Poroelastic Responses of Human Brain Under Sustained High Overloads

TIAN Jin; LIU Shaobao; LU Tianjian; XU Feng

doi:10.21656/1000-0887.450130

Volume 45 Issue 6

Jun. 2024

Turn off MathJax

Article Contents

Article Navigation > Applied Mathematics and Mechanics > 2024 > 45(6): 691-709

TIAN Jin, LIU Shaobao, LU Tianjian, XU Feng. Poroelastic Responses of Human Brain Under Sustained High Overloads[J]. Applied Mathematics and Mechanics, 2024, 45(6): 691-709. doi: 10.21656/1000-0887.450130

Citation:

PDF( 6560 KB)

Poroelastic Responses of Human Brain Under Sustained High Overloads

doi: 10.21656/1000-0887.450130

TIAN Jin^{1, 2, 3
,},
LIU Shaobao^{4, 5},
LU Tianjian^{4, 5},
XU Feng^{2, 3
,
,}

1.
The Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an 710061, P.R. China
2.
Key Laboratory of Biomedical Information Engineering of Ministry of Education, School of Life Science and Technology, Xi'an Jiaotong University, Xi'an 710049, P.R.China
3.
Bioinspired Engineering and Biomechanics Center (BEBC), Xi'an Jiaotong University, Xi'an 710049, P.R.China
4.
State Key Laboratory of Mechanics and Control for Aerospace Structures, Nanjing University of Aeronautics and Astronautics, Nanjing 210016, P.R.China
5.
MIIT Key Laboratory of Multifunctional Lightweight Materials and Structures, Nanjing University of Aeronautics and Astronautics, Nanjing 210016, P.R.China

Received Date: 2024-05-09
Rev Recd Date: 2024-05-20
Publish Date: 2024-06-01

Abstract

Abstract

Sustained high overloads often acting during aerospace flights can significantly affect the passenger brain function dependent on the mechanical behavior of brain tissue and highly correlated with load characteristics. To predict the mechanical responses of human brain under sustained high overloads, the poroelastic constitutive model was adopted to characterize the mechanical behaviors of brain tissue. Built on an idealized 1D multi-layer structural model for human heads, the poroelastic control equation and the state transfer matrix for the brain tissue were derived. Through the Laplace transform and its inverse transform, the spatiotemporal distribution of the intracranial fluid pressure, the intracranial fluid seepage velocity, the brain tissue effective stress, and the brain tissue displacement were obtained. The results indicate that, the intracranial fluid infiltration has a significant impact on the responses of the brain tissue under sustained high overloads. The present work emphasizes the appropriateness and necessity of using poroelastic constitutive models to describe the mechanical behavior of brain tissue, providing important theoretical insights for the study of brain biomechanics under extreme load conditions.
- brain tissue mechanical response,
- sustained high overload,
- poroelastic constitutive model

(Contributed by LIU Shaobao, LU Tianjian, M. AMM Editorial Board)

FullText(HTML)

References(55)

