The meninges are membranous tissues that are pivotal in maintaining homeostasis of the central nervous system. Despite the importance of the cranial meninges in nervous system physiology and in head injury mechanics, our knowledge of the tissues' mechanical behavior and structural composition is limited. This systematic review analyzes the existing literature on the mechanical properties of the meningeal tissues. Publications were identified from a search of Scopus, Academic Search Complete, and Web of Science and screened for eligibility according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. The review details the wide range of testing techniques employed to date and the significant variability in the observed experimental findings. Our findings identify many gaps in the current literature that can serve as a guide for future work for meningeal mechanics investigators. The review identifies no peer-reviewed mechanical data on the falx and tentorium tissues, both of which have been identified as key structures in influencing brain injury mechanics. A dearth of mechanical data for the pia-arachnoid complex also was identified (no experimental mechanics studies on the human pia-arachnoid complex were identified), which is desirable for biofidelic modeling of human head injuries. Finally, this review provides recommendations on how experiments can be conducted to allow for standardization of test methodologies, enabling simplified comparisons and conclusions on meningeal mechanics.
Get full access to this article
View all access options for this article.
References
1.
MariebE.N. and HoehnK. (2007). Human Anatomy and Physiology. Pearson education: London, U.K.
2.
RuaR. and McGavernD.B. (2018). Advances in meningeal immunity. Trends Mol. Med. 24, 542–559.
3.
DecimoI., FumagalliG., BertonV., KramperaM., and BifariF. (2012). Meninges: from protective membrane to stem cell niche. Am. J. Stem Cells, 1, 92–105.
4.
HerissonF., FrodermannV., CourtiesG., RohdeD., SunY., VandoorneK., WojtkiewiczG.R., MassonG.S., VinegoniC., KimJ., KimD.E., WeisslederR., SwirskiF.K., MoskowitzM.A., and NahrendorfM. (2018). Direct vascular channels connect skull bone marrow and the brain surface enabling myeloid cell migration. Nat. Neurosci. 21, 1209–1217.
5.
RussoM.V., LatourL.L., and McGavernD.B. (2018). Distinct myeloid cell subsets promote meningeal remodeling and vascular repair after mild traumatic brain injury. Nat. Immunol. 19, 442–452.
6.
ColesJ.A., MyburghE., BrewerJ.M., and McMenaminP.G. (2017). Where are we?. The anatomy of the murine cortical meninges revisited for intravital imaging,, immunology, and clearance of waste from the brain. Prog. Neurobiol. 156, 107–148.
7.
KnoppU., ChristmannF., ReuscheE., and SepehrniaA. (2005). A new collagen biomatrix of equine origin versus a cadaveric dura graft for the repair of dural defects–a comparative animal experimental study. Acta Neurochir. (Wien) 147, 877–887.
8.
MirjanaP., DamirS., DamirJ., and MartinJ. (2019). Biomechanical comparison of the temporalis muscle fascia, the fascia lata, and the dura mater. J. Neurol. Surg. B Skull Base, 80, 23–30.
9.
QuagliniV. and VillaT. (2007). Mechanical properties of solvent-dehydrated bovine pericardium xenograft for dura mater repair. J. Appl. Biomater. Biomech. 5, 34–40.
10.
RothT.L., NayakD., AtanasijevicT., KoretskyA.P., LatourL.L., and McGavernD.B. (2014). Transcranial amelioration of inflammation and cell death after brain injury. Nature, 505, 223–228.
11.
MaasS.A., ErdemirA., HalloranJ.P., and WeissJ.A. (2016). A general framework for application of prestrain to computational models of biological materials. J. Mech. Behav. Biomed. Mater. 61, 499–510.
12.
GhajariM., HellyerP.J., and SharpD.J. (2017). Computational modeling of traumatic brain injury predicts the location of chronic traumatic encephalopathy pathology. Brain, 140, 333–343.
13.
YangK.H., HuJ., WhiteN.A., KingA.I., ChouC.C., and PrasadP. (2006). Development of numerical models for injury biomechanics research: a review of 50 years of publications in the Stapp Car Crash Conference. Stapp Car Crash J. 50, 429–490.
