Collaterals between intracranial and extracranial circulation leptomeningeal anastomosis circle of wills acute stroke venous collateral circulation primary secondary tertiary collaterals orbital plexus tectal plexus IMAGING METHODS TO ASSESS THE STRUCTURE OF COLLATERALS ct angiography CTA MRA transcranial doppler TCD Augmentation of cerebral blood flow in acute stroke pathophysiology

1. Collaterals between intracranial and
extracranial circulation
Dr. Ahmed Mostafa Khalaf ,MD
Lecturer of Diagnostic and Interventional Radiology
Faculty of Medicine, South Valley University

3. Collateral cerebral circulation refers to a backup network of blood vessels that stabilizes
cerebral blood flow when primary arteries supplying an area of the brain become stenosed or
occluded.
Collateral vessels help maintain adequate blood supply to brain tissue; their quality
significantly influences the severity and extent of cerebral infarction.
Pathophysiological recruitment of these potential anastomotic connections is frequently
observed in various ischemic conditions, yet knowledge of the collateral circulation remains
limited.

4.  ANATOMY
 PATHOPHYSIOLOGY
 IMAGING METHODS
 AUGMENTATION OF CEREBRAL BLOOD FLOW IN ACUTE STROKE
 CONCLUSION
 REFRENCES

6. COLLATERAL CIRCULATION
EXTRACRANIAL INTRACRANIAL
PRIMARY
COLLATERALS
Circle of Willis
SECONDARY
COLLATERALS
Leptomeningeal
anastomoses
(LMA)
Orbital plexus Tectal plexus
TERTIARY
COLLATERALS

7. Extracranial arterial collateral circulation
 ECA → ICA
(facial/maxillary/superficial temporal artery → ophthalmic artery → carotid
siphon)
 Subclavian artery → ECA
(thyrocervical trunk, inferior and superior thyroid artery)
 Subclavian artery → VA
(thyrocervical trunk → muscular branches → VA)
 ECA → VA
(occipital artery → muscular branches → VA)
 VA → contralateral VA
(via spinal branches)

8. A. Anastomosis from facial artery,
B. Anastomosis from maxillary artery,
C. Middle meningeal artery >>>>>>>>>>>
the ophthalmic artery
D. Dural arteriolar anastomosis from middle
meningeal artery,
E. Occipital artery through the mastoid
foramen
F. Occipital artery through the parietal foramen
Extracranial arterial collateral circulation.
(Patel, S.D. and Liebeskind, D., 2023)

9. Intracranial arterial collateral circulation
 The circle of Willis allows for the redirection of blood flow between both
sides of the brain and between the vertebrobasilar and carotid circulations.
 It is used in stenoses and occlusions of large arteries (CCA, ICA, VA)
 it is a heptagon consisting of the following components:
 left and right ICA
 left and right A1 segments, connected by an unpaired Acom artery
 left and right P1 segments
 left and right Pcom arteries (connecting ICA and P1 segment on
each side)
 basilar artery tip
 Anatomic studies note absence of the anterior communicating artery
in 1% of subjects, absence or hypoplasia of the proximal anterior
cerebral artery in 10%, and absence or hypoplasia of either posterior
communicating artery in 30%.
A) Primary collaterals (Circle of
Willis)
Circle of Willis.
(collateral cerebral circulation-Stroke manual )

10. Axial maximum intensity projection (MIP) CT angiography slices showing examples of circle of Willis (CoW)
configurations. (A) A complete CoW. (B) A CoW with absence of the left posterior communicating artery (arrow).
(Maguida G, Shuaib A, 2023)

11.  the presence of secondary collateral pathways is considered a marker of impaired cerebral
hemodynamics.
LEPTOMENINGEAL ANASTOMOSES (LMAS)
 They refer to the collateral vascular network within the pia mater.
 They serve as alternative pathways for cerebral blood flow.
 They are formed by end-to-end anastomoses of major cerebral arteries (MCA-ACA, MCA-PCA,
ACA-PCA, both ACAs).
 They play a crucial role in acute stroke due to occlusion of the artery forming the circle of Willis
or in the peripheral segments.
Orbital plexus
 Connecting the ophthalmic artery with the facial, maxillary, ethmoid, and middle meningeal
arteries.
Tectal plexus
 Connecting the supratentorial branches of the PCA with the infratentorial branches of the
superior cerebellar artery (SCA)
 Tertiary collaterals refer to newly developed microvessels through angiogenesis at
B) Secondary
collaterals
C) Tertiary collaterals

