Вы находитесь на странице: 1из 9

International Journal of Crashworthiness

ISSN: 1358-8265 (Print) 1754-2111 (Online) Journal homepage: https://www.tandfonline.com/loi/tcrs20

Coup-contrecoup brain injury: fluid–structure


interaction simulations

Milan Toma & Paul D. H. Nguyen

To cite this article: Milan Toma & Paul D. H. Nguyen (2019): Coup-contrecoup brain
injury: fluid–structure interaction simulations, International Journal of Crashworthiness, DOI:
10.1080/13588265.2018.1550910

To link to this article: https://doi.org/10.1080/13588265.2018.1550910

Published online: 01 Mar 2019.

Submit your article to this journal

Article views: 2

View Crossmark data

Full Terms & Conditions of access and use can be found at


https://www.tandfonline.com/action/journalInformation?journalCode=tcrs20
INTERNATIONAL JOURNAL OF CRASHWORTHINESS
https://doi.org/10.1080/13588265.2018.1550910

Coup-contrecoup brain injury: fluid–structure interaction simulations


Milan Tomaa and Paul D. H. Nguyenb
a
Department of Mechanical Engineering, College of Engineering & Computing Sciences, New York Institute of Technology, New York, NY,
USA; bPenn State College of Medicine, Hershey, PA, USA

ABSTRACT ARTICLE HISTORY


The brain can be severely injured even without the skull being fractured by the impact to the head. Received 24 May 2018
For example, when the head is stationary and struck by a moving object the brain shifts inside the Revised 2 November 2018
skull which results in injuries at point of impact and opposite the side of impact, i.e. coup and contre- Accepted 12 November 2018
coup injuries, respectively. This article presents the results of three-dimensional computational fluid–
KEYWORDS
structure interaction simulations of a frontal impact to the head using a comprehensive finite-element Coup; contrecoup; brain;
model of the head. The cerebrospinal fluid flow inside the head surrounding the brain is modelled injury; cerebrospinal
using smoothed-particle hydrodynamics. For the first time, the cerebrospinal fluid is modelled using a fluid; trauma
fluid domain. The numerical method is validated against known cadaveric experiments by comparing
the coup and contrecoup pressure responses. The results of the fluid–structure interaction analysis are
compared with those from structural only analysis. It is demonstrated that the impact to the frontal
lobe has the potential to cause injuries on both sides of the brain and brain stem. Additional high
stress values are also found on the parietal lobe. The use of fluid-structure interaction analysis provides
additional information and is more realistic.

1. Introduction as the brain rebounds, see Figure 1. Most common causes


of coup-contrecoup brain injury include circumstances
In 1981, Goldsmith’s letter to the editor states, ‘The state of
when the head jerks violently during motor vehicle acci-
knowledge concerning trauma of the human head is so
dents or in sports where baseball players are colliding dur-
scant that the community cannot agree on new and
ing the chase for a ball, football players tackling, boxers
improved criteria even though it is generally admitted that punching, but any sport that puts the head at risk of suffer-
present designations are not satisfactory’ [1]. Even decades ing a blow could cause this type of brain injury.
later, this assessment can still be considered reasonable to a The brain can be structurally divided into the cerebrum,
degree. In automobile, personal protective gear, and sport cerebellum, and brain–stem. The cerebrum is divided into
equipment safety, the head injury criterion (HIC) is a meas- two roughly equal hemispheres connected by the corpus cal-
ure of the likelihood of head injury arising from an impact. losum and a shared ventricular system. The brainstem is
The HIC is derived from the measurements of an acceler- further divided into the midbrain, pons and medulla oblon-
ometer at the centre of gravity of a crash test dummy’s gata. Cerebrospinal fluid (CSF) fills a system of cavities at
head, when the dummy is exposed to crash forces. the center of the brain, known as ventricles, and the sub-
According to the insurance institute for highway safety, an arachnoid space surrounding the brain and spinal cord
HIC value of 700 is the maximum allowed under the provi- (Figure 2). The CSF cushions the brain within the skull and
sions of the U.S. advanced airbag regulation [2], it repre- serves as a shock absorber for the central nervous
sents a 5% risk of a severe injury [3]. Generally, experts system [4].
agree that HIC values above 1000 are life threatening. This The three published constitutive models representing
still commonly used criterion is based only on the measure- CSF behaviour are the solid-like, viscoelastic, and fluid-like
ments from the accelerometer and does not provide any- CSF. However, they all are solid material models with differ-
thing beyond a percentage to assess the risk of injury. More ent material properties. The solid-like constitutive model
advanced models and numerical methods can provide the represents CSF as a linear, nearly incompressible elastic
insight into the mechanism of closed head injury and allow solid with a bulk modulus much larger than the shear
us to study the method by which trauma to the brain hap- modulus [5, 6]. The viscoelastic CSF constitutive model is a
pens inside the skull when exposed to loading conditions. linear viscoelastic model with shear relaxation behaviour [7,
Coup-contrecoup injury is dual impacting of the brain 8]. The fluid-like CSF is modelled using elastic solid mater-
into the skull; coup injury occurs at the point of impact; ial with fluid-like constitutive behaviour using an equation
countercoup injury occurs on the opposite side of impact, of state constitutive model [9].