14.
MadhukarA. and Ostoja-StarzewskiM. (2019). Finite element methods in human head impact simulations: a review. Ann. Biomed. Eng. 47, 1832–1854.
15.
MacManusD.B., PierratB., MurphyJ.G., and GilchristM.D. (2017). Protection of cortex by overlying meninges tissue during dynamic indentation of the adolescent brain. Acta Biomater. 57, 384–394.
16.
PrevostT.P., JinG., de MoyaM.A., AlamH.B., SureshS., and SocrateS. (2011). Dynamic mechanical response of brain tissue in indentation in vivo, in situ, and in vitro. Acta Biomater. 7, 4090–4101.
17.
GuL.X., ChafiM.S., GanpuleS., and ChandraN. (2012). The influence of heterogeneous meninges on the brain mechanics under primary blast loading. Composites Part B Eng. 43, 3160–3166.
18.
ScottG.G., MarguliesS.S., and CoatsB. (2016). Utilizing multiple scale models to improve predictions of extra-axial hemorrhage in the immature piglet. Biomech. Model. Mechanobiol. 15, 1101–1119.
19.
HernandezF., GiordanoC., GoubranM., ParivashS., GrantG., ZeinehM., and CamarilloD. (2019). Lateral impacts correlate with falx cerebri displacement and corpus callosum trauma in sports-related concussions. Biomech. Model. Mechanobiol. 18, 631–649.
20.
HoJ., ZhouZ., LiX.G., and KleivenS. (2017). The peculiar properties of the faix and tentorium in brain injury biomechanics. J. Biomech. 60, 243–247.
21.
LuY.C., DaphalapurkarN.P., KnutsenA.K., GlaisterJ., PhamD.L., ButmanJ.A., PrinceJ.L., BaylyP.V., and RameshK.T. (2019). A 3D computational head model under dynamic head rotation and head extension validated using live human brain data, including the calx and the tentorium. Ann. Biomed. Eng. 47, 1923–1940.
22.
JacobsonS. andM. MarcusE. (2011). Neuroanatomy for the Neuroscientist. Springer.
23.
ProtasoniM., SangiorgiS., CividiniA., CuluvarisG.T., TomeiG., Dell'OrboC., RaspantiM., BalbiS., and ReguzzoniM. (2011). The collagenic architecture of human dura mater. J. Neurosurg. 114, 1723–1730.
24.
SacksM.S., HamannM.C.J., Otaño-LataS.E., and MalininT.I. (1998). Local mechanical anisotropy in human cranial dura mater allografts. J. Biomech. Eng. 120, 541.
25.
HamannM.C., SacksM.S., and MalininT.I. (1998). Quantification of the collagen fiber architecture of human cranial dura mater. J. Anat. 192 (Pt 1), 99–106.
26.
WalshD.R., LynchJ.J., O' ConnorD.T.et al. (2020). Mechanical and structural characterisation of the dural venous sinuses. Sci Rep, 10, 21763. [Epub ahead of print; DOI: 10.1038/s41598-020-78694-4].
27.
AbsintaM., HaS.K., NairG., SatiP., LucianoN.J., PalisocM., LouveauA., ZaghloulK.A., PittalugaS., KipnisJ., and ReichD.S. (2017). Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI. eLife. 6.
28.
AdeebN., MortazaviM.M., TubbsR.S., and Cohen-GadolA.A. (2012). The cranial dura mater: a review of its history, embryology, and anatomy. Childs Nervous Syst. 28, 827–837.
29.
KriewallT.J., AkkasN., BylskiD.I., MelvinJ.W., and WorkB.A. (1983). Mechanical behavior of fetal dura mater under large axisymmetric inflation. J. Biomech. Eng. 105, 71–76.
30.
Sellés de LucasV., DutelH., EvansS.E., GröningF., SharpA.C., WatsonP.J., and FaganM.J. (2018). An assessment of the role of the falx cerebri and tentorium cerebelli in the cranium of the cat (Felis silvestris catus). J. R. Soc. Interface. 15.
31.
