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Risk stratification of delayed causative aneurysm detection and long-term outcome in angiographically negative spontaneous subarachnoid haemorrhage

Jie Wang, Jian-Feng Meng, Shuo Wang, Ji-Zong Zhao, Yong Cao
DOI: 10.1136/svn-2023-002546 Published 31 January 2024
Jie Wang
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Jian-Feng Meng
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Shuo Wang
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Ji-Zong Zhao
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Yong Cao
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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  • Figure 1
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    Figure 1

    The flow chart of the study patient. NPAN-SAH, non-perimesencephalic angiogram-negative SAH; PAN-SAH, perimesencephalic angiogram-negative subarachnoid haemorrhage.

  • Figure 2
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    Figure 2

    Kaplan-Meier curves showing the poor outcome rates in different subgroups. (A) Kaplan-Meier curve analysis showing the overall poor outcome rates; (B) Kaplan-Meier curve analysis (log-rank test) showing the different cumulative poor outcome rates between NPAN-SAH and PAN-SAH; (C) Kaplan-Meier curve analysis (log-rank test) showing the different cumulative poor outcome rates between GCS 13–15 and GCS 3–12. NPAN-SAH, non-perimesencephalic angiogram-negative SAH; PAN-SAH, perimesencephalic angiogram-negative subarachnoid haemorrhage.

Tables

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  • Table 1

    Baseline characteristics and hospitalisation complications of all anSAH patients

    VariablesOverallPAN-SAHNPAN-SAHP value
    (n=303)(n=110)(n=193)
    Age mean (years)54.7±11.252.7±11.555.7±11.10.027†*
     >60 years, no (%)104 (34.3)24 (21.8)80 (41.5)0.001‡*
     Female, no (%)159 (52.5)59 (53.6)100 (51.8)0.760‡
     Smoking history, no (%)64 (21.1)23 (20.9)41 (21.2)0.993‡
    Medical history, no (%)
     Hypertension118 (38.9)35 (31.8)83 (43.0)0.055‡
     Hyperlipidaemia136 (44.9)53 (48.2)83 (43.0)0.384‡
     Diabetes mellitus50 (16.5)15 (13.6)35 (18.1)0.310‡
     Coronary heart disease22 (7.3)7 (6.4)15 (7.8)0.650‡
     Ischaemic cerebrovascular disease18 (5.9)5 (4.5)13 (6.7)0.410‡
     Antithrombotic drugs, no (%)19 (6.3)8 (7.3)11 (5.7)0.587‡
     HH grades 3–520 (6.6)020 (10.4)<0.001‡*
     mFS 3–476 (25.1)17 (15.0)59 (30.6)0.004‡*
     GCS 3–1212 (4.0)2 (1.8)10 (5.2)0.255‡
    Complications
     Rebleed, no (%)2 (0.7)02 (1.0)0.536§
     Ictal infarction, no (%)2 (0.7)1 (0.9)1 (0.5)0.999§
     Delayed cerebral infarction, no (%)6 (2.0)2 (1.8)4 (2.1)0.999§
     Vasospasm, no (%)6 (2.0)1 (0.9)5 (2.6)0.423§
     Hydrocephalus, no (%)50 (16.5)5 (4.5)45 (23.3)<0.001‡*
     CSF drainage, no (%)5 (1.7)05 (2.6)0.163§
     Pulmonary infection, no (%)20 (6.6)1 (0.9)19 (9.8)0.001‡*
     Electrolyte imbalance, no (%)171 (56.4)45 (40.9)126 (65.3)<0.001‡*
     Acute gastric ulcer, no (%)19 (6.3)2 (1.8)17 (8.8)0.016‡*
     Deep venous thrombosis, no (%)14 (4.6)6 (5.5)8 (4.1)0.602‡
     Death, no (%)3 (1.0)03 (1.6)0.556§
     LOS mean (days)12.9±5.812.0±5.013.4±6.20.041†*
    • *p<0.05.

    • †T-test.

    • ‡χ2 test.

    • §Fisher’s exact test.

