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Home Articles Authors Reviewers About this journal My ETSMo Too Abstracto Reviewo !eight"dro m###o $luid ercuss###o %ontrolled co###o %ryogenic inj###o &ther models
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Experimental traumatic $rain in%uryC"ristiane l$ert'eissen$erger45and nna(eena Sir)n*
5%orresonding author6 %hristiane Albert"!eissenbergerAlbert7%*8'lini'#uni"wuer9burg#de
Author A:liations
4;niversity of !eurology= !
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This is an &en Access article distributed under the terms of the %reative %ommons Attribution License
-htt622creativecommons#org2licenses2by2*#?1= which ermits unrestricted use= distribution= and reroduction
in any medium= rovided the original wor' is roerly cited#
$stract
Traumatic brain injury= a leading cause of death and disability= is a result of an outside force causing
mechanical disrution of brain tissue and delayed athogenic events which collectively eacerbate the injury#
These athogenic injury rocesses are oorly understood and accordingly no eective neurorotective
treatment is available so far# Eerimental models are essential for further clariIcation of the highly comle
athology of traumatic brain injury towards the develoment of novel treatments# Among the rodent models
of traumatic brain injury the most commonly used are the weight"dro= the Juid ercussion= and the cortical
contusion injury models# As the entire sectrum of events that might occur in traumatic brain injury cannot
be covered by one single rodent model= the design and choice of a seciIc model reresents a major
challenge for neuroscientists# This review summari9es and evaluates the strengths and wea'nesses of the
currently available rodent models for traumatic brain injury#
!e#iew
Traumatic brain injury -T0K1 is a result of an outside force causing immediate mechanical disrution of brain
tissue and delayed athogenic events which collectively mediate widesread neurodegeneration -reviewed
by 41# Kt is a heterogeneous disorder that can vary in the tye of brain injury= distribution of brain damage
and mechanisms of damage -Table41# The rimary damage of brain tissue can be diuse or focal whereby
the circumstances of injury determine the relative degree to which diuse and focal trauma develos#
+rimary injury caused by direct imact to the head is considered to be largely focal= and results in cortical
contusion= vascular injury and hemorrhages accomanied by ischemia# Kn contrast= diuse brain injury
characteri9ed by diuse aonal injury is caused by acceleration2deceleration forces# ,eending uon the
nature of rimary injury= various cell resonses are triggered that can eacerbate the injury# To date= these
secondary injury rocesses are oorly understood#
Ta$le +,Leading clinical causes and tyes of T0K in the ;nited States *??* " *??@ *
T0K remains a leading cause of death and disability in the industrali9ed countries *=. and reresents a
growing health roblem also in the develoing countries B"CF therefore even a modest outcome
imrovement could have major ublic health imlications# As the immediate cell death resulting from the
initial imact on the brain tissue is irreversible= treatments focus on interrution or inhibition of the
secondary injury cascades eanding this rimary injury# >onetheless= no eective neurorotective
treatment is available so far "44# The use of animal models is essential for better understanding of the
secondary injury rocesses and for the develoment on novel theraies# Although large animal models may
be necessary to investigate seciIc asects of T0K= rodents -mice and rats1 have emerged as the mostcommonly used secies -for a review see 4*1= since they are easily available to many researchers=
normative data for a wide range of hysiological and behavioral variables in rodents are well documented
and transgenic technologies allow the generation of rodent lines with seciIc genetic alterations# A number
of mouse and rat models have been develoed to induce brain trauma# &f these the most commonly used
are weight"dro injury= Juid ercussion injury -$+K1= and cortical contusion injury -%%K1# However= the entire
sectrum of events that might occur in T0K cannot be covered by one single rodent model# Therefore= this
review evaluates the strengths and wea'nesses of the currently available rodent models for T0K -Table*1#
