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Research ArticleBrain

Double Inversion Recovery MR Sequence for the Detection of Subacute Subarachnoid Hemorrhage

J. Hodel, R. Aboukais, B. Dutouquet, E. Kalsoum, M.A. Benadjaoud, D. Chechin, M. Zins, A. Rahmouni, A. Luciani, J.-P. Pruvo, J.-P. Lejeune and X. Leclerc
American Journal of Neuroradiology February 2015, 36 (2) 251-258; DOI: https://doi.org/10.3174/ajnr.A4102
J. Hodel
aFrom the Departments of Neuroradiology (J.H., B.D., E.K., J.-P.P., X.L.)
eDepartment of Radiology (J.H., M.Z.), Hôpital Saint Joseph, Paris, France
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R. Aboukais
bNeurosurgery (R.A., J.-P.L.), Hôpital Roger Salengro, Lille, France
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B. Dutouquet
aFrom the Departments of Neuroradiology (J.H., B.D., E.K., J.-P.P., X.L.)
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E. Kalsoum
aFrom the Departments of Neuroradiology (J.H., B.D., E.K., J.-P.P., X.L.)
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M.A. Benadjaoud
cInstitut National De La Santé et De La Recherche Médicale (M.A.B.), Centre for Research in Epidemiology and Population Health, Villejuif, France
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D. Chechin
dPhilips Medical Systems (D.C.), Suresnes, France
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M. Zins
eDepartment of Radiology (J.H., M.Z.), Hôpital Saint Joseph, Paris, France
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A. Rahmouni
fDepartment of Radiology (A.R., A.L.), Centre Hospitalier Universitaire, Henri Mondor, Créteil, France.
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A. Luciani
fDepartment of Radiology (A.R., A.L.), Centre Hospitalier Universitaire, Henri Mondor, Créteil, France.
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J.-P. Pruvo
aFrom the Departments of Neuroradiology (J.H., B.D., E.K., J.-P.P., X.L.)
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J.-P. Lejeune
bNeurosurgery (R.A., J.-P.L.), Hôpital Roger Salengro, Lille, France
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X. Leclerc
aFrom the Departments of Neuroradiology (J.H., B.D., E.K., J.-P.P., X.L.)
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  • Fig 1.
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    Fig 1.

    Axial DIR images in a 37-year-old healthy volunteer showing the basal cisterns (A and B) and the subarachnoid spaces at the brain convexity (C). In all the healthy volunteers scanned with the DIR sequence, the CSF appeared hypointense without CSF flow-related artifacts (B, arrowheads). Note the regional variation of gray matter signal intensity by using DIR, such as the difference between the prefrontal (C, arrows) and motor (C, arrowheads) cortices. The absence of CSF signal abnormality on DIR images in all the healthy volunteers and the strong agreement among readers suggest that the hyperintensities observed in patients with SAH by using DIR were not linked to artifacts.

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    Fig 2.

    Subacute SAH related to an aneurysm of the anterior communicating artery in a 42-year-old woman. No signal abnormality is visible on 3D FLAIR (A). SAH is visible by using axial SWI minimum-intensity-projection reformations in the right Sylvian fissure (B, arrows). The hypointensity visible in the left Sylvian fissure on SWI was considered a cortical vein by the 3 blinded readers by using both average and minimum-intensity-projection reformations (B, arrowhead). On the axial T2* image, SAH is bilateral, involving the Sylvian fissures (C, arrows). The DIR sequence reveals extensive SAH prevailing in the Sylvian fissures (D, arrows) and interhemispheric and occipital sulci (D, arrowheads).

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    Fig 3.

    Subacute SAH related to an aneurysm of the anterior communicating artery in a 63-year-old man. With 2D FLAIR (A), 3D FLAIR (B), or T2* (C) images, no subacute hemorrhage is visible. Conversely, marked subarachnoid signal abnormalities along the anterior and posterior interhemispheric sulci are observed by using DIR (D, arrows). SAH involving the parietal lobes is also visible (D, arrowheads).

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    Fig 4.