CONTACT Milan Toma tomamil@tomamil.eu


ß 2019 Informa UK Limited, trading as Taylor & Francis Group
2 M. TOMA AND P. NGUYEN

Figure 1. Coup-contrecoup injuries, brain shifts inside the skull resulting in injuries at point of impact and away from point of impact, e.g. forehead injury can
result in additional injury to occipital area.

Figure 2. The schematic of the cerebrospinal fluid in which the brain is submerged. The 3D computational model used is designed based on this schematic.

While the significance of including CSF in the numerical pituitary gland and brainstem each have unique material
simulations has been shown [10], the current finite element properties. The patient-specific model is based on the
studies reported in the literature often lack more detailed Digital Imaging and Communications in Medicine
anatomical structures [7, 11–14]. The brain has a more (DICOM) images acquired from an online database.
complex structure than what has been described in prior Anatomical features missing in this model include the skin,
models. For example, CSF is commonly presented as exist- spinal cord, meninges and the arachnoid granulation, Figure
ing only outside of the brain, i.e. between the skull and a 2. When compared to the very short impact impulse time
single, solid mass representing the brain. Moreover, none of history used in these simulations, the CSF ow in the head
the existing models simulates the interaction between the can be neglected, too. The CSF flow is relatively slow,
CSF with actual fluid material properties and brain/skull, 0.05–0.08 m s1, i.e. during the impact impulse time history
even the newest models still use a simple (n ¼ 1) hyperelas- the CSF flows by 0.2–0.3 mm. These assumptions also make
tic material for the CSF [15]. The model used in this study the presence of the granulations negligible.
is the first fluid–structure interaction (FSI) model that uses The skull part is assigned rigid material properties with
fluid material properties to represent the CSF and includes density 1900 kg m3 [17]. Data from studies characterizing
all major anatomical features of the brain [16]. A detailed the macroscopic physical characteristics of the brain show
analysis of the CSF cushioning mechanism is useful for the that it is a viscoelastic material [18]. The cerebrum, cerebel-
treatment and prevention of brain injuries. lum, pituitary gland and brainstem are simulated using a
non-linear elastic constitutive material model with varying
material properties based from the literature [19–23]. The
2. Methods cerebrum, cerebellum, brainstem, and pituitary gland are
each composed of a different number of tetrahedral ele-
2.1. Head model
ments; 96385, 40808, 18634, 310, respectively. The CSF was
The five distinct anatomical structures used in this model modelled using the smoothed-particle hydrodynamics (SPH)
are shown in Figure 3. The skull, cerebrum, cerebellum, method with the bulk modulus of 21.9 GPa [7] and density
INTERNATIONAL JOURNAL OF CRASHWORTHINESS 3

Figure 3. The depiction of the entire head model with skull, cerebrum, cerebellum, pituitary gland and brainstem, respectively. The subarachnoid space and other
cavities are filled with fluid particles (blue dots surrounding the brain model, in the lower right corner). The entire model with half the skull is also shown
(lower left).

