Optical coherence tomography angiography and microvessel density quantification in penumbra after traumatic brain injury in rats

  • Peng ZHONG ,
  • Xiaodan HU ,
  • Zhenzhou WANG
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  • 1. Department of Ultrasound, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China
    2. School of Basic Medical Sciences, Peking University, Beijing 100191, China
    3. Trauma Center, National Center for Trauma Medicine, Key Laboratory of Trauma and Neural Regeneration, Peking University People's Hospital, Beijing, 100044, China
WANG Zhenzhou, e-mail, 13522470752@163.com

Received date: 2022-09-24

  Online published: 2025-04-12

Supported by

Grants from Peking University People' s Hospital Research and Development Funds(RDJ2022-05)

Copyright

, 2025, All rights reserved. Unauthorized reproduction is prohibited.

Abstract

Objective: To observe the dynamic changes of microvascular injury and repair in the penumbra of traumatic brain injury (TBI) rats with effective cerebral perfusion microvascular imaging using optical coherence tomography angiography (OCTA). Methods: Transparent closed cranial windows were placed in craniotomy rats after TBI caused by weight drop. All the rats in TBI group and control group underwent head MRI examination on the first postoperative day, and the changes of cerebral cortical microvessel density were measured by OCTA through cranial windows on d0, d2, d4, d6, and d8. On the second day after the operation, the same number of rats in the two groups were selected to complete the immunohistochemical staining of brain tissue with pimonidazole, an indicator of hypoxia. Results: MRI T2W1 and immunohistochemical staining demonstrated that edema and hypoxia in the traumatic brain tissue extended deeply throughout the entire cortex. OCTA showed that the cortical surface veins of the rats in both groups were significantly dilated and tortuous after operation, and recovered to the postoperative day level on d8. The effective perfusion microvessel density of the rats in both groups gradually recovered after a temporary decrease, and the TBI group decreased from 39.38%±4.48% on d0 to 27.84%±6.01% on d2, which was significantly lower than that on d0, d6, and d8 (P < 0.05). The highest value was 61.71%±7.69% on d8, which was significantly higher than that on d0, d2, and d4 (P < 0.05). The control group decreased from 44.59%±7.78% on d0 to 36.69%±5.49% on d2, which was significantly lower than that on d0, d6, and d8 (P < 0.05). The highest value was 51.92%±5.96% on d8, which was significantly higher than that on d2, and d4 (P < 0.05). Comparing the two groups, the effective perfusion microvessel density in the TBI group was significantly lower than that in the control group on d2 (P=0.021), and significantly higher than that in the control group on d8 (P=0.030). Conclusion: OCTA can be used as a method of imaging and measurement of effective perfusion microvessels in the injured cerebral cortex of TBI rats. After TBI, the effective perfusion microvessel density in the wound penumbra gradually recovered after decreasing, and increased significantly on d8.

Cite this article

Peng ZHONG , Xiaodan HU , Zhenzhou WANG . Optical coherence tomography angiography and microvessel density quantification in penumbra after traumatic brain injury in rats[J]. Journal of Peking University(Health Sciences), 2025 , 57(2) : 262 -266 . DOI: 10.19723/j.issn.1671-167X.2025.02.006

