Imaging Scores in Subarachnoid Hemorrhage: Performance on Prediction of Functional Outcome, Mortality, and Complications
Abstract
1. Introduction
2. Methods
2.1. Patient Identification and Inclusion Criteria
2.2. Clinical Parameters
2.3. Imaging
2.4. Outcome Measures
2.5. Statistical Analyses
3. Results
3.1. Imaging Assessment on Admission
3.2. Outcomes
3.3. ROC Analyses of Initial Imaging with the Primary Endpoint
3.4. ROC Analyses of Secondary Endpoints
3.5. Multivariable Analysis
3.6. Subgroup Analyses Regarding the Primary Endpoint
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
| DCI | Delayed cerebral ischemia |
| SAH | Subarachnoid hemorrhage |
| ICH | Intracerebral hemorrhage |
| HH | Hunt and Hess |
| WFNS | World Federation of Neurosurgical Societies |
| IVH | Intraventricular hemorrhage |
| mRS | Modified Rankin scale |
| CSF | Cerebrospinal fluid |
| CI | Confidence interval |
| aOR | Adjusted odds ratio |
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| SAH-Scores | IVH Scores | ||||
|---|---|---|---|---|---|
| Modified Fisher Scale | Claassen Score | Hijdra Score | Graeb Score | IVH Score | |
| Publication date | 2001 | 2001 | 1990 | 1982 | 2009 |
| Range | 0–4 | 1–5 | 0–42 | 0–12 | 0–23 |
| Score definition/calculation | 0: No SAH or IVH 1: Thin SAH, no IVH in both lateral ventricles 2: Thin SAH, with IVH in both lateral ventricles 3: Thick SAH, no IVH in both lateral ventricles 4: Thick SAH, with IVH in both lateral ventricles | 1: No SAH or IVH 2: Thin SAH, no IVH in both lateral ventricles 3: Thin SAH, with IVH in both lateral ventricles 4: Thick SAH, no IVH in both lateral ventricles 5: Thick SAH, with IVH in both lateral ventricles | 10 basal cisterns (0–3): 0: no blood 1: small amount of blood 2: moderately filled with blood 3: completely filled with blood Each ventricle (0–3): 0: no blood 1: sedimentation of blood 2: partly filled with blood 3: completely filled with blood | Each lateral ventricles: 1: trace of blood or mild bleeding 2: less than half of the ventricle filled with blood 3: more than half of the ventricle filled with blood 4: ventricle filled with blood and expanded Third and fourth ventricles: 0: no blood 1: blood present, ventricle size normal 2: ventricle filled with blood and expanded | IVHS = 3x (RV + LV) + III + IV+ 3x H Grade each lateral ventricle (RV/LV): 0: no blood or small amount 1: up to one-third filled with blood 2: one-to-two-thirds filled with blood 3: mostly or completely filled with blood Third and fourth ventricle (III/IV): 0: no blood 1: partially or completely filled with blood Hydrocephalus (H) present (1) or absent (0). |
| Validated for: | |||||
| Yes | Yes | Yes | Yes | No |
| Yes | Yes | No | Yes | No |
| No | No | No | Yes | No |
| Yes | Yes | Yes | No | No |
| No | No | Yes | Yes | Yes |
| No | No | No | Yes | Yes |
| SAH Patients (n = 479) | |
|---|---|
| Age, y, mean (SD) | 56.1 (±13.6) |
| Female sex, n (%) | 307 (64.1) |
| Prior comorbidities: | |