2.2. Loading conditions


Based on whether the head is stationary and struck by a
moving object, or is moving and strikes a stationary object,
the type of brain injury differs, according to [25]. The sta-
tionary head is usually hit by objects which are of similar
mass to the head. In this study, the scenario in Figure 1 is
used and it is assumed that the impacting object does not
penetrate the skull. Thus, local deformation of the skull in
the frontal area is not resulting in direct contact injury to
the underlying brain tissue. It has been estimated that for a
contact area of approximately 6.5 cm2 the force required to
produce a clinically significant skull fracture in the frontal
area of the cadaver skull is twice that required in the tem-
Figure 4. Impact impulse time history used to simulate the cadaveric experi- poroparietal area [26].
ments in [27] and applied to the skull in the current model. Corresponding loading conditions from cadaveric experi-
ments in [27] are used to perform the computational ana-
lysis of a frontal impact. The experiments examined the
1000 kg m3 [24]. The number of fluid particles filling the blow to the head of a seated human cadaver. The impact
subarachnoid space between the skull and brain, and other pulse history applied to the skull of the computational
cavities, is 94,690. model is shown in Figure 4.
4 M. TOMA AND P. NGUYEN

Figure 5. Coup (a) and contrecoup (b) pressure responses in cerebrospinal fluid compared to the experimental results of Nahum et al. [27].

2.3. Computer simulations as a response to the loading conditions. And, lastly, the FSI
analysis is compared with the structural analysis where, as
Fluid motion and boundary interaction calculations were
in other models from the literature, the CSF is modelled
solved with the IMPE-TUS Afea SPH SolverV (IMPETUS
R

using solid finite elements.


Afea AS, Norway), while large deformations in the solid
parts were simultaneously solved with the IMPETUS Afea
SolverV. Both the solvers use a commodity GPU for parallel
R
3.1. Validation
processing. All solid elements were fully integrated, remov-
ing the possibility of hourglass modes and element inversion The loading conditions from cadaveric experiments (Figure
that plagues the classic under-integrated elements. Both 4) applied to the frontal lobe yield corresponding coup and
fluid and solid domains and their interaction were solved contrecoup pressure responses in CSF, see Figure 5 where
with an explicit integration scheme. All simulations were both experimental [27] and computational results are shown
solved on a standard workstation. Parallel acceleration was for comparison.
achieved with a Tesla K40 GPU with 12 GB of Graphic
DDR memory and 2880 CUDA Cores. To confirm that con-
3.2. Principal stress
vergence was reached, h-refinement of the finite element
mesh was performed, and the solution was found to yield The stress values on the cerebrum resulting from the frontal
same results. Similarly, smaller number of fluid particles was impact are shown in Figure 6. The stress maxima can be
used to obtain results within 5% of the values obtained with found also on the occipital lobe which supports the experi-
the higher number of particles. The above stated number of mental observations that forehead injury can result in add-
particles, 94,690, is high considering that the volume of the itional injury to occipital area. Similar conclusion, i.e.
cavities and subarachnoid space is much smaller than rest of stresses and strains seen in both frontal and occipital lobes,
the model. This confirmed that the results are converged. is also found in other more simplified computational stud-
Our prior publication describes the SPH equations in ies [12].
greater detail [28]. The SPH method is chosen for this study Similar results, i.e. high stress values on both anterior
because traditional FSI techniques can be computationally and posterior sides, can be seen on the brain stem alone as
expensive and challenging regarding their parallelization well (Figure 7). Additionally, some areas with maximum
[29]. In order to use traditional FSI techniques, geometrical stress values are found also on the parietal lobe (Figure 8).
simplifications would need to occur, and the anatomical Moreover, here it is possible to make an additional observa-
accuracy would have to be sacrificed. Moreover, in recent tion that they only occur on the posterior aspects of
years the SPH has been increasingly used in biomedical the gyri.
applications [30]. The ventricles are structures that produce CSF, and
transport it around the cranial cavity. Large CSF pressure in
ventricles can lead to a disease called hydrocephalus which
3. Results
is the buildup of CSF in the ventricles. Inside each ventricle
In the results section, the validation is shown compared is a network of small blood vessels that continually produce
with the experimental results. Also, stress values are shown CSF by extracting the basic ingredients from the
INTERNATIONAL JOURNAL OF CRASHWORTHINESS 5

Figure 6. High values of the second deviatoric principal stress are observed in both the frontal and occipital lobes of the brain, i.e. forehead injury can result in
additional injury to occipital area.

Figure 7. High values of the second deviatoric principal stress are observed on both sides of the brain stem.

and minimum values are more localized, as shown in


Figure 10.

