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A 90-Day Prognostic Model Based on the Early Brain Injury Indicators after Aneurysmal Subarachnoid Hemorrhage: the TAPS Score

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Abstract

This study aimed to establish a new scoring model based on the early brain injury (EBI) indicators to predict the 90-day functional outcomes in patients with aneurysmal subarachnoid hemorrhage (aSAH). We retrospectively enrolled 825 patients and prospectively enrolled 108 patients with aSAH who underwent surgical clipping or endovascular coiling (derivation cohort = 640; validation cohort = 185; prospective cohort = 108) in our institute. We established a logistic regression model based on independent risk factors associated with 90-day unfavorable outcomes. The discrimination of the prognostic model was assessed by the area under the curve in a receiver operating characteristic curve analysis. The Hosmer–Lemeshow goodness-of-fit test and a calibration plot were used to evaluate the calibration of the prediction model. The developed scoring model named “TAPS” (total score, 0–7 points) included the following admission variables: age > 55 years old, WFNS grade of 4–5, mFS grade of 3–4, Graeb score of 5–12, white blood cell count > 11.28 × 109/L, and surgical clipping. The model showed good discrimination with the area under the curve in the derivation, validation, and prospective cohorts which were 0.816 (p < 0.001, 95%CI = 0.77–0.86), 0.810 (p < 0.001, 95%CI = 0.73–0.90), and 0.803 (p < 0.001, 95%CI = 0.70–0.91), respectively. The model also demonstrated good calibration (Hosmer–Lemeshow goodness-of-fit test: X2 = 1.75, df = 8, p = 0.988). Compared with other predictive models, TAPS is an easy handle tool for predicting the 90-day unfavorable outcomes of aSAH patients, which can help clinicians better understand the concept of EBI and quickly identify those patients at risk of poor prognosis, providing more positive treatment strategies. Trial registration: NCT04785976. Registered 5 March 2021-retrospectively registered, http://www.clinicaltrials.gov.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004;24:916–25.

    Article  CAS  PubMed  Google Scholar 

  2. Tso MK, Macdonald RL. Subarachnoid hemorrhage: a review of experimental studies on the microcirculation and the neurovascular unit. Transl Stroke Res. 2014;5:174–89.

    Article  PubMed  Google Scholar 

  3. Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33:1225–32.

    Article  PubMed  Google Scholar 

  4. Fujii M, Yan J, Rolland WB, Soejima Y, Caner B, Zhang JH. Early brain injury, an evolving frontier in subarachnoid hemorrhage research. Transl Stroke Res. 2013;4:432–46.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ray B, Pandav VM, Mathews EA, et al. Coated-platelet trends predict short-term clinical outcomeafter subarachnoid hemorrhage. Transl Stroke Res. 2018;9:459–70.

    Article  CAS  PubMed  Google Scholar 

  6. Rass V, Helbok R. Early brain injury after poor-grade subarachnoid hemorrhage. Curr Neurol Neurosci Rep. 2019;19:78.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sehba FA, Friedrich V. Early events after aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl. 2015;120:23–8.

    Article  PubMed  Google Scholar 

  8. Taki W, Sakai N, Suzuki H, et al. Determinants of poor outcome after aneurysmal subarachnoid hemorrhage when both clipping and coiling are available: Prospective Registry of Subarachnoid Aneurysms Treatment (PRESAT) in Japan. World Neurosurgery. 2011;76:437–45.

    Article  PubMed  Google Scholar 

  9. Fu C, Yu W, Sun L, Li D, Zhao C. Early cerebral infarction following aneurysmal subarachnoid hemorrhage: frequency, risk factors, patterns, and prognosis. Curr Neurovasc Res. 2013;10:316–24.

    Article  PubMed  Google Scholar 

  10. Radolf S, Smoll N, Drenckhahn C, Dreier JP, Vajkoczy P, Sarrafzadeh AS. Cerebral lactate correlates with early onset pneumonia after aneurysmal SAH. Transl Stroke Res. 2014;5:278–85.

    Article  CAS  PubMed  Google Scholar 

  11. Suzuki H, Sakurai M, Fujimoto M, Tsuchiya T, Sakaida H, Taki W. Complete recovery from aneurysmal subarachnoid hemorrhage associated with out-of-hospital cardiopulmonary arrest. Eur J Emerg Med. 2010;17:42–4.

