Dynamic changes of brain cavity in rats after traumatic brain injury detected by MRI-based three-dimensional reconstruction

doi:10.3969/j.issn.2095-4344.2016.40.003

Abstract

Abstract:

BACKGROUND: Currently, morphological observations of brain cavity after traumatic brain injury (TBI) via cadavers or animal specimen are difficult to obtain dynamic changes.

OBJECTIVE: To explore the application effect of MRI-based three-dimensional (3D) reconstruction for evaluating the prognosis of TBI.

METHODS: Five male Sprague-Dawley rats were enrolled to establish TBI models by Electronic Cortical Contusion Injury (eCCI), and scanned by 3.0T MRI with Rat-coil to obtain the DICOM date of brain at 1 day, 1, 2 and 3 months after modeling. Brain cavities were 3-dimensionally reconstructed by Mimics16.0 software, and analyzed in the Meshmixer software.

RESULTS AND CONCLUSION: (1) The outline of reconstruction model image was clear, and could be observed and measured from different sides and perspectives. (2) The cavity volume and surface area at different time points after TBI showed significant differences between each other except that at 2 and 3 months (P < 0.05). (3) The results of cavity change suggested that the cavity tended to be regular after 3 months of TBI. (4) In conclusion, 3D reconstruction software Mimics combining with model analysis software Meshmixer can conveniently and quickly obtain the cavity model, and provide an intuitive way for evaluating the dynamic variations of the brain cavity after TBI.

中国组织工程研究杂志出版内容重点：肾移植；肝移植；移植；心脏移植；组织移植；皮肤移植；皮瓣移植；血管移植；器官移植；组织工程

Key words: Models, Animal, Imaging, Three-Dimensional, Craniocerebral Trauma, Tissue Engineering

CLC Number:

R318

Fu Feng, Zhao Ming-liang, Li Xiao-hong, Chen Chong, Wang Li-na, Sun Hong-tao, Tu Yue, Zhang Sai . Dynamic changes of brain cavity in rats after traumatic brain injury detected by MRI-based three-dimensional reconstruction[J]. Chinese Journal of Tissue Engineering Research, 2016, 20(40): 5946-5952.

Figures/Tables 1

2.1 实验动物数量分析纳入的5只SD大鼠致伤24 h后行神经功能缺陷评分，符合重度颅脑创伤模型标准，所有大鼠均进入最终的结果分析，无中途死亡或脱失情况发生。 2.2 模型方法的改进利用电子控制性脑皮质撞击仪制备的颅脑创伤大鼠模型，通过调整打击深度、打击速度、打击最低点持续时间等参数精确控制损伤程度，在大鼠存活情况下，采用MRI技术获得了颅内空腔连续动态监测数据。 2.3 模型更接近临床实践且具有较好稳定性大鼠颅脑创伤后24 h神经功能缺陷评分均大于10分，符合重型颅脑创伤标准[14]。进一步行MRI检查发现，5只大鼠损伤处脑皮质均有明显挫伤，且周围脑组织出现不同范围的水肿及血肿，中线发生偏移(图1)。与先期文献报道的人类颅脑创伤MRI表现类似[15]。各时间点5只大鼠之间的颅内病灶范围无明显差异，显示出该造模方法具有良好的稳定性。 2.4 颅脑创伤后大脑与空腔三维模型结果应用大鼠脑部MRI扫描数据，通过 Mimics软件中动态区域增长法和阈值分割法分别得到SD大鼠颅脑创伤后空腔和大脑三维模型(图2)，模型结构完整、轮廓清晰、达到了连续观察颅脑创伤后空腔变化的可视化效果；STL格式模型导入Meshmixer，经过面网格优化后的模型可自由旋转、从任意角度及平面剖切，操作者能从不同侧面和视角进行测量；通过对三维模型透明度、着色等设置可实现空腔与大脑模型融合，可在大脑中直观、准确定位空腔位置与范围(图3)。 2.5 三维重建模型与实际样本在形态学上对比将SD大鼠颅脑创伤3个月后大脑样本与重建模型进行比较显示，大脑大体样本与大脑模型比较，可见两者的大脑整体形态、空腔开口位置和轮廓一致；脑组织切片甲苯胺蓝染色后与空腔模型剖切比较发现，样本与模型空腔截面吻合(图4)。 2.6 SD大鼠颅脑创伤后空腔体积变化情况 SD大鼠颅脑创伤后空腔体积从第1天到第2个月呈线性上升，并于第3个月趋于稳定。不同时间点结果比较，先进行Mauchly的球形度检验，结果满足随机区组方差分析的球对称要求(MauchlyW=0.073，P=0.064)，进一步采用随机区组方差分析，结果显示，不同时间点空腔体积差异有显著性意义(F=287.857，P < 0.05)；进一步LSD进行两两比较发现，第1天(25.94±5.03) mm3、第1个月(40.71±4.76) mm3、第2个月(52.78±6.22) mm3两两之间差异均有显著性意义(P < 0.05)，第2个月、第3个月(56.89±5.55) mm3之间差异无显著性意义(P > 0.05)，即空腔体积于第3个月趋于稳定(图5) 。2.7 SD大鼠颅脑创伤空腔表面积变化情况 SD大鼠颅脑创伤后空腔表面积从第1天到第1个月、第2个月上升趋势明显，进入第3个月后有降低趋势。不同时间点结果比较，先进行Mauchly的球形度检验，结果满足随机区组方差分析的球对称要求(MauchlyW=0.054，P=0.057)，进而采用随机区组方差分析，结果显示，不同时间点，空腔表面积差异有显著性意义(F=24.424 977，P < 0.05)，进一步LSD进行两两比较发现：除了第2个月(84.55± 9.25) mm2与第3个月(80.89±9.01) mm2差异无显著性意义(P > 0.05)，其他各个时间点之间两两比较显示差异均有显著性意义(图6)。"