    • anSAH, angiogram-negative subarachnoid haemorrhage; CSF, cerebrospinal fluid; GCS, Glasgow Coma Score; HH grade, Hunt-Hess grade; LOS, length of stay; mFS, modified Fisher Scale; NPAN-SAH, non-perimesencephalic angiogram-negative SAH; PAN-SAH, perimesencephalic angiogram-negative SAH.

  • Table 2

    Diagnosis of causative vascular lesions by repeated imaging in anSAH patients

    OverallPAN-SAHNPAN-SAHP value
    (n=303)(n=110)(n=193)
    Repeated imaging, no (%)272 (89.8)96 (87.3)176 (91.2)0.279†
     CTA242 (89.0)85 (88.5)157 (89.2)0.868†
     DSA120 (44.1)41 (42.7)79 (44.9)0.525†
     MRA9 (3.3)6 (6.3)3 (1.7)0.085†
    Diagnosis, no (%)21 (7.7)2 (2.1)19 (10.8)0.010†*
     Saccular aneurysm18 (6.6)1 (1.0)17 (9.7)
     Dissecting aneurysm3 (1.1)1 (1.0)2 (1.1)
    • *p<0.05.

    • †χ2 test.

    • anSAH, angiogram-negative subarachnoid haemorrhage; CTA, CT angiography; DSA, digital subtraction angiography; MRA, MR angiography; NPAN-SAH, non-perimesencephalic angiogram-negative SAH; PAN-SAH, perimesencephalic angiogram-negative SAH.

  • Table 3

    Logistic analyses of risk factors associated with detection of causative aneurysm by repeated imaging†

    VariablenUnivariate analysisMultivariate analysis
    OR (95% CI)P valueOR (95% CI)P value
    NPAN-SAH195.688 (1.296 to 24.968)0.021*4.682 (1.050 to 20.872)0.043*
    Age >60 years81.315 (0.524 to 3.330)0.559
    Female110.945 (0.388 to 2.305)0.901
    Smoker30.477 (0.136 to 1.672)0.247
    Hypertension111.661 (0.680 to 4.056)0.265
    Hyperlipidaemia100.581 (0.251 to 1.343)0.987
    Diabetes mellitus41.279 (0.408 to 4.005)0.673
    Coronary heart disease11.553 (0.184 to 13.075)0.686
    Ischaemic cerebrovascular disease21.927 (0.405 to 9.174)0.410
    HH grades 1–2‡20
    HH grades 3–510.688 (0.087 to 5.442)0.723
    mFS 1–2 ‡9
    mFS 3–4124.437 (1.781 to 11.053)0.001*3.790 (1.502 to 9.566)0.005*
    GCS 13–15‡19
    GCS 3–1222.830 (0.570 to 14.044)0.203
    Hydrocephalus51.601 (0.555 to 4.613)0.384
    • *p<0.05.

    • †Thirty-one patients without repeated imaging were excluded for the logistic analysis.

    • ‡Reference.

    • GCS, Glasgow Coma Score; HH grade, Hunt-Hess grade; mFS, modified Fisher Scale; n, number of events; NPAN-SAH, non-perimesencephalic angiogram-negative subarachnoid haemorrhage.

  • Table 4

    The incidence rate for aneurysm detection in different risk groups

    GroupAneurysm detection
    n/NIR (95% CI)
    Low risk*1/801.250 (0.176 to 8.874)
    intermediate risk*9/1386.522 (3.393 to 12.534)
    high risk*11/5420.370 (5.034 to 36.783)
    Overall21/2727.721 (5.034 to 11.841)
    • *The patients were stratified into three groups according to the presence of two risk factors (NPAN-SAH and mFS 3–4): the low-risk group was without any of the two risk factors, the intermediate-risk group only had one risk factor, and the high-risk group had >1 risk factor.

    • IR, incidence rate; mFS, modified Rankin Scale; N, total number in the corresponding group; n, number of events; NPAN-SAH, non-perimesencephalic angiogram-negative subarachnoid haemorrhage.