12. Sequential AP images in DSA after contrast injection in the right ICA in a patient with an occlusion of the M1 segment
of the right MCA (arrow). Notice the contrast filling of the left anterior circulation through the ACOM artery (dashed
arrow) in the earliest image. The direction of the blood flow through the leptomeningeal collaterals from ACA to MCA
is shown with a curved arrow. (Maguida G, Shuaib A, 2023)

13. A. PCOM artery.
B. Leptomeningeal anastomosis between
anterior and middle cerebral arteries.
C. Leptomeningeal anastomosis between
posterior and middle cerebral arteries.
D. Tectal plexus between posterior cerebral
and superior cerebellar arteries
E. Anastomosis of distal cerebellar arteries
F. ACOM artery
Intracranial arterial collateral circulation , lateral (A) and frontal (B) views.
(Patel, S.D. and Liebeskind, D., 2023)

14.  Venous collaterals augment drainage of
cerebral blood flow when principal routes are
occluded, or venous hypertension results.
A. Pterygoid plexus.
B. deep middle cerebral vein.
C. inferior petrosal sinus and basilar plexus.
D. superior petrosal sinus.
E. Anastomotic vein of Trolard.
F. anastomotic vein of Labbé.
G. Condyloid emissary vein.
H. mastoid emissary vein.
I. parietal emissary vein.
J. occipital emissary vein.
Venous collateral circulation.
Venous collateral circulation.
(Patel, S.D. and Liebeskind, D., 2023)

16.  The process of collateral recruitment depends on :
 The caliber and patency of primary collaterals that may rapidly compensate for
decreased blood flow.
 The adequacy and capacity of secondary collaterals that require time to develop.
 The opening of collaterals likely depends on several compensatory hemodynamic,
metabolic, and neural mechanisms.
 The efficacy of collateral vessels likely depends on age, duration of ischemia, and
associated comorbidities.
 The presence of secondary collateral pathways is considered a marker of impaired
cerebral hemodynamics.
Pathophysiology

18. IMAGING METHODS
STRUCTURAL
TYPES
(DIRECT)
FUNCTIONAL
TYPES
(INDIRECT)

19. IMAGING METHODS TO ASSESS THE STRUCTURE OF COLLATERALS
Digital subtraction
angiography (DSA) CT angiography MR angiography
Transcranial
doppler (TCD)

20. 1-DIGITAL SUBTRACTION ANGIOGRAPHY (DSA)
 Conventional angiography is considered the gold standard method.
 It provides uniform recanalization grading, a high resolution of the flow caused by leptomeningeal
collaterals, and precise information about the site of the occlusion.
 However, there are several limitations :
 It is invasive, requires a higher level of expertise, requires more time, and has a small risk of
thromboembolism.
 A simultaneous examination of anterior and posterior circulation collaterals is impossible.
 There are no contralateral views, or the venous phase is incomplete.
 Anterior and lateral views cannot easily be compared with axial images from CT or MR imaging.

21.  Grading systems
 Retrograde filling of three or more branches of the MCA up to the M2 segment to be evidence of
good collaterals, whereas anything less was rated as poor. (Kucinski et al)
 A five-point scale by Higashida et al, to study collaterals that was based on a score endorsed by
the American Society of Interventional and Therapeutic Neuroradiology and the Society of
Interventional Radiology to study collateral status.
(Shuaib A. et al,

22. (Shuaib A. et al,

23. 2- CT ANGIOGRAPHY (CTA)
 CT angiography is an ideal method for study of status and anatomical configuration of collaterals .
 It requires minimal radiation, has a non-invasive nature and a rapid availability for patients with acute
stroke.
 However, it has a low temporal resolution and can result in overestimation of collateral flow.
 Grading systems
 Three categories for collateral status by Mitef et al ; Good, Moderate and Poor collaterals. The
National Institutes of Health Stroke Scale (NIHSS) score was significantly lower in patients with good
collaterals than in patients in the other two groups.
 A five-point scale to study collaterals by Mass et al.
 A four-point scale to study collaterals by Tan et al.

