Abstract
The 30-day mortality rate of spontaneous cerebral hemorrhage (ICH) is approximately 30–50%. Surgery may improve the prognosis of patients with severe ICH. However, ICH survivors after surgery still face the risks of postoperative intracranial rebleeding (PIB), and clinical tools that accurately predict the risk of PIB occurrence are not available. Therefore, a retrospective study was performed. The population was divided into two groups according to the occurrence of PIB. Univariate and multivariate logistic regression analyses were performed to screen risk factors for PIB. Next, an early PIB risk nomogram prediction model was constructed. In addition, the impact of PIB on the prognosis of ICH was evaluated. In total, 150 ICH patients were continuously enrolled in this study; 21 patients suffered from PIB, and the overall incidence of PIB was 14.0% (21/150). Coronary heart disease history, a lower GCS score, and subarachnoid hemorrhage absence were screened as risk factors for early PIB. The early PIB risk nomogram showed good calibration and discrimination with a concordance index of 0.807 (95% confidence interval (CI), 0.715–0.899), which was confirmed to be 0.788 through bootstrapping validation. In addition, a significant difference in discharged GOS scores (P = 0.043) was observed between the PIB group and the n-PIB group. These results showed that a history of coronary heart disease, a lower GCS score, and absence of subarachnoid hemorrhage were risk factors for early PIB. In addition, the early PIB risk nomogram prediction model exhibits good discrimination and calibration. The occurrence of PIB could reduce the prognosis of ICH patients.
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Data that support the findings of this study are available from the corresponding author on reasonable request.
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Codes for analyzing the data of this study are available from the corresponding author on reasonable request.
References
An SJ, Kim TJ, Yoon B-W (2017) Epidemiology, risk factors, and clinical features of intracerebral hemorrhage: an update. J Stroke 19:3–10. https://doi.org/10.5853/jos.2016.00864
van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ (2010) Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. The Lancet Neurology 9:167–176. https://doi.org/10.1016/S1474-4422(09)70340-0
Luzzi S, Elia A, Del Maestro M, Morotti A, Elbabaa SK, Cavallini A, Galzio R (2019) Indication, timing, and surgical treatment of spontaneous intracerebral hemorrhage: systematic review and proposal of a management algorithm. World Neurosurgery 124:e769–e778. https://doi.org/10.1016/j.wneu.2019.01.016
Qureshi AI, Mendelow AD, Hanley DF (2009) Intracerebral haemorrhage. Lancet 373:1632–1644. https://doi.org/10.1016/S0140-6736(09)60371-8
Hemphill JCRD, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, Fung GL, Goldstein JN, Macdonald RL, Mitchell PH, Scott PA, Selim MH, Woo D (2015) Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 46:2032–60
Wu J, Liu Q, Wang K, Yang J, Jiang P, Li M, Wang N, Cao Y, Ren Z, Zhang Y, Wang S (2021) Emergency surgery is an effective way to improve the outcome of severe spontaneous intracerebral hemorrhage patients on long-term oral antiplatelet therapy. Neurosurg Rev 44:1205–1216. https://doi.org/10.1007/s10143-020-01319-x
Zhou H, Zhang Y, Liu L, Han X, Tao Y, Tang Y, Hua W, Xue J, Dong Q (2011) A prospective controlled study: minimally invasive stereotactic puncture therapy versus conventional craniotomy in the treatment of acute intracerebral hemorrhage. BMC Neurol 11:76–76
Nittby HR, Maltese A, Ståhl N (2016) Early postoperative haematomas in neurosurgery. Acta Neurochir 158:837–846
Ren Y, Zheng J, Liu X, Li H, You C (2018) Risk factors of rehemorrhage in postoperative patients with spontaneous intracerebral hemorrhage : a case-control study. Journal of Korean Neurosurgical Society 61:35–41
