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CLINICAL STUDIES
NEUROSURGERY
DOI: 10.1227/01.NEU.0000186950.54075.3B
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VIANO
ET AL.
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CONCUSSION
cussion. Concussion is an injury with many signs and symptoms, which can have their origin in specific regions of the
brain as well as from diffuse injury. It is also a threshold injury
in the spectrum of brain injuries involving contusion, diffuse
axonal injury, and coma.
Twenty-two NFL concussions were known to interrupt brain
function, whereas an additional six cases of severe impact without injury were used to determine a threshold for loss of brain
function. Head kinematics of the helmeted Hybrid III headform
was defined by three translational and three rotational acceleration components in an anatomic, body-fixed reference frame. The
data were measured directly from the laboratory reenactment of
the head collisions and were used as input to the WSUHIM. By
defining the outer surface of the cranium as a rigid body and
applying the head kinematics at the head cg, the loading boundary conditions of the head were prescribed.
IN
PROFESSIONAL FOOTBALL
NEUROSURGERY
VIANO
ET AL.
Brain Model
Figure 2 shows the representation of the brain. It includes
cerebrum with gray and white matter, brainstem, and cerebellum (90). The right and left hemispheres of cerebrum are
connected internally by a corpus callosum. The length and
transverse diameter of the brain are 167 mm and 134 mm,
respectively. The midbrain of the brainstem is located in the
opening of the tentorium. The medulla oblongata is represented in the posterior cranial fossa just superior to the level of
the foramen magnum. The brainstem diameter measures 7
mm. The brain weighs 1.4 kg.
Subarachnoid Space
The dura mater is firmly attached to the internal surface of
the cranium. The outer layer of the arachnoid membrane
slides freely with respect to the innermost layer of the dura.
The subarachnoid space is filled with CSF. The CSF and the
arachnoid trabaculae suspend the brain in the cranium.
Several algorithms were reviewed by Al-Bsharat et al. (7) to
determine which one was the most suitable to model the CSF
layer and brain-cranium interface. The best approach was to
model the CSF with solid elements in addition to the definition
sliding interface between the dura and the CSF. The model used
a low shear modulus solid, which allowed relative displacement
between the brain and the cranium
as well as intracranial pressure to
match that obtained experimentally.
Pudenz and Shelden (128), and
Meaney (91) suggested that puresliding condition was a realistic interface for the simulation of headbrain kinematics. According to
Ueno et al. (155), separation of the
brain from the dura mater is unlikely to occur in blunt head impacts because of nearly incompressible nature of the brain tissue.
Face Model
Because the input acceleration was to the cranium, which
was assumed rigid, the face was not a factor except for its mass
in the simulations. However, for completeness, it will be described. The FE face model consists of 14 bones, two zygomatic bones in the cheek, two maxillae forming the upper jaw,
most of the side walls of the nose, and front part of the hard
palate, two palate bones forming the rest of the hard palate
and part of the floor and side walls of the nasal cavity, two
lacrimal bones (one in each eye socket or orbit), two nasal
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CONCUSSION
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PROFESSIONAL FOOTBALL
NEUROSURGERY
VIANO
ET AL.
Density
g/cc
Poissons
ratio
Falx, tentorium
1.13
0.45
E 0.0315b
CSFa
1.04
G 1.0E-06c
Ventricle
1.04
K 2.19d
Bridging Vein
1.13
0.48
0.219
Density
g/cc
Elastic modulus
Mpa
Poissons
ratio
Cortical
2.10
6000
0.25
Cancellous
1.00
560
0.30
Cartilage
1.50
30
0.45
Soft Tissue
1.10
Ligament
1.00
1.0
32
0.45
0.40
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CONCUSSION
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NEUROSURGERY
VIANO
ET AL.
Parametric Study of
Brain Responses
Whereas pressure responses validated well, the
correlation between modelpredicted relative displacements and experimental
measurements was less satisfactory at some NDT locations. Several factors may
contribute to the variations.
First, the geometry and material properties used by the
WSUHIM might be different
from those cadaver heads
tested. Therefore, it is unrealistic to expect an exact match
between experimental measurements and model predictions. Second, the model assumed a rigid cranium,
whereas the cadaver head
may deform during impact.
