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Research ArticleNeurovascular/Stroke Imaging

Timing of Spot Sign Appearance, Spot Sign Volume, and Leakage Rate among Phases of Multiphase CTA Predict Intracerebral Hemorrhage Growth

MacKenzie Horn, Ericka Teleg, Koji Tanaka, Abdulaziz Al Sultan, Linda Kasickova, Tomoyuki Ohara, Piyush Ojha, Sanchea Wasyliw, Sina Marzoughi, Ankur Banerjee, Girish Kulkarni, Kennedy Horn, Amy Bobyn, Anneliese Neweduk, Nishita Singh, Wu Qiu, David Rodriguez-Luna, Dar Dowlatshahi, Mayank Goyal, Bijoy K. Menon and Andrew M. Demchuk
American Journal of Neuroradiology June 2024, 45 (6) 693-700; DOI: https://doi.org/10.3174/ajnr.A8254
MacKenzie Horn
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Ericka Teleg
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Koji Tanaka
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Abdulaziz Al Sultan
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Linda Kasickova
dDepartment of Neurology (L.K.), University Ostrava, Ostrava, Czech Republic
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Tomoyuki Ohara
eDepartment of Neurology (T.O.), Kyoto Prefectural University of Medicine, Kyoto, Japan
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Piyush Ojha
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Sanchea Wasyliw
fDepartment of Medicine (S.W.), Division of Neurology, University of Saskatchewan, Saskatoon, Canada
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Sina Marzoughi
gDepartment of Medicine (S.M.), Division of Neurology, University of British Columbia, Vancouver, British Columbia, Canada
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Ankur Banerjee
hDepartment of Medicine (A. Banerjee), Division of Neurology, University of Alberta, Edmonton, Alberta, Canada
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Girish Kulkarni
iDepartment of Neurology (G.K.), National Institute of Mental Health and Neurosciences, Bengaluru, India
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Kennedy Horn
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Amy Bobyn
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Anneliese Neweduk
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Nishita Singh
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
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Wu Qiu
lDepartment of Biomedical Engineering (W.Q.), Huazhong University of Science and Technology, Wuhan, China
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David Rodriguez-Luna
jDepartment of Neurology (D.R.-L.), Vall d’Hebron University Hospital, Barcelona, Spain
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Dar Dowlatshahi
kDepartment of Medicine (D.D.), Division of Neurology, University of Ottawa, Ottawa, Ontario, Canada
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Mayank Goyal
bDepartment of Radiology (M.G., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
mHotchikiss Brain Institute (M.G., B.K.M., A.M.D.), Cumming School of Medicine, University of Calgary, Calgary, Canada
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Bijoy K. Menon
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
bDepartment of Radiology (M.G., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
cDepartment of Community Health Sciences (B.K.M.), University of Calgary, Calgary, Alberta, Canada
mHotchikiss Brain Institute (M.G., B.K.M., A.M.D.), Cumming School of Medicine, University of Calgary, Calgary, Canada
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Andrew M. Demchuk
aFrom the Foothills Medical Centre, Department of Clinical Neurosciences (M.H., E.T., K.T., A.A.S., P.O., K.H., A. Bobyn, A.N., N.S., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
bDepartment of Radiology (M.G., B.K.M., A.M.D.), University of Calgary, Calgary, Alberta, Canada
mHotchikiss Brain Institute (M.G., B.K.M., A.M.D.), Cumming School of Medicine, University of Calgary, Calgary, Canada
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  • FIG 1.
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    FIG 1.

    Patient inclusion/exclusion flow chart. Patients were screened according to the inclusion/exclusion criteria of the study. Of the 350 patients screened, 217 patients were included in the study.

  • FIG 2.
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    FIG 2.

    Representative slices of the spot sign in each phase of mCTA. A, Noncontrast CT shows a hematoma in the left putamen. B, mCTA shows a spot sign in the hematoma in the first phase (arrow). C, Segmentation of the spot sign in each phase. The volume of the spot sign in the first phase increases in the second phase. In the third phase, the contrast seems to partially disperse into the hematoma, and the volume of the spot sign decreases.

  • FIG 3.
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    FIG 3.

