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Research ArticleBrain

Systematic Review of Methods for Assessing Leptomeningeal Collateral Flow

F. McVerry, D.S. Liebeskind and K.W. Muir
American Journal of Neuroradiology March 2012, 33 (3) 576-582; DOI: https://doi.org/10.3174/ajnr.A2794

Abstract

BACKGROUND AND PURPOSE: The importance of LMF in the outcome after acute ischemic stroke is increasingly recognized, but imaging presents a wide range of options for identification of collaterals and there is no single system for grading collateral flow. The aim of this study was to systematically review the literature on the available methods for measuring LMF adequacy.

MATERIALS AND METHODS: We performed a systematic review of Ovid, MEDLINE, and Embase databases for studies in which flow in the leptomeningeal collateral vessels was evaluated. Imaging technique, grading scale, and reliability assessment for collateral flow measurement were recorded.

RESULTS: We found 81 publications describing 63 methods for grading collateral flow on the basis of conventional angiography (n = 41), CT (n = 7), MR imaging (n = 9), and transcranial Doppler (n = 6). Inter- and/or intraobserver agreement was assessed in only 8 publications.

CONCLUSIONS: There is inconsistency in how LMF is graded, with a variety of grading scales and imaging modalities being used. Consistency in evaluating collateral flow at baseline is required for the impact of collateral flow to be fully appreciated.

ABBREVIATIONS:

ACA
anterior cerebral artery
ASL
arterial spin-labeling
IA
intra-arterial
LMF
leptomeningeal collateral flow
PCA
posterior cerebral artery
TCD
transcranial Doppler
TIMI
Thrombolysis in Myocardial Infarction

Leptomeningeal collaterals are anastomotic vessels providing alternative routes for blood flow in stroke.1 In chronic hypoperfusion due to severe carotid stenosis or occlusion, flow via leptomeningeal vessels can maintain cerebral blood flow when primary collateral flow (via the arterial segments of the circle of Willis) is insufficient.2,3 Better LMF is associated with less infarct growth and better outcome following acute stroke,4,5 while poor collateralization is associated with hemorrhage after IA thrombolysis.6 Numerous studies, using several imaging modalities and grading methods, suggest that leptomeningeal collaterals confer a benefit in stroke. Because the influential role of collaterals has been repeatedly reported, we conducted a systematic literature review to investigate the available LMF assessment methods.

Materials and Methods

MEDLINE and Embase were searched from inception to week 32, 2009, by using the Ovid on-line portal for LMF assessments. The search strategy is shown in Appendix 1. The search was supplemented by review of journal electronic tables of contents and by searching the bibliographies of relevant articles; when full text was unavailable, authors were contacted. Studies that graded LMF, published in English and performed on humans, were considered, with assessments on patients with Moyamoya disease excluded. The target population included patients with acute stroke (<24 hours from onset) or patients with known cerebrovascular disease who had collateral flow assessed at later time points. Studies that graded collateral flow and provided a description of the assessment method were included. Terms such as “cortical/pial anastomoses” were judged as being synonymous with leptomeningeal collaterals and were assessed according to the same criteria. Positron-emission tomography and single-photon emission CT examinations, which indirectly evaluated collaterals, were excluded. Included publication dates ranged from January 1965 to October 2010.

Results

MEDLINE and Embase searches yielded 9456 and 6847 publications, respectively, 195 of which were screened as relevant and had full texts reviewed. After screening, we included 39 articles. A further 42 articles were obtained by handsearching bibliographies and review of electronic tables of contents, providing a total of 81 different publications for inclusion (n = 4686 patients, Table 1). In total, 41 different criteria for grading LMF with conventional angiography (n = 3467 patients), including both acute and nonacute patient groups with collateral assessments in anterior and posterior circulation, were recorded (Table 2).4,6⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓–62 Reliability assessments were available for 2 of these methods, demonstrating good and very good inter-/intraobserver agreement (n = 172).6,14,40 Arterial injection sites, when described, included unilateral carotid/MCA (n = 3),34,54,56 bilateral carotid (n = 3),24,52,63 a minimum of ipsilateral carotid and vertebral (n = 10),9,31,36,38,39,45,51,53,55,58 and other combinations (n = 5).10,11,28,49,50

View this table:
Table 1:

Number of LMF assessments per imaging modality

View this table:
Table 2:

Catheter angiography collateral scoring methodsa

Seven grading scales by using CTA were identified, with LMF assessments performed on 593 patients with suspected acute stroke (Table 3).5,34,64⇓⇓⇓⇓⇓⇓⇓⇓–73 Interobserver agreement was assessed for 5 CTA methods, ranging from moderate to excellent (n = 247). One grading scale used a combination of CTP in addition to CTA to confirm the retrograde direction of true LMF.5 MR imaging (n = 358 patients) and TCD (n = 268 patients) were used according to 9 and 6 grading methods respectively, with no assessments of interobserver agreement being reported (Tables 4 and 5).2,13,19,27,31,35,51,74⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓–86 A total of 8 publications compared noninvasive LMF assessments with MR imaging (n = 5), CT (n = 2), or TCD (n = 1) with a reference standard by using DSA; in each, a different grading scale for the criterion standard was used.13,19,27,31,34⇓–36,51

View this table:
Table 3:

CT-based collateral scoring methods

View this table:
Table 4:

MR imaging-based grading methods

View this table:
Table 5:

TCD-based grading methods

Discussion

The quality of LMF is reported to be an independent predictor of outcome after acute ischemic stroke, after adjustment for other known prognostic factors such as age, clinical stroke severity, baseline imaging characteristics, occlusion site, treatment, and recanalization/reperfusion4,5,43,63,65,69,72 and suggests that, as a minimum, there is a need to account for its influence on outcomes after stroke. Good collateral flow is assumed to be associated with favorable outcome as a consequence of maintaining the ischemic penumbra for longer until reperfusion occurs, though the effect of collaterals appears to be independent of conventional indices of penumbra such as arterial recanalization/reperfusion.5,65

It is unclear whether the collateral grade represents an inherent characteristic of individual subjects or a potential therapeutic target. Collateral flow grades on CTA are reportedly better in patients who undergo imaging later after symptom onset, while better collateral flow grades on conventional angiography have been reported in patients treated with statins before stroke,18 suggesting that collateral flow is dynamic and could potentially be modified.

The fact that LMF is not accounted for in occlusion classifications may be important in defining arterial occlusions at the entry to a clinical trial and adoption of scoring systems from coronary artery disease; notably, the TIMI87 system or minor modifications of such systems (eg, thrombolysis in cerebral ischemia) ignore fundamental differences in the acquisition of images and the anatomy of the different vascular beds. For example, when applied to the cerebral circulation, a “good” TIMI score on CTA (eg, TIMI 2) could actually represent a complete arterial occlusion (no anterograde flow) with extensive retrograde flow via collaterals. A consistent method for assessment and grading is required to investigate collaterals in acute stroke. Our review revealed wide variation in the methods for grading LMF, few of which are supported even by measurement of observer agreement.

Conventional angiography, considered the criterion standard for assessing cerebrovascular anatomy, can reveal retrograde collateral perfusion in a dynamic fashion and has been used for LMF assessments in the largest number of patients. The most frequently used scale was proposed by the American Society of Interventional and Therapeutic Neuroradiology in an effort to homogenize grading with angiography16, but an assessment of interobserver agreement has not yet been reported. Good intraobserver agreement has been demonstrated with angiography when LMF was graded according to the anatomic extent of retrograde flow (κ = 0.81).6,14 The Qureshi scale also demonstrates good interobserver agreement but does not focus on LMF independently. One collateral grading scale quantified collateral flow according to the time taken for contrast to travel from the ICA to the M2 segment of the MCA via collaterals but described flow through primary collaterals of the circle of Willis rather than through cortical anastomoses.88 Although not truly grading LMF, it provides a quantitative time-based measurement that could potentially be used for collateral assessments. Because LMF is derived from neighboring arterial territories, its quality may only be fully evaluated when the contribution of all potential inflow sources is assessed. Descriptions of arterial injection sites are infrequently provided, and even when available, the contribution of the whole cerebral circulation is seldom evaluated. Conventional angiography is invasive and is usually performed when a patient is being considered for IA therapy which, in general, is reserved for those with contraindications to intravenous treatment (eg, presentation beyond 4.5 hours with favorable appearances on CT), meaning that angiographic LMF assessments are predominantly restricted to this group. Because multimodal CT and MR imaging are increasingly used in clinical practice and before entry to clinical trials, they offer a larger potential population in which LMF can be assessed noninvasively.

