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Table of Contents
Year : 2023  |  Volume : 26  |  Issue : 1  |  Page : 10-16

Collateral circulation- Evolving from time window to tissue window

Department of Neurology, All India Institute of Medical Sciences, New Delhi, India

Date of Submission05-May-2022
Date of Decision02-Apr-2022
Date of Acceptance08-Apr-2022
Date of Web Publication21-Nov-2022

Correspondence Address:
Ayush Agarwal
Department of Neurology, AIIMS, New Delhi
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/aian.aian_413_22

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Cerebral collateral circulation refers to the auxiliary vascular structures which compensate cerebral blood flow when it has been compromised due to stenosis or occlusion of the principal supplying arteries. They play a vital role in sustaining blood flow to the ischemic areas in acute, subacute or chronic phases of ischemic stroke or TIA. Good collateral circulation has shown protective effects towards a favorable functional outcome and a lower risk of recurrence of stroke. The benchmark mechanical thrombectomy trials utilized these collateral scoring methods to guide patient selection and prognosticate favorable outcome models. This shows a promising future of the collateral circulation for extending the time frame of the reperfusion therapies by optimally guiding patient selection and moving from a “time window” to a “tissue window.”

Keywords: Circulation, collateral, functional, penumbra, stroke

How to cite this article:
Sharma A, Agarwal A, Vishnu VY, Padma Srivastava M V. Collateral circulation- Evolving from time window to tissue window. Ann Indian Acad Neurol 2023;26:10-6

How to cite this URL:
Sharma A, Agarwal A, Vishnu VY, Padma Srivastava M V. Collateral circulation- Evolving from time window to tissue window. Ann Indian Acad Neurol [serial online] 2023 [cited 2023 Feb 1];26:10-6. Available from:

   Introduction Top

Cerebral collateral circulation refers to the auxiliary vascular structures which compensate cerebral blood flow when it has been compromised due to stenosis or occlusion of the principal supplying arteries.[1] The phrase “time is brain” emphasizes that human nervous tissue is rapidly and irretrievably lost as time progresses and that therapeutic interventions should be emergently pursued. The concept of collateral circulation has been evolving since its first description by Libeskind[2] with a shift from time-frame to tissue-frame. In acute stroke patients, accurate assessment of the structure and function of cerebral collateral circulation is an indispensable part of management. They were optimally utilized and their importance emphasized in the benchmark mechanical endovascular thrombectomy trials. Various imaging criteria have been developed to gauge the collateral status and correlate with stroke prognosis in patients with acute stroke. There are also emerging therapies that enhance collateral circulation in acute stroke patients.

   Overview of Anatomy Top

  • Collateral vessels are capable of supplying flow to an area normally supplied by another vessel. These vessels are subsidiary network of vascular channels that stabilize cerebral blood flow when the principal conduit fails. In the setting of an acute ischemic stroke, well-developed collaterals have a protective effect on the penumbra by maintaining perfusion, thereby minimizing the area of damage of cerebral tissues (ischemic core). The presence or absence of good collateral is responsible for the heterogeneity in the time course and severity of individual ischemic stroke patients.[3]
  • Collaterogenesis—It denotes the embryonic formation of native collaterals. Acute obstruction induces flow across this collateral network (recruitment), followed by remodeling. Chronic obstructive disease leads to the formation of additional collaterals in neo-collateral formation.
  • Loss of native collaterals (rarefaction) can be caused by aging and other vascular risk factors.
  • No consensus or unified criteria exists for precise classification of collateral circulation. However, it can be divided on the following basis.[4]

  • • Anatomical basis: Collaterals between the intracranial and extracranial arteries and collaterals between the intracranial arteries.

    • Activation period: collaterals which act immediately or in minutes (early activation of collaterals) and collaterals which act with a delayed action (delayed recruitment).

    • Primary, secondary and tertiary collaterals: Primary collaterals refer to the arterial segments of the circle of Willis (Willisian collaterals); Secondary collaterals include the ophthalmic artery and leptomeningeal arteries, as well as other anastomoses between the distal, small-caliber arteries; Tertiary collaterals refer to newly developed micro-vessels through angiogenesis at the periphery of ischemic regions.

