Imaging Evaluation of Secondary Brain Injury in Spontaneous Intracerebral Hemorrhage

doi:10.3969/j.issn.1673-5765.2023.03.014

Abstract

Abstract: When the best therapy for primary injury caused by spontaneous intracerebral hemorrhage is still controversial, the impact of secondary brain injury has been paid more and more attention. Secondary brain injury is an inevitable pathophysiological process after spontaneous intracerebral hemorrhage. Many studies have shown that secondary brain injury has a significant impact on the prognosis. Imaging is the most commonly used method to evaluate secondary brain injury in clinical research. Different imaging techniques are helpful in determining the relationship between secondary brain injury and the prognosis. Therefore, this paper reviewed the research status of various image methods in evaluating secondary brain injury.

Key words: Spontaneous intracerebral hemorrhage; Secondary brain injury; Computed tomography; Magnetic resonance imaging; Prognosis

摘要： 在自发性脑出血所致原发性损伤的最佳治疗方法尚存争议的情况下，继发性脑损伤带来的影响越来越得到重视。继发性脑损伤是自发性脑出血后必然发生的病理生理过程，诸多研究表明继发性脑损伤对预后有着显著影响。影像学手段是临床研究中用于评估继发性脑损伤最常用的手段，不同的影像学方法均可对明确继发性脑损伤与预后的关系提供一定帮助。本文对继发性脑损伤各种影像学评估方法的研究现状展开综述，希望从中获取继发性脑损伤准确预测方法的新思路。

关键词: 自发性脑出血; 继发性脑损伤; 计算机断层成像; 磁共振成像; 预后

LI Bo, HU Yongzhen, LI Xuesong.

Imaging Evaluation of Secondary Brain Injury in Spontaneous Intracerebral Hemorrhage

[J]. Chinese Journal of Stroke, 2023, 18(03): 347-352.

李波, 胡永珍, 李雪松. 自发性脑出血后继发性脑损伤的影像学研究进展[J]. 中国卒中杂志, 2023, 18(03): 347-352.