JefferyN. (2002). Differential regional brain growth and rotation of the prenatal human tentorium cerebelli. J. Anat. 200, 135–144.
32.
ScottG.G. and CoatsB. (2015). Microstructural characterization of the pia-arachnoid complex using optical coherence tomography. IEEE Trans. Med. Imaging, 34, 1452–1459.
33.
Marín-PadillaM. and KnopmanD.S. (2011). Developmental aspects of the intracerebral microvasculature and perivascular spaces: insights into brain response to late-life diseases. J. Neuropathol. Exp. Neurol. 70, 1060–1069.
34.
FabrisG., SuarZ.M., and KurtM. (2019). Micromechanical heterogeneity of the rat pia-arachnoid complex. Acta Biomater. 100, 29–37.
35.
FrantzC., StewartK.M., and WeaverV.M. (2010). The extracellular matrix at a glance. J. Cell. Sci. 123, 4195–4200.
36.
OhtaniO. (1992). The maceration technique in scanning electron microscopy of collagen fiber frameworks: its application in the study of human livers. Arch. Histol. Cytol. 55, Suppl, 225–232.
37.
WalshD.R., RossA.M., MalijauskaiteS., FlanaganB.D., NewportD.T., McGourtyK.D., and MulvihillJ.J.E. (2018). Regional mechanical and biochemical properties of the porcine cortical meninges. Acta Biomater. 80, 237–246.
38.
McGarveyK.A., LeeJ.M., and BoughnerD.R. (1984). Mechanical suitability of glycerol-preserved human dura mater for construction of prosthetic cardiac valves. Biomaterials, 5, 109–117.
39.
van NoortR., BlackM.M., MartinT.R.P., and MeanleyS. (1981). A study of the uniaxial mechanical properties of human dura mater preserved in glycerol. Biomaterials, 2, 41–45.
40.
MaikosJ.T., EliasR.A.I., and ShreiberD.I. (2008). Mechanical properties of dura mater from the rat brain and spinal cord. J. Neurotrauma, 25, 38–51.
41.
RaiR., IwanagaJ., ShokouhiG., OskouianR.J., and TubbsR.S. (2018). The tentorium cerebelli: a comprehensive review including its anatomy, embryology, and surgical techniques. Cureus, 10, e3079–e3079.
42.
TanakaY. and TakeuchiK. (1974). Dural calification from the neurosurgical point of view. Neurol. Med. Chir. 14pt1, 5–10.
43.
TatarliN., CeylanD., CanazH., TokmakM., BayH.H., SekerA., KelesE., KilicT., and CavdarS. (2013). Falcine venous plexus within the falx cerebri: anatomical and scanning electron microscopic findings and clinical significance. Acta Neurochir. 155, 2183–2189.
44.
LeeS.-H., ShinK.-J., KohK.S., and SongW.C. (2020). Visualization of the tentorial innervation of human dura mater. J. Anat, 231, 683–689.
45.
MortazaviM.M., QuadriS.A., KhanM.A., GustinA., SuriyaS.S., HassanzadehT., FahimdaneshK.M., AdlF.H., FardS.A., TaqiM.A., ArmstrongI., MartinB.A., and TubbsR.S. (2018). Subarachnoid trabeculae: a comprehensive review of their embryology, histology, morphology, and surgical significance. World Neurosurg. 111, 279–290.
46.
BenkoN., LukeE., AlsaneaY., and CoatsB. (2020). Spatial distribution of human arachnoid trabeculae. J. Anat. 237, 275–284
47.
Zoghi-MoghadamM. and SadeghA.M. (2009). Global/local head models to analyse cerebral blood vessel rupture leading to ASDH and SAH. Comput. Methods Biomech. Biomed. Eng. 12, 1–12.
48.
ReinaM.A., LópezA., DittmannM., and De AndrésJ.A. (2015). Ultrastructure of spinal dura mater, in: Atlas of Functional Anatomy for Regional Anesthesia and Pain Medicine: Human Structure, Ultrastructure and 3D Reconstruction Images. ReinaM.A., DeJ.A. Andrés, and HadzicA., (eds). Springer International Publishing: London, U.K., pps. 411–434.