  • Table 5

    Univariate and multivariate Cox analyses of risk factors associated with poor outcome†

    VariablenUnivariate analysisMultivariate analysis
    HR (95% CI)P valueHR (95% CI)P value
    NPAN-SAH179.931 (1.321 to 74.670)0.026*8.792 (1.162 to 66.528)0.035*
    Age >60 years90.855 (0.305 to 2.401)0.767
    Female121.059 (0.418 to 2.684)0.904
    Smoker31.211 (0.431 to 3.402)0.716
    Hypertension90.809 (0.303 to 2.155)0.671
    Hyperlipidaemia40.467 (0.166 to 1.311)0.148
    Diabetes mellitus40.753 (0.173 to 3.276)0.705
    Coronary heart disease32.028 (0.466 to 8.832)0.346
    Ischaemic cerebrovascular disease22.994 (0.685 to 13.084)0.145
    Antithrombotic drugs10.802 (0.107 to 6.033)0.830
    HH grades 1–2‡16
    HH grades 3–522.879 (0.830 to 9.985)0.096
    mFS 1–2‡3
    mFS 3–4152.207 (0.823 to 5.917)0.116
    GCS 13–15‡14
    GCS 3–1248.218 (2.362 to 28.590)0.001*6.090 (1.744 to 21.258)0.005*
    Hydrocephalus22.229 (0.794 to 6.254)0.128
    Pulmonary infection20.924 (0.123 to 6.947)0.939
    Deep venous thrombosis13.258 (0.747 to 14.216)0.116
    • *p<0.05.

    • †Thirty-one patients without repeated imaging and 21 patients with aneurysm detection were excluded for the Cox analysis.

    • ‡Reference.

    • GCS, Glasgow Coma Score; HH grade, Hunt-Hess grade; mFS, modified Fisher Scale; n, number of events; NPAN-SAH, non-perimesencephalic angiogram-negative subarachnoid haemorrhage.

  • Table 6

    Annual and 5-year incidence rates of poor outcome in the different groups

    Groupn/NAnnual IR (95% CI)Cumulative IR (95% CI)
    5 years
    Low risk*1/920.215 (0.030 to 1.527)1.875 (0.264 to 13.310)
    Intermediate risk*14/1521.817 (1.076 to 3.067)10.744 (4.630 to 27.573)
    High risk*3/79.883 (3.187 to 30.643)75.302 (10.607 to 534.573)
    Overall18/2511.422 (0.896 to 2.257)8.431 (3.352 to 24.405)
    • *The patients were stratified into three groups according to the presence of two risk factors (NPAN-SAH and GCS 3–12): the low-risk group is without any of the two risk factors, intermediate-risk group only has one risk factor, and high-risk group has >1 risk factor.

    • GCS, Glasgow Coma Score; IR, incidence rate; N, total number in the corresponding group; n, number of events; NPAN-SAH, non-perimesencephalic angiogram-negative subarachnoid haemorrhage.

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Risk stratification of delayed causative aneurysm detection and long-term outcome in angiographically negative spontaneous subarachnoid haemorrhage
Jie Wang, Jian-Feng Meng, Shuo Wang, Ji-Zong Zhao, Yong Cao
Stroke and Vascular Neurology Jan 2024, svn-2023-002546; DOI: 10.1136/svn-2023-002546

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Risk stratification of delayed causative aneurysm detection and long-term outcome in angiographically negative spontaneous subarachnoid haemorrhage
Jie Wang, Jian-Feng Meng, Shuo Wang, Ji-Zong Zhao, Yong Cao
Stroke and Vascular Neurology Jan 2024, svn-2023-002546; DOI: 10.1136/svn-2023-002546
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Risk stratification of delayed causative aneurysm detection and long-term outcome in angiographically negative spontaneous subarachnoid haemorrhage
Jie Wang, Jian-Feng Meng, Shuo Wang, Ji-Zong Zhao, Yong Cao
Stroke and Vascular Neurology Jan 2024, svn-2023-002546; DOI: 10.1136/svn-2023-002546
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