4. Discussion
The different layers of the brain move at different times
because each layer has a different density. Simplified com-
putational models are not able to incorporate this important
aspect. Moreover, interaction between CSF and brain gyri
Figure 8. High values of the second deviatoric principal stress are observed and sulci cannot be analysed computationally if the methods
also in the parietal lobe. However, in the parietal lobe the areas with high val- used do not model the CSF as fluid. The model used in this
ues are observed only in the posterior aspects of the gyri (schematic and
dashed ellipsoid).
study uses a comprehensive head/brain model with detailed
representation of all the parts and the computational ana-
lysis used is an FSI method with fluid properties for the
CSF. The validation of this model and the computational
cardiovascular system. The response of lateral ventricle to
method is shown comparing the coup and contrecoup pres-
head trauma is shown in Figure 9.
sure responses in CSF with the experimental results from
cadaveric experiments.
In Figure 5, where coup and contrecoup pressure
3.3. Structural analysis
responses in CSF compared to the experimental results of
When the CSF fluid domain is replaced by solid finite ele- Nahum et al. [27] are shown, it can be observed that the
ments, as it is common with the current head models from agreement with the experimental results is better in the
the literature, the locations of the principal stress maximum coup response as opposed to that in the contrecoup
6 M. TOMA AND P. NGUYEN

Figure 9. High values of the second deviatoric principal stress observed in the lateral ventricle during the contrecoup response.

Figure 10. The second deviatoric principal stress obtained using (a) FSI analysis and (b) structural analysis.

response. The contrecoup pressure response reaches slightly backwards relative to the skull the fluid particles move to
higher values compared to the experimental data because concentrate in the space between the skull and occipital lobe
the contrecoup response is secondary and therefore more to provide the cushioning effect and prevent the brain from
dependent on the patient-specific geometry used. However, impacting to the skull. At that point the moving particles
both coup and contrecoup computational pressure responses affect mostly the anterior sides of the gyri. When the brain
can be considered of good agreement with the experimental rebounds and wants to move forward relative to the skull the
measurements. fluid particles move to the space between the skull and
As discussed, if the interaction of CSF with the brain is frontal lobe to provide the cushioning effect there. At that
to be analysed the CSF has to be modeled with fluid ele- point the moving particles affect mostly the posterior side of
ments or particles and not just with fluid-like solid ele- the gyri. Other parts of the brain, such as the brain stem, are
ments. The results then have potential to show more equally affected by the coup-contrecoup injury. In Figure 7,
complex responses to the loading conditions. For example, similar results, i.e. high stress values on both anterior and
Figure 6 shows that the contrecoup stress response is preva- posterior sides of the brain stem, can be seen. Hence, it can
lent mostly in the inner areas of the two hemispheres close be concluded that the impact to the frontal lobe has the
to the edges where longitudinal fissure separates the two potential to cause injuries on both sides of the brain stem.
halves of the brain. The brain model is comprehensive con- The vasculature, spinal cord and meninges are omitted to
taining multiple parts each with detailed realistic patient- make the simulations less computationally expensive but
specific geometry. The complexity of the model enables the may be considered in future studies. A major uncertainty in
analysis of the brain down to the exact gyrus and sulcus. In the current study is the omission of cerebral vasculature
Figure 8, additional areas of high stress values can be found [31], and it is to be integrated in the next stage. Similarly,
outside the frontal and occipital lobes. However, interest- the displacement of CSF into the spinal subarachnoid space
ingly, only the posterior aspect of the gyrus seems to be is to be included. The final goal is to simulate a closed
affected. This can be explained by following the wave in the model of the entire CSF space [32].
CSF that occurs after the impact to the frontal lobe. During As mentioned above, the current head models assume
the acceleration phase when the brain wants to move that the CSF is hyperelastic solid material to simplify the
INTERNATIONAL JOURNAL OF CRASHWORTHINESS 7