Third, the test setup we used
was quite complex, and thereFIGURE 4. A, comparison of the brain/cranium relative motion for two targets (a3 and p3) between model predictions and fore experimental artifacts
experimental measurements for Test 291-T1. These two targets were located at the tranverse plane through the anterior might exist. Fourth, the expercommissure and pineal body. A2 and p3 were approximately 10 mm anterior and 30 mm posterior to the cg of the head, imental methods used to derespectively. B, comparison of the brain/cranium relative motion for target a3 and p4 between model predictions and
rive material properties are
experimental measurements for Test C383-T1. C, relative displacements in the x- and z-directions observed experimentally
complex and subject to many
and from baseline model or from the 10B Model for targets a3 and p4.
influencing factors. Fifth, the
volume compliance of FE
model is assumed equal to that of water and is several orders in
relevant to the duration of collision sustained by football players.
magnitude great than that of the human (160). The last factor
The model displacements in z-direction were comparable with
alone contributes to lower brain displacements with translational
the test data in terms of magnitude. However, x-displacements
acceleration.
were under predicted by the model, and the predicted directions
A series of parametric studies was conducted to confirm the
were opposite to the direction of x-displacement seen in experisensitivity of brain response to varying viscosity defined for
mentally. The inconsistency in displacement direction may be a
the shear relaxation modulus. Three new simulations, namely,
consequence of the difference in the cg location between the
the 0.1BModel, 0.5BModel, and 10BModel, were conducted in
cadaver head and the FE model.
this parametric study using a decay constant that was 0.1 (
When displacements are compared for each NDT, the x-direction
relative displacements for anterior and posterior targets 1, 2, and 3
8 s-1), 0.5 (40 s-1), and 10 (800 s-1) times that used in the
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CONCUSSION
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FE Model Simulations
The three translational and three rotational accelerations at the cg
of the head were used as input into the WSUHIM to simulate the
game impact. By defining the cranium as a rigid body, the FE
cranium is moved in the same way as the Hybrid III in the laboratory reconstruction. The primary duration of NFL impacts was 15 to
20 ms, and the duration of the simulation was 30 ms to capture brain
displacements and deformation. Twenty-eight cases of struck players were analyzed in this study including helmet-facemask, helmethelmet, and helmet-ground impacts. Biomechanical responses in
the brain included intracranial pressure, maximum shear stress, first
principal strain, and first principal strain rate to assess the association between FE model responses and injury, signs, and symptoms
and other on-field outcomes.
VIANO
ET AL.
RESULTS
Head and Brain Responses: Example Case 124
Case 124 from the NFL game reconstructions is presented to
illustrate head and brain responses in the helmet impacts. Figure 5
shows the head dynamics measured in the Hybrid III dummy. Plots
on the left show the translational response and those on the right,
the rotational response. The primary impact causes a rise in translational acceleration to a peak in 8 ms, and the impact is essentially
over by 15 ms. This causes a delta V of 6.2 m/s and 42 mm
displacement of the head cg at 15 ms. The initial rotation is about the
z-axis and then it shifts to the y and x direction, causing a resultant
rotational velocity of 26 r/s and rotation of 110 at 15 ms. Between 15
and 25 ms, head displacement increases to 115 mm and the rotation
to 240. These responses are secondary to the momentum exchange
in the impact, but the cranium motion continues to deform the brain
because of the rapid motion.
Figure 6 shows the distortion of the brain at 15 ms and 25 ms.
The impact displaces and rotates the cranium, producing curvature in the midline between the hemispheres at 15 ms. This
focuses deformation in the midbrain at 25 ms, with substantial
distortion of brain tissues. The displacement time histories show
the lag in brain motion at the midbrain (center), particularly in
the y-displacement, which approaches 6 mm at 25 ms. The displacements under the impact point (impact) and along the axis of
loading (remote) show earlier and lower responses.
Figure 7 shows hot spots of strain and strain-rate at three times
in the impact. The early pattern occurs at 8 ms during peak head
acceleration while strain is gradually increasing in magnitude. The
hot spots are in the temporal lobe adjacent to the impact site in this
oblique lateral collision. The mid response is at 18 ms and occurs
after the primary impact. It shows a shift in hot spots to the
temporal lobe in the far side of the brain. By the late response at 22
ms, the hot spots have moved to the midbrain regions including
the fornix and Ammon. Nine of the 22 concussions showed this
specific migration of strain from the near to far temporal lobes and
then to the midbrain. When condition D was excluded, it occurred
in approximately half of the cases. All 22 concussions showed the
later strain hot spots in the regions of the fornix, midbrain, and
corpus callosum.
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CONCUSSION
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FIGURE 5. Hybrid III head dynamics for Case 124, including 3D translational and rotational acceleration of the cranium. The x, y, and z compo-
nents of the response and resultant are given. Integration gives the component translational and rotational velocities and displacements of the head.