References

[1] HOSTETTLER I C，SEIFFGE D J，WERRING D J. Intracerebral hemorrhage：an update on diagnosis and treatment[J]. Expert Rev Neurother，2019，19（7）：679-694.
[2] GROSS B A，JANKOWITZ B T，FRIEDLANDER R M. Cerebral intraparenchymal hemorrhage：a review[J]. JAMA，2019，321（13）：1295-1303.
[3] QURESHI A I，PALESCH Y Y，BARSAN W G，et al. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage[J]. N Engl J Med，2016，375（11）：1033-1043.
[4] HANLEY D F，THOMPSON R E，ROSENBLUM M，et al. Efficacy and safety of minimally invasive surgery with thrombolysis in intracerebral haemorrhage evacuation（MISTIE Ⅲ）：a randomised，controlled，open-label，blinded endpoint phase 3 trial[J]. Lancet，2019，393（10175）：1021-1032.
[5] SHI K B，TIAN D C，LI Z G，et al. Global brain inflammation in stroke[J]. Lancet Neurol，2019，18（11）：1058-1066.
[6] BAUTISTA W，ADELSON P D，BICHER N，et al. Secondary mechanisms of injury and viable pathophysiological targets in intracerebral hemorrhage[J/OL]. Ther Adv Neurol Disord，2021，14：17562864211049208[2022-06-06]. https://doi.org/10.1177/17562864211049208.
[7] HAUPENTHAL D，KURAMATSU J B，VOLBERS B，et al. Disability-adjusted life-years associated with intracerebral hemorrhage and secondary injury[J/OL]. JAMA Network Open，2021，4（7）：e2115859[2022-06-06]. https://doi.org/10.1001/jamanetworkopen.2021.15859.
[8] ZHU H M，WANG Z Q，YU J X，et al. Role and mechanisms of cytokines in the secondary brain injury after intracerebral hemorrhage[J/OL]. Prog Neurobiol，2019，178：101610[2022-06-06]. https://doi.org/10.1016/j.pneurobio.2019.03.003.
[9] JAIN A，MALHOTRA A，PAYABVASH S. Imaging of spontaneous intracerebral hemorrhage[J]. Neuroimaging Clin N Am，2021，31（2）：193-203.
[10] SELIM M，NORTON C. Perihematomal edema：implications for intracerebral hemorrhage research and therapeutic advances[J]. J Neurosci Res，2020，98（1）：212-218.
[11] IRONSIDE N，CHEN C，DING D，et al. Perihematomal edema after spontaneous intracerebral hemorrhage[J]. Stroke，2019，50（6）：1626-1633.
[12] HAQUE M E，GABR R E，GEORGE S D，et al. Serial metabolic evaluation of perihematomal tissues in the intracerebral hemorrhage pig model[J/OL]. Front Neurosci，2019，13：888[2022-06-06]. https://doi.org/10.3389/fnins.2019.00888.
[13] LV X N，LI Z Q，DENG L，et al. Early perihematomal edema expansion：definition，significance，and association with outcomes after intracerebral hemorrhage[J/OL]. Oxid Med Cell Longev，2021，2021：6249509[2022-06-06]. https://doi.org/10.1155/2021/6249509.
[14] VOLBERS B，GIEDE-JEPPE A，GERNER S T，et al. Peak perihemorrhagic edema correlates with functional outcome in intracerebral hemorrhage[J/OL]. Neurology，2018，90（12）：e1005-e1012[2022-06-06]. https://doi.org/10.1212/WNL.0000000000005167.
[15] VOLBERS B，WILLFARTH W，KURAMATSU J B，et al. Impact of perihemorrhagic edema on short-term outcome after intracerebral hemorrhage[J]. Neurocrit Care，2016，24（3）：404-412.
[16] GRUNWALD Z，BESLOW L A，URDAY S，et al. Perihematomal edema expansion rates and patient outcomes in deep and lobar intracerebral hemorrhage[J]. Neurocrit Care，2017，26（2）：205-212.
[17] WU T Y，SHARMA G，STRBIAN D，et al. Natural history of perihematomal edema and impact on outcome after intracerebral hemorrhage[J]. Stroke，2017，48（4）：873-879.
[18] SPRÜGEL M I，KURAMATSU J B，VOLBERS B，et al. Perihemorrhagic edema：revisiting hematoma volume，location，and surface[J/OL]. Neurology，2019，93（12）：e1159-e1170[2022-06-06]. https://doi. org/10.1212/WNL.0000000000008129.
[19] 周剑，高培毅，李小光，等. 脑出血亚急性及慢性期血肿周围组织低灌注损伤的CT灌注成像研究[J]. 中华放射学杂志，2006，40（5）：453-457.
[20] 周剑，高培毅，李小光. 实验性脑出血周围组织脑血流变化与脑水肿形成的相关研究[J]. 中华放射学杂志，2005，39（9）：938-942.
[21] MOROTTI A，BUSTO G，BERNARDONI A，et al. Association between perihematomal cerebral blood volume and intracerebral hemorrhage expansion：a computed tomography perfusion study[J]. Ann Neurol，2019，85（6）：943-947.