calculation. In this study, for the first time, the CSF is mod- Funding
elled as an actual fluid, using SPH. For comparison, the
This study has been partially supported by New York
fluid domain has been replaced by solid elements to observe
Thoroughbred Horsemen’s Association. No benefits in any
the difference between these two approaches.
form have been or will be received from a commercial party
The comparison is shown in Figure 10. Much more local-
related directly or indirectly to the subject of this manuscript.
ized high values of principal stress can be seen in the struc-
tural analysis. Solid elements, although hyperelastic, cannot
travel back and forth to provide the cushioning effect. They Disclosure statement
provide the cushioning effect by sitting there between the
The authors declare that they have no conflict of interest.
skull and brain. The effect of CSF flow/movement cannot be
analysed using solid material for CSF.
The ventricles, i.e. structures where CSF is produced, are Ethical approval
shown to be affected as well, primarily in the anterior horn This article does not contain any studies with human participants or
of the lateral ventricle. When an injury (or illness) alters the animals performed by any of the authors.
circulation of CSF, one or more of the ventricles can
become enlarged yielding excess accumulation of CSF. A
condition in which excess CSF builds up within the ven- Data availability statement
tricles is called Hydrocephalus. Since the skull is rigid and The datasets generated during and/or analyzed during the current study
cannot expand, the pressure in the brain increases. A treat- are available from the corresponding author on reasonable request.
ment can be performed by implanting a shunt to divert the
excess CSF away from the brain. The future use of this References
model is to be focused on assessing this procedure. This
procedure cannot be studied by structural models that omit [1] Goldsmith W. Current controversies in the stipulation of head
injury criteria—letter to the editor. J Biomech. 1981;14:
the CSF or model it with solid elements. 883–884.
Other intended use of this FSI model is in assessing the [2] IIHS. 2014. Moderate overlap frontal crashworthiness evalu-
efficacy of head protective equipments. Running these simu- ation—Guidelines for rating injury measures. Technical Report.
lations with multiple competing designs of helmets and Insurance Institute for Highway Safety.
comparing the interactions between CSF and brain struc- [3] Mertz HJ, Prasad P, Irwin AL. Injury risk curves for children
and adults in frontal and rear collisions. SAE Transactions.
tures can yield useful insight into which of the designs is 1997;973318.
the best to protect the brain and all its structures. While [4] Rengachary SS, Ellenbogen RG. 2005. Principles of neurosur-
other existing models can be used for this very purpose, gery. Maryland Heights (MO): Elsevier Mosby.
only FSI model can provide the information on the inter- [5] Chen Y, Ostoja-Starzewski M. MRI-based finite element model-
ing of head trauma: spherically focusing shear waves. Acta
action between the brain structures and CSF. Mech. 2010;213:155–167.
[6] Ho J, Kleiven S. Dynamic response of the brain with vascula-
ture: a three-dimensional computational study. J Biomech.
5. Conclusion 2007;40:3006–3012.
[7] Cha MS, Dirisala V, Karami G, et al. A finite element method
This validated model, where an FSI method is used to ana-
parametric study of the dynamic response of the human brain
lyse the interaction between CSF and brain, is a step closer with different cerebrospinal fluid constitutive properties. Proc
to understanding the mechanisms of brain injuries. Closer Inst Mech Eng H: J Eng Med. 2009;223:1003–1019.
collaboration with concussion experts is necessary to find [8] Watanabe D, Yuge K, Nishimoto T, et al. Impact injury ana-
the relationship between the computational results here pre- lysis of the human head. AutoTechnology. 2007;7:34–37.
[9] Madhukar A, Chen Y, Ostoja-Starzewski M. Effect of cerebro-
sented and symptoms typical for this kind of head impact. spinal fluid modelling on spherically convergent shear waves
Concussions are typically diagnosed symptomatically. during blunt head trauma. Int J Numer Meth Biomed. Eng.
Patients may exhibit a range of symptoms, such as head- 2017;33:e2881.
ache, photophobia, tinnitus, dizziness, sleepiness, confusion [10] Vorwerk J, Clerc M, Burger M, et al. Comparison of boundary
element and finite element approaches to the EEG forward
and behavioural changes. Different area of brain affected problem. Biomed Eng/Biomed Tech. 2012;57:795.
would potentially result in different set of symptoms. The [11] Bei L, Shijie R, Haiyan L, et al. 2016. The effects of different
model and method presented in this study can predict the mesh density of the cerebrospinal fluid on the dynamic
areas affected based on the loading conditions. Therefore, responses of a 6 years old child finite element head model.
the symptoms can be predicted, too. Since the signs and Eighth International Conference on Measuring Technology and
Mechatronics Automation (ICMTMA). pp. 756–767.
symptoms of a concussion can be subtle and may not show [12] Gilchrist MD, O’Donoghue D. Simulation of the development of
up immediately, a numerical analysis of this kind could the frontal head impact injury. Comput Mech. 2000;26:229–235.
serve as a predictor for the physicians and patients who [13] Liang Z, Luo Y. A QCT-based nonsegmentation finite element
then could be warned about what symptoms they are to head model for studying traumatic brain injury. Appl Bionics
Biomech. 2015;2015:1–8.
expect and be ready for. Hence, if used in practice, it has [14] Luo Y, Li Z, Chen H. Finite-element study of cerebrospinal
the potential to contribute to early diagnosis that is import- fluid in mitigating closed head injuries. Proc Inst Mech Eng H.
ant in treatment of concussion. 2012;226:499–509.
8 M. TOMA AND P. NGUYEN