Rowe AS, Rinehart DR, Lezatte S, Langdon JR (2018) Intracerebral hemorrhage after external ventricular drain placement: an evaluation of risk factors for post-procedural hemorrhagic complications. BMC Neurol 18:22. https://doi.org/10.1186/s12883-018-1030-7
Sussman ES, Kellner CP, Nelson E, McDowell MM, Bruce SS, Bruce RA, Zhuang Z, Connolly ES (2014) Hemorrhagic complications of ventriculostomy: incidence and predictors in patients with intracerebral hemorrhage. J Neurosurg 120:931–936. https://doi.org/10.3171/2013.12.JNS131685
Wu S, Zheng J, Li Y, Yu H, Shi S, Xie W, Liu H, Su Y, Huang J, Lin T (2017) A radiomics nomogram for the preoperative prediction of lymph node metastasis in bladder cancer. Clin Cancer Res 23:6904–6911
Xie X, Xiong Z, Li X, Huang X, Ye F, Tang H, Xie X (2019) Nomogram to predict internal mammary lymph nodes metastasis in patients with breast cancer. Front Oncol 9. https://doi.org/10.3389/fonc.2019.01193
Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, Khoury J (1996) The ABCs of measuring intracerebral hemorrhage volumes. Stroke 27:1304–1305. https://doi.org/10.1161/01.str.27.8.1304
Taylor WA, Thomas NW, Wellings JA, Bell BA (1995) Timing of postoperative intracranial hematoma development and implications for the best use of neurosurgical intensive care. J Neurosurg 82:48–50. https://doi.org/10.3171/jns.1995.82.1.0048
Wu G, Shen Z, Wang L, Sun S, Luo J, Mao Y (2017) Post-operative re-bleeding in patients with hypertensive ICH is closely associated with the CT blend sign. BMC Neurol 17:131. https://doi.org/10.1186/s12883-017-0910-6
Luan L, Li M, Sui H, Li G, Pan W (2019) Efficacies of minimally invasive puncture and small bone window craniotomy for hypertensive intracerebral hemorrhage, evaluation of motor-evoked potentials and comparison of postoperative rehemorrhage between the two methods. Exp Ther Med 17:1256–1261
Shi J, Cai Z, Han W, Dong B, Mao Y, Cao J, Wang S, Guan W (2019) Stereotactic catheter drainage versus conventional craniotomy for severe spontaneous intracerebral hemorrhage in the basal ganglia. Cell Transplant 28:1025–1032
Sharifpour M, Moore LE, Shanks AM, Didier TJ, Kheterpal S, Mashour GA (2013) Incidence, predictors, and outcomes of perioperative stroke in noncarotid major vascular surgery. Anesth Analg 116:424–434. https://doi.org/10.1213/ANE.0b013e31826a1a32
Wang P, Sun Y, Yi D, Xie Y, Luo Y (2020) Clinical features of Chinese patients in different age groups with spontaneous intracerebral hemorrhage based on multicenter inpatient information. Neurol Res 42:657–664. https://doi.org/10.1080/01616412.2020.1782082
Kobiyama K, Ley K (2018) Atherosclerosis. Circ Res 123:1118–1120. https://doi.org/10.1161/CIRCRESAHA.118.313816
Sato S, Uehara T, Hayakawa M, Nagatsuka K, Minematsu K, Toyoda K (2013) Intra- and extracranial atherosclerotic disease in acute spontaneous intracerebral hemorrhage. J Neurol Sci 332:116–120. https://doi.org/10.1016/j.jns.2013.06.031
Chen Y-C, Wei X-E, Lu J, Qiao R-H, Shen X-F, Li Y-H (2019) Correlation between intracranial arterial calcification and imaging of cerebral small vessel disease. Front Neurol 10:426. https://doi.org/10.3389/fneur.2019.00426
Pektezel MY, Arsava EM, Gocmen R, Topcuoglu MA (2021) Intracerebral hematoma expansion and intracranial internal carotid artery calcifications. Clin Neurol Neurosurg 200:106361. https://doi.org/10.1016/j.clineuro.2020.106361
Son W, Park J (2017) Significant risk factors for postoperative enlargement of basal ganglia hematoma after frameless stereotactic aspiration: antiplatelet medication and concomitant IVH. J Korean Neurosurg Soc 60:591–596
Biffi A, Halpin A, Towfighi A, Gilson A, Busl K, Rost N, Smith EE, Greenberg MS, Rosand J, Viswanathan A (2010) Aspirin and recurrent intracerebral hemorrhage in cerebral amyloid angiopathy. Neurology 75:693–698. https://doi.org/10.1212/WNL.0b013e3181eee40f
