Arena John D, Smith Douglas H, Diaz Arrastia Ramon, Cullen D Kacy, Xiao Rui, Fan Jiaxin, Harris Danielle C, Lynch Cillian E, Johnson Victoria E
Department of Neurosurgery, Penn Center for Brain Injury and Repair, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Acta Neuropathol Commun. 2024 Dec 4;12(1):189. doi: 10.1186/s40478-024-01883-z.
Mild traumatic brain injury (mTBI) or concussion is a substantial health problem globally, with up to 15% of patients experiencing persisting symptoms that can significantly impact quality of life. Currently, the diagnosis of mTBI relies on clinical presentation with ancillary neuroimaging to exclude more severe forms of injury. However, identifying patients at risk for a poor outcome or protracted recovery is challenging, in part due to the lack of early objective tests that reflect the relevant underlying pathology. While the pathophysiology of mTBI is poorly understood, axonal damage caused by rotational forces is now recognized as an important consequence of injury. Moreover, serum measurement of the neurofilament light (NfL) protein has emerged as a potentially promising biomarker of injury. Understanding the pathological processes that determine serum NfL dynamics over time, and the ability of NfL to reflect underlying pathology will be critical for future clinical research aimed at reducing the burden of disability after mild TBI. Using a gyrencephalic model of head rotational acceleration scaled to human concussion, we demonstrate significant elevations in serum NfL, with a peak at 3 days post-injury. Moreover, increased serum NfL was detectable out to 2 weeks post-injury, with some evidence it follows a biphasic course. Subsequent quantitative histological examinations demonstrate that axonal pathology, including in the absence of neuronal somatic degeneration, was the likely source of elevated serum NfL. However, the extent of axonal pathology quantified via multiple markers did not correlate strongly with the extent of serum NfL. Interestingly, the extent of blood-brain barrier (BBB) permeability offered more robust correlations with serum NfL measured at multiple time points, suggesting BBB disruption is an important determinant of serum biomarker dynamics after mTBI. These data provide novel insights to the temporal course and pathological basis of serum NfL measurements that inform its utility as a biomarker in mTBI.
轻度创伤性脑损伤(mTBI)或脑震荡是全球范围内一个严重的健康问题,高达15%的患者会出现持续症状,这会对生活质量产生重大影响。目前,mTBI的诊断依赖于临床表现及辅助神经影像学检查,以排除更严重的损伤形式。然而,识别预后不良或恢复时间延长的高危患者具有挑战性,部分原因是缺乏能够反映相关潜在病理的早期客观检测方法。虽然mTBI的病理生理学尚未完全了解,但旋转力导致的轴突损伤现已被认为是损伤的一个重要后果。此外,血清神经丝轻链(NfL)蛋白的检测已成为一种潜在的有前景的损伤生物标志物。了解决定血清NfL随时间变化的病理过程,以及NfL反映潜在病理的能力,对于未来旨在减轻轻度TBI后残疾负担的临床研究至关重要。使用一种按人类脑震荡比例缩放的脑回状头部旋转加速模型,我们发现血清NfL显著升高,在损伤后3天达到峰值。此外,在损伤后2周内均可检测到血清NfL升高,有证据表明其呈双相过程。随后的定量组织学检查表明,轴突病理改变,包括在无神经元体细胞变性的情况下,可能是血清NfL升高的来源。然而,通过多种标志物量化的轴突病理程度与血清NfL程度的相关性并不强。有趣的是,血脑屏障(BBB)通透性程度与多个时间点测量的血清NfL具有更强的相关性,这表明BBB破坏是mTBI后血清生物标志物动态变化的一个重要决定因素。这些数据为血清NfL测量的时间进程和病理基础提供了新的见解,为其作为mTBI生物标志物的应用提供了依据。