References

[1]	ERCAN E, GUNDUZ S H. The effects of acceleration forces on cognitive functions[J]. Microgravity Science and Technology, 2020, 32(4): 681-686. doi: 10.1007/s12217-020-09793-0
[2]	孙喜庆, 姜世忠. 航空航天生物动力学[M]. 西安: 第四军医大学出版社, 2013. SUN Xiqing, JIANG Shizhong. Aerospace Biodynamics[M]. Xi'an: Forth Military Medical University Press, 2013. (in Chinese)
[3]	BUDDAY S, OVAERT T C, HOLZAPFEL G A, et al. Fifty shades of brain: a review on the mechanical testing and modeling of brain tissue[J]. Archives of Computational Methods in Engineering, 2020, 27: 1187-1230. doi: 10.1007/s11831-019-09352-w
[4]	SU L, WANG M, YIN J, et al. Distinguishing poroelasticity and viscoelasticity of brain tissue with time scale[J]. Acta Biomaterialia, 2023, 155: 423-435. doi: 10.1016/j.actbio.2022.11.009
[5]	BUDDAY S, STEINMANN P, KUHL E, et al. Secondary instabilities modulate cortical complexity in the mammalian brain[J]. Philosophical Magazine, 2015, 95(28/30): 3244-3256.
[6]	WEICKENMEIER J, KUHL E, GORIELY A, et al. Multiphysics of prionlike diseases: progression and atrophy[J]. Physical Review Letters, 2018, 121(15): 158101. doi: 10.1103/PhysRevLett.121.158101
[7]	CHENG S, BILSTON L E. Computational model of the cerebral ventricles in hydrocephalus[J]. Journal of Biomechanical Engineering, 2010, 132(5): 054501. doi: 10.1115/1.4001025
[8]	EHLERS W, WAGNER A. Multi-component modelling of human brain tissue: a contribution to the constitutive and computational description of deformation, flow and diffusion processes with application to the invasive drug-delivery problem[J]. Computer Methods in Biomechanics and Biomedical Engineering, 2015, 18(8): 861-879. doi: 10.1080/10255842.2013.853754
[9]	WEICKENMEIER J, SAEZ P, BUTLER C, et al. Bulging brains[J]. Journal of Elasticity, 2017, 129(1): 197-212.
[10]	WANG F, HAN Y, WANG B, et al. Prediction of brain deformations and risk of traumatic brain injury due to closed-head impact: quantitative analysis of the effects of boundary conditions and brain tissue constitutive model[J]. Biomechanics and Modeling in Mechanobiology, 2018, 17(4): 1165-1185. doi: 10.1007/s10237-018-1021-z
[11]	COMELLAS E, BUDDAY S, PELTERET J P, et al. Modeling the porous and viscous responses of human brain tissue behavior[J]. Computer Methods in Applied Mechanics and Engineering, 2020, 369: 113128. doi: 10.1016/j.cma.2020.113128
[12]	任立海. 弥散性脑损伤生物力学特性的数值分析研究[D]. 长沙: 湖南大学, 2015. REN Lihai. Numerical analysis of biomechanical characteristics of diffuse brain injury[D]. Changsha: Hunan University, 2015. (in Chinese)
[13]	栗志杰, 由小川, 柳占立, 等. 爆炸冲击波作用下颅脑损伤机理的数值模拟研究[J]. 爆炸与冲击, 2020, 40(1): 015901. https://www.cnki.com.cn/Article/CJFDTOTAL-BZCJ202001013.htm LI Zhijie, YOU Xiaochuan, LIU Zhanli, et al. Numerical simulation of the mechanism of traumatic brain injury induced by blast shock waves[J]. Explosion and Shock Waves, 2020, 40(1): 015901. (in Chinese) https://www.cnki.com.cn/Article/CJFDTOTAL-BZCJ202001013.htm
[14]	CHAFI M, KARAMI G, ZIEJEWSKI M, et al. Biomechanical assessment of brain dynamic responses due to blast pressure waves[J]. Annals of Biomedical Engineering, 2010, 38(2): 490-504. doi: 10.1007/s10439-009-9813-z
[15]	CHENG S, BILSTON L E. Unconfined compression of white matter[J]. Journal of Biomechanics, 2007, 40(1): 117-124. doi: 10.1016/j.jbiomech.2005.11.004
[16]	BOOKER J, SMALL J. A method of computing the consolidation behaviour of layered soils using direct numerical inversion of Laplace transforms[J]. International Journal for Numerical and Analytical Methods in Geomechanics, 1987, 11(4): 363-380. doi: 10.1002/nag.1610110405
[17]	TALBOT A. The accurate numerical inversion of Laplace transforms[J]. IMA Journal of Applied Mathematics, 1979, 23(1): 97-120. doi: 10.1093/imamat/23.1.97
[18]	TAYLOR Z, MILLER K. Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus[J]. Journal of Biomechanics, 2004, 37(8): 1263-1269. doi: 10.1016/j.jbiomech.2003.11.027