References

1 Capizzi A , Woo J , Verduzco-Gutierrez M . Traumatic brain injury: An overview of epidemiology, pathophysiology, and medical management[J]. Med Clin North Am, 2020, 104 (2): 213- 238.
2 Graham DI , Adams JH . Ischaemic brain damage in fatal head injuries[J]. Lancet, 1971, 1 (7693): 265- 266.
3 Sahuquillo J , Poca MA , Amoros S . Current aspects of patho-physiology and cell dysfunction after severe head injury[J]. Curr Pharm Des, 2001, 7 (15): 1475- 1503.
4 Demers-Marcil S , Coles JP . Cerebral metabolic derangements following traumatic brain injury[J]. Curr Opin Anaesthesiol, 2022, 35 (5): 562- 569.
5 Hays L , Udy A , Adamides AA , et al. Effects of brain tissue oxygen (PbtO2) guided management on patient outcomes following severe traumatic brain injury: A systematic review and meta-analysis[J]. J Clin Neurosci, 2022, 99, 349- 358.
6 Reddy L , Murugan D , Mullick M , et al. Recent approaches for angiogenesis in search of successful tissue engineering and rege-neration[J]. Curr Stem Cell Res Ther, 2020, 15 (2): 111- 134.
7 Bragin DE , Bragina OA , Kameneva MV , et al. Resuscitation with drag reducing polymers after traumatic brain injury with hemor-rhagic shock reduces microthrombosis and oxidative stress[J]. Adv Exp Med Biol, 2020, 1232, 39- 45.
8 de Carlo TE , Romano A , Waheed NK , et al. A review of optical coherence tomography angiography (OCTA)[J]. Int J Retina Vitreous, 2015, 1, 5.
9 Feeney DM , Boyeson MG , Linn RT , et al. Responses to cortical injury: Ⅰ. Methodology and local effects of contusions in the rat[J]. Brain Res, 1981, 211 (1): 67- 77.
10 Liu X , Huang Z , Wang Z , et al. A deep learning based pipeline for optical coherence tomography angiography[J]. J Biophotonics, 2019, 12 (10): e201900008.
11 Wang Z , Liu J , Liu X , et al. Perfusion microvessel density in the cerebral cortex of septic rats is negatively correlated with endothe-lial microparticles in circulating plasma[J]. Metab Brain Dis, 2021, 36 (5): 1029- 1036.
12 Veenith TV , Carter EL , Geeraerts T , et al. Pathophysiologic mechanisms of cerebral ischemia and diffusion hypoxia in traumatic brain injury[J]. JAMA Neurol, 2016, 73 (5): 542- 550.
13 Sandsmark DK , Bashir A , Wellington CL , et al. Cerebral microvascular injury: A potentially treatable endophenotype of traumatic brain injury-induced neurodegeneration[J]. Neuron, 2019, 103 (3): 367- 379.
14 Kenney K , Amyot F , Haber M , et al. Cerebral vascular injury in traumatic brain injury[J]. Exp Neurol, 2016, 275 (Pt 3): 353- 366.
15 Manglani M , McGavern DB . Intravital imaging of neuroimmune interactions through a thinned skull[J]. Curr Protoc Immunol, 2018, 120, 24.2.1- 24.2.12.
16 Hattori R , Komiyama T . Longitudinal two-photon calcium imaging with ultra-large cranial window for head-fixed mice[J]. STAR Protoc, 2022, 3 (2): 101343.
17 Qin D , Wang J , Le A , et al. Traumatic brain injury: Ultrastructural features in neuronal ferroptosis, glial cell activation and polarization, and blood-brain barrier breakdown[J]. Cells, 2021, 10 (5): 1009.
18 Grutzendler J , Murikinati S , Hiner B , et al. Angiophagy prevents early embolus washout but recanalizes microvessels through embolus extravasation[J]. Sci Transl Med, 2014, 6 (226): 226ra31.
19 van der Wijk AE , Georgakopoulou T , Majolée J , et al. Microembolus clearance through angiophagy is an auxiliary mechanism preserving tissue perfusion in the rat brain[J]. Acta Neuropathol Commun, 2020, 8 (1): 195.
20 van der Wijk AE , Lachkar N , de Vos J , et al. Extravasation of microspheres in a rat model of silent brain infarcts[J]. Stroke, 2019, 50 (6): 1590- 1594.
21 Park E , Bell JD , Siddiq IP , et al. An analysis of regional microvascular loss and recovery following two grades of fluid percussion trauma: A role for hypoxia-inducible factors in traumatic brain injury[J]. J Cereb Blood Flow Metab, 2009, 29 (3): 575- 584.
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