[22] MOROTTI A，BUSTO G，BOULOUIS G，et al. Delayed perihematomal hypoperfusion is associated with poor outcome in intracerebral haemorrhage[J/OL]. Eur J Clin Invest，2022，52（4）：e13696[2022-06-06]. https://doi.org/10.1111/eci.13696.
[23] 冯皓，赵性泉. 脑出血后血-脑屏障破坏与血肿周围水肿形成[J]. 中国现代神经疾病杂志，2018，18（11）：774-779.
[24] ZHANG X，ZHU H C，YANG D，et al. Association between cerebral blood flow changes and blood-brain barrier compromise in spontaneous intracerebral haemorrhage[J]. Clin Radiol，2022，77（11）：833-839.
[25] 蔡勇，钟兴明，汪一棋，等. 磁共振波谱成像联合弥散加权成像对自发性脑出血后二次脑损伤的预测价值[J]. 中华危重病急救医学，2020，32（11）：1336-1339.
[26] LIU R，ZHANG H R，CHENG S J，et al. Association of brain iron overload with brain edema and brain atrophy after intracerebral hemorrhage[J/OL]. Front Neurol，2020，11：602413[2022-06-06]. https://doi.org/10.3389/fneur.2020.602413.
[27] BUTCHER K S，BAIRD T，MACGREGOR L，et al. Perihematomal edema in primary intracerebral hemorrhage is plasma derived[J]. Stroke，2004，35（8）：1879-1885.
[28] 王苇，张新江，殷小平，等. 急性期脑出血灶周水肿的磁共振弥散加权成像临床初步研究[J]. 中国卒中杂志，2006，1（5）：326-331.
[29] WILLIAMSON M R，DIETRICH K，HACKETT M J，et al. Rehabilitation augments hematoma clearance and attenuates oxidative injury and ion dyshomeostasis after brain hemorrhage[J]. Stroke，2017，48（1）：195-203.
[30] WEI J，NOVAKOVIC N，CHENEVERT T L，et al. Perihematomal brain tissue iron concentration measurement by MRI in patients with intracerebral hemorrhage[J]. CNS Neurosci Ther，2020，26（9）：896-901.
[31] NOVAKOVIC N，WILSECK Z M，CHENEVERT T L，et al. Assessing early erythrolysis and the relationship to perihematomal iron overload and white matter survival in human intracerebral hemorrhage[J]. CNS Neurosci Ther，2021，27（10）：1118-1126.
[32] ZHOU J，LIU T，GUO H，et al. Lactate potentiates angiogenesis and neurogenesis in experimental intracerebral hemorrhage[J]. Exp Mol Med，2018，50（7）：1-12.
[33] LIU Y，YANG S S，CAI E L，et al. Functions of lactate in the brain of rat with intracerebral hemorrhage evaluated with MRI/MRS and in vitro approaches[J]. CNS Neurosci Ther，2020，26（10）：1031-1044.
[34] NIIBO T，OHTA H，MIYATA S，et al. Prediction of blood-brain barrier disruption and intracerebral hemorrhagic infarction using arterial spin-labeling magnetic resonance imaging[J]. Stroke，2017，48（1）：117-122.
[35] YANG J，LI Q，WANG Z Y，et al. Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice[J/OL]. Sci Rep，2017，7：40358[2022-06-06]. https://doi.org/10.1038/srep40358.
[36] SWEENEY M D，SAGARE A P，ZLOKOVIC B V. Blood-brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders[J]. Nat Rev Neurol，2018，14（3）：133-150.
[37] MATTIONI A，CENCIARELLI S，EUSEBI P，et al. Transcranial doppler sonography for detecting stenosis or occlusion of intracranial arteries in people with acute ischaemic stroke[J/OL]. Cochrane Database Syst Rev，2020，2（2）：CD010722[2022-06-06]. https://doi.org/10.1002/14651858.CD010722.pub2.
[38] KUMAR G，SHAHRIPOUR R B，HARRIGAN M R. Vasospasm on transcranial Doppler is predictive of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage：a systematic review and meta-analysis[J]. J Neurosurg，2016，124（5）：1257-1264.
[39] 金占强，于腾飞，何文，等. 经颅超声造影评价脑出血血肿周围水肿区血流灌注的临床价值[J]. 中国医学影像学杂志，2020，28（6）：416-421.
[40] 朴莲花，冉红伟，申平花，等. 超声多模式评估脑出血患者颅内压增高的临床价值[J]. 中风与神经疾病杂志，2022，39（1）：22-24.
[41] ZIVADINOV R，CHUNG C P. Potential involvement of the extracranial venous system in central nervous system disorders and aging[J/OL]. BMC Med，2013，11：260[2022-06-06]. https://doi.org/10.1186/1741-7015-11-260.
[42] FENG H，JIN Z Q，HE W，et al. Cerebral venous outflow participates in perihematomal edema after spontaneous intracerebral hemorrhage：a cross-sectional study[J/OL]. Medicine（Baltimore），2018，97（35）：e12034[2022-06-06]. https://doi.org/10.1097/MD.0000000000012034.
[43] FENG H，ZHANG H X，HE W，et al. Jugular venous reflux is associated with perihematomal edema after intracerebral hemorrhage[J/OL]. Biomed Res Int，2017，2017：7514639[2022-06-06]. https://doi.org/10.1155/2017/7514639.