References

[1] Pohl KM, Bouix S, Nakamura M, et al. A hierarchical algorithm for MR brain image parcellation. IEEE Trans Med Imaging. 2007;26(9):1201-1212.
[2] Kelly ML, Roach MJ, Banerjee A, et al. Functional and long-term outcomes in severe traumatic brain injury following regionalization of a trauma system. J Trauma Acute Care Surg. 2015;79(3):372-377.
[3] Palma G, Tedeschi E, Borrelli P, et al. A Novel Multiparametric Approach to 3D Quantitative MRI of the Brain. PloS One. 2015;10(8):e0134963.
[4] Zöllner FG, Daab M, Sourbron SP, et al. An open source software for analysis of dynamic contrast enhanced magnetic resonance images: UMMPerfusion revisited. BMC Med Imaging. 2016;16:7.
[5] Chen X, Egger J. Development of an open source software module for enhanced visualization during MR-guided interstitial gynecologic brachytherapy. Springer Plus. 2014;3:167.
[6] 陈以胜,王景景,陈旭义,等. 3D打印技术制备大鼠脊髓仿生支架的研究[J].中国修复重建外科杂志, 2015,29(3): 364-367
[7] Simons CJ, Cobb L, Davidson BS. A fast, accurate, and reliable reconstruction method of the lumbar spine vertebrae using positional MRI. Ann Biomed Eng. 2014; 42(4):833-842.
[8] Rubenstein R, Chang B, Davies P, et al.A novel, ultrasensitive assay for tau: potential for assessing traumatic brain injury in tissues and biofluids. J Neurotrauma. 2015;32(5):342-352.
[9] Peng W, Xing Z, Yang J, et al. The efficacy of erythropoietin in treating experimental traumatic brain injury: a systematic review of controlled trials in animal models. J Neurosurg. 2014;121(3):653-664.
[10] Johnstone VP, Wright DK, Wong K, et al. Experimental Traumatic Brain Injury Results in Long-Term Recovery of Functional Responsiveness in Sensory Cortex but Persisting Structural Changes and Sensorimotor, Cognitive, and Emotional Deficits. J Neurotrauma. 2015;32(17):1333-1346.
[11] 樊继宏.Mimics建模到Marc有限元分析的系统工程和实例[D].南方医科大学,2010.
[12] Schmidt R, Ratto M. Design-to-fabricate: maker hardware requires maker software. IEEE Comput Graph Appl. 2013;33(6):26-34.
[13] Budde MD, Shah A, McCrea M, et al. Primary blast traumatic brain injury in the rat: relating diffusion tensor imaging and behavior. Front Neurol. 2013;4:154.
[14] Guan J, Zhu Z, Zhao RC, et al.Transplantation of human mesenchymal stem cells loaded on collagen scaffolds for the treatment of traumatic brain injury in rats. Biomaterials. 2013;34(24):5937-5946.
[15] Ricciardi MC, Bokkers R, Butman J, et al. Trauma specific brain abnormalities in suspected mild TBI patients identified in the first 48 hours after injury: a blinded MRI comparative study including suspected acute minor stroke patients. J Neurotrauma. 2016. [Epub ahead of print]
[16] Bruns J, Hauser WA. The epidemiology of traumatic brain injury: a review. Epilepsia. 2003;44 (Suppl.10): 2-10.
[17] Brown AW, Leibson CL, Malec JF et al. Long-term survival after traumatic brain injury: a population-based analysis. Neuro Rehabilitation. 2004; 19: 37-43.
[18] Gómez PA, Castaño-Leon AM, de-la-Cruz J, et al. Trends in epidemiological and clinical characteristics in severe traumatic brain injury: Analysis of the past 25 years of a single centre data base. Neurocirugia (Astur). 2014;25(5):199-210.
[19] Marklund N, Hillered L. Animal modelling of traumatic brain injury in preclinical drug development: where do we go from here? Br J Pharmacol. 2011;164:1207-1229.
[20] Zhou Y, Lui YW. Changes in brain organization after TBI: evidence from functional MRI findings. Neurology. 2013;80(20):1822-1823.