    Article  PubMed  Google Scholar 

  12. Rass V, Helbok R. Early brain injury after poor-grade subarachnoid hemorrhage. Current Neurology and Neuroscience Reports. 2019 19.

  13. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012;43:1711–37.

    Article  PubMed  Google Scholar 

  14. Report of World Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg. 1988 68: 985–986.

  15. Claassen J, Bernardini GL, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20.

    Article  CAS  PubMed  Google Scholar 

  16. Graeb DA, Robertson WD, Lapointe JS, Nugent RA, Harrison PB. Computed tomographic diagnosis of intraventricular hemorrhage. Etiology and prognosis Radiology. 1982;143:91–6.

    CAS  PubMed  Google Scholar 

  17. Ahn SH, Savarraj JP, Pervez M, et al. The subarachnoid hemorrhage early brain edema score predicts delayed cerebral ischemia and clinical outcomes. Neurosurgery. 2018;83:137–45.

    Article  PubMed  Google Scholar 

  18. Fujiki Y, Matano F, Mizunari T, et al. Serum glucose/potassium ratio as a clinical risk factor for aneurysmal subarachnoid hemorrhage. J Neurosurg. 2018;129:870–5.

    Article  CAS  PubMed  Google Scholar 

  19. Giede-Jeppe A, Reichl J, Sprügel M, et al. Neutrophil-to-lymphocyte ratio as an independent predictor for unfavorable functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2019;132:400–7.

    Article  PubMed  Google Scholar 

  20. Wang Z, Pei W, Chen L, Ning Y, Luo Y. Mean platelet volume/platelet count ratio is associated with poor clinical outcome after aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovas Dis: Official J Nat Stroke Assoc. 2020;29:105208.

    Article  Google Scholar 

  21. Yun S, Jun Yi H, Hoon Lee D, Hoon SJ. Clinical significance of platelet to neutrophil ratio and platelet to lymphocyte ratio in patients with aneurysmal subarachnoid hemorrhage. J Clin Neurosci Official J Neurosurg Soc Australasia. 2021;92:49–54.

    CAS  Google Scholar 

  22. Zhang P, Li Y, Zhang H, et al. Prognostic value of the systemic inflammation response index in patients with aneurismal subarachnoid hemorrhage and a Nomogram model construction. British journal of neurosurgery. 2020: 1–7. online ahead of print.

  23. Sullivan LM, Massaro JM, D’Agostino RB Sr. Presentation of multivariate data for clinical use: the Framingham Study risk score functions. Stat Med. 2004;23:1631–60.

    Article  PubMed  Google Scholar 

  24. Time trends in outcome of subarachnoid hemorrhage. population-based study and systematic review. Neurology. 2010;74:1494–501.

    Article  Google Scholar 

  25. The falling rates of hospital admission. case fatality, and population-based mortality for subarachnoid hemorrhage in England, 1999–2010. J Neurosurg. 2016;125:1–7.

    Google Scholar 

  26. Zhang JH. Vascular neural network in subarachnoid hemorrhage. Transl Stroke Res. 2014;5:423–8.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sehba FA, Pluta RM, Zhang JH. Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol. 2011;43:27–40.

    Article  CAS  PubMed  Google Scholar 

  28. Yue Q, Liu Y, Leng B, et al. A prognostic model for early post-treatment outcome of elderly patients with aneurysmal subarachnoid hemorrhage. World Neurosurg. 2016;95:253–61.

    Article  PubMed  Google Scholar 

  29. Lai X, Zhang W, Ye M, Liu X, Luo X. Development and validation of a predictive model for the prognosis in aneurysmal subarachnoid hemorrhage. J Clin Lab Anal. 2020;34:e23542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jaja B, Saposnik G, Lingsma H, et al. Development and validation of outcome prediction models for aneurysmal subarachnoid haemorrhage: the SAHIT multinational cohort study. BMJ (Clinical research ed). 2018;360:j5745.

    Article  PubMed  Google Scholar 

  31. Lee V, Ouyang B, John S, et al. Risk stratification for the in-hospital mortality in subarachnoid hemorrhage: the HAIR score. Neurocrit Care. 2014;21:14–9.

    Article  PubMed  Google Scholar 

  32. Witsch J, Frey H, Patel S, et al. Prognostication of long-term outcomes after subarachnoid hemorrhage: the FRESH score. Ann Neurol. 2016;80:46–58.

