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Can sulci protect the brain from traumatic injury?
Johnson Ho
Ã
, Svein Kleiven
Division of Neuronic Engineering, School of Technology and Health, Royal Institute of Technology, Stockholm, Sweden
a r t i c l e i n f o
Article history:
Accepted 2 June 2009
Keywords:
Human head modelFinite element analysisCerebral convolutionTraumatic brain injury
a b s t r a c t
The influence of sulci in dynamic finite element simulations of the human head has been investigated.First, a detailed 3D FE model was constructed based on an MRI scan of a human head. A second modelwith a smoothed brain surface was created based on the same MRI scan as the first FE model. Thesemodels were validated against experimental data to confirm their human-like dynamic responsesduring impact. The validated FE models were subjected to several acceleration impulses and themaximum principle strain and strain rate in the brain were analyzed. The results suggested that theinclusion of sulci should be considered for future FE head models as it alters the strain and straindistribution in an FE model.
&
2009 Elsevier Ltd. All rights reserved.
1. Introduction
Traumatic brain injuries (TBI) is a great burden for the society,e.g. in the UK, TBI accounts for 15–20% of deaths between the ageof 5 and 35 years (Teasdale, 1995). In the US, there are about 1.4million people who sustained TBI each year and estimated onefifth of the hospitalized persons cannot return to work (Selassieet al., 2008). The same was shown in studies made in China (Wuet al., 2008) and France (Masson et al., 2001). With the help of a
finite element (FE) head model, the mechanism behind TBI suchas diffuse axonal injury (DAI) and hematoma can be studied. Withbetter understanding, these injuries can be reduced by construct-ing better protection systems and patients can leave the hospitalearlier after better treatment.During the last decade, 3D FE models have been developed byvarious researchers (Zhang et al., 2001;Horgan and Gilchrist,
2003;Kleiven, 2007). Some of these models have demonstrated
goodbiomechanicalcorrelation toexperimental data (Hardyet al.,2001;Nahum et al.,1977). Improvements in the models are madecontinuously to better predict the mechanical response of animpact to the head. The aforementioned models includedstructures such as the skull, brain, ventricles, falx, tentoriumand even bridging veins but excluded the convolutions of thecerebral cortex. The shape and size of sulci are irregular andcomplex. From a modeling point of view, it is difficult to create anFE mesh with good qualityelements to represent the convolutionsand sulci even if the topology had been successfully extractedfrom images. The elementquality is closely related tothe accuracyof the solution to an FE analysis and it is considered good when amesh consists of equilateral elements.The sulci are a network of folds that cover the surface of thebrain and the prevailing opinion is that these convolutionsprovide a larger surface for the brain to create a complex networkof neurons (Seeley et al., 2005; Ruppin et al., 1993). Since the piamater envelops the brain and exists in every sulcus, it is intuitiveto suggest that stiffness is increased tangential to the cerebralcortex. Hence, there is a need to investigate the influence of sulcion impact dynamic of the head and if there exists a significantinfluence, a convenient method to create an FE model with sulci isalso needed.There have been a few efforts to investigate the influence of sulci,suchas therecent study (Clootsetal., 2008) inwhichseveral2D FE models of a small part of the cortex with different sulcigeometry were compared to one with homogenous geometrywithout sulci. Different loading conditions were calculated basedon either the input acceleration or the output acceleration of asmall parasagittal region in a 3D FE model which were applied tothe 2D sub structural models as body forces. The stresses fromthese models were found to be different and suggested that sulcishould be included in the FE head models for more accurate injuryassessments.In another study (Bradshaw et al., 2001), 2D physical modelswith and without sulci were created to investigate the mechanismfor acute subdural hematoma and diffuse axonal injury. Inaddition, the influence of the sulci on gross cerebral motion wasstudied. The idealized sulci were placed on either side of the falxin the model, oriented radiallyat 30
1
intervals. A pendulum strucka cam connected to the model at 250mm from the center of rotation which coincided with the axis of the cylinder to generatedisplacement of the markers in the models. It was found that thesulci have an overall insignificant effect on the displacements.
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Please cite this article as: Ho, J., Kleiven, S., Can sulci protect the brain from traumatic injury? Journal of Biomechanics (2009),doi:10.1016/j.jbiomech.2009.06.051
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However, strain local to the sulci was reduced and increased inother areas. The authors also discussed that a 3D FE model cantest the insights from that study with in vivo tolerance limits.Thus, there is inconclusiveness regarding the influence of the sulcibased on these previous studies. A 3D study with detailed FEmodels having anatomical correct sulci might shed some lightinto this matter.The current study uses two detailed 3D FE models with andwithout sulci which are constructed based on an MR T1-weightedimage. The mechanical responses ofthese models arecompared inseveral impact simulations. A large number of brain trauma casesinvolve diffuse axonal injuries (DAI) which can cause complica-tions to the patients and even years of living with disability afterhospitalization (O’Connor et al., 2007). The occurrence of DAI canbepredicted bystrainin thecerebraltissue (Margulies etal.,1990)and the most commonly occurring cerebral regions for DAI are thecorpus callosum and brainstem(Gennarelli etal.,1982). Therefore,there is a special interest to compare the peak strains in thoseregions between models in the different simulations. The peakstrains in the different lobes of the brain are also compared.