49.
FungY.C. (1998). Biomechanics: Mechanical Properties of Living Tissues. Springer-Verlag: New York, NY.
50.
RacklM. (2015). Material testing and hyperelastic material model curve fitting forOgden, Polynomial andYeoh models. www.researchgate.net/publication/312119182_Material_testing_and_hyperelastic_material_model_curve_fitting_for_Ogden_Polynomial_and_Yeoh_models (Last accessed December4, 2020).
51.
DestradeM., SaccomandiG., and SguraI. (2017). Methodical fitting for mathematical models of rubber-like materials. Proc. Royal Soc. A, 473, 20160811.
52.
RamiãoN.G., MartinsP.S., RynkevicR., FernandesA.A., BarrosoM., and SantosD.C. (2016). Biomechanical properties of breast tissue, a state-of-the-art review. Biomech. Model. Mechanobiol. 15, 1307–1323.
53.
McKeeC.T., LastJ.A., RussellP., and MurphyC.J. (2011). Indentation versus tensile measurements of young's modulus for soft biological tissues. Tissue Eng. Part, B, Rev. 17, 155–164.
54.
PorterM.M. and NiksiarP. (2018). Multidimensional mechanics: Performance mapping of natural biological systems using permutated radar charts. PLOS One, 13, e0204309.
55.
GuimarãesC.F., GasperiniL., MarquesA.P., and ReisR.L. (2020). The stiffness of living tissues and its implications for tissue engineering. Nat. Rev. Materials, 5, 351–370.
56.
BiewenerA.A. (2008). Tendons and ligaments: structure, mechanical behavior and biological function, in: Collagen: Structure and Mechanics. P, Fratzl, (ed). Springer US: Boston, MA, pps. 269–284.
57.
WilsonA.M., McGuiganM.P., SuA., and van den BogertA.J. (2001). Horses damp the spring in their step. Nature, 414, 895–899.
58.
FratzlP. (2008). Collagen: Structure and Mechanics. Springer US: Boston M.A.
59.
YangW., ShermanV.R., GludovatzB., SchaibleE., StewartP., RitchieR.O., and MeyersM.A. (2015). On the tear resistance of skin. Nat. Commun. 6, 6649–6649.
60.
JacquemoudC., Bruyere-GarnierK., and CoretM. (2007). Methodology to determine failure characteristics of planar soft tissues using a dynamic tensile test. J. Biomech. 40, 468–475.
61.
MoherD., LiberatiA., TetzlaffJ., and AltmanD.G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6, e1000097.
62.
SauleauP., LapoubleE., Val-LailletD., and MalbertC.H. (2009). The pig model in brain imaging and neurosurgery. Animal, 3, 1138–1151.
63.
HoffmannA., StoffelM.H., NitzscheB., LobsienD., SeegerJ., SchneiderH., and BoltzeJ. (2014). The ovine cerebral venous system: comparative anatomy, visualization, and implications for translational research. PLOS One, 9, e92990–e92990.
64.
BuddayS., OvaertT.C., HolzapfelG.A., SteinmannP., and KuhlE. (2020). Fifty shades of brain: a review on the mechanical testing and modeling of Brain tissue. Arch. Comput. Methods Eng, 7, 1187–1230
65.
LiX.G., SandlerH., and KleivenS. (2017). The importance of nonlinear tissue modeling in finite element simulations of infant head impacts. Biomech. Model. Mechanobiol. 16, 823-840.
66.
GalfordJ.E. and McElhaneyJ.H. (1970). A viscoelastic study of scalp, brain, and dura. J. Biomech. 3, 211–221.
67.
Wolfinbarger JrL., ZhangY., AdamB.L.T., HomsiD., GatesK., and SutherlandV. (1994). Biomechanical aspects on rehydrated freeze-dried human allograft dura mater tissues. J Appl. Biomater. 5, 265–270.
68.
DunnM.G. and SilverF.H. (1983). Viscoelastic behavior of human connective tissues: Relative contribution of viscous and elastic components. Connect. Tissue Res. 12, 59–70.
69.