    Predicted spot sign volume by mCTA phase time stratified by hematoma growth category. A mixed-effects regression model estimated a change in spot sign volume across time stratified by different ICH growth category. The x-axis measures time in seconds under the assumption that phase 1 of the mCTA is acquired at time = 0 seconds, and the relationship between the predicted spot sign volume change and time are shown in patients without hematoma growth and hematoma growth of ≤6 mL and >6 mL. The area shows 95% CIs.

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    FIG 4.

    Hematoma growth probability as predicted by absolute spot sign leakage rate. The probability of hematoma growth of >6 mL is predicted by the absolute spot sign leakage rate ([|leakage rate between first and second phases| + |leakage rate between second and third phases|]/2). The area shows 95% CIs.

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    Table 1:

    Baseline characteristics stratified by presence or absence of hematoma growtha

    VariableTotal (n = 217)Hematoma GrowthP Value
    Yes (n = 44)No (n = 173)
    Age (yr)70 (59.5–80)75 (61–83)69 (59–79).209
    Sex (male)131 (60.4)27 (61.4)104 (60.1).880
    History of stroke21 (9.7)9 (20.5)12 (6.9).018
     Ischemic16 (7.4)8 (18.2)8 (4.6)
     Hemorrhagic5 (2.3)1 (2.3)4 (2.3)
    Hypertension182 (83.9)39 (88.6)143 (82.7).491
    Diabetes mellitus41 (18.9)10 (22.7)31 (17.9).467
    Current smoking23 (10.6)3 (6.8)20 (11.6).583
    Alcohol consumption9 (4.2)1 (2.3)8 (4.6).690
    Prior antithrombotic medication59 (27.2)17 (38.6)42 (24.3).056
     Antiplatelets26 (12.0)8 (18.2)18 (10.4).192
     Anticoagulants37 (17.1)11 (25.0)26 (15.0).116
    SBP (mm Hg)190 (171–205)200 (174–210)190 (168–200).160
    Hemoglobin (g/L)141 (131–153)141 (132–148)142 (131–154).432
    Serum glucose (mmol/L)6.9 (5.7–8.2)6.9 (5.7–8.2)6.7 (4.9–8.1).751
    International normalized ratio1 (1.0–1.1)1 (1.0–2.4)1 (1.0–1.1).146
    NIHSS score on admission10 (5–20)18.5 (9–23)8 (3.25–17)<.001
    Onset-to-imaging time (min)225 (109–392)151 (102–248)243 (134–422).008
    Baseline ICH volume (mL)18.9 (5.4–34.4)28.7 (13.7–58.8)12.8 (4.2–30.9)<.001
    Hematoma location.150
     Deep cerebral115 (53.0)26 (59.1)89 (51.5)
     Lobar80 (36.9)17 (38.6)63 (36.4)
     Infratentorial22 (10.1)1 (2.3)21 (12.1)
    Timing of spot sign appearance<.001
     No spot sign148 (68.2)10 (22.7)138 (79.8)
     First appearing in the first phase47 (21.7)26 (59.1)21 (12.1)
     First appearing in the second phase20 (9.2)8 (18.2)12 (6.9)
     First appearing in the third phase2 (0.9)0 (0)2 (1.2)
    • Note:—SBP indicates systolic blood pressure.

    • ↵a Hematoma growth is defined as a >6-mL increase in volume of the hematoma from baseline. Data are presented as No. (%) or median (interquartile range).

    • View popup
    Table 2:

    Spot sign parameters when compared with hematoma growth

    Spot Sign Volume ParameterTotalaSpot Sign First Appearing in the First PhaseSpot Sign First Appearing in the Second Phase
    Hematoma GrowthP ValueHematoma GrowthP Value
    Yes (n = 26)No (n = 21)Yes (n = 8)No (n = 12)
    Volume in the first phase (μL)19.7 (5.7–64.3)32.7 (12.9–74.3)6.7 (4.4–59.0).033
    Leakage rate between first and second phases (μL/sec)2.6 (0.6–7.7)3.8 (1.1–9.7)1.2 (0.4–6.5).034
    Volume in the second phase (μL)31.4 (7.4–108.8)95.9 (44.1–172.0)19.7 (8.2–133.0).01717.0 (5.8–40.3)6.3 (4.8–14.4).216
    Leakage rate between second and third phases (μL/sec)0.1 (−0.2–1.3)0.4 (−0.1–2.5)0.0 (−2.1–2.1).1530.6 (−0.1–2.1)0.1 (0.1–0.5).396
    Volume in the third phase (μL)34.8 (10.0–129.0)58.0 (32.9–172.6)34.8 (7.3–156.7).12131.5 (1.9–79.1)10.8 (6.2–18.5).440
    Absolute leakage rate (μL/sec)1.02 (0.5–4.7)3.5 (1.0–8.1)0.9 (0.5–3.8).017
    • ↵a The number of patients was 47 for volume in the first phase and leakage rate between the first and second phases, 67 for volume in the second phase and leakage rate between second and third phases, and 69 for volume in the third phase. Data are presented as median (interquartile range).

    • View popup
    Table 3:

    Logistic regression analysis for hematoma growth

    OR (95% CI)P valueC-StatisticBICAIC
    Model 10.735190.2183.5
     No spot sign in the first phase (reference)1.0
     Spot sign in the first phase10.5 (5.0–22.7)<.001
    Model 20.798182.8172.7
     No spot sign (reference)1.0
     Spot sign first appearing in the first phase17.1 (7.2–40.4)<.001
     Spot sign first appearing in the second or third phase7.9 (2.7–23.2)<.001
    Model 30.807185.6172.3
     No spot sign (reference)1.0
     Spot sign first appearing in the first phase with volume <19.7 μL10.6 (3.7–30.9)<.001
     Spot sign first appearing in the first phase with volume ≥19.7 μL27.6 (9.9–84.6)<.001
     Spot sign first appearing in the second or third phase7.9 (2.7–23.2)<.001
    Model 40.800182.4172.2
     No spot sign (reference)1.0
     Spot sign with positive leakage rate between phases10.1 (4.2–24.1)<.001
     Spot sign with negative leakage rate between any phases23.0 (8.1–65.5)<.001
    Model 5a0.71395.499.9
     Absolute leakage rate (per 1-μL/sec increase)1.26 (1.04–1.52).019
    • Note:—AIC indicates Akaike information criterion; BIC, Bayesian information criterion.

    • ↵a Model 5 includes only patients with the spot sign (n = 69).

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American Journal of Neuroradiology: 45 (6)
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Timing of Spot Sign Appearance, Spot Sign Volume, and Leakage Rate among Phases of Multiphase CTA Predict Intracerebral Hemorrhage Growth
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MacKenzie Horn, Ericka Teleg, Koji Tanaka, Abdulaziz Al Sultan, Linda Kasickova, Tomoyuki Ohara, Piyush Ojha, Sanchea Wasyliw, Sina Marzoughi, Ankur Banerjee, Girish Kulkarni, Kennedy Horn, Amy Bobyn, Anneliese Neweduk, Nishita Singh, Wu Qiu, David Rodriguez-Luna, Dar Dowlatshahi, Mayank Goyal, Bijoy K. Menon, Andrew M. Demchuk
Timing of Spot Sign Appearance, Spot Sign Volume, and Leakage Rate among Phases of Multiphase CTA Predict Intracerebral Hemorrhage Growth
American Journal of Neuroradiology Jun 2024, 45 (6) 693-700; DOI: 10.3174/ajnr.A8254

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Spot Sign and Intracerebral Hemorrhage Growth
MacKenzie Horn, Ericka Teleg, Koji Tanaka, Abdulaziz Al Sultan, Linda Kasickova, Tomoyuki Ohara, Piyush Ojha, Sanchea Wasyliw, Sina Marzoughi, Ankur Banerjee, Girish Kulkarni, Kennedy Horn, Amy Bobyn, Anneliese Neweduk, Nishita Singh, Wu Qiu, David Rodriguez-Luna, Dar Dowlatshahi, Mayank Goyal, Bijoy K. Menon, Andrew M. Demchuk
American Journal of Neuroradiology Jun 2024, 45 (6) 693-700; DOI: 10.3174/ajnr.A8254
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