Chen T, Xu G, Tan D, Wu C (2015) Effects of platelet infusion, anticoagulant and other risk factors on the rehaemorrhagia after surgery of hypertensive cerebral hemorrhage. Eur Rev Med Pharmacol Sci 19:795–799
Li X, Sun Z, Zhao W, Zhang J, Chen J, Li Y, Ye Y, Zhao J, Yang X, Xiang Y, Li G, Mao J, Zhang W, Zhang M, Zhang W (2013) Effect of acetylsalicylic acid usage and platelet transfusion on postoperative hemorrhage and activities of daily living in patients with acute intracerebral hemorrhage. J Neurosurg 118:94–103
RESTART Collaboration (2019) Effects of antiplatelet therapy after stroke due to intracerebral haemorrhage (RESTART): a randomised, open-label trial. Lancet 393:2613–2623. https://doi.org/10.1016/S0140-6736(19)30840-2
Cheng Y, Liu X, Zhao Y, Sun Y, Zhang D, Liu F, Ma Y, Zhou Y (2020) Risk factors for postoperative events in patients on antiplatelet therapy undergoing off-pump coronary artery bypass grafting surgery. Angiology 71:704–712. https://doi.org/10.1177/0003319720919319
Hanalioglu S, Sahin B, Sahin OS, Kozan A, Ucer M, Cikla U, Goodman SL, Baskaya MK (2020) Effect of perioperative aspirin use on hemorrhagic complications in elective craniotomy for brain tumors: results of a single-center, retrospective cohort study. J Neurosurg 132:1529–1538. https://doi.org/10.3171/2018.12.JNS182483
Murthy SB, Biffi A, Falcone GJ, Sansing LH, Torres Lopez V, Navi BB, Roh DJ, Mandava P, Hanley DF, Ziai WC, Kamel H, Rosand J, Sheth KN, VISTA-ICH Steering Committee Collaborators (2019) Antiplatelet therapy after spontaneous intracerebral hemorrhage and functional outcomes. Stroke 50:3057–3063. https://doi.org/10.1161/STROKEAHA.119.025972
Yu S-X, Zhang Q-S, Yin Y, Liu Z, Wu J-M, Yang M-X (2016) Continuous monitoring of intracranial pressure for prediction of postoperative complications of hypertensive intracerebral hemorrhage. Eur Rev Med Pharmacol Sci 20:4750–4755
Naranjo D, Arkuszewski M, Rudzinski W, Melhem ER, Krejza J (2013) Brain ischemia in patients with intracranial hemorrhage: pathophysiological reasoning for aggressive diagnostic management. Neuroradiol J 26:610–628. https://doi.org/10.1177/197140091302600603
Calviere L, Viguier A, Patsoura S, Rousseau V, Albucher J-F, Planton M, Pariente J, Cognard C, Olivot J-M, Bonneville F, Raposo N (2019) Risk of intracerebral hemorrhage and mortality after convexity subarachnoid hemorrhage in cerebral amyloid angiopathy. Stroke 50:2562–2564. https://doi.org/10.1161/STROKEAHA.119.026244
Viguier A, Raposo N, Patsoura S, Calviere L, Albucher JF, Ruidavets JB, Chollet F, Cognard C, Olivot JM, Bonneville F (2019) Subarachnoid and subdural hemorrhages in lobar intracerebral hemorrhage associated with cerebral amyloid angiopathy. Stroke 50:1567–1569. https://doi.org/10.1161/STROKEAHA.119.024837
Funding
This study is supported by two projects: National Natural Science Foundation of China (Grant Nos. 81471210 and 81671129) and major special projects in the 13th five-year plan (Grant No. 2016YFC1301800).
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All authors contributed to the study’s conception and design. Conceptualization: Shuo Wang; methodology: Junhua Yang, Yang Liu, Jiaming Zhang, and Pengjun Jiang; formal analysis and investigation: Junghua Yang, Qingyuan Liu, Kaiwen Wang, Maogui Li, and Shaohua Mo; writing – original draft preparation: Junhua Yang; writing – review and editing: Jun Wu, Shuzhe Yang, Rui Guo, and Yi Yang; Supervision: Shuo Wang and Yong Cao.
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Yang, J., Liu, Y., Liu, Q. et al. A nomogram to predict the risk of postoperative intracranial rebleeding in patients with spontaneous intracranial hematoma. Neurosurg Rev 45, 1571–1578 (2022). https://doi.org/10.1007/s10143-021-01682-3
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DOI: https://doi.org/10.1007/s10143-021-01682-3