Although lacking dynamic information, CTA permits visualization of the extent of LMF. The independent predictive value of collaterals has been confirmed with different CTA methods, and interobserver agreement within different grading scales has been assessed.64,69,71,72 Retrograde flow relative to a proximal arterial occlusion provides a measurement of LMF adequacy, but grading LMF this way for more distal occlusions may be more difficult. A collateral scoring system based on contrast enhancement in defined regions of interest provides a scale not dependant on a specific occlusion, which could potentially be applied in a larger patient population.64 The addition of CT perfusion to CTA adds important dynamic information to confirm that collateral flow is truly retrograde and demonstrates excellent interobserver agreement.5 New multidetector scanners that enable simultaneous acquisition of both CTA and CTP allow dynamic collateral flow assessment with CT.89

LMF assessments with MR imaging use different imaging characteristics to infer the presence of collaterals. FLAIR vascular hyperintensities due to retrograde flow in leptomeningeal vessels have been associated with larger mismatch volumes and smaller subacute infarct volumes, while abnormal vessels on T2* imaging may be due to deoxygenated blood in collaterals and are associated with smaller infarct volumes.80,81 ASL, by using different criteria, has also been used to grade collateral flow with MR imaging.13,51,78 These and other LMF assessments with MR imaging have not been replicated nor has interobserver reliability been graded, and it remains to be seen if they represent robust means of assessing collateral flow.

Relative blood flow velocity and vessel pulsatility have been used as surrogate markers for leptomeningeal collateral flow by using TCD in a small number of studies, but the criteria for defining LMF varied among publications (Table 5). The lack of an agreed definition for LMF on TCD, absence of direct collateral visualization, and difficulty in finding acoustic windows are limitations of TCD, though these are offset by the lack of radiation and contrast requirements.90 Flow diversion on TCD, defined as increased flow velocity in ipsilateral ACA/PCA, did correlate with angiographic collateral grade when methods were compared, suggesting a possible role for TCD to measure LMF.35

When collaterals were measured by using DSA, CTA, and MR imaging, CTA compared favorably, but the methods used for grading LMF on CTA were not clearly stated, so this finding must be interpreted with caution.36

Conclusions

The presence of flow in leptomeningeal collaterals is linked with positive outcomes after stroke, but there is little consistency in the methods used to grade the efficacy of collateral flow. Although the importance of leptomeningeal collaterals is consistently reported, the inconsistency in imaging methods and grading currently limits the emphasis that can be placed on collaterals. For targeting collateral vessels in stroke therapeutic strategies, consistency in examining their extent at baseline is required to permit further expansion of this area. At present, conventional angiography remains the method that can best measure collateral extent and number, but CT-based techniques, which have demonstrated good interobserver reliability and correlation with clinical outcome, may provide an accessible and reliable assessment method for grading collateral flow in a larger patient population, particularly with the development of dynamic CTA combined with perfusion imaging. MR imaging and TCD have been used less frequently than angiography or CT but can also provide noninvasive measurements of LMF.

Appendix

Search Strategy MEDLINE (1950 to July Week 1 2009) and Embase before 1980 to 2009 Week 32.

  • 1) stroke.mp. or *Stroke/ (112119)

  • 2) acute stroke.mp. or *Stroke/ (34761)

  • 3) *Adult/ or *Aged/ or *Ischemic Attack, Transient/ or *Cerebrovascular Circulation/ or *Cerebrovascular Disorders/ or *Brain/ or *Middle Aged/ or *Brain Ischemia/ or ischemic stroke.mp. or *Cerebral Infarction/ (93464)

  • 4) cerebral infarction.mp. or *Cerebral Infarction/ (13177)

  • 5) occlusion.mp. (91391)

  • 6) stenosis.mp. or Constriction, Pathologic/ (85260)

  • 7) carotid stenosis.mp. or *Carotid Stenosis/ (7417)

  • 8) *Cerebral Arteries/ or *Cerebrovascular Disorders/ or *Aged/ or *Carotid Artery Diseases/ or *Ischemic Attack, Transient/ or *Cerebral Infarction/ or *Arterial Occlusive Diseases/ or intracranial occlusion.mp. or *Stroke/ (70577)