[19]	KACZMAREK M, SUBRAMANIAM R P, NEFF S R. The hydromechanics of hydrocephalus: steady-state solutions for cylindrical geometry[J]. Bulletin of Mathematical Biology, 1997, 59: 295-323. doi: 10.1007/BF02462005
[20]	WIIG H, REED R. Rat brain interstitial fluid pressure measured with micropipettes[J]. American Journal of Physiology-Heart and Circulatory Physiology, 1983, 244(2): H239-H246. doi: 10.1152/ajpheart.1983.244.2.H239
[21]	FORTE A E, GENTLEMAN S M, DINI D, et al. On the characterization of the heterogeneous mechanical response of human brain tissue[J]. Biomechanics and Modeling in Mechanobiology, 2017, 16(3): 907-920. doi: 10.1007/s10237-016-0860-8
[22]	THAPA K, KHAN H, SINGH T G, et al. Traumatic brain injury: mechanistic insight on pathophysiology and potential therapeutic targets[J]. Journal of Molecular Neuroscience, 2021, 71(9): 1725-1742. doi: 10.1007/s12031-021-01841-7
[23]	CHEN H, GARCIA-GONZALEZ D, JÉRUSALEM A. Computational model of the mechanoelectrophysiological coupling in axons with application to neuromodulation[J]. Physical Review E, 2019, 99(3): 032406. doi: 10.1103/PhysRevE.99.032406
[24]	ZHAO W, CHOATE B, JI S. Material properties of the brain in injury-relevant conditions-experiments and computational modeling[J]. Journal of the Mechanical Behavior of Biomedical Materials, 2018, 80: 222-234. doi: 10.1016/j.jmbbm.2018.02.005
[25]	JI S, GHADYANI H, BOLANDER R P, et al. Parametric comparisons of intracranial mechanical responses from three validated finite element models of the human head[J]. Annals of Biomedical Engineering, 2014, 42: 11-24. doi: 10.1007/s10439-013-0907-2
[26]	BUDDAY S, NAY R, DE ROOIJ R, et al. Mechanical properties of gray and white matter brain tissue by indentation[J]. Journal of the Mechanical Behavior of Biomedical Materials, 2015, 46: 318-330. doi: 10.1016/j.jmbbm.2015.02.024
[27]	MA H, LI F, LIU B, et al. Study on responses of HUMOS dummy in typical body posture under spacecraft re-entry overload[J]. International Journal of Crashworthiness, 2022, 27(4): 979-984. doi: 10.1080/13588265.2021.1889234
[28]	MACMANUS D B, MURPHY J G, GILCHRIST M D, et al. Mechanical characterisation of brain tissue up to 35% strain at 1, 10, and 100/s using a custom-built micro-indentation apparatus[J]. Journal of the Mechanical Behavior of Biomedical Materials, 2018, 87(1): 256-266.
[29]	ERNESTON C G. Costs and benefits of physical therapy program implementation for air force fighter pilots[R]. Ohio: Department of the Air Force, 2021.
[30]	BRON D, HEGGLI U. Flying sports[M]//KRUTSCH W, MAYR H O, MUSAHL V, et al. Injury and Health Risk Management in Sports: a Guide to Decision Making. Springer, 2020: 621-626.
[31]	BUDDAY S, SOMMER G, BIRKL C, et al. Mechanical characterization of human brain tissue[J]. Acta Biomaterialia, 2017, 48(1): 319-340.
[32]	HARA M, KOBAYAKAWA K, OHKAWA Y, et al. Interaction of reactive astrocytes with type I collagen induces astrocytic scar formation through the integrin-N-cadherin pathway after spinal cord injury[J]. Nature Medicine, 2017, 23(7): 818-828. doi: 10.1038/nm.4354
[33]	ADAMS K L, GALLO V. The diversity and disparity of the glial scar[J]. Nature Neuroscience, 2018, 21(1): 9-15. doi: 10.1038/s41593-017-0033-9
[34]	刘妍, 徐钊, 程波, 等. 考虑细胞外基质刚度的神经轴突力学模型[J]. 科学通报, 2023, 68(21): 2748-2755. https://www.cnki.com.cn/Article/CJFDTOTAL-KXTB202321008.htm LIU Yan, XU Zhao, CHENG Bo, et al. Mechanical model of nerve axon considering the stiffness of extracellular matrix[J]. Chinese Science Bulletin, 2023, 68(21): 2748-2755. (in Chinese) https://www.cnki.com.cn/Article/CJFDTOTAL-KXTB202321008.htm
[35]	郭卉, 贺昱昇, 刘梦洁, 等. 肿瘤力医学[J]. 中华肿瘤杂志, 2024, 46(6): 536-548. GUO Hui, HE Yusheng, LIU Mengjie, et al. Tumor mechanomedicine[J]. Chinese Journal of Oncology, 2024, 46(6): 536-548. (in Chinese)
[36]	HE Z, ZHU Y N, CHEN Y, et al. A deep unrolled neural network for real-time MRI-guided brain intervention[J]. Nature Communications, 2023, 14(1): 8257. doi: 10.1038/s41467-023-43966-w