http://creativecommons.org/licenses/by/2.0http://www.etsmjournal.com/content/2/1/16#B1http://www.etsmjournal.com/content/2/1/16/table/T1http://www.etsmjournal.com/content/2/1/16/table/T1http://www.etsmjournal.com/content/2/1/16/table/T1http://www.etsmjournal.com/content/2/1/16/table/T1http://www.etsmjournal.com/content/2/1/16#B2http://www.etsmjournal.com/content/2/1/16#B2http://www.etsmjournal.com/content/2/1/16#B3http://www.etsmjournal.com/content/2/1/16#B3http://www.etsmjournal.com/content/2/1/16#B4http://www.etsmjournal.com/content/2/1/16#B7http://www.etsmjournal.com/content/2/1/16#B7http://www.etsmjournal.com/content/2/1/16#B8http://www.etsmjournal.com/content/2/1/16#B8http://www.etsmjournal.com/content/2/1/16#B11http://www.etsmjournal.com/content/2/1/16#B11http://www.etsmjournal.com/content/2/1/16#B12http://www.etsmjournal.com/content/2/1/16/table/T2http://www.etsmjournal.com/content/2/1/16/table/T2http://creativecommons.org/licenses/by/2.0http://www.etsmjournal.com/content/2/1/16#B1http://www.etsmjournal.com/content/2/1/16/table/T1http://www.etsmjournal.com/content/2/1/16/table/T1http://www.etsmjournal.com/content/2/1/16#B2http://www.etsmjournal.com/content/2/1/16#B2http://www.etsmjournal.com/content/2/1/16#B3http://www.etsmjournal.com/content/2/1/16#B4http://www.etsmjournal.com/content/2/1/16#B7http://www.etsmjournal.com/content/2/1/16#B8http://www.etsmjournal.com/content/2/1/16#B11http://www.etsmjournal.com/content/2/1/16#B12http://www.etsmjournal.com/content/2/1/16/table/T2 -
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Ta$le *,Eerimental rodent models of closed"head injury
'eig"tdrop models
The weight"dro models use the gravitational forces of a free falling weight to roduce a largely focal 4."4N
or diuse 4@"4O brain injury# The imact of the free falling weight is delivered to the eosed s'ull in
rat 4B and mouse *? or the intact dura in rat *4=**# !hen the imact is delivered to the eosed s'ull=
generally soft tis= e#g# silicon"covered 4Nreduce the ris' of s'ull fractures# $or inducing focal brain injury=
the animals are laced on non"Jeible latforms in order to minimi9e dissiation of energy 4."4N# Kn
contrast= crucial for inducing a diuse brain injury is an imact widely distributed over the s'ull and the use
of Jeible latforms allowing the head to accelerate= e#g# foam"tye latforms 4@=4C=4O or latforms with
elastic srings 4# The severity of head trauma can be varied by using dierent weights and2or heights of
the weight"dro# The high mortality rate due to anea can be reduced by early resiratory suort and the
usage of animals with a certain age and weight 4@=4C#
Feeney-s weig"tdrop modelTyically this rat model in which an imact is delivered to the intact dura *4=** results in a cortical
contusion with hemorrhage *. and damage of the blood"brain barrier *B=*N# KnJammatory rocesses leadto activation of microglia and astrocytes= activation of the comlement system and invasion of neutrohils
and macrohages **=*.=*N".4# ,elayed microcirculatory disturbances and cortical sreading
deression .*have also been reorted in this model# The attern of osttraumatic cell death deends on
the severity of imact ..# Although the rimary injury is largely focal= diusely distributed aonal injury has
been observed in the neuroil of the cortical lesion *.#
S"o"ami-s weig"tdrop modelShaira et al# and %hen et al#= later introduced a model for closed"head injury using a weight"dro imact to
one side of the unrotected s'ull in rat 4B and mouse 4N=*?= resectively# The injury severity in this model
is deendent on the mass and falling height of the weight used# Thus= heavier weights and2or increased
falling height roduces an isilateral cortical brain contusion and blood"brain barrier disrution followed by
brain edema= activation of the comlement system= cell death evolving over time from the contusion site and
invasion of inJammatory cells 4.=4N=*.=.B".C# A modiIed model using lighter weights and2or shorter fall
heights resulted in a concussive"li'e brain injury= bilateral cell loss= short duration of brain edema and long"
lasting cognitive deIcits*.# Moreover= bilateral diuse brain damage= cell death -bilateral and beneath the
imact site1= and inJammatory resonses were reorted ."B4# Kn general mild weight"dro injuries are
associated with a diuse injury attern whereas more severe weight"dro injuries roduce a focal contusion#
A disadvantage of the weight"dro model is the high variability of the injury severity# A major advantage of
this model is that it can be Puic'ly erformed under gas"anesthesia and thus allows neurological scoring
immediately after injury 4N=*?# Thus clinically relevant randomi9ation of animals into the various treatment
grous is ossible#
Marmarou-s weig"tdrop model ./mpact acceleration model0To model Qwhole headQ motion resulting in a diuse brain injury= Marmarou et al# 4@=4Callows the head to
accelerate at imact# ,eending on the severity of injury= the induced brain injury results in hemorrhages=neuronal cell death= astrogliosis= diuse aonal injury= and cytotoic brain edema 4C=*.=*@=B*=B.# This
imact acceleration model using a weight"dro is a useful model for investigating diuse brain injuries
ranging from mild to severe#
Ta'en together= weight"dro models rovide a straightforward way to assess brain injuries close to the
clinical conditions ranging from focal to diuse brain injuries#
Fluid percussion in%ury models
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$luid ercussion injury -$+K1 models roduce brain injury by raidly injecting Juid volumes onto the intact
dural surface through a craniotomy# The craniotomy is made either centrally -%$+= M$+1= over the sagittal
suture midway between bregma and lambda= or laterally -L$+1= over the arietal corte# Graded levels of