  • The recently proposed concept of “collaterome” represents the elaborate neurovascular architecture within the brain that regulates and determines the compensatory ability, response and outcome of cerebrovascular pathophysiology.

   Factors Affecting Collateral Status Top

There are certain modifiable and nonmodifiable factors that determine the collateral extent of the brain circulation. Modifiable ones include the typical vascular risk factors like hypertension, metabolic syndrome, cigarette smoking and alcohol use. Nonmodifiable ones are age and genetic factors.[5]

   Imaging Methods and Grading Criteria for Cerebral Collateral Circulation Top

Collateral status is described either by angiography or in terms of resultant perfusion or infarction patterns. Collateral imaging parallels the basic four Ps of stroke imaging (pipes, perfusion, penumbra and parenchyma).[6] Primary conduit failure leads to sprouting up of new vessels as well as dormant vessels which are low flow cerebral collateral vessels and maintains the blood flow to the compromised tissue. Maintenance of the blood flow to the penumbral tissue is of utmost importance and helps decrease the infarct growth, lessen the hemorrhagic transformation and widen the therapeutic time window for action.[7] Studies have revealed that better MTT and ASPECTS scores correlated with better collateral circulation. A better collateral circulation is associated with a smaller infarct core and a larger mismatch ratio.

The most accurate measures of collateral function are the assessment of delay and dispersion through these conduits.[6],[7] This delay and dispersion of blood flow through these auxiliary vessels determines the tissue outcome. Maintained perfusion of the clot also assists in delivering endo/exogenous tPA thus increasing the chances of recanalization. These imaging methods gauge the cerebral blood flow direction, velocity, volume or perfusion to reflect the compensating function of collaterals. Some novel imaging techniques like QMRA could simultaneously reveal both: the structure and function of collateral circulation.

Multiple imaging modalities are used to assess collaterals in clinical practice and research.[7] These include transcranial doppler (TCD), transcranial color-coded duplex sonography (TCCD), computed tomographic angiography (CTA), CT perfusion (CTP), magnetic resonance angiography (MRA) and digital subtraction angiography (DSA). Amongst these, DSA has been considered the gold standard. However, because of the invasive nature of DSA, noninvasive methods are more commonly performed for collateral assessment.

CTA is also a noninvasive method that bears a high accuracy in assessing patency of the arterial segments in the circle of Willis, with >90% agreement with DSA, but its sensitivity (53%) is limited in depicting hypoplastic arterial segments. It can be done via four methods: single-phase CTA, timing-invariant CTA, whole brain dynamic time-resolved CTA/4D-CTA and multiphase CTA. Traditional single-phase CTA misinterprets and commonly over-represents findings as it provides a single snapshot of the collateral circulation. Blood flow through the collaterals might be delayed when compared with the normal antegrade flow, thus underestimating the compensating flow. Multiphase CTA is an imaging tool that overcomes this flaw. Its images are acquired in three phases: peak arterial, peak venous and late venous, and thereby provides temporal information about the degree and extent of the pial collateral filling. It does not need any mathematical algorithm or complex post processing and has an excellent interrater reliability.

MRA-based various methods have also been used to assess the collateral status such as time-of-flight (TOF) MRA, phase contrast MRA and quantitative MRA. MRA-based methods bear certain limitations of being comparatively expensive than CTA, longer scanning time requirement and an absence of a standardized collateral grading system. TOF-MRA is commonly utilized noninvasive method in patients with acute ischemic stroke. In reference to DSA, the sensitivity and specificity of TOF-MRA in detecting collateral flow via the anterior and posterior part of the circle of Willis were 83% and 77%, and 33% and 88% respectively. Its assessment of leptomeningeal collaterals is limited by its relatively low spatial resolution and therefore, is usually used to assess primary collaterals via the circle of Willis. Contrast-enhanced MRA is preferred for the assessment of leptomeningeal collaterals as it is superior in localizing vessel occlusion and has a shorter acquisition time. It also provides more accurate assessment and a larger coverage, including extracranial vessels. ASL-MRI utilizes a nonexternal contrast agent-based method. Arterial transit artifact is observed in ASL-MRI where serpiginous high signal (hyperintense vessels) is seen on the ASL maps at the edge of the infarct depicting God collateral status.