NEUROSURGERY
VIANO
ET AL.
DISCUSSION
FIGURE 6. Deformation pattern of the FE brain elements from a superior view of the
hemispheres at 15 and 25 ms for Case 124, along with brain displacements along the axis
of impact adjacent to the contact (impact), central, and remote (contrecoup).
ring after the primary head impact and momentum transfer. This
phase of the response involves rapid displacement and rotation of
the head once the delta V and rotational velocity have occurred.
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CONCUSSION
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areas of the brain with high levels of response relative to the surrounding tissues
of the brain. They show regions of the brain with proportionally greater deformation. The arrow shows the direction of impact in the early response.
VIANO
ET AL.
Return to Play
TABLE 4. Significant t test results P < 0.10 for the occurrence of concussion versus the hybrid III
and finite element responses. Finite element brain responses are for strain and strain rates in regions
of the brain early or latea
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CONCUSSION
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TABLE 5. Significant t test results P < 0.10 for the occurrence of specific signs symptoms and outcomes from concussion versus finite
element brain responses. Finite element brain responses are strain and strain rates in regions of the brain early or latea
n
Mean
SD
Mean
SD
t test
df
0.318
78.1
0.125
40.5
Yes
12
12
0.199
54.9
0.136
24.0
2.393
1.886
26
25
0.024
0.071
40.9
No
24
64.2
35.2
2.145
26
0.042
1.99
1.97
26
26
0.057
0.060
1.783
26
0.086
Return to play
Fornix
Corpus callosumb
Strain
Strain rate
Mid-late
Mid-late
No
16
16
Loss of consciousness
Midbrain
Strain rate
Mid-late
Yes
4
Strain
Strain
Mid-late
Mid-late
Yes
10
10
Strain rate
Mid-late
Yes
6
Strain
Early
Yes
12
0.164
0.103
No
16
0.104
0.066
1.866
26
0.073
Strain
Strain
Mid-late
Mid-late
12
12
0.410
0.443
0.190
0.189
16
16
0.284
0.303
0.158
0.161
1.917
2.103
26
26
0.066
0.045
Strain
Strain
Early
Early
Yes
9
9
0.176
0.146
0.099
0.070
No
19
19
0.108
0.095
0.075
0.069
1.994
1.800
26
26
0.057
0.083
Memory problems
Fornix
Fornix and/or
midbrain
Cognitive problems
Midbrain
Cranial nerve problems
Orbito-frontal
temporal
Hypothalamus
Ammon, parahippa
Dizziness
Orbital-frontal cortex
Temporal lobe
a
b
105.8
0.334
0.491
93.8
0.150
0.210
38.6
No
18
18
No
22
0.229
0.347
63.6
0.124
0.170
36.3
TABLE 6. Significant t test results P < 0.10 for the direction of impact versus hybrid III dummy and finite element brain responses.
Finite element brain responses are strain and strain rates in regions of the brain early or latea
n
Impact directions
Midbraina
Strain rate
Mid-late
Strain
Strain
Strain rate
Strain rate
Strain rate
Mid-late
Mid-late
Early
Mid-late
Mid-late
HICa
Delta Vb
HICa
a
b
Mean
SD
A
11 83.6
50.0
B
9
38.9
12.8
9
0.477
0.153
9
0.436
0.168
9
64.2
24.1
9
72.8
27.2
9
70.4
32.4
D
2 644
122
2
8.4
0.1
D
2 644
122
Mean
SD
C
6
48.2
22.9
C
6
25.2
12.2
6
0.292
0.182
6
0.272
0.176
6
42.2
20.5
6
48.2
22.9
6
42.5
22.3
ABC
26
265
193
26
6.3
2.0
BC
15
306
228
t test
df
1.99
15
0.064
2.07
2.14
1.82
1.84
1.82
1.83
13
13
13
13
13
13
0.058
0.052
0.092
0.089
0.091
0.090
2.71
5.19
26
26
0.012
0.000
2.02
15
0.062
NEUROSURGERY
VIANO
ET AL.
after head trauma (48, 146, 164). Such lesions are a sign of
more severe injury. High strain rates in the mid-late time
frame in the corpus callosum may be related to the presence of
such white matter lesions, perhaps by direct causation. This
could explain the link between high strain rates in the corpus
callosum and the clinical marker of severity of MTBI.