[21] Hart T, Novack TA, Temkin N, et al. Duration of Posttraumatic Amnesia Predicts Neuropsychological and Global Outcome in Complicated Mild Traumatic Brain Injury. J Head Trauma Rehabil. 2015.[Epub ahead of print]
[22] Hiekkanen H, Kurki T, Brandstack N, et al. Association of injury severity, MRI-results and ApoE genotype with 1-year outcome in mainly mild TBI: a preliminary study. Brain Inj. 2009;23(5):396-402.
[23] Wang S, Chopp M, Nazem-Zadeh MR, et al. Comparison of neurite density measured by MRI and histology after TBI. PLoS One. 2013;8(5):e63511.
[24] Mollayeva T, Pratt B, Mollayeva S, et al. The relationship between insomnia and disability in workers with mild traumatic brain injury/concussion: Insomnia and disability in chronic mild traumatic brain injury. Sleep Med. 2015.pii: S1389-9457(15)01987-5.
[25] Bramlett HM, Dietrich WD. Long-Term Consequences of Traumatic Brain Injury:Current Status of Potential Mechanisms of Injury and Neurological Outcomes. J Neurotrauma. 2015;32(23):1834-1848.
[26] 张竞文. 弥散张量成像及磁敏感加权成像对创伤性脑损伤的实验与临床动态研究[D].天津医科大学,2011.
[27] Tsuda S, Hou J, Nelson RL, et al.,Prolonged hippocampal cell death following closed-head traumatic brain injury in rats. Neuroreport. 2016. [Epub ahead of print]
[28] Emery CA, Barlow KM, Brooks BL, et al. A Systematic Review of Psychiatric, Psychological, and Behavioural Outcomes following Mild Traumatic Brain Injury in Children and Adolescents. Can J Psychiatry. 2016; 61(5): 259-269.
[29] Grandhi R, Bonfield CM, Newman WC, et al. Surgical management of traumatic brain injury: a review of guidelines, pathophysiology, neurophysiology, outcomes, and controversies. J Neurosurg Sci. 2014; 58(4):249-259.
[30] Bahar S, Bolat D, Dayan MO, et al. Two- and three-dimensional anatomy of paranasal sinuses in Arabian foals. J Vet Med Sci. 2014;76(1):37-44.
[31] Wang J, Lui Z, Qian Z, et al.Soft tissue artifact evaluation of the cervical spine in motion patterns of flexion and lateral bending: a preliminary study. Peer J. 2016;4:e1893.
[32] Su XY, Zhao JX, Zhao Z, et al. Three-Dimensional Analysis of the Characteristics of the Femoral Canal Isthmus: An Anatomical Study. Bio Med Res Int. 2015, [Epub ahead of print].
[33] 步国强,毛仲轩.Mimics 软件模拟置钉在腰椎关节突重度退变椎弓根螺钉内固定中的应用[J].中国组织工程研究, 2015,19(17):2745-2751.
[34] Tan PY, Chen JH, Li P, et al. Improving Threshold Segmentation in 3D Reconstruction of Mandible CT Image. Sichuan da xue xue bao Yi xue ban Journal of Sichuan University. Med Sci. 2015;46(3):458-462.
[35] 邱锋,马向阳,杨进城. 应用Mimics测量脊髓容积[J]. 中国脊柱脊髓杂志, 2013,23(11):1043-1045.
[36] Schmidt R, Ratto• M. Design-to-fabricate: maker hardware requires maker software. IEEE Comput Graph Appl. 2013;33(6):26-34.
[37] Li Z, Zou D, Zhang J, et al. Use of 3D reconstruction of emergency and postoperative craniocerebral CT images to explore craniocerebral trauma mechanism. Forensic Sci Int. 2015;255:106-111.
[38] Tejszerska D, Wolanski W, Larysz D, et al. Morphological analysis of the skull shape in craniosynostosis. Acta Bioeng Biomech. 2011;13(1):35-40.
[39] Wu ZF, Lei YH, Li WJ, et al. Construction and validation of a three-dimensional finite element model of cranio-maxillary complex with sutures in unilateral cleft lip and palate patient. Shanghai kou qiang yi xue. 2013;22(1):35-40.
[40] Qin Z, Compton BG, Lewis JA, et al. Structural optimization of 3D-printed synthetic spider webs for high strength. Nat Commun. 2015;6:7038.