DSA is an invasive and the gold standard method to evaluate the collateral status. The standard criterion for assessment of collateral flow is multivessel DSA. This generates images with high spatial and temporal resolution, which allows the evaluation of contrast flow into the ischemic regions via collaterals. However, it is considered impractical in patients with acute ischemic stroke because speed of treatment is an important factor in these cases.

TCD can noninvasively reflect real-time cerebral blood flow velocity, collateral status and cerebrovascular reactivity at a relatively low cost. Collateral flow through anterior and posterior communicating arteries, ophthalmic artery and leptomeningeal arteries can be detected directly or indirectly by TCD. The sensitivities of TCD in detecting a patent anterior communicating artery and collateral flow through basilar artery were reported to be 95% and 87%, and the specificities were 100% and 95% respectively (DSA being the reference standard). In addition, the flow diversion phenomenon (high-velocity and low-resistance flow in the anterior cerebral artery (ACA) or posterior cerebral artery (PCA) in the presence of the middle cerebral artery (MCA) occlusion or severe stenosis) implies the presence of leptomeningeal collateral anastomoses between the ACA-PCA and distal MCA branches. The sensitivity and specificity of flow diversion by TCD was 81.1% and 76.7%, respectively whereas the positive and negative predictive values were 70.8% and 85.2%, respectively.

   Commonly Used Grading Scales for Cerebral Collateral Circulation Top

[Table 1] shows examples of various CTA-based collateral grading methods.
Table 1: CT angiography-based collateral scoring methods

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There have been studies comparing the clinical relevance of these grading methods, but the findings were heterogeneous and none of the collateral grading systems have been well validated in large-scale studies. Further investigation is needed to establish an optimal method to noninvasively assess collateral circulation.

   Clinical Significance of Collaterals Top

Hyperacute reperfusion therapies for ischemic stroke include intravenous thrombolysis and endovascular therapies including intra-arterial thrombolysis and mechanical thrombectomy. Timely restoration of the blood flow salvages the ischemic penumbra and thus improves the functional outcome and reduces mortality. Cerebral collateral circulation helps in utilizing the extended time frame and provides better tissue perfusion status as well.

Few prospective studies have investigated the role of collateral circulation in determining the outcomes of patients receiving intravenous thrombolytic therapy. Post hoc analysis of several RCTs indicated better collateral status prior to intravenous thrombolysis was associated with less severe clinical symptoms,[15] a smaller infarct core in diffusion-weighted MRI and a larger diffusion perfusion mismatch[16] and a favorable functional outcome at 3 months after the treatment.[15],[17]

A number of previous endovascular treatment trials failed to prove the superiority of endovascular treatment over routine medical treatment with or without intravenous thrombolysis in acute ischemic stroke. IMS III trial[17] was the first one to demonstrate no effect of EVT in acute ischemic stroke. MR RESCUE[18] showed that successful recanalization failed to improve the functional outcome in a significant proportion of patients, ranging from 26% to 49%. There was a dire need to improve the patient selection based on individual pathophysiology. In 2015, several pivotal RCTs and their meta-analysis[19] demonstrated the safety and efficacy of endovascular treatment in ischemic stroke with cervical or intracranial arterial occlusion. Based on these landmark trials the American and Chinese guidelines on early management of ischemic stroke were updated, recommending endovascular treatment for eligible patients presenting within 6 h of symptom onset with or without prior intravenous thrombolytic therapy. Apart from usage of newer generation thrombectomy devices, certain imaging eligibility criteria were used for patient selection.

The factors including moderate-to-good collateral circulation, a smaller infarct core or evidence of salvageable brain tissue, may have contributed to the positive findings in these more recent RCTs. DEFUSE 3 trial[20] demonstrated that endovascular thrombectomy for patients with ischemic stroke between 6–16 h with proximal MCA or internal carotid artery (ICA) occlusion, an initial infarct size of less than 70 mL, and a ratio of the volume of ischemic tissue on perfusion imaging to infarct volume of 1.8 or more had a significant favorable functional outcomes at 90 days compared with the medical therapy-alone group (OR, 2.77; P < 0.001). The DAWN trial[21] witnessed a significant increase (an absolute increase of 35%) in the incidence of a 90-day favorable functional outcome (mRS 0–2) in patients with intracranial ICA or M1 MCA occlusion, yet a small infarct core treated with mechanical thrombectomy 6–24 h after the stroke onset as compared with routine medical treatment. Both these extended window trials indirectly based EVT eligibility on good collateral circulation leading to slower infarct growth and salvageable penumbra.