    Subacute SAH related to an aneurysm of the left internal carotid artery in a 25-year-old woman. With 2D FLAIR images, the detection of SAH is challenging due to potential CSF flow-related artifacts (A, arrow). With an axial average SWI reformat, a slight rim of hemorrhage is visible within the interpeduncular fossa (B, arrow). On the 3D FLAIR image, SAH is subtle due to a lack of contrast (C, arrows). With DIR images, SAH is obvious, with a marked hyperintensity within the interpeduncular fossa, vermis, and left Sylvian fissure (D, arrows). Note the marked signal intensity of SAH with DIR compared with the other MR images.

Tables

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    Table 1:

    Demographic and clinical data at admission

    PatientsControls
    No.2520
    Sex16 M/9 F13 M/7 F
    Age (yr) (mean) (range)52 (28–71)50 (26–69)
    Fisher grading (mean)3
        Grade 1 (No.)5
        Grade 2 (No.)2
        Grade 3 (No.)6
        Grade 4 (No.)12
    GCS (mean) (range)14.1 (10–15)
    WFNS score (mean) (range)1.5 (1–4)
        No vascular lesion (No.)10
        Brain aneurysm (No.)15
    Etiologic work-up (CTA and DSA)
        ACA (No.)6
        MCA (No.)(right 2, left 2)
        Right PcomA (No.)2
        Left vertebral artery (No.)1
        Left ICA (No.)1
        Basilar artery (No.)1
    • Note:—GCS indicates Glasgow Coma Scale; WFNS, World Federation of Neurosurgical Societies; ACA, anterior communicating artery; PcomA, posterior communicating artery.

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    Table 2:

    MR imaging sequence parameters

    2D FLAIR2D T2*3D FLAIR3D SWI3D DIR
    Acquisition planeAxialAxialSagittalSagittalSagittal
    TR/TE (ms)11,000/1251077/164800/26713/195500/255
    TI (ms)2800–1650–2600/625
    Acquired voxel size (mm)0.8 × 1.4 × 40.9 × 1.2 × 41.2 × 1.2 × 1.21.2 × 1.2 × 1.21.2 × 1.2 × 1.2
    Bandwidth (Hz)27121614331721433
    Echo-train length31–182–173
    No. of sections3636280280280
    SENSE1.4–2.52.52.5
    CLEARYesYesYesYesYes
    Fat suppressionNoNoSPIRNoSPIR
    Acquisition time3 min3 min3 min 20 sec3 min4 min
    • Note:—SENSE indicates sensitivity encoding; CLEAR, inhomogeneity correction; SPIR, spectral presaturation with inversion recovery.

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    Table 3:

    Interobserver agreement among readers 1, 2, and 3 for each set of images according to the area considered