[37]	PILLAI E K, FRANZE K. Mechanics in the nervous system: from development to disease[J]. Neuron, 2023, 112(3): 342-361.
[38]	LIU Y, LU Y, SHAO Y, et al. Mechanism of the traumatic brain injury induced by blast wave using the energy assessment method[J]. Medical Engineering & Physics, 2022, 101: 103767.
[39]	MAO H, ZHANG L, JIANG B, et al. Development of a finite element human head model partially validated with thirty five experimental cases[J]. Journal of Biomechanical Engineering, 2013, 135(11): 111002. doi: 10.1115/1.4025101
[40]	KANG H S, WILLINGER R E M, DIAW B M, et al. Validation of a 3D anatomic human head model and replication of head impact in motorcycle accident by finite element modeling[J]. SAE Transactions, 1997, 106(6): 3849-3858.
[41]	GHBMC. Finite element human body models[EB/OL]. 2023[2024-05-20]. http://www.ghbmc.com.
[42]	TOYOTA. What is THUMS?[EB/OL]. 2023[2024-05-20]. https://www.toyota.co.jp/thums/about.
[43]	阮世捷, 李超, 崔世海, 等. 颅骨厚度对颅内生物力学响应的影响[J]. 医用生物力学, 2021, 36(4): 560-567. https://www.cnki.com.cn/Article/CJFDTOTAL-YISX202104011.htm RUAN Shijie, LI Chao, CUI Shihai, et al. The influence of skull thickness on intracranial biomechanical response[J]. Journal of Medical Biomechanics, 2021, 36(4): 560-567. (in Chinese) https://www.cnki.com.cn/Article/CJFDTOTAL-YISX202104011.htm
[44]	李凡, 叶铭杰, 黄巍, 等. 行人碰撞事故中颈部肌肉主动力对头部损伤的影响[J]. 汽车工程, 2022, 44(3): 385-391. https://www.cnki.com.cn/Article/CJFDTOTAL-QCGC202203010.htm LI Fan, YE Mingjie, HUANG Wei, et al. Effects of neck muscle's active force on head injury in pedestrian collision accidents[J]. Automotive Engineering, 2022, 44(3): 385-391. (in Chinese) https://www.cnki.com.cn/Article/CJFDTOTAL-QCGC202203010.htm
[45]	HUANG X Y, CHANG L J, ZHAO H, et al. Study on craniocerebral dynamics response and helmet protective performance under the blast waves[J]. Materials & Design, 2022, 224: 111408.
[46]	CLOOTS R J, VAN DOMMELEN J, KLEIVEN S, et al. Multi-scale mechanics of traumatic brain injury: predicting axonal strains from head loads[J]. Biomechanics and Modeling in Mechanobiology, 2013, 12: 137-150. doi: 10.1007/s10237-012-0387-6
[47]	CEN H, GONG H, LIU H, et al. A comparative study on the multiscale mechanical responses of human femoral neck between the young and the elderly using finite element method[J]. Frontiers in Bioengineering and Biotechnology, 2022, 10: 893337. doi: 10.3389/fbioe.2022.893337
[48]	HODGKIN A L, HUXLEY A F. A quantitative description of membrane current and its application to conduction and excitation in nerve[J]. The Journal of Physiology, 1952, 117(4): 500-544. doi: 10.1113/jphysiol.1952.sp004764
[49]	KOCH C. Biophysics of Computation: Information Processing in Single Neurons[M]. Oxford: Oxford University Press, 2004.
[50]	TEKIEH T, SHAHZADI S, RAFII-TABAR H, et al. Are deformed neurons electrophysiologically altered? A simulation study[J]. Current Applied Physics, 2016, 16(10): 1413-1417. doi: 10.1016/j.cap.2016.07.012
[51]	CHEMIN J Y, DESJARDINS B, GALLAGHER I, et al. Mathematical Geophysics: an Introduction to Rotating Fluids and the Navier-Stokes Equations[M]. New York: Clarendon Press, 2006.
[52]	HOSSEINI-FARID M, RAMZANPOUR M, MCLEAN J, et al. A poro-hyper-viscoelastic rate-dependent constitutive modeling for the analysis of brain tissues[J]. Journal of the Mechanical Behavior of Biomedical Materials, 2020, 102: 103475. doi: 10.1016/j.jmbbm.2019.103475
[53]	BUDDAY S, SOMMER G, PAULSEN F, et al. Region- and loading-specific finite viscoelasticity of human brain tissue[J]. PAMM, 2018, 18(1): e201800169. doi: 10.1002/pamm.201800169
[54]	BUDDAY S, SAREM M, STARCK L, et al. Towards microstructure-informed material models for human brain tissue[J]. Acta Biomaterialia, 2020, 104: 53-65. doi: 10.1016/j.actbio.2019.12.030
[55]	REITER N, ROY B, PAULSEN F, et al. Insights into the microstructural origin of brain viscoelasticity: prospects for microstructure-informed constitutive modeling[J]. Journal of Elasticity, 2021, 145(8): 99-116.