24. (Shuaib A. et al,

25. (Shuaib A. et al,
2011)

26. • MR angiography usually used to assess primary collaterals through the circle of Willis.
• Hyperintense proximal intracranial vessels on MR obtained with FLAIR in patients with acute stroke
are indicative of intraluminal thrombus.
• however, distal hyperintense vessels have a serpentine appearance, and might be an indicator of
slow retrograde collateral flow.
• Drawback; assessment of leptomeningeal collaterals is limited by its relatively. is generally limited to
proximal arterial segments at the circle of Willis.
• Grading system
3- MR ANGIOGRAPHY (MRA)

27. Collaterals on MRI and MRA
(A) FLAIR vascular hyperintensity in the distal left MCA territory (blue arrow) resulting from slow collateral filling of an
occluded left MCA in a 48-year-old woman with aphasia due to acute ischaemic stroke.
(B) (B) Asymmetry and apparent elongation of the PCA (red arrow) ipsilateral to an acute occlusion of the left MCA (green
arrow) in a 73-year-old man with right hemiparesis and aphasia. (Shuaib A. et al,
2011)

28.  The researchers used TCD to judge collateral status within 24 h of a stroke secondary to carotid
dissection and showed how this non-invasive technique could help to establish the long-term
prognosis in such patients.
 Flow velocity was systematically measured within the ophthalmic, anterior, and posterior
communicating arteries
 Good collateral status was reported if two or all three vessels were opened within 24 h of stroke
onset (ie, flow diversion occurred).
 Drawback; TCD provides little information about collateral flow and only at the circle of Willis.
4- TRANSCRANIAL DOPPLER (TCD)

29.  Grading system
Blood flow assessed with TCD
Increased MFV in the cranial blood vessels before (A) and after insertion of an aortic occlusion device (B) in a 63-year-old
man with acute ischaemic stroke.
MFV increased from 17 cm/s to 34 cm/s in the distal MCA, and from 33 cm/s to 77 cm/s in the terminal ICA. Additionally,
anterior communicator flow was detected only after insertion of the aortic device.

30. IMAGING METHODS TO ASSESS THE FUNCTION OF COLLATERALS
 Tissue perfusion studies allow for the assessment of the compensation by the collateral circulation.
 They include; cerebrovascular reserve by TCD, xenon CT, single-photon emission CT (SPECT), positron
emission tomography (PET), CTP, QMRA, traditional dynamic susceptibility contrast MR perfusion,
arterial spin labelling (ASL), MR perfusion and others.
 These imaging methods usually estimate the cerebral blood flow direction/velocity/volume or
perfusion status to reflect the blood flow compensating function of collaterals.

31.  Some novel imaging techniques could reveal the structure and function of collateral circulation at the
same time; such as QMRA could reveal directions of blood flow via collateral channels and quantify
total/regional cerebral blood flow.
 Rusanen et al used collateral circulation to predict infarct size and penumbra following thrombolytic
therapy of acute ischaemic stroke. They used the Alberta Stroke Program Early CT Score (ASPECTS) of
mean transit time (MTT) to evaluate the brain tissue at ischemic risk and cerebral blood volume (CBV)
score to evaluate the infarct core. The results showed that better MTT and ASPECTS score based on CBV
correlated with better collateral circulation. A better collateral circulation is associated with a smaller
infarct core and a larger mismatch ratio.

32. Augmentation of cerebral blood flow in acute stroke
 Supportive medical care for patients with acute stroke, including adequate hydration and the
avoidance of wide fluctuations in blood pressure, can help to maintain collateral flow
capabilities.
 Optimization of systemic factors could help to minimize the risk of collateral failure,
particularly in patients with proximal arterial occlusions.
 Experimental techniques aimed at increasing cerebral blood flow:
• Volume expansion with or without increased blood pressure
• Stimulation of the sphenopalatine ganglion
• Partial aortic occlusion
• External pressure cuffs
• Lower-body positive-pressure application
• Counterpulsation

33. (Shuaib A. et al, 2011)

35.  In acute stroke, the severity of ischemia detect Speed of irreversible brain damage.
 Well-developed pial collaterals may support tissue survival when a large intracranial
blood vessel is occluded proximally.
 The development of noninvasive approaches that combine angiographic information
with perfusion data would support our understanding of the collateral circulation
considerably.

37.  Patel SD, Liebeskind D. Collaterals and elusive ischemic penumbra.
Translational Stroke Research. 2023 Feb;14(1):3-12.
 Maguida G, Shuaib A. Collateral Circulation in Ischemic Stroke: An Updated
Review. Journal of Stroke. 2023 Mar 13;25(2):179-98.
 Shuaib A, Butcher K, Mohammad AA, Saqqur M, Liebeskind DS. Collateral blood
vessels in acute ischaemic stroke: a potential therapeutic target. The Lancet
Neurology. 2011 Oct 1;10(10):909-21.
 Liebeskind DS. Collateral circulation. Stroke. 2003 Sep 1;34(9):2279-84.
 Liu L, Ding J, Leng X, Pu Y, Huang LA, Xu A, Wong KS, Wang X, Wang Y.
Guidelines for evaluation and management of cerebral collateral circulation in
ischaemic stroke 2017. Stroke and vascular neurology. 2018 Sep 1;3(3).