    CTMRI
    2D FLAIR3D FLAIR2D T2*3D SWI3D DIR
    Total
        R1 vs R2 (95% CI)1 (1–1)0.85 (0.77–0.93)0.79 (0.69–0.89)0.84 (0.76–0.91)0.79 (0.72–0.87)0.94 (0.91–0.97)
        R1 vs R3 (95% CI)0.94 (0.85–1)0.68 (0.57–0.79)0.65 (0.53–0.76)0.74 (0.65–0.83)0.64 (0.55–0.73)0.90 (0.87–0.93)
        R2 vs R3 (95% CI)0.94 (0.85–1.02)0.70 (0.60–0.81)0.70 (0.59–0.80)0.72 (0.63–0.81)0.73 (0.65–0.81)0.93 (0.91–0.96)
    Subarachnoid
        Interhemispheric
            R1 vs R2 (95% CI)1 (1–1)0.91 (0.74–1)0.83 (0.60–1)0.76 (0.54–0.98)0.68 (0.44–0.92)1 (1–1)
            R1 vs R3 (95% CI)1 (1–1)0.83 (0.60–1.06)0.76 (0.50–1.02)0.87 (0.70–1.05)0.44 (0.11–0.77)1 (1–1)
            R2 vs R3 (95% CI)1 (1–1)0.91 (0.74–1.08)0.76 (0.50–1.02)0.77 (0.56–0.99)0.63 (0.39–0.88)1 (1–1)
        Sylvian fissures
            R1 vs R2 (95% CI)1 (1–1)1 (1–1)1 (1–1)0.94 (0.83–1)0.82 (0.63–1)0.95 (0.88–1)
            R1 vs R3 (95% CI)1 (1–1)0.88 (0.66–1.11)1 (1–1)1 (1–1)0.59 (0.31–0.86)0.90 (0.81–1)
            R2 vs R3 (95% CI)1 (1–1)0.88 (0.66–1.11)1 (1–1)0.94 (0.83–1.06)0.73 (0.50–0.96)0.95 (0.89–1.02)
        Convexity
            R1 vs R2 (95% CI)1 (1–1)0.83 (0.68–0.98)0.56 (0.27–0.84)0.73 (0.57–0.89)0.63 (0.43–0.84)0.90 (0.85–0.95)
            R1 vs R3 (95% CI)0.83 (0.60–1.07)0.61 (0.42–0.81)0.48 (0.23–0.73)0.60 (0.42–0.78)0.63 (0.44–0.83)0.87 (0.81–0.92)
            R2 vs R3 (95% CI)0.83 (0.60–1.07)0.60 (0.40–0.79)0.56 (0.33–0.80)0.56 (0.37–0.74)0.70 (0.55–0.86)0.90 (0.85–0.95)
        Basal cisterns
            R1 vs R2 (95% CI)1 (1–1)0.33 (−0.33–0.98)0.70 (0.41–0.99)0.74 (0.39–1)0.64 (0.36–0.92)0.94 (0.88–1)
            R1 vs R3 (95% CI)1 (1–1)0.43 (−0.07–0.92)0.25 (−0.20–0.70)0.45 (−0.01–0.98)0.25 (−0.13–0.62)0.89 (0.82–0.97)
            R2 vs R3 (95% CI)1 (1–1)0.39 (−0.29–1.07)0.30 (−0.17–0.77)0.74 (0.39–1.10)0.41 (0.09–0.73)0.95 (0.90–1)
    Intraventricular
        R1 vs R2 (95% CI)1 (1–1)1 (1–1)1 (1–1)1 (1–1)0.95 (0.85–1)1 (1–1)
        R1 vs R3 (95% CI)1 (1–1)0 (−1.12–1.12)0 (−1.95–1.95)0.66 (0.19–1.13)0.86 (0.70–1.02)0 (−1.38–1.38)
        R2 vs R3 (95% CI)1 (1–1)0 (−1.12–1.12)0 (−-1.95–1.95)0.66 (0.19–1.13)0.82 (0.64–1)0 (−1.38–1.38)
    • Note:—R1–R3 indicate readers 1–3; Total, all the subarachnoid and ventricular areas; Convexity, bilateral frontal, parietal, temporal, and occipital convexity areas; Basal cisterns, perimesencephalic and prepontine cisterns and cisterna magna.

    • View popup
    Table 4:

    Number of patients with at least 1 subarachnoid and/or ventricular signal abnormality (diagnosis of SAH and IVH, respectively) for each imaging modality after consensus among readers

    CTMRI
    2D FLAIR3D FLAIR2D T2*3D SWI3D DIR
    Patients with SAH71215141525
    Interhemispherica067131525
    Sylvian fissuresa4449817
    Convexitya388101119
    Basal cisternsa0154723
    Patients with IVH000350
    • ↵a Number of patients with at least 1 subarachnoid signal abnormality.

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J. Hodel, R. Aboukais, B. Dutouquet, E. Kalsoum, M.A. Benadjaoud, D. Chechin, M. Zins, A. Rahmouni, A. Luciani, J.-P. Pruvo, J.-P. Lejeune, X. Leclerc
Double Inversion Recovery MR Sequence for the Detection of Subacute Subarachnoid Hemorrhage
American Journal of Neuroradiology Feb 2015, 36 (2) 251-258; DOI: 10.3174/ajnr.A4102

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Double Inversion Recovery MR Sequence for the Detection of Subacute Subarachnoid Hemorrhage
J. Hodel, R. Aboukais, B. Dutouquet, E. Kalsoum, M.A. Benadjaoud, D. Chechin, M. Zins, A. Rahmouni, A. Luciani, J.-P. Pruvo, J.-P. Lejeune, X. Leclerc
American Journal of Neuroradiology Feb 2015, 36 (2) 251-258; DOI: 10.3174/ajnr.A4102
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