| Premorbid mRS, median (IQR) | 0 (0–0) |
| Arterial hypertension, n (%) | 267 (55.7) |
| Nicotine abuse, n (%) | 137 (28.6) |
| Prior SAH, n (%) | 5 (1.0) |
| Admission status: | |
| GCS, median (IQR) | 14 (11–15) |
| Hunt and Hess, median (IQR) | 2 (1–4) |
| WFNS, median (IQR) | 2 (2–4) |
| Poor-grade SAH (WFNS ≥ 4), n (%) | 179/477 (37.5) |
| SAH characteristics: | |
| Aneurysmal SAH, n (%) | 361/466 (75.4%) |
| Intraventricular hemorrhage, n (%) | 287/479 (59.9%) |
| Imaging scores: | |
| mFisher score, median (IQR) | 2 (1–3) |
| 0, n (%) | 23 (4.8) |
| 1 or 2, n (%) | 251 (52.4) |
| 3 or 4, n (%) | 205 (42.7) |
| Claassen score, median (IQR) | 3 (2–4) |
| 1, n (%) | 24 (5) |
| 2 or 3, n (%) | 257 (53.7) |
| 4 or 5, n (%) | 197 (41.2) |
| Hijdra score, median (IQR) | 8 (4–8) |
| 0–10, n (%) | 322 (67.2) |
| 11–20, n (%) | 150 (31.3) |
| 21–30, n (%) | 7 (1.4) |
| Graeb score, median (IQR) | 1 (1–3) |
| 0–4, n (%) | 423 (88.3) |
| 5–8, n (%) | 39 (8.1) |
| 9–12, n (%) | 17 (3.5) |
| IVH Score, median (IQR) | 4 (4–9) |
| 0–7, n (%) | 326 (68.0) |
| 8–15, n (%) | 125 (26.0) |
| 16–23, n (%) | 28 (5.8) |
| Outcome: | |
| Doppler sonographic vasospasm n (%) | 182/402 (45.3) |
| DCI, n (%) | 134/472 (28.4) |
| CSF shunt, n (%) | 99 (20.7) |
| Epilepsy, n (%) | 34/334 (10.2) |
| Mortality at discharge | 69 (14.4) |
| Mortality at 12-month, n (%) | 94 (19.6) |
| mRS at discharge, median (IQR) | 3 (2–5) |
| Favorable 0–3, n (%) | 248 (51.8) |
| Unfavorable 4–6, n (%) | 231 (48.2) |
| mRS at 3 months, median (IQR) | 2 (1–5) |
| Favorable 0–3, n (%) | 275/415 (66.3) |
| Unfavorable 4–6, n (%) | 140/415 (33.7) |
| mRS at 12 months, median (IQR) | 2 (1–4) |
| Favorable 0–3, n (%) | 313/435 (72.0) |
| Unfavorable 4–6, n (%) | 122/435 (28.0) |
| Return to work, n (%) | 137/236 (58.1%) |
| EQ-VAS index, median (IQR) | 75 (55–90) |
| Unfavorable 0–74, n (%) | 154/333 (46.2) |
| Favorable 75–100, n (%) | 179/333 (53.8) |
| EQ-5D domains: | |
| Mobility = 0, n (%) | 66/332 (19.9) |
| Self-care = 0, n (%) | 60/332 (18.1) |
| Usual activities = 0, n (%) | 115/332 (34.6) |
| Pain/discomfort = 0, n (%) | 122/331 (36.9) |
| Anxiety/depression = 0, n (%) | 158/330 (47.9) |
| Imaging Score | mRS 4–6 (12 m) | Mortality (12 m) | CSF Shunt | EQ-5D | ||||
|---|---|---|---|---|---|---|---|---|
| AUROC (95% CI) | Adj. OR (95% CI) | AUROC (95% CI) | Adj. OR (95% CI) | AUROC (95% CI) | Adj. OR (95% CI) | AUROC (95% CI) | Adj. OR (95% CI) | |
| Modified Fisher | 0.713 (0.662–0.764) | 1.060 (1.022–1.101) | 0.713 (0.654–0.772) | 1.042 (1.009–1.076) | 0.721 (0.661–0.780) | 1.053 (1.018–1.089) | 0.410 (0.349–0.471) | 0.968 (0.923–1.016) |
| Claassen | 0.724 (0.675–0.774) | 1.070 (1.030–1.110) | 0.721 (0.662–0.779) | 1.045 (1.011–1.080) | 0.736 (0.679–0.793) | 1.058 (1.022–1.095) | 0.402 (0.341–0.463) | 0.961 (0.915–1.009) |
| Hijdra | 0.688 (0.635–0.740) | 1.009 (1.001–1.018) | 0.702 (0.641–0.764) | 1.009 (1.001–1.017) | 0.740 (0.683–0.796) | 1.010 (1.002–1.018) | 0.422 (0.361–0.484) | 0.995 (0.983–1.008) |
| Graeb | 0.732 (0.682–0.782) | 1.046 (1.028–1.065) | 0.735 (0.675–0.794) | 1.036 (1.016–1.056) | 0.761 (0.703–0.819) | 1.020 (1.001–1.041) | 0.407 (0.346–0.468) | 0.967 (0.944–0.991) |
| IVH Score | 0.721 (0.671–0.771) | 1.018 (1.010–1.026) | 0.711 (0.651–0.771) | 1.013 (1.004–1.021) | 0.771 (0.716–0.826) | 1.011 (1.003–1.020) | 0.402 (0.341–0.464) | 0.985 (0.974–0.996) |
| Imaging Score | Epilepsy | Return to work | Rebleeding | DCI | ||||
| AUROC (95% CI) | Adj. OR (95% CI) | AUROC (95% CI) | Adj. OR (95% CI) | AUROC (95% CI) | Adj. OR (95% CI) | AUROC (95% CI) | Adj. OR (95% CI) | |
| Modified Fisher | 0.592 (0.487–0.698) | 1.007 (0.974–1.042) | 0.302 (0.245–0.359) | 0.965 (0.916–1.016) | 0.580 (0.485–0.676) | 1.016 (0.990–1.044) | 0.643 (0.588–0.698) | 1.084 (1.043–1.126) |
| Claassen | 0.601 (0.497–0.706) | 1.010 (0.976–1.045) | 0.289 (0.234–0.345) | 0.955 (0.907–1.005) | 0.584 (0.489–0.680) | 1.018 (0.990–1.046) | 0.651 (0.596–0.705) | 1.090 (1.049–1.132) |
| Hijdra | 0.621 (0.525–0.717) | 1.001 (0.994–1.008) | 0.311 (0.254–0.368) | 0.986 (0.974–0.998) | 0.644 (0.551–0.738) | 1.007 (1.001–1.013) | 0.634 (0.580–0.688) | 1.014 (1.004–1.023) |
| Graeb | 0.632 (0.528–0.735) | 1.020 (0.996–1.044) | 0.292 (0.237–0.348) | 0.984 (0.954–1.014) | 0.537 (0.451–0.622) | 0.996 (0.985–1.007) | 0.601 (0.545–0.656) | 1.020 (1.000–1.041) |
| IVH Score | 0.623 (0.519–0.727) | 1.006 (0.997–1.015) | 0.312 (0.255–0.369) | 0.995 (0.982–1.009) | 0.519 (0.429–0.609) | 0.998 (0.993–1.004) | 0.604 (0.550–0.658) | 1.009 (1.000–1.017) |
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Biburger, L.; Mers, L.; Bogdanova, A.; Sekita, A.; Borutta, M.; Delev, D.; Bozhkov, Y.; Schnell, O.; Engelhorn, T.; Singer, L.; et al. Imaging Scores in Subarachnoid Hemorrhage: Performance on Prediction of Functional Outcome, Mortality, and Complications. Brain Sci. 2026, 16, 28. https://doi.org/10.3390/brainsci16010028
Biburger L, Mers L, Bogdanova A, Sekita A, Borutta M, Delev D, Bozhkov Y, Schnell O, Engelhorn T, Singer L, et al. Imaging Scores in Subarachnoid Hemorrhage: Performance on Prediction of Functional Outcome, Mortality, and Complications. Brain Sciences. 2026; 16(1):28. https://doi.org/10.3390/brainsci16010028
Chicago/Turabian StyleBiburger, Luise, Lena Mers, Anna Bogdanova, Alexander Sekita, Matthias Borutta, Daniel Delev, Yavor Bozhkov, Oliver Schnell, Tobias Engelhorn, Ludwig Singer, and et al. 2026. "Imaging Scores in Subarachnoid Hemorrhage: Performance on Prediction of Functional Outcome, Mortality, and Complications" Brain Sciences 16, no. 1: 28. https://doi.org/10.3390/brainsci16010028
APA StyleBiburger, L., Mers, L., Bogdanova, A., Sekita, A., Borutta, M., Delev, D., Bozhkov, Y., Schnell, O., Engelhorn, T., Singer, L., Sprügel, M., Schwab, S., & Gerner, S. T. (2026). Imaging Scores in Subarachnoid Hemorrhage: Performance on Prediction of Functional Outcome, Mortality, and Complications. Brain Sciences, 16(1), 28. https://doi.org/10.3390/brainsci16010028