Two recent systematic reviews and meta-analyses[22],[23] investigated the effects of pretreatment collateral circulation status on the clinical and imaging outcomes of stroke patients receiving endovascular treatment. Data from over 25 studies with ≥2000 stroke patients treated with intra-arterial thrombolysis and/or mechanical thrombectomy, with or without intravenous thrombolysis was analyzed. They revealed better pretreatment collateral circulation was associated with higher rates of successful recanalization (RR 1.23; 95%CI 1.06 to 1.42; P = 0.006) and reperfusion (RR 1.28; 95%CI 1.17 to 1.40; P < 0.001), a lower risk of symptomatic intracranial hemorrhage within 7 days or before discharge (RR 0.59; 95%CI 0.43 to 0.81; P = 0.001), better chance of achieving a favorable functional outcome at 3 months (RR 1.98; 95%CI 1.64 to 2.38; P < 0.001), and a halved risk of death at 3 months (RR 0.49; 95%CI 0.38 to 0.63; P < 0.001).

Two main studies depicted that collateral status significantly altered the risk of recurrent stroke in patients with symptomatic intracranial atherosclerotic disease (ICAD). Chinese Intracranial Atherosclerosis Study (CICAS)[24] observed that 46.6% of the 2864 patients with ischemic stroke or TIA had ICAD. It was largest study reporting the correlation between the completeness of the circle of Willis with stroke recurrence risk in patients with ischemic stroke or TIA. However, no conclusion could be drawn from such analysis concerning the protective or harmful effect of collateral flow through the circle of Willis in patients with ICAD. WASID trial[25] observed that 569 patients were recruited to the trial with 50%–99% symptomatic atherosclerotic stenosis of a major intracranial artery. Adequate angiographic data to assess the leptomeningeal collaterals was available in 287 patients. Analyses by the severity of arterial stenosis indicated that more robust leptomeningeal collaterals were associated with a lower risk of recurrence among patients with 70%–99% symptomatic ICAD.

   Interventions to Enhance Cerebral Collateral Circulation in Ischemic Stroke Top

Nonpharmacological interventions

  • Extracranial-intracranial bypass surgery—Extracranial-intracranial (EC-IC) bypass surgery may improve hemodynamic parameters in patients with symptomatic cervico-cerebral artery stenosis or occlusion. Largest RCT of EC-IC bypass was conducted 30 years ago which included 1377 patients[26] and inferred the inferiority of direct EC-IC bypass surgery over medical treatment. Carotid Occlusion Surgery Study (COSS)[27] and Japanese EC-IC Bypass Trial (JET)[28] compared direct EC-IC bypass surgery plus medical management versus medical treatment alone among patients with symptomatic atherosclerotic ICA occlusion. Both studies indicated inferiority of direct EC-IC bypass surgery over medical treatment among these patients.
  • Encephaloduroarteriosynangiosis (EDAS)—This is an indirect surgical EC-IC bypass method which has recently been reported safe and possibly effective in improving collateral circulation and reducing risk of recurrence.[29] This requires further investigation as previous studies were done on small symptomatic ICAD patient groups with stroke recurrence despite the best medical treatment.
  • Partial aortic occlusion by the NeuroFlo technology—The NeuroFlo Catheter has two balloons which when mounted and inflated in the aorta could partially occlude the aortic lumen above and below the renal arteries, to increase cerebral blood flow. The safety and efficacy of this technology was studied in Safety and Efficacy of NeuroFlo in Acute Ischemic Stroke (SENTIS) trial.[30] In this trial total 515 patients were recruited and partial aortic occlusion by NeuroFlo Catheter was done to increase cerebral blood flow versus standard medical treatment. No significant difference was observed between the two groups in the primary efficacy outcome, a favorable function outcome (OR 1.17; 95%CI 0.81 to 1.67; P = 0.407), but a trend of decreased all-cause mortality was observed in the Neuroflo treated group. It needs further evaluation by appropriate selection of the patients.
  • External counter pulsation—This is a noninvasive method that enhances cardiac output and blood flow to vital organs including the brain by inflating pressure cuffs around the lower extremities and the buttocks during the diastole and deflating the cuffs during the systole. This method was studied in the CUFFS trial[31] which included 23 patients and a single 1 h session of ECP. This trial showed transient improvement in the neurological symptoms of patients with stroke. Another pilot study also showed a slightly more significant decrease in the NIHSS score after 35 daily sessions of ECP than no ECP treatment.[32] Therefore, ECP might be considered a safe alternative to augment cerebral blood flow and improve outcomes of patients with ischemic stroke.
  • Flat head positioning—Cerebral autoregulation is impaired in patients with acute ischemic stroke. Lying flat may increase the cerebral blood flow through collateral circulation or gravity, as compared with an upright head positioning. Olavarría et al.[33] conducted a systematic review and meta-analysis of four small studies (57 patients in total) which indicated that ipsilesional but not contralesional MCA flow velocities were significantly higher when patients were in a lying-flat head position at 0° or 15° as compared with an upright head position of 30°. The Head Position in Acute Stroke Trial (HeadPoST)[34] also investigated the effects of different head positions on outcomes of 11,000 patients with acute ischemic or hemorrhagic stroke. The patients were nursed in a lying-flat or sitting-up (≥30°) head position and remained in that position for 24 h. It did not show any difference in the head positions and the 3-month function outcome. Thus, no conclusion can be drawn based on current evidence regarding the effects of different head positions on clinical outcomes of patients with ischemic stroke.