  • 9) middle cerebral artery occlusion.mp. or *Infarction, Middle Cerebral Artery/ (7330)

  • 10) *Thrombosis/ or *Intracranial Thrombosis/ or *Carotid Artery Thrombosis/ or *“Intracranial Embolism and Thrombosis”/ or thrombosis.mp. (116053)

  • 11) clinical outcome.mp. (26854)

  • 12) contrast media.mp. or *Contrast Media/ (11586)

  • 13) tomography, x-ray computed.mp. or *Tomography, X-Ray Computed/ (55062)

  • 14) *Angiography, Digital Subtraction/ or *Angiography/ or Angiography.mp. or *Cerebral Angiography/ or *Magnetic Resonance Angiography/ (113286)

  • 15) CT angiography.mp. (3058)

  • 16) CT angiogram.mp. (148)

  • 17) CT angiography source images.mp. (7)

  • 18) *Brain Ischemia/ or *Brain/ or *Diffusion Magnetic Resonance Imaging/ or *Magnetic Resonance Imaging/ or MR, diffusion weighted.mp. (111259)

  • 19) MR angiography.mp. or *Magnetic Resonance Angiography/ (12630)

  • 20) digital subtraction angiography.mp. or *Angiography, Digital Subtraction/ (8851)

  • 21) angiogram.mp. (5291)

  • 22) *Ultrasonography, Doppler, Transcranial/ or transcranial.mp. (15831)

  • 23) *Cerebrovascular Circulation/ or *Collateral Circulation/ or pial collaterals.mp. or *Cerebral Arteries/ (4354)

  • 24) leptomeningeal collaterals.mp. (35)

  • 25) collateral circulation.mp. or *Collateral Circulation/ (6309)

  • 26) collateral vessels.mp. (1376)

  • 27) collateral flow.mp. (1333)

  • 28) collateral blood supply.mp. (203)

  • 29) CT perfusion.mp. (380)

  • 30) recanalization.mp. (7177)

  • 31) *Thrombolytic Therapy/ or thrombolysis.mp. or *Stroke/ (45637)

  • 32) angiogram.m_titl. (312)

  • 33) angiography.m_titl. (15333)

  • 34) collateral.m_titl. (3356)

  • 35) 33 or 32 or 21 or 17 or 12 or 20 or 15 or 14 or 22 or 34 or 30 or 13 or 16 or 19 (196091)

  • 36) 6 or 11 or 3 or 7 or 9 or 2 or 8 or 1 or 4 or 30 or 10 or 5 (460879)

  • 37) 27 or 25 or 28 or 30 or 24 or 26 or 23 (17675)

  • 38) 35, or 29 (196193)

  • 39) 38, and 36 and 37 (9774)

  • 40) limit 39 to humans (8311)

  • 41) limit 40 to English language (6887)

  • 42) from 41 keep 84,96,99,126,143,161,181,241,247,262–263,290,304,311–312,314,400,439,446,489,492,507,532,613,616,623,694,891,949 (29).

Footnotes

  • Disclosures: Ferghal McVerry—supported by an award from Chest Heart and Stroke Scotland* and the Translational Medicine Research Collaboration. David S. Liebeskind—RELATED: Grant: NINDS-NIH;* UNRELATED: Consultancy: Concentric Medical, CoAxia. Keith W. Muir—supported by the Scottish Imaging Network, A Platform for Scientific Excellence (SINAPSE) network; UNRELATED: Consultancy: ReNeuron, Lundbeck, MScience, Comments: preparation for a clinical trial in relation to stem cells (ReNeuron),* an ongoing trial in acute stroke thrombolysis (Lundbeck),* analysis of clinical trial data from acute stroke regenerative drug treatment (MScience);* Grants/Grants Pending: Penumbra, Concentric, ev3.* (*Money paid to institution)

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  • Received May 4, 2011.
  • Accepted after revision June 24, 2011.
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Systematic Review of Methods for Assessing Leptomeningeal Collateral Flow
F. McVerry, D.S. Liebeskind, K.W. Muir
American Journal of Neuroradiology Mar 2012, 33 (3) 576-582; DOI: 10.3174/ajnr.A2794
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