De KegelD., VastmansJ., FehervaryH., DepreitereB., Vander SlotenJ., and FamaeyN. (2018). Biomechanical characterization of human dura mater. J. Mech. Behav. Biomed. Mater. 79, 122–134.
70.
ZwirnerJ., ScholzeM., WaddellJ.N., OndruschkaB., and HammerN. (2019). Mechanical properties of human dura mater in tension—an analysis at an age range of 2 to 94 years. Sci. Rep. 9, 1–11.
71.
NoortR.v., MartinT.R.P., BlackM.M., BarkerA.T., and MonteroC.G. (1981). The mechanical properties of human dura mater and the effects of storage media. Clin. Phys. Physiol. Meas. 2, 197–197.
72.
ShulyakovA.V., CenkowskiS.S., BuistR.J., and Del BigioM.R. (2011). Age-dependence of intracranial viscoelastic properties in living rats. J. Mech. Behav. Biomed. Mater. 4, 484–497.
73.
ChauvetD., CarpentierA., AllainJ.M., PolivkaM., CrepinJ., and GeorgeB. (2010). Histological and biomechanical study of dura mater applied to the technique of dura splitting decompression in Chiari type I malformation. Neurosurg. Rev. 33, 287–294.
74.
GolmanA., WickwireA., HarriganT., IwaskiwA., ArmigerR., and MerkleA. (2013). Hierarchical model validation of the falx cerebri and tentorium cerebelli. www-nrd.nhtsa.dot.gov/pdf/BIO/Proceedings/2013_41/41-3.pdf (Last accessed December4, 2020)
75.
StaquetH., FrancoisP.M., SandozB., LaporteS., DecqP., and GoutagnyS. (2020). Surface reconstruction from routine CT-scan shows large anatomical variations of falx cerebri and tentorium cerebelli. Acta Neurochir. 2020 Feb 7; Epub ahead of. print.
76.
JinX., LeeJ.B., LeungL.Y., ZhangL., YangK.H., and KingA.I. (2006). Biomechanical response of the bovine pia-arachnoid complex to tensile loading at varying strain-rates. Stapp Car Crash J. 50, 637–649.
77.
JinX., MaC., ZhangL., YangK.H., KingA.I., DongG., and ZhangJ. (2007). Biomechanical response of the bovine pia-arachnoid complex to normal traction loading at varying strain rates. Stapp Car Crash J. 51, 115–126.
78.
JinX., YangK.H., and KingA.I. (2011). Mechanical properties of bovine pia & arachnoid complex in shear. J. Biomech. 44, 467–474.
79.
AimedieuP. and GrebeR. (2004). Tensile strength of cranial pia mater: Preliminary results. J. Neurosurg. 100, 111–114.
80.
JinX., YangK.H. and KingA.I. (2011). Mechanical properties of bovine pia and arachnoid complex in shear. J. Biomech. 44, 467–474.
81.
HartmannK., SteinK.P., NeyaziB., and SandalciogluI.E. (2019). First in vivo visualization of the human subarachnoid space and brain cortex via optical coherence tomography. Ther. Adv. Neurol. Disord. 2, 1756286419843040.
82.
MacManusD.B., PierratB., MurphyJ.G., and GilchristM.D. (2017). Region and species dependent mechanical properties of adolescent and young adult brain tissue. Sci. Rep. 7, 13729–13729.
83.
HoffmanA.H., RobichaudD.R. 2nd, DuquetteJ.J., and GriggP. (2005). Determining the effect of hydration upon the properties of ligaments using pseudo Gaussian stress stimuli. J. Biomech. 38, 1636–1642.
84.
MeyerJ.P., McAvoyK.E., and JiangJ. (2013). Rehydration capacities and rates for various porcine tissues after dehydration. PLoS One, 8, e72573.
85.
VilksY.K., SaulgozisY.Z., and YansonK.A. (1975). Effect of temperature on changes of tensile stress at constant elongation in certain human soft tissues. Polymer Mech. 11, 780-784.
86.