injury severity can be achieved by adjusting the force of the Juid ressure ulse# Li'e in various other T0K
models= a high mortality rate due to anea is evidentBB=BN#
The central -%$+1 and lateral -L$+1 Juid ercussion injury models were adated to rats in 4OCB@=BCand in
4OO B=BO= resectively# These models roduce a mied tye of brain injury# Traumatic athology includes
cortical contusion= hemorrhage and a cytotoic and2or vasogenic brain edema either tyically bilateral for
%$+ injury or isilateral for L$+ injury *.=*@=N?# The delayed rogression of brain damage is accomanied
by astrogliosis= diuse aonal injury= inJammatory events= cortical sreading deression and
neurodegeneration *.=*@=BN=N?"@4# Regardless of injury location= $+K leads to cognitive
dysfunction *.=N4=NN=@4=@* and thus it can be a useful model for osttraumatic dementia# $urthermore= $+K
delivered laterally is an aroriate model for osttraumatic eilesy @.#
The $+K model in the rat has been the most widely used model for T0K# >evertheless= for both %$+ and L$+
variability(s in injury arameters between laboratories are evident# $or instance= initial studies using L$+
detected an isilateral brain injury @B whereas some later studies detected a widesread= bilateral brain
injury @N"@C# &ne crucial factor determining the outcome severity in this model seems to be the ositioning
of the craniotomy as already a small shift in the craniotomy site is associated with mar'ed dierences inneurological outcome= lesion location and si9e@=@O# Thus= establishing a $+K model necessitates etensive
methodological Ine"tuning to obtain a standardi9ed outcome in resect to its severity and athohysiology#
&nce the $+K model is established= the induced brain trauma seems to be highly reroducible#
To enable the use of transgenic mice= %arbonell et al# BO adated the $+K model to the mouse# Similar to the
rat= the inJicted injury in mice leads to cognitive dysfunction= microglial activation and neuronal and aonal
damage *.=BO=N4=@.=C?=C4#
Controlled cortical impact in%ury model
%ontrolled cortical imact -%%K1 models utili9e a neumatic istol to deform laterally the eosed dura and
rovide controlled imact and PuantiIable biomechanical arameters# This model was adated to rat in4OO4 C* and to mouse in 4OON C. and roduces graded= reroducible brain injury#
,eendent on the severity of injury= %%K results in an isilateral injury with cortical contusion= hemorrhage
and blood"brain barrier disrution CB# >euronal cell death and degeneration= astrogliosis= microglial
activation= inJammatory events= aonal damage= cognitive deIcits= ecitotoicity and cortical sreading
deressions are reorted to ensue *.=*@=.?=C.=CN"*# +articularly with regard to brain edema= %%K is an
imortant model as it resumably causes a cytotoic and a vasogenic brain edema *.=*@=."O and thus it
reJects the clinical situation of osttraumatic brain edema formation# The redominantly focal brain injury
caused by %%K ma'es this model to a useful tool for studying the athohysiology of the secondary rocesses
induced by focal brain injury# Knterestingly= %%K in rodents is associated with osttraumatic sei9ure activity
similar to the injury"induced eilesy in humans O?=O4# Thus this model is articularly suitable to study
athomechanisms of osttraumatic eilesy#
Cryogenic in%ury model
The method of cryogenic injury in rodents O*=O. leads to a focal brain lesion# The brain injury in this model
is generally roduced by alying a cold rod to the eosed dura in rats -e#g# on the arietal corte using a
coer cylinder Illed with an miture of acetone and dry ice -"C%1 OB1 or s'ull in mice -e#g# on the
arietal corte using a coer cylinder Illed with liPuid nitrogen -"4.%1 ON1# Kn some studies= a dry ice
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ellet was directly alied to the s'ull of the rat or mouse O@=OC# ,ierent injury severities can be achieved
by varying the contact time to the eosed corte O#
Kn rodents= cortical cryogenic injury results in a focal brain lesion and brea'down of the blood"brain
barrier OB=ON# The rimary lesion is surrounded by a enumbral 9one where secondary rocesses lead to an
etension of lesion si9e accomanied by neuronal cell death and cytotoic and vasogenic edema O=OO#
These secondary rocesses also include activation of astrocytes and inJammation ON=O@=4??"4?.#
Moreover= it was reorted recently that a discrete cryogenic lesion to the arietal corte of juvenile mice
causes delayed global neurodegeneration 4?B# ,ue to eiletic activities surrounding the focal lesion= this
method is also used for mimic'ing certain asects of eilesy 4?N"4?C#
The cryogenic brain lesion model is articularly suited for investigating T0K"associated blood"brain barrier
lea'age and vasogenic brain edema# However= this focal trauma model lac's the countracou and diuse
aonal injuries that tyically comlicate human head injuries 4# Thus the cryogenic brain lesion model only
conditionally mimics the clinical situation# Although various other models reJect more realistic the
athohysiological characteristic of T0K= the cryogenic brain lesion model has one major advantage6 The
