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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
F. McVerry
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D.S. Liebeskind
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K.W. Muir
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    Table 1:

    Number of LMF assessments per imaging modality

    ModalityDifferent Assessment MethodsNo. of PublicationsStudies with Inter-/Intraobserver Agreement Assessed
    Angiography415826,14,40
    CT71255,64,69,71,72
    MR imaging9130
    TCD670
    • View popup
    Table 2:

    Catheter angiography collateral scoring methodsa

    DescriptionGradingAuthor (No.)Acute (<24 hr from Symptom Onset)/Non-AcuteReliability Assessed?Prognostic Significance of Good Collateral Flow Grade in Acute Stroke
    Extent of anterograde and retrograde vessel filling0–3Brandt7 (20)AcuteNoBeneficial7,8
    Arnold et al8 (40)
    No. and rapidity of collateral vessel filling0–2von Kummer9 (53)AcuteNoBeneficial
    No. and rapidity of collateral vessel fillingN/ABozzao et al10 (36)AcuteNoNS10
    Bozzao et al11 (36)NS11, beneficial63
    Toni et al63 (80)
    Filling extent of main and distal vessels via collaterals0–3Wu et al13 (51)NonacuteNoN/A
    Reconstitution of vessel relative to occlusion1–5Christoforidis et al6 (104)AcuteYes, κ = 0.816,14Beneficial6,14
    Christoforidis et al14 (53)
    Retrograde MCA flow to insulaPresent, absent, indeterminateDerdeyn et al15 (117)NonacuteNoN/A
    Rapidity and extent of retrograde collateral flow0–4Bang et al4 (44)AcuteNoBeneficial4,17,20
    Higashida et al16 (0)aN/A16
    Bang et al17 (119)No effect18
    Ovbiagele et al18 (95)NS19,21–23
    Sanossian et al19 (74)
    Liebeskind20 (120)
    Liebeskind21 (120)
    Liebeskind22 (50)
    Liebeskind23 (66)
    Flow extent across cortical surfaceN/APowers et al24 (19)NonacuteNoN/A
    Visual inspectionN/AKlijn et al25 (76)NonacuteNoN/A
    Delayed contrast washoutN/AEssig et al26 (30)NonacuteNoN/A
    Visualization of slow flowN/AKamran et al27 (8)AcuteNoNS
    Visualization of flow patternGrade 4 = leptomeningeal flowOzgur et al28 (27)NonacuteNoN/A
    Cortical branches from contralateral ACA/PCAN/ARutgers et al29 (112)NonacuteNoN/A
    Visualization of pial vesselsN/AZappe et al30 (86)UnclearNoNS
    Visualization of anastomoses from adjacent vascular territoriesN/ANoguchi et al31 (5)AcuteNoNS
    Visualization of arteriogramN/AGrubb et al32 (81)NonacuteNoN/A
    Cortical arteries from PCAN/AFukuyama et al33 (3)NonacuteNoN/A
    No. and rapidity of vessel filling0–2Lee et al34 (8)AcuteNoNS
    Distal MCA branches filling through ACA or PCAN/AKim et al35 (51)AcuteNoNS
    Retrograde vessel fillingN/AKinoshita et al36 (10)UnclearNoNS
    Cortical branches from PCA to MCAN/Avan Laar et al37 (23)NonacuteNoN/A
    Retrograde filling of MCA branchesN/AYamauchi et al38 (42)NonacuteNoN/A
    Extent and no. of vessels filling via collateral flowAbsent, mild, or prominentUemura et al39 (25)CombinationNoNS
    Combination of occlusion site and extent of collateral flow0–5Qureshi40 (15)AcuteYes, κ = 0.7340Beneficial40–42
    Mohammad et al41 (57)
    Mohammad et al42 (55)
    Extent of retrograde flow in MCAGood, poorKucinski et al43 (111)AcuteNoBeneficial
    Gasparotti et al44 (27)
    Capillary blush in MCAGrade 4 = leptomeningeal flowRussell et al45 (14)NonacuteNoN/A
    MCA/PCA filling from posterior circulationN/ABischopps et al46 (68)NonacuteNoN/A
    Opacification of basilar artery by collateralsDistal vs distal and proximalCross et al47 (24)AcuteNoBeneficial
    Cortical branches filling MCA/ACA from PCAN/ABokkers et al48 (17)NonacuteNoN/A
    Pial collateral flow from ACA and PCAN/ADerdeyn et al49 (10)NonacuteNoN/A
    Flow via anastomotic channels on brain surfaceN/ASmith et al50 (18)NonacuteNoN/A
    Collateral flow assessment based on ASPECTS (13 areas)0–3 in corresponding anatomic locationsChng et al51 (18)NonacuteNoN/A
    No. and rapidity of vessel filling from ACAGood or scarcevon Kummer et al52 (77)AcuteNoNo effect
    No. and rapidity of vessel filling from ACA and PCA0–2von Kummer et al53 (32)AcuteNoBeneficial
    Filling extent of at risk territory1–3Roberts et al54 (180)AcuteNoBeneficial
    Collateral flow assessment based on ASPECTS (15 areas)0–3 in corresponding anatomic locationsKim et al55 (44)AcuteNoBeneficial
    MCA branch filling in early venous phaseGood, moderate, poorRingelstein et al56 (34)AcuteNoBeneficial
    Retrograde arterioles visualized in capillary phaseN/AWeidner et al57 (4)UnclearNoNS57
    Presence of superficial PCA/ACA cortical branchesN/AHoffmeijer et al58 (70)NonacuteNoN/A
    Extent of leptomeningeal anastomoses in occluded territoryPoor, goodArnold et al59 (98)AcuteNoNo effect59
    Meier et al60 (311)Beneficial60
    Presence of collaterals in affected territoryNone/minimal, moderate/maxGonner et al61 (43)AcuteNoNo effect61
    Brekenfeld et al62 (294)Beneficial62
    • Note:—NS indicates not stated; N/A, not applicable; ASPECTS, Alberta Stroke Program Early CT Score; max., maximal; PCA, posterior cerebral artery.