WalshM.T., CunnaneE.M., MulvihillJ.J., AkyildizA.C., GijsenF.J.H., and HolzapfelG.A. (2014). Uniaxial tensile testing approaches for characterisation of atherosclerotic plaques. J. Biomech. 47, 793–804.
87.
HendersonJ.H., NacamuliR.P., ZhaoB., LongakerM.T., and CarterD.R. (2005). Age-dependent residual tensile strains are present in the dura mater of rats. J. R. Soc. Interface, 2, 159–167.
88.
Caro-BretelleA.S., GountsopP.N., IennyP., LegerR., CornS., BazinI., and BretelleF. (2015). Effect of sample preservation on stress softening and permanent set of porcine skin. J. Biomech. 48, 3135–3141.
89.
Müller-SchweinitzerE. (2009). Cryopreservation of vascular tissues. Organogenesis, 5, 97–104.
90.
O'LearyS.A., DoyleB.J., and McGloughlinT.M. (2013). Comparison of methods used to measure the thickness of soft tissues and their influence on the evaluation of tensile stress. J. Biomech. 46, 1955–1960.
91.
ZwirnerJ., OndruschkaB., ScholzeM., Schulze-TanzilG., and HammerN. (2019). Mechanical and morphological description of human acellular dura mater as a scaffold for surgical reconstruction. J. Mech. Behav. Biomed. Mater. 96, 38–44.
92.
ZwirnerJ., ScholzeM., OndruschkaB., and HammerN. (2019). Tissue biomechanics of the human head are altered by Thiel embalming, restricting its use for biomechanical validation. Clin. Anat. 32, 903-913.
93.
HolzapfelG.A., GasserT.C., and OgdenR.W. (2000). A new constitutive framework for arterial wall mechanics and a comparative study of material models. J. Elasticity Phys. Sci. Solids, 61, 1–48.
94.
TongeT.K., MurienneB.J., CoudrillierB., AlexanderS., RothkopfW., and NguyenT.D. (2013). Minimal preconditioning effects observed for inflation tests of planar tissues. J. Biomech. Eng. 135, 114502–114502.
95.
CooneyG.M., MoermanK.M., TakazaM., WinterD.C., and SimmsC.K. (2015). Uniaxial and biaxial mechanical properties of porcine linea alba. J. Mech. Behav. Biomed. Mater. 41, 68–82.
96.
MulvihillJ.J. and WalshM.T. (2013). On the mechanical behavior of carotid artery plaques: the influence of curve-fitting experimental data on numerical model results. Biomech. Model Mechanobiol. 12, 975–985.
97.
ZhouB., RavindranS., FerdousJ., KidaneA., SuttonM.A., and ShazlyT. (2016). Using digital image correlation to characterize local strains on vascular tissue specimens. J. Vis. Exp. 1, 53625–53625.
98.
SabooriP. and SadeghA. (2015). Histology and morphology of the brain subarachnoid trabeculae. Anat. Res. Int. 2015, 279814
99.
ScimecaM., BischettiS., LamsiraH.K., BonfiglioR., and BonannoE. (2018). Energy Dispersive X-ray (EDX) microanalysis: a powerful tool in biomedical research and diagnosis. Eur. J. Histochem. 62, 2841–2841.
100.
LiJ, ZhangJ, YoganandanN, PintarF, GennarelliT. (2007). Regional brain strains and role of falx in lateral impact-induced head rotational acceleration. Biomed. Sci. Instrument. 43, 24–29.
101.
LindN.M., MoustgaardA., JelsingJ., VajtaG., CummingP., and HansenA.K. (2007). The use of pigs in neuroscience: modeling brain disorders. Neurosci. Biobehav. Rev. 31, 728–751.
102.
RashidB., DestradeM., and GilchristM.D. (2014). Mechanical characterization of brain tissue in tension at dynamic strain rates. J. Mech. Behav. Biomed. Mater. 33, 43–54.
103.
PervinF. and ChenW.W. (2009). Dynamic mechanical response of bovine gray matter and white matter brain tissues under compression. J. Biomech. 42, 731–735.
104.
PerssonC., EvansS., MarshR., SummersJ.L., and HallR.M. (2010). Poisson's ratio and strain rate dependency of the constitutive behavior of spinal dura mater. Ann. Biomed. Eng. 38, 975–983.
