Abstract

Computational simulations of traumatic brain injury (TBI) are commonly used to advance understanding of the injury–pathology relationship, tissue damage thresholds, and design of protective equipment such as helmets. Both human and animal TBI models have developed substantially over recent decades, partially due to the inclusion of more detailed brain geometry and representation of tissues like cerebral blood vessels. Explicit incorporation of vessels dramatically affects local strain and enables researchers to investigate TBI-induced damage to the vasculature. While some studies have indicated that cerebral arteries are rate-dependent, no published experimentally based, rate-sensitive constitutive models of cerebral arteries exist. In this work, we characterize the mechanical properties of axially failed porcine arteries, both quasi-statically (0.01 s−1) and at high rate (>100 s−1), and propose a rate-sensitive model to fit the data. We find that the quasi-static and high-rate stress–stretch curves become significantly different (p < 0.05) above a stretch of 1.23. We additionally find a significant change in both failure stretch and stress as a result of strain rate. The stress–stretch curve is then modeled as a Holzapfel–Gasser–Ogden material, with a Prony series added to capture the effects of viscoelasticity. Ultimately, this paper demonstrates that rate dependence should be considered in the material properties of cerebral arteries undergoing high strain-rate deformations and provides a ready-to-use model for finite element implementation.

References

1.
Hayashi
,
T.
,
1970
, “
Brain Shear Theory of Head Injury Due to Rotational Impact
,”
J. Fac. Eng. Univ. Tokyo
,
30
, pp.
307
313
.
2.
Shugar
,
T. A.
,
Asce
,
A. M.
, and
Katona
,
M. G.
,
1975
, “
Development of Finite Element Head Injury Model
,”
J. Eng. Mech. Div.
,
101
(
3
), pp.
223
239
.10.1061/JMCEA3.0002012
3.
Ruan
,
J. S.
,
Khalil
,
T.
, and
King
,
A. I.
,
1994
, “
Dynamic Response of the Human Head to Impact by Three-Dimensional Finite Element Analysis
,”
ASME J. Biomech. Eng.
,
116
(
1
), pp.
44
50
.10.1115/1.2895703
4.
Mao
,
H.
,
Zhang
,
L.
,
Jiang
,
B.
,
Genthikatti
,
V. V.
,
Jin
,
X.
,
Zhu
,
F.
,
Makwana
,
R.
,
Gill
,
A.
,
Jandir
,
G.
,
Singh
,
A.
, and
Yang
,
K. H.
,
2013
, “
Development of a Finite Element Human Head Model Partially Validated With Thirty Five Experimental Cases
,”
ASME J. Biomech. Eng.
,
135
(
11
), p.
111002
.10.1115/1.4025101
5.
Kleiven
,
S.
,
2003
, “
Influence of Impact Direction on the Human Head in Prediction of Subdural Hematoma
,”
J. Neurotrauma
,
20
(
4
), pp.
365
379
.10.1089/089771503765172327
6.
Zhao
,
W.
, and
Ji
,
S.
,
2019
, “
White Matter Anisotropy for Impact Simulation and Response Sampling in Traumatic Brain Injury
,”
J. Neurotrauma
,
36
(
2
), pp.
250
263
.10.1089/neu.2018.5634
7.
Goriely
,
A.
,
Geers
,
M. G.
,
Holzapfel
,
G. A.
,
Jayamohan
,
J.
,
Jerusalem
,
A.
,
Sivaloganathan
,
S.
,
Squier
,
W.
,
van Dommelen
,
J. A.
,
Waters
,
S.
, and
Kuhl
,
E.
,
2015
, “
Mechanics of the Brain: Perspectives, Challenges, and Opportunities
,”
Biomech. Model Mechanobiol.
,
14
(
5
), pp.
931
965
.10.1007/s10237-015-0662-4
8.
Cloots
,
R. J.
,
van Dommelen
,
J. A.
,
Kleiven
,
S.
, and
Geers
,
M. G.
,
2013
, “
Multi-Scale Mechanics of Traumatic Brain Injury: Predicting Axonal Strains From Head Loads
,”
Biomech. Model. Mechanobiol.
,
12
(
1
), pp.
137
150
.10.1007/s10237-012-0387-6
9.
Zhang
,
L.
,
Makwana
,
R.
, and
Sharma
,
S.
,
2013
, “
Brain Response to Primary Blast Wave Using Validated Finite Element Models of Human Head and Advanced Combat Helmet
,”
Front. Neurol.
,
4
, p.
88
.10.3389/fneur.2013.00088
10.
Zhang
,
L.
,
Bae
,
J.
,
Hardy
,
W. N.
,
Monson
,
K. L.
,
Manley
,
G. T.
,
Goldsmith
,
W.
,
Yang
,
K. H.
, and
King
,
A. I.
,
2002
, “
Computational Study of the Contribution of the Vasculature on the Dynamic Response of the Brain
,”
Stapp Car Crash J.
,
46
, pp.
145
164
.10.4271/2002-22-0008
11.