2. Methods
2.1. Models
From a biomechanical perspective, FE models of the head should include theskull, cerebrospinal fluid (CSF), pia mater, falx, tentorium, gray matter, whitematterand brainstem. The skull is the most rigid part of the complexthat transfersexternal forces tothe intracranial region. The CSF is a fluid that baths the brain andkeeps the brain from hitting the skull in blunt impacts but does little to reducebrain motion relative to the skull. The falx and tentorium are parts of the duramater that divide the brain into different compartments. These membranes havemechanical properties stiffer than both the brain and pia mater (van Noort et al.,1981) and since dura mater is connected to the skull, the falx and tentoriumprovide constraint to the brain motion (Bradshaw et al., 2001). The pia materenvelopes the brain completely and has stiffer mechanical properties than thebrain (Aimedieu and Grebe, 2004). Gray matter, white matter and the brainstemhave all slightly different material properties (Arbogast and Margulies, 1997;Franceschini, 2006) but no statistically significant difference has been foundbetween white and gray matter due to individual variations. Therefore, the samematerial properties are used in this study for the gray and white matter.The geometry of the different anatomical structures were extracted from a256
Â
256
Â
156 MRIscan (Ax3D SPGR)of a healthy person, withvoxeldimensionsof 1.02
Â
1.02
Â
1.00mm
3
, taken from a GE 1.5T Signa Excite. An in-housealgorithm (Ho, 2008;Ho et al., 2009) based on expectation maximization
classification together with bias correction (van Leemput et al., 1999;Wells
et al., 1996) and skull stripping (Smith, 2002) was used for segmentation. The
classification of brain tissue and CSF of the in-house-algorithm was evaluatedusing phantom MR images with known ground truth from Brain Web (Kwan et al.,1999) and the segmentation result (Fig. 1, left) was as good as the assessment
reported in a previous study (Zaidi et al., 2006) with an accuracy of around 90% forthe brain tissue. As for the falx and tentorium which were not visible in the MR dataset, these were created manually based on the classification of the brain tissueand anatomical illustrations (Netter, 1953). With some changes in the skullstripping algorithm, the model without sulci was created. The main differencebetween the models was the surface of the brain (Fig. 1, right) while theanthropometry of the two models was almost identical and the weightof the brainmodels was around 1.2kg. The mesh of the models have an average element size of about 1mm
3
, since the displacement frequency in dynamic simulations of headimpact is around 100Hz and to minimize solution inaccuracy, the mesh shouldhave at least 10 elements per wavelength (Bradshaw and Morfey, 2001). Bothmodels were validated against experimental data of relative brain–skull motion(Hardy et al., 2001).
2.2. Material properties
The material properties of the different anatomical structures are listed below(Table 1). The skull was modeled with rigid shell elements and the brain andbrainstem as solid elements, with non-linear elastic material properties using anOgden hyperelastic constitutive model (Kleiven, 2007). The CSF was modeled as anelastic fluid. The pia mater was modeled with third-order quasilinear viscoelasticshell elements and the material model has two additive terms; a hyperelasticstress term and a viscoelastic term. The hyperelastic stress term is given by
s
e
ð
e
Þ¼
X
ki
¼
1
C
i
e
i
where
C
i
are the coefficients of the instantaneous elastic response and
e
is thestrain. The coefficients were extracted by curve fitting the result from the study byAimedieu and Grebe (2004). To obtain the coefficients of the instantaneous elasticresponse from the experimental results, the iterative least-square algorithm of Levenberg–Marquardt (MATLAB) was used to fit the stress–strain curve. Thecorrelation coefficient between the curve of the hyperelastic stress and theexperimental data was
R
¼
0.998. The comparison is shown inFig. 2.The viscoelastic term includes a relaxation function that is given by
G
ð
t
Þ¼
X
ni
¼
1
G
i
e
À
b
t
where
G
i
are the relaxation moduli and
b
i
are the time decay constants.The relaxation function of the pia mater was obtained from the experiment byWilcox et al. (2003), which studied the viscoelastic properties of dura mater.Recalling the study byAimedieu and Grebe (2004), it was found that the duramater was substantially stiffer than the pia mater in the second part of theS-shaped stress–strain curve. The resulting stiffness of both pia mater and duramater were calculated and the difference was determined to be a factor of 20.Hence,byscalingdownthe coefficients obtained fromthe duramaterbyafactorof 20 and letting the decay constants remain, the relaxation function for pia materwas estimated with appropriate stiffness.The falx and tentorium were modeled as shell elements with simplifiedrubber/foam material properties based on the experiment byvan Noort et al.(1981). This work investigated the tensile properties of several strips of humancadaver dura mater and resulted in a mean stress–strain curve.Fig. 2shows thestress–strain curve used in the model compared to the mean stress–strain curvefrom the experiment.