Pharmacological interventions

  • Statins—Statin therapy has pleiotropic effects. It reduces the concentration of low- density lipoproteins (LDL) cholesterol, lowers blood pressure and has antiinflammatory effects. A recent systematic review and meta-analysis[35] has demonstrated that prestroke statin use is associated with milder initial stroke severity (OR 1.24; 95%CI 1.05 to 1.48; P = 0.013), better functional outcome (OR 1.50; 95%CI 1.29 to 1.75; P < 0.001), and lower mortality (OR 0.42; 95%CI 0.21 to 0. 82; P = 0.011). Small studies also showed that prestroke use of statins might be independently associated with better collateral circulation in cardioembolic, large artery atherosclerotic strokes or strokes of unknown aetiologias by increasing nitric oxide synthesis and promoting ischemia-induced neovascularization.[36]
  • Drug-induced Hypertension—Animal studies results have hinted that drug-induced mild hypertension might increase the cerebral outflow and cerebral oxygen metabolism in the infarct core and penumbra, which might lead to smaller infarct size. SETIN-HYPERTENSION trial[37] also showed that phenylephrine-induced hypertension resulted in early neurological improvement and functional independence.
  • Hypervolemic treatment—Preclinical studies and pilot clinical studies showed possible neuroprotective effect of hypervolemic treatment by utilizing albumin in patients with acute ischemic stroke. However, early initiation of albumin treatment has been shown to have no additional clinical benefit versus isotonic saline in adult patients with ischemic stroke with a baseline NIHSS score of 6 or higher who were treated within 5 h of symptoms onset, in a multicentre, double-blinded RCT.[38] The trial was stopped early because of more events of pulmonary edema or congestive heart failure.

   Conclusion Top

Collateral circulation plays a vital role in sustaining blood flow to the ischemic areas in acute, subacute or chronic phases of acute ischemic stroke or TIA. Good collateral circulation has shown protective effects toward a favorable functional outcome and a lower risk of recurrence of stroke. Over the past few decades, the importance of collateral circulation has been realized and is a research hotspot. The diversity of the imaging methods and their structural and functional assessment has hindered the comparability of findings from different cohorts. The benchmark mechanical thrombectomy trials utilized these collateral scoring methods to guide patient selection and prognosticate favorable outcome models. This shows a promising future of the collateral circulation for extending the time frame of the reperfusion therapies by optimally guiding patient selection according to the tissue perfusion status. Further studies need to be explored to enhance the collateral flow.

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Conflicts of interest

There are no conflicts of interest.

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