The present study demonstrated a significant correlation
between high strain or strain-rates in the mid-late time frame
in the midbrain, the fornix, and the corpus callosum and
cognitive/memory problems, loss of consciousness, or interval to full functional recovery (i.e., as manifested by ability to
return to play). All of these structures are in the deep midline
brain regions. This suggests that protective devices that could
lower the mid-late time frame strain-strain rates in these midline brain regions might lessen the severity of MTBI.
Loss of Consciousness
Loss of consciousness occurs infrequently with concussion
in the NFL (118). Many authors have suggested that it is a
result of upper brainstem dysfunctions (109, 139, 142, 164).
The results of the present study confirm these earlier statements. High strain rates during the mid-late time frame in the
midbrain are statistically correlated with the occurrence of loss
of consciousness. This is most likely caused by dysfunction in
the ascending reticular activating system, which plays a major
role in the maintenance of consciousness (109, 139, 142, 164).
ysis was attention problems. This function is at least partially related to levels of arousal and alertness. Its is well
known that the ARAS arises in the midbrain and connects
with widespread areas of the limbic lobes and cerebral hemispheres, and modulates consciousness, arousal and alertness
(139, 164). Perhaps high strain and/or strain-rate in the midbrain impair the functioning of the ARAS, secondarily resulting in clinical difficulties with attention.
The midbrain is interconnected by multiple pathways to the
diencephalon, the temporal lobes, the limbic lobes, and multiple other areas of both cerebral hemispheres (139, 164). High
strain or strain-rates in the midbrain could affect some or all of
these pathways, resulting in clinically apparent dysfunction in
some or all of those other brain areas. In this way, cognitive or
memory impairments of seemingly medial temporal lobe and
medial diencephalic origin could arise secondarily to midbrain dysfunction. Another possible way to explain the correlation with midbrain strain and strain-rate is more biomechanical and less neurobiological.
Dizziness
Dizziness is a nonspecific complaint that encompasses a
wide variety of sensory experiences including lightheadedness, wooziness, faint feeling, unsteadiness, feelings of ab-
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CONCUSSION
Biomechanics
Migration of hot spots
The FE model shows a delayed response of the brain for
impact acceleration of the cranium. An early, low strain response occurs during the primary impact. This is focused to
the regions of the brain adjacent to the impact site (coup site).
Because the NFL concussion impacts are primarily oblique or
lateral, the early region of hot spot strain is in the temporal
lobe. Hot spots during the mid-response move to the opposite side on the brain from the impact loading (contrecoup
site). This is the far-side temporal lobe. Late in the response,
the hot spots move to the midbrain above the brainstem and
near midline.
This migration of hot spots is not a wave propagation
phenomena as that would occur at much shorter durations
than occur in the FE simulation. The migration appears to be
driven by the motion of the head secondary to the delta V and
during the rapid free-motion displacement and rotation of the
cranium. To our knowledge, this type of timing for the migration of strain has not been reported for concussions and offers
insights into the possible underlying mechanisms of injury
NEUROSURGERY
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related to head kinematics and the various signs and symptoms of MTBI in players.
Coup-Contrecoup Injury
Much has been written about coup-contrecoup injuries to
the brain. The classical definition of coup injuries are those
adjacent to the site of head impact and have been thought to
be related to the local deformation of the cranium and brain
directly under the impact. Contrecoup injuries have often
been restricted to brain contusions on the opposite side of the
brain in line with the axis of impact; however, the original
definition was for any brain contusions away from the direct
site of impact. There have been many theories for coup and
contrecoup injury, including wave propagation, cavitation,
and cranium deformation (26, 27, 49, 51, 111). The FE modeling offers a new mechanism for contrecoup injury associated
with rather long-duration head impacts involving helmets and
padding. This is related to the migration of relatively high
strain and strain-rate from the coup region during the primary
impact to the contrecoup regions of the brain during the rapid
motion of the cranium after the primary impact. Clearly, depending on the tolerance to strain, brain injuries can occur at
different times in the near and far temporal lobes and midbrain regions over the 30 ms brain response.
Injury Criteria
The correlation of Hybrid III responses with concussion and
not the specific signs, symptoms, and outcomes is particularly
interesting. The initial analyses showed the strongest correlation of concussion with HIC and SI. These are the traditional
measures of head injury risk that have widespread use in all
kinds of automotive, sport, and defense safety evaluations. At
the time, it was comforting to see that the risk for concussion
in the NFL could be accurately predicted by traditional measures of translational acceleration. The measurement of rotational accelerations was encouraged for research purposes,
even though there was an inherent relationship between translational and rotational acceleration (123).