    • ↵a Proposal on working group on collateral grading.

    • View popup
    Table 3:

    CT-based collateral scoring methods

    ModalityDescriptionGradingAuthor (No.)Acute (<24 hr from Symptom Onset)/Non-AcuteReliability Assessed?Prognostic Significance of Good Collateral Flow Grade in Acute Stroke
    Axial CTA-SIExtent of perilesional vessel fillingNone, moderate, good, excellentLiebeskind64 (36)AcuteYes, ICC = 0.81NS
    CTA-SIComparison of Sylvian collaterals with contralateral hemisphereAbsent, less, equal to, greater than contralateral hemisphere, exuberantRosenthal et al65 (44)AcuteNoBeneficial65–67
    Maas et al66 (135)
    Lima et al67 (196)
    CTA-SI and MPRExtent of perilesional enhancementGood, poorSchramm et al68 (20)AcuteYes, κ = 0.494Beneficial68,69
    Tan et al69 (113)
    CTA-SI and reconstructionsMCA filling in Sylvian fissureGood, moderate, absentWildermuth et al70 (40)AcuteYesBeneficial70,71
    Knauth et al71 (21)88% agreement between 2 raters71
    CTA MIPExtent of filling in territory of occluded vessel0–3Tan et al69 (113)AcuteYesBeneficial69.72,73
    Tan et al72 (85)κ = 0.66969, ICC 0.8772
    Soares et al73 (22)
    CTA, MIP, CTPRetrograde filling of MCAGood, moderate, poorMiteff et al5 (92)AcuteYesBeneficial
    κ = 0.93
    (TCTP)Extent of perfusion deficit on TCTPSevere, moderateLee et al34AcuteNoNS
    • Note:—NS indicates not stated; ICC, intraclass correlation coefficient; CTA-SI, CT angiography source images; MPR, multiplanar reconstruction; MIP, maximum intensity projection; TPCT, triphasic CTP.

    • View popup
    Table 4:

    MR imaging-based grading methods

    ModalityDescriptionAuthor (No.)Acute (<24 hr from Symptom Onset)/NonacuteReliability Assessed?Prognostic Significance of Good Collateral Flow Grade in Acute Stroke
    FADSLate FADS implies collateral flowMartel et al84 (22)AcuteNoNS
    QMRAIncreased flow ipsilateral to steno-occlusive diseaseRuland et al83 (16)NonacuteNoN/A
    Phase-contrast MRAFlow from posterior to anterior circulationSchomer et al82 (29)NonacuteNoN/A
    FLAIRFLAIR hyperintensities as a marker of collateral flowLiebeskind85 (91)AcuteNoNS85,19,27,31,81
    Kamran et al27 (8)
    Noguchi et al31 (5)
    Sanossian et al19 (74)
    Lee et al81 (52)
    T2*-weighted MRIAbnormal visualization of leptomeningeal vesselsHermier et al80 (48)AcuteNoNS
    PWIDelayed perfusion sign visualized on PWIHermier et al79 (29)AcuteNoNS
    ASLQuantitative distal collateral flow measurementWu et al13 (51)NonacuteNoN/A
    TASLCollateral flow assessment based on ASPECTSChng et al51 (18)NonacuteNoN/A
    CASLCollateral flow inferred from delayed arterial flowChalela et al78 (15)AcuteNoNS
    • Note:—NS indicates not stated; N/A, not applicable; FADS, factor analysis of dynamic structures; QMRA, quantitative MRA; TASL, territorial arterial spin labelling; CASL, continuous arterial spin-labeled/labeling; ASPECTS, Alberta Stroke Program Early CT Score.

    • View popup
    Table 5:

    TCD-based grading methods

    DescriptionAuthor (No.)Acute (<24 hr from Symptom Onset)/NonacuteReliability Assessed?Prognostic Significance of Good Collateral Flow Grade in Acute Stroke
    Asymmetry of flow in ipsilateral ACA and PCAZanette et al77 (56)AcuteNoNS
    Asymmetric P2 flow and reduced pulsatilityReinhard et al76 (30)NonacuteNoN/A
    Reinhard et al75 (111)
    Asymmetric mean blood velocity in proximal ACA or P2 segment of ACAMuller and Schimrigk2 (48)NonacuteNoN/A
    Accelerated flow in A1 segment of ACAKaps et al74 (23)AcuteNoNS
    Flow direction relative to Doppler probeHennerici et al86,aUnclearNoNS
    Asymmetric flow velocity and pulsatility indexKim et al35 (51)AcuteNoNS
    • Note:—NS indicates not stated; N/A, not applicable.

    • ↵a Number not stated.

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American Journal of Neuroradiology: 33 (3)
American Journal of Neuroradiology
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F. McVerry, D.S. Liebeskind, K.W. Muir
Systematic Review of Methods for Assessing Leptomeningeal Collateral Flow
American Journal of Neuroradiology Mar 2012, 33 (3) 576-582; DOI: 10.3174/ajnr.A2794

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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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