Hua
,
Y.
,
Lin
,
S.
, and
Gu
,
L.
,
2015
, “
Relevance of Blood Vessel Networks in Blast-Induced Traumatic Brain Injury
,”
Comput. Math. Methods Med.
,
2015
, pp.
1
8
.10.1155/2015/928236
12.
Unnikrishnan
,
G.
,
Mao
,
H.
,
Sundaramurthy
,
A.
,
Bell
,
E. D.
,
Yeoh
,
S.
,
Monson
,
K.
, and
Reifman
,
J.
,
2019
, “
A 3-D Rat Brain Model for Blast-Wave Exposure: Effects of Brain Vasculature and Material Properties
,”
Ann. Biomed. Eng.
,
47
(
9
), pp.
2033
2044
.10.1007/s10439-019-02277-2
13.
Zhao
,
W.
, and
Ji
,
S.
,
2020
, “
Incorporation of Vasculature in a Head Injury Model Lowers Local Mechanical Strains in Dynamic Impact
,”
J. Biomech.
,
104
, p.
109732
.10.1016/j.jbiomech.2020.109732
14.
Farajzadeh Khosroshahi
,
S.
,
Yin
,
X.
,
C
,
K. D.
,
McGarry
,
A.
,
Yanez Lopez
,
M.
,
Baxan
,
N.
,
Sharp
,
D. J.
,
Sastre
,
M.
, and
Ghajari
,
M.
,
2021
, “
Multiscale Modelling of Cerebrovascular Injury Reveals the Role of Vascular Anatomy and Parenchymal Shear Stresses
,”
Sci. Rep.
,
11
(
1
), p.
12927
.10.1038/s41598-021-92371-0
15.
Hosseini-Farid
,
M.
,
Ramzanpour
,
M.
,
McLean
,
J.
,
Ziejewski
,
M.
, and
Karami
,
G.
,
2020
, “
A Poro-Hyper-Viscoelastic Rate-Dependent Constitutive Modeling for the Analysis of Brain Tissues
,”
J. Mech. Behav. Biomed. Mater.
,
102
, p.
103475
.10.1016/j.jmbbm.2019.103475
16.
Lang
,
G. E.
,
Vella
,
D.
,
Waters
,
S. L.
, and
Goriely
,
A.
,
2015
, “
Propagation of Damage in Brain Tissue: Coupling the Mechanics of Oedema and Oxygen Delivery
,”
Biomech. Model. Mechanobiol.
,
14
(
6
), pp.
1197
1216
.10.1007/s10237-015-0665-1
17.
Monson
,
K. L.
,
Converse
,
M. I.
, and
Manley
,
G. T.
,
2019
, “
Cerebral Blood Vessel Damage in Traumatic Brain Injury
,”
Clin. Biomech.
,
64
, pp.
98
113
.10.1016/j.clinbiomech.2018.02.011
18.
Bell
,
E. D.
,
Converse
,
M.
,
Mao
,
H.
,
Unnikrishnan
,
G.
,
Reifman
,
J.
, and
Monson
,
K. L.
,
2018
, “
Material Properties of Rat Middle Cerebral Arteries at High Strain Rates
,”
ASME J. Biomech. Eng.
,
140
(
7
), p.
071004
.10.1115/1.4039625
19.
Holzapfel
,
G. A.
,
Gasser
,
T. C.
, and
Ogden
,
R. W.
,
2000
, “
A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models
,”
J. Elast.
,
61
(
1/3
), pp.
1
48
.10.1023/A:1010835316564
20.
Weizsacker
,
H. W.
,
Lambert
,
H.
, and
Pascale
,
K.
,
1983
, “
Analysis of the Passive Mechanical Properties of Rat Carotid Arteries
,”
J. Biomech.
,
16
(
9
), pp.
703
715
.10.1016/0021-9290(83)90080-5
21.
Comm
,
S. T. I. S.
,
1995
,
Instrumentation for Impact Test - Part 1 - Electronic Instrumentation
,
SAE International
, Warrendale, PA.
22.
Megevand
,
P.
,
2021
, “
games_howell
,”
GitHub
, Geneva, Switzerland.
23.
Budday
,
S.
,
Sommer
,
G.
,
Holzapfel
,
G. A.
,
Steinmann
,
P.
, and
Kuhl
,
E.
,
2017
, “
Viscoelastic Parameter Identification of Human Brain Tissue
,”
J. Mech. Behav. Biomed. Mater.
,
74
, pp.
463
476
.10.1016/j.jmbbm.2017.07.014
24.
Monson
,
K. L.
,
Barbaro
,
N. M.
, and
Manley
,
G. T.
,
2008
, “
Biaxial Response of Passive Human Cerebral Arteries
,”
Ann. Biomed. Eng.
,
36
(
12
), pp.
2028
2041
.10.1007/s10439-008-9578-9
25.
Bell
,
E. D.
,
Kunjir
,
R. S.
, and
Monson
,
K. L.
,
2013
, “
Biaxial and Failure Properties of Passive Rat Middle Cerebral Arteries
,”
J. Biomech.
,
46
(
1
), pp.