Surprisingly, the Hybrid III head responses did not correlate
with any of specific signs, symptoms, and outcomes of concussion. There was no correlation with return to play, which is
arguably a good indicator of the more severely injured players. No Hybrid III measures correlated with players experiencing memory, cognitive, or somatic problems after injury.
It was interesting that strain and strain-rate responses in
specific regions of the brain and phases of the brain response
correlated with return to play, cognitive, and memory problems (Table 5). The mid-late strain and strain-rate in the midbrain, fornix, parahippocampus, Ammon horn, and corpus
callosum correlated with the more severe signs and symptoms
of concussion. These correlations imply that FE models and
tissue-level injury criteria may provide effective means of
addressing specific concussion injuries, particularly the ones
responsible for removal from play and longer recovery times.
Clearly, the prevention of memory and cognitive problems
VIANO
ET AL.
Limitations
Laboratory reconstructions
Extra effort was taken to determine the validity and accuracy of measuring the 3D impact velocity from the NFL game
video and rotational acceleration in the Hybrid III dummy
(105). However, there is an additional limitation in how realistically the response of the Hybrid III dummy simulates the
actual players head in the helmet. Although care was taken to
closely match helmet kinematics before and after the impact,
there has been no means to determine possible difference in
the head interaction with the helmet padding and face mask.
This is thought to be a small source of error but one that has
not been quantified.
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Bridging veins
The helmet impacts caused sufficient brain motion that the
FE simulation of the bridging veins was not stable in some
cases. This required the bridging vein calculation to be turned
off for several runs because of excessive deformation at the
brain insertion points. Future simulation efforts need to modify this aspect for improved, stable performance.
Vestibular effects
NEUROSURGERY
Concussion
The NFL research used a very broad and inclusive definition of concussion to capture as many possible cases as possible. From 1996 to 2001, only 7% of the concussion involved
players out 7 days, and even these most severely affected
players showed a rapid recovery of function in a few days.
Forty-nine percent of players were removed from play, which
represents another subsample of the more severely injured
players with concussion. Removal from play often involved
memory, cognition, or somatic problems that lead team physicians to prohibit return to player on the day of injury.
VIANO
ET AL.
Research Methodology
This is the first time, to our knowledge, that local deformations of the brain have been used to correlate with the signs
and symptoms of concussion. We believe there is a limitation
in not being able to validate the research methods, which
involved the integration of laboratory and analytical approaches. Each step builds upon the previous. The steps involved analysis of game video to determine impact velocity
and helmet kinematics, laboratory reconstructions using instrumented Hybrid III dummies wearing helmets, and FE
modeling of brain responses using the measured accelerations
from the laboratory tests. Time will tell how useful and valid
these observations prove to be in setting directions for the
future design of helmets and protective systems. One obvious
conclusion is that the more severe deformations of the brain
occur after the primary impact acceleration. This offers an
interesting challenge in considering safety equipment that
reduces the mid-late responses and whether interventions
applied at the end of the primary impact may influence the
more significant signs and symptoms of concussion.
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DISCLOSURE
David C. Viano, Dr. med, Ph.D., Ira R. Casson, M.D., and
Elliot J. Pellman, M.D. are members of the Mild Traumatic
Brain Injury (MTBI) Committee, National Football League,
New York, New York.
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ET AL.
APPENDIX 1A
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CONCUSSION
IN
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APPENDIX 1B
NEUROSURGERY
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ET AL.
COMMENTS
chanical forces of the injury. This work gives further evidence of the
clinical correlation of concussion, including observations of high
strain rates in deep white matter locations, which may well explain the
common symptoms of concussion including loss of consciousness,
cognitive memory problems, vertigo, and others. The issue of hot
spots, the regions of the brain adjacent to the primary impact site, is
described and further elucidated, including the phenomena of hot
spot migration, which seems to be related to rotatory injury mechanisms.
Although there are some inherent limitations of this study, as the
authors acknowledge, this is novel research using sophisticated techniques analyzing local deformations of the brain to correlate with
signs and symptoms of concussion. There was, for instance, no correlation with players ability to return to play. Irrespective of the fact
that the major mechanism of mild traumatic brain injury is thought to
be caused by diffuse forces, focal origin may also occur. This model
clearly demonstrates the deformation that occurs in these NFL impacts in a coup fashion, with transmission to remote areas, including
the mesencephalon and brainstem. The authors are to be congratulated on continuing to further explore mechanisms in injury and brain
responses to mild traumatic brain injury.
Julian E. Bailes
Morgantown, West Virginia
Alex B. Valadka
Houston, Texas