105.
MoneaA.G., BaeckK., VerbekenE., VerpoestI., SlotenJ.V., GoffinJ., and DepreitereB. (2014). The biomechanical behavior of the bridging vein–superior sagittal sinus complex with implications for the mechanopathology of acute subdural haematoma. J. Mech. Behav. Biomed. Mater. 32, 155–165.
106.
MaoH.J., ZhangL.Y., JiangB.H., GenthikattiV.V., JinX., ZhuF., MakwanaR., GillA., JandirG., SinghA., and YangK.H. (2013). Development of a finite element human head model partially validated with thirty five experimental cases. J. Biomech. Eng. 135.
107.
HardyW.N., MasonM.J., FosterC.D., ShahC.S., KopaczJ.M., YangK.H., KingA.I., BishopJ., BeyM., AnderstW., and TashmanS. (2007). A study of the response of the human cadaver head to impact. Stapp Car Crash J. 51, 17–80.
108.
HardyW.N., FosterC.D., MasonM.J., YangK.H., KingA.I., and TashmanS. (2001). Investigation of head injury mechanisms using neutral density technology and high-speed biplanar X-ray. Stapp Car Crash J. 45, 337–368.
109.
MacManusD.B., MurphyJ.G., and GilchristM.D. (2018). Mechanical characterisation of brain tissue up to 35% strain at 1, 10, and 100/s using a custom-built micro-indentation apparatus. J. Mech. Behav. Biomed. Mater. 87, 256–266.
110.
QianL. and ZhaoH. (2018). Nanoindentation of soft biological materials. Micromachines. 9.
111.
CahalaneR.M. and WalshM.T. (2020). Nanoindentation of calcified and non-calcified components of atherosclerotic tissues. Exp. Mech.
112.
Centers for Disease Control and Prevention. (2003). Report to Congress on mild traumatic brain injury in the United States; steps to prevent a serious public health problem. www.cdc.gov/traumaticbraininjury/pdf/mtbireport-a.pdf (Last accessed December4, 2020).
113.
VossJ.D., ConnollyJ., SchwabK.A., and ScherA.I. (2015). Update on the epidemiology of concussion/mild traumatic brain injury. Curr. Pain Headache Rep. 19, 32–32.
114.
ZhouZ., LiX., and KleivenS. (2020). Biomechanics of acute subdural hematoma in the elderly: a fluid-structure interaction study. J. Neurotrauma, 36, 2099–2108.
115.
LiX. and KleivenS. (2018). Improved safety standards are needed to better protect younger children at playgrounds. Sci. Rep. 8, 15061–15061.
116.
ZhouZ., LiX., and KleivenS. (2019). Fluid-structure interaction simulation of the brain-skull interface for acute subdural haematoma prediction. Biomech. Model. Mechanobiol. 18, 155–173.
117.
HolzapfelG.A., MulvihillJ.J., CunnaneE.M., and WalshM.T. (2014). Computational approaches for analyzing the mechanics of atherosclerotic plaques: a review. J. Biomech. 47, 859–869.
118.
MillerL.E., UrbanJ.E., and StitzelJ.D. (2016). Development and validation of an atlas-based finite element brain model. Biomech. Model. Mechanobiol. 15, 1201–1214.
119.
GaulR.T., NolanD.R., and LallyC. (2017). Collagen fiber characterisation in arterial tissue under load using SALS. J. Mech. Behav. Biomed. Mater. 75, 359–368.
120.
ChenX., NadiarynkhO., PlotnikovS., and CampagnolaP.J. (2012). Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat. Protocols, 7, 654–669.
121.
DurgamS., SinghB., ColeS.L., BrokkenM.T., and StewartM. (2020). Quantitative assessment of tendon hierarchical structure by combined second harmonic generation and immunofluorescence microscopy. Tissue Eng. Part C Methods, 26, 253–262.
122.
FungY.C. (1967). Elasticity of soft tissues in simple elongation. Am. J. Physiol. Legacy Content, 213, 1532–1544.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