[15] Ghajari M, Hellyer PJ, Sharp DJ. Computational modelling of [25] Yanagida Y, Fujiwara S, Mizoi Y. Differences in the intracranial
traumatic brain injury predicts the location of chronic trau- pressure caused by a blow and/or a fall—experimental study
matic encephalopathy pathology. Brain. 2017;140:333–343. using physical models of the head and neck. Forensic Sci Int.
[16] Toma M, Nguyen PDH. Fluid structure interaction analysis of 1989;41:135–145.
cerebrospinal uid with a comprehensive head model subject to a [26] Nahum AM, Gatts JD, Gadd CW, et al. 1968. Impact tolerance
rapid acceleration and deceleration. Brain Inj. 2018;32:1576–1584. of the skull and face. 12th Stapp Car Crash Conference. Society
[17] Fry FJ, Barger JE. Acoustical properties of the human skull. J of Automotive Engineers, Warrendale, PA; pp. 302–316.
Acoust Soc Am. 1978;63:1576–1590. [27] Nahum AM, Smith RW, Ward CC. 1977. Intracranial
[18] Tyler WJ. The mechanobiology of brain function. Nat Rev pressure dynamics during head impact. 21st Stapp Car Crash
Neurosci. 2012;13:867–878. Conference.
[19] Barser TW, Brockway JA, Higgins LS. The density of tissues in [28] Toma M, Einstein DR, Bloodworth CH, et al. Fluid structure
and about the head. Acta Neurol Scand. 1970;46:85–92. interaction and structural analyses using a comprehensive
[20] Elkin BS, Azeloglu EU, Costa KD, et al. Mechanical heterogen- mitral valve model with 3D chordal structure. Int J Numer
eity of the rat hippocampus measured by atomic force micro- Meth Biomed Eng. 2017;33:e2815.
scope indentation. J Neurotrauma. 2007;24:812–822. [29] Toma M, Oshima M, Takagi S. Decomposition and paralleliza-
[21] Gefen A, Gefen N, Zhu Q, et al. Age-dependent changes in tion of strongly coupled fluid structure interaction linear sub-
material properties of the brain and braincase of the rat. J systems based on the Q1/P0 discretization. Comp Struct. 2016;
Neurotrauma. 2003;20:1163–1177. 173:84–94.
[22] Kruse SA, Rose GH, Glaser KJ, et al. Magnetic resonance elas- [30] Toma M. The emerging use of SPH in biomedical applications.
tography of the brain. Neuroimage. 2008;39:231–237. Signif Bioeng Biosci. 2017;1:SBB.000502.
[23] Moore SW, Sheetz MP. Biophysics of substrate interaction: [31] Linninger AA, Tangen K, Hsu CY, et al. Cerebrospinal fluid
influence on neural motility, differentiation, and repair. Dev mechanics and its coupling to cerebrovascular dynamics. Annu
Neurobiol. 2011;71:1090–1101. Rev Fluid Mech. 2016;48:219–257.
[24] Lui AC, Polis TZ, Cicutti NJ. Densities of cerebrospinal fluid [32] Sweetman B, Xenos M, Zitella L, et al. Three-dimensional com-
and spinal anaesthetic solutions in surgical patients at body putational prediction of cerebrospinal uid ow in the human
temperature. Can J Anaesth. 1998;45:297–303. brain. Comput Biol Med. 2011;41:67–75.

Вам также может понравиться