2.3. Validation
The FE models used in the study were validated against experimental data of relative brain–skull motion (Hardy et al., 2001), (see Supplementary data).
2.4. Impact simulations
The simulations were conducted with LS-Dyna (LSTC, 2007) using an explicitdynamic solving method. The FE models were subjected to three different loadingssimilar to that used in previous studies (Bradshaw et al., 2001;Cloots et al., 2008;
Nishimoto and Murakami, 2000). All acceleration impulses were squaredsinusoidal (sin
2
) with a duration of 5ms. The rotational pulse peaked at10,000rad/s
2
which is in the range of the proposed threshold for diffuse axonalinjuries (DAI) (Margulies and Thibault, 1992). The translational pulse had anamplitude of 100G. These impulses were applied to the skull and the strain andstrain rate (Fig. B1 in Supplementary data) in the different models were compared.
Fig. 1.
The interior of the head models (left). The surface of the brain models (right).
J. Ho, S. Kleiven / Journal of Biomechanics
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Please cite this article as: Ho, J., Kleiven, S., Can sulci protect the brain from traumatic injury? Journal of Biomechanics (2009),doi:10.1016/j.jbiomech.2009.06.051
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3. Results
3.1. Influence of sulci
The brain in the models is divided into different regions asdepicted inFig. 3. The peak maximum principal strains (MPS) arelisted by region and compared between the model without sulciand themodelwithsulciinFig.4.Sincecurrent modelsarewithoutsulci, the strain values from a model without sulci will be used asthe reference value when calculating the percentage difference.In the translational acceleration simulations, the strain in thebrain stem and corpus callosum was reduced in the model withsulci by 9% and 18%, respectively. In other regions, the reductionswere between 9% and 28% and the highest difference was found inthe frontal lobe.In the coronal rotational acceleration simulations, the strainwas reduced in all regions except in the cerebellum and parietallobe. In the parietal lobe, the strain was increased by about 16%.The strain in the corpus callosumwas reduced by about 18% whileno differencewas foundatall for thebrainstem. In otherareas, thestrain differences were lower than 6%. The strain distribution on acoronal cross-section of this simulation is shown inFig. 5anddistinct maxima can be seen in the white tissue adjacent to thesulci.Forthesagittalrotationalaccelerationsimulations,thereductionwas 6% in the brain stem and 19% in the corpus callosum whilereductions for the rest of the brain ranged from 4% to 48%. Onceagain,thebiggestdifferencewasinthefrontallobe.Onthecontrary,the peak strain in the parietal lobe was higher in the model withsulci. The strain distribution on a parasagittal cross-section of thissimulation is shown inFig. 6, also in this loading direction, strainmaxima was found in the white tissue adjacent to the sulci.
4. Discussion
The findings in this study indicated that the sulci wouldinfluence the biomechanical response of an FE head model in
Table 1
Material properties used for the head models.
Tissue
Material constants
Density (kg/dm
3
)
Poisson’s ratio
Skull
E
¼
15.0GPa 2.00 0.22Brain
a
1
¼
10.1,
m
1
¼
53.8Pa,
a
2
¼À
12.9,
m
2
¼À
120.4Pa 1.04
$
0.5Brain stem
a
1
¼
28.1,
m
1
¼
15.8Pa,
a
2
¼À
29.5,
m
2
¼À
106.8Pa 1.04
$
0.5Cerebrospinal fluid
K
¼
C
1
¼
4.84E5,
C
2
¼
0.00,
C
3
¼
6.86E7Pa 1.13 N/A
E
¼
Young’s modulus;
K
¼
bulk modulus; N/A
¼
not applicable.
Fig. 2.
Fitting of the coefficients of the instantaneous elastic response to the study by (Aimedieu and Grebe, 2004) (left). Comparison between the curve used as materialdata and the mean stress strain curve of the experiment (van Noort et al., 1981) (right).
Fig. 3.
The different lobes of the brain, brain stem and cerebellum in the two models.
J. Ho, S. Kleiven / Journal of Biomechanics
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Please cite this article as: Ho, J., Kleiven, S., Can sulci protect the brain from traumatic injury? Journal of Biomechanics (2009),doi:10.1016/j.jbiomech.2009.06.051
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