    Article  PubMed  Google Scholar 

  33. Medzhitov R. Origin and physiological roles of inflammation. Nature. 2008;454:428–35.

    Article  CAS  PubMed  Google Scholar 

  34. Saand A, Yu F, Chen J, Chou S. Systemic inflammation in hemorrhagic strokes - a novel neurological sign and therapeutic target? Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 2019;39:959–88.

    Article  PubMed  Google Scholar 

  35. Al-Mufti F, Misiolek K, Roh D, et al. White blood cell count improves prediction of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Neurosurgery. 2019;84:397–403.

    Article  PubMed  Google Scholar 

  36. Ma X, Lan F, Zhang Y. Associations between C-reactive protein and white blood cell count, occurrence of delayed cerebral ischemia and poor outcome following aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Acta Neurol Belg. 2021;121:1311–24.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mahta A, Azher A, Moody S, et al. Association of early white blood cell trend with outcomes in aneurysmal subarachnoid hemorrhage. World Neurosurgery. 2021;151:e803–9.

    Article  PubMed  Google Scholar 

  38. Hu P, Yang X, Li Y, et al. Predictive effects of admission white blood cell counts and hounsfield unit values on delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2022;212:107087.

    Article  PubMed  Google Scholar 

  39. Kasius K, Frijns C, Algra A, Rinkel G. Association of platelet and leukocyte counts with delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage. Cerebrovascular Dis (Basel, Switzerland). 2010;29:576–83.

    Article  CAS  Google Scholar 

  40. Li R, Lin F, Chen Y, et al. In-hospital complication-related risk factors for discharge and 90-day outcomes in patients with aneurysmal subarachnoid hemorrhage after surgical clipping and endovascular coiling: a propensity score-matched analysis. Journal of Neurosurgery. 2021: 1–12. online ahead of print.

  41. Shen J, Yu J, Huang S, et al. Scoring model to predict functional outcome in poor-grade aneurysmal subarachnoid hemorrhage. Front Neurol. 2021;12:601996.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Takemoto Y, Hasegawa Y, Hashiguchi A, Moroki K, Tokuda H, Mukasa A. Predictors for functional outcome in patients with aneurysmal subarachnoid hemorrhage who completed in-hospital rehabilitation in a single institution. J Stroke Cerebrovasc Dis. 2019;28:1943–50.

    Article  PubMed  Google Scholar 

  43. McDougall CG, Spetzler RF, Zabramski JM, et al. The Barrow Ruptured Aneurysm Trial. J Neurosurg. 2012;116:135–44.

    Article  PubMed  Google Scholar 

  44. Molyneux AJ, Kerr RS, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366:809–17.

    Article  PubMed  Google Scholar 

  45. Stienen MN, Germans M, Burkhardt JK, et al. Predictors of in-hospital death after aneurysmal subarachnoid hemorrhage: analysis of a nationwide database (Swiss SOS [Swiss Study on Aneurysmal Subarachnoid Hemorrhage]). Stroke. 2018;49:333–40.

    Article  PubMed  Google Scholar 

  46. Jabbarli R, Reinhard M, Roelz R, et al. The predictors and clinical impact of intraventricular hemorrhage in patients with aneurysmal subarachnoid hemorrhage. International journal of stroke : official journal of the International Stroke Society. 2016;11:68–76.

    Article  PubMed  Google Scholar 

  47. Eagles ME, Jaja BNR, Macdonald RL. Incorporating a modified Graeb score to the modified fisher scale for improved risk prediction of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Neurosurgery. 2018;82:299–305.

    Article  PubMed  Google Scholar 

  48. Xu P, Tao C, Zhu Y, et al. TAK1 mediates neuronal pyroptosis in early brain injury after subarachnoid hemorrhage. J Neuroinflammation. 2021;18:188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Deng HJ, Deji Q, Zhaba W, et al. A20 establishes negative feedback with TRAF6/NF-kappaB and attenuates early brain injury after experimental subarachnoid hemorrhage. Front Immunol. 2021;12:623256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kuang H, Wang T, Liu L, et al. Treatment of early brain injury after subarachnoid hemorrhage in the rat model by inhibiting p53-induced ferroptosis. Neurosci Lett. 2021;762:136134.