91
96
.10.1016/j.jbiomech.2012.10.015
26.
Holzapfel
,
G.
,
2000
,
Nonlinear Solid Mechanics: A Continuum Approach for Engineering
,
Wiley
,
Chichester, UK
.
27.
Dassault Systèmes, 2009, “
Abaqus Analysis User's Manual
,” Dassault Systèmes, Vélizy-Villacoublay, France, accessed Dec. 14, 2021, http://130.149.89.49:2080/v6.9ef/books/usb/default.htm?startat=pt05ch19s07abm12.html
28.
Maas, S., Herron M., Weiss J., and Ateshian G., 2021, “
FEBio Theory Manual
,” FEBio Software Suite, accessed Dec. 14, 2021, https://help.febio.org/FEBioTheory/FEBio_tm_3-4-Section-5.4.html
29.
Ji
,
S.
,
Zhao
,
W.
,
Ford
,
J. C.
,
Beckwith
,
J. G.
,
Bolander
,
R. P.
,
Greenwald
,
R. M.
,
Flashman
,
L. A.
,
Paulsen
,
K. D.
, and
McAllister
,
T. W.
,
2015
, “
Group-Wise Evaluation and Comparison of White Matter Fiber Strain and Maximum Principal Strain in Sports-Related Concussion
,”
J. Neurotrauma
,
32
(
7
), pp.
441
454
.10.1089/neu.2013.3268
30.
Puso
,
M. A.
, and
Weiss
,
J. A.
,
1998
, “
Finite Element Implementation of Anisotropic Quasi-Linear Viscoelasticity Using a Discrete Spectrum
,”
ASME J. Biomech. Eng.
,
120
(
1
), pp.
62
70
.10.1115/1.2834308
31.
Kraus
,
M. A.
,
Schuster
,
M.
,
Kuntsche
,
J.
,
Siebert
,
G.
, and
Schneider
,
J.
,
2017
, “
Parameter Identification Methods for Visco- and Hyperelastic Material Models
,”
Glass Struct. Eng.
,
2
(
2
), pp.
147
167
.10.1007/s40940-017-0042-9
32.
Chalupnik
,
J. D.
,
Daly
,
C. H.
, and
Merchant
,
H. C.
,
1971
,
Material Properties of Cerebral Blood Vessels
,
University of Washington
,
Seattle
, Final Report Contract No. NIH-69-2232.
33.
Monson
,
K. L.
,
Goldsmith
,
W.
,
Barbaro
,
N. M.
, and
Manley
,
G. T.
,
2003
, “
Axial Mechanical Properties of Fresh Human Cerebral Blood Vessels
,”
ASME J. Biomech. Eng.
,
125
(
2
), pp.
288
294
.10.1115/1.1554412
34.
Marino
,
M.
,
Converse
,
M. I.
,
Monson
,
K. L.
, and
Wriggers
,
P.
,
2019
, “
Molecular-Level Collagen Damage Explains Softening and Failure of Arterial Tissues: A Quantitative Interpretation of CHP Data With a Novel Elasto-Damage Model
,”
J. Mech. Behav. Biomed. Mater.
,
97
, pp.
254
271
.10.1016/j.jmbbm.2019.04.022
35.
Hardy
,
W. N.
,
Mason
,
M. J.
,
Foster
,
C. D.
,
Shah
,
C. S.
,
Kopacz
,
J. M.
,
Yang
,
K. H.
,
King
,
A. I.
,
Bishop
,
J.
,
Bey
,
M.
,
Anderst
,
W.
, and
Tashman
,
S.
,
2007
, “
A Study of the Response of the Human Cadaver Head to Impact
,”
Stapp Car Crash J.
,
51
, pp.
17
80
.10.4271/2007-22-0002
36.
Zhao
,
W.
, and
Ji
,
S.
,
2022
, “
Cerebral Vascular Strains in Dynamic Head Impact Using an Upgraded Model With Brain Material Property Heterogeneity
,”
J. Mech. Behav. Biomed. Mater.
,
126
, p.
104967
.10.1016/j.jmbbm.2021.104967
37.
Yu
,
Y.
,
Perdikaris
,
P.
, and
Karniadakis
,
G. E.
,
2016
, “
Fractional Modeling of Viscoelasticity in 3D Cerebral Arteries and Aneurysms
,”
J. Comput. Phys.
,
323
, pp.
219
242
.10.1016/j.jcp.2016.06.038
38.
Gasser
,
T. C.
,
Ogden
,
R. W.
, and
Holzapfel
,
G. A.
,
2006
, “
Hyperelastic Modelling of Arterial Layers With Distributed Collagen Fibre Orientations
,”
J. R. Soc. Interface
,
3
(
6
), pp.
15
35
.10.1098/rsif.2005.0073
39.
Fung
,
Y.-C.
,
1993
,
Biomechanics: Mechanical Properties of Living Tissues
,
Springer-Verlag
,
New York
.
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