lesions caused by the cryogenic injury model are clearly circumscribed and highly reroducible in si9e=
location and athohysiological rocesses of the secondary lesion eansion at the cortical imact site# The
high reroducibility of the cortical lesion is articularly useful to screen the imact of harmacological
treatments or gene 'noc'out on secondary lesion develoment after focal brain injury#
1t"er models
Models to induce di2use $rain in%uryKn addition to the original Marmarou(s weight"dro model= various other imact acceleration models that
induce diuse brain injuries have been described in the literature# As an eamle= in one model the rat is
laced on its bac' while the head is accelerated uward by a iston 4?# The severity of injury deends on
the imact velocity of the iston# Kn another study= rats were subjected to imact acceleration head injury=
using a neumatic imact targeted to a steel disc centered onto their s'ull# The animal(s head was suorted
by a soft ad to decelerate the head after the imact 4?O# To induce moderate head concussion without
focal injury= a endulum can be used that stro'e on the s'ull midline of rats 44?#Models to induce 3ocal $rain in%uryKn an attemt to create a model of focal cerebral contusion without diuse brain injury= Shreiber et al# -4OOO1
generated cerebral contusions and associated evolving damage by a transient non"ablative vacuum ulse
alied to the eosed cerebral corte 444# &ther models designed to generate focal cortical injury inject
Juids leading to an inJammatory resonse and a rogressive cavitation 44*= aly a mechanical suction
force through the intact dura 44. or aly a stab wound 44B# Each of these models result in clearly
circumcised focal lesions and thus= similar to the cryogenic injury model= they might be helful in studies
evaluating utative treatments by monitoring the focal lesion si9e#
Models to mimic $lastinduced neurotraumaKn recent years= eosure to blast is becoming more frePuent foremost in military oulations# 0rain injuries
due to blast are caused by articles roelled by blast"force= acceleration and declaration forces and2or the
blast wave itself 44N# The non"imact blast injury ehibits an interesting athohysiology characteri9ed by
diuse cerebral brain edema= etreme hyeremia and a delayed vasosasm 44N# To investigate blast"
induced neurotrauma dierent models have been established# As an eamle= to mimic a non"imact blast"
induced neurotrauma= rodents were Ied and eosed to blast waves caused by detonation of
elosive 44@ or comressed air44C# Recently the athobiology of T0K caused by blast and the animal
models for non"imact blast injury have been recently reviewed by %erna' and >oble"Haeusslein 44N#
Com$ined and modi4ed in%ury models
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Kf no convenient model is available to address seciIc research toics= the modiIcation of already eisting
animal models might be useful# As an eamle human T0K is often induced by angular -a combination of
linear and rotational1 accelerations= e#g# T0K caused by car accidents# This clinical scenario was mimic'ed in
rats by instantly rotating the animal to reroduce rotational acceleration after it had sustained the imact
that roduced linear acceleration using the Marmarou(s weight dro model 44# Another eamle is the
Maryland model= in which /ilbourne et al# mimic'ed a frontal imact by modifying the imact"acceleration
model of Marmarou 44O# To simulate concussions in >ational $ootball League layers= a rat model was
develoed in which a neumatic ressure in the style of %%K models is used to imact laterally the helmet"
rotected head 4*?# %linical T0K is frePuently accomanied by comlications such as hyoic eisodes and
sesis# Kn order to mimic those clinical situations= they can be integrated in the study design
-hyoia4*4=4**and sesis 4*.1#
Cell culture models
%ell culture is currently the most romising alternative to animal research# The use of cell culture models
simulating T0K might be useful for certain research goals= such as high throughut drug screenings or the
assessment of the eect of trauma on individual cell tyes# The current available cell culture models include
models using disrution of various cell cultures by laceration= comression= acceleration or stretch injury
-reviewed by 4*B1#
1utlook
Knitially= the rodent models for T0K were designed to mimic closely the clinical sePuelae of human T0K# Kn this
resect= the most straightforward rodent models are the weight"dro models by Marmarou and Shohami as
they closely mimic the real life T0K# The inJicted injuries are redominantly diuse or focal in nature=
resectively# Similarly the $+K model and %%K model mimic various injury rocesses associated with human
T0K# +robably due to the ecellent reroducibility of induced brain trauma= $+K and %%K are the most widely
used rodent models for T0K# However= even small modiIcations in the eerimental design often lead to
dierences in rimary injury and hence to dierences in athobiological rocesses leading to secondaryinjury# %onsidering the heterogeneity of human T0K= scientiIc hyothesis should be tested in multile rodent
models resulting in distinct tyes