    Article  CAS  PubMed  Google Scholar 

  51. Dodd WS, Noda I, Martinez M, Hosaka K, Hoh BL. NLRP3 inhibition attenuates early brain injury and delayed cerebral vasospasm after subarachnoid hemorrhage. J Neuroinflammation. 2021;18:163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Yuan JY, Chen Y, Kumar A, et al. Automated quantification of reduced sulcal volume identifies early brain injury after aneurysmal subarachnoid hemorrhage. Stroke. 2021;52:1380–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. McIntyre MK, Halabi M, Li B, et al. Glycemic indices predict outcomes after aneurysmal subarachnoid hemorrhage: a retrospective single center comparative analysis. Sci Rep. 2021;11:158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Wang Y, Tian Y, Wang D, et al. High angiopoietin-1 levels predict a good functional outcome within 72 h of an aneurysmal subarachnoid hemorrhage: a prospective study from a single center. J Neurol Sci. 2015;356:72–6.

    Article  CAS  PubMed  Google Scholar 

  55. Feghali J, Kim J, Gami A, et al. Monocyte-based inflammatory indices predict outcomes following aneurysmal subarachnoid hemorrhage. Neurosurg Rev. 2021;44:3499–507.

    Article  PubMed  Google Scholar 

  56. Zheng S, Wang H, Chen G, et al. Higher serum levels of lactate dehydrogenase before microsurgery predict poor outcome of aneurysmal subarachnoid hemorrhage. Front Neurol. 2021;12:720574.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We acknowledge the contribution of all staff who participated in the present study.

Funding

This study was supported by the National Key Research and Development Program of China (Grant Nos. 2021YFC2501101 and 2020YFC2004701) and the National Natural Science Foundation of China (Grant Nos. 82071296, 81671129, and 81471210).

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Authors and Affiliations

Authors

Contributions

Runting Li: conceptualization (equal); data curation (lead); formal analysis (lead); investigation (lead); methodology (equal); project administration (equal); software (lead); validation (lead); visualization (lead); writing original draft (lead); and writing review and editing (equal). Fa Lin: data curation (equal); methodology (equal); and software (equal). Yu Chen: data curation (equal); methodology (equal); and software (equal). Junlin Lu: data curation (equal); methodology (equal); and software (equal). Heze Han: data curation (equal); methodology (equal); and software (equal). Li Ma: data curation (equal). Yahui Zhao: data curation (equal). Debin Yan: data curation (equal). Ruinan Li: data curation (equal). Jun Yang: data curation (equal). Shihao He: data curation (equal). Zhipeng Li: data curation (equal). Haibin Zhang: data curation (equal). Kexin Yuan: data curation (equal). Ke Wang: data curation (equal). Qiang Hao: data curation (equal) and supervision (equal). Xun Ye: data curation (equal) and supervision (equal). Hao Wang: data curation (equal) and supervision (equal). Hongliang Li: data curation (equal) and supervision (equal). Linlin Zhang: data curation (equal) and supervision (equal). Guangzhi Shi: data curation (equal) and supervision (equal). Jianxin Zhou: data curation (equal) and supervision (equal). Yang Zhao: data curation (equal); resources (equal); and supervision (equal). Yukun Zhang: data curation (equal); resources (equal); and supervision (equal). Youxiang Li: data curation (equal); resources (equal); and supervision (equal). Shuo Wang: conceptualization (equal); funding acquisition (equal); resources (equal); supervision (equal); and writing review and editing (equal). Xiaolin Chen: conceptualization (equal); funding acquisition (equal); resources (equal); supervision (equal); and writing review and editing (equal). Yuanli Zhao: conceptualization (equal); resources (equal); supervision (equal); and writing review and editing (equal).

Corresponding author

Correspondence to Xiaolin Chen.

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Ethics Approval and Consent to Participate

This study was approved by the Institutional Review Board of the Beijing Tiantan Hospital (KY 2021–008-01). Informed consent was obtained from all individual participants or their authorized representatives included in the study. All the analyses were performed in accordance with the Declaration of Helsinki and the local ethics policies.

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The authors declare no competing interests.

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Li, R., Lin, F., Chen, Y. et al. A 90-Day Prognostic Model Based on the Early Brain Injury Indicators after Aneurysmal Subarachnoid Hemorrhage: the TAPS Score. Transl. Stroke Res. 14, 200–210 (2023). https://doi.org/10.1007/s12975-022-01033-4

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