with acute ischemic stroke due to occlusion at the M1 segment (arrow). Note the retrograde opacification of the MCA branches via pial collateral vessels extending from the ACA (arrowheads). Because there is reverse opacification of the MCA extending to the distal M1 segment, a pial collateral formation score of 1 was assigne
Global scoring that use >50 but <100% descriptor for grade 2 collaterals. This collateral filling of more than 50% may still denote a large infarct core in cases of ICA or proximal M1 occlusion, which may reach 150ml of infarcted brain tissue which is the threshold for not performing EVT due to high chances of hemorrhagic conversion. So a grade of 2 which is supposed to be a good collateral score, is to be taken with caution using this scoring system.
As one of the first studies to use CTA in collateral assessment
Global and simplistic with vague descriptors
Global and simplistic
Arteries in the Sylvian sulcus are given a higher score, ie, 0, 2, or 4 (0, not seen; 2; less; 4, same or prominent compared with the opposite Sylvian sulcus) because opacification of these vessels is a strong indicator of good retrograde flow via these collateral networks
Menon et al again!
ACA-MCA and PCA-MCA pial arterial backfilling are each scored from 0 to 5 (0-absent, 1-minimal, 2-significantly decreased prominence and extent of pial arteries with regions of no vessels, 3-moderately decreased prominence and extent, 4-mildly decreased prominence and extent, 5-normal or increased prominence and extent) when compared with the opposite normal hemisphere; the total score combines scores from these 2 regions to give an ordinal score ranging from 0 to 10.14
Same scoring system as the previous study
Compared sCTA and mCTA
Aortic arch vertex CT athe peak arterial phase - <7sec
skull base to the vertex in the equilibrium/peak venous and late venous phases a 0.625-mm section thickness. 8 secs apart 80 ml of contrast 50 ml saline chase @ 6ml/sec
All patients underwent standard unenhanced CT with 5-mm section thickness followed by head and neck CT angiography, including multiphase CT angiography and perfusion CT.
Tables show the sCTA and mCTA scoring systems in this study. The difference is that sCTA is only able to compare for the prominence and extent of collaterals, while the mCTA scoring also detects for delay in contrast filling.
Graph shows the incongruence between scores between sCTA and mCTA.
We can see that more patients are labelled as having good collaterals with scores of 4 and 5 using mCTA, which means that there is mislabeling of many patients as having a poor score if we use sCTA.
Study also compared mCTA with CTP
B, A proximal right M1 MCA occlusion is seen (i). Multiphase CT angiography (three phases) maximum intensity projection images are shown (ii, iii, iv). Pial arterial filling is modest, with delay of two phases and some regions indicating minimal filling when compared with the contralateral side, thus indicating that no treatment be performed. C, Perfusion CT Tmax and cerebral blood flow (CBF) maps (i, ii ). Tissue with Tmax greater than 6 seconds (pink) is superimposed onto the CT perfusion average maps for both gray and white matter (iii and iv, respectively). CBF less than 10 mL·min21 ·100 g21 and less than 7 mL·min21 ·100 g21 for gray and white, respectively, is flooded in blue on the CT perfusion average maps (iii, iv). CBF-defined infarct core is 100 mL. A mismatch ratio (total Tmax hypoperfusion volume/ total CBF infarct volume) of 1.7 and a large infarct core indicates that no treatment should be performed. Multiphase CT angiography and perfusion CT imaging are congruent for treatment decision
association of each CS with mRS at 3 months
Primary outcome – functional independence at 3mo defined by a mRS of 0-2
Secondary outcome – ordinal mRS score at 3 mo
We hypothesize that differences in sympathetic innervation and autoregulatory capacity between the two circulations could be a potential explanation for the observed differences
Many previous CTA-based leptomeningeal collateral scores have used relative size of back-filling pial arteries as a marker of leptomeningeal collateral status.1,3,4,13,15,27,28 We note significant variability in size of these pial arteries when compared with anatomically similar vessels in the contralateral hemisphere. This temporal variability could be an indicator of the functional status of leptomeningeal collaterals and/or autoregulatory capacity of pial arteries. Further studies are needed to understand the relationship between leptomeningeal collateral status and the rate of backfilling in pial arteries
Relative advantages of the rCS include (1) assessing differences between anterior cerebral artery-MCA- and posterior cerebral arteryMCA-collateral status and (2) capturing hemodynamic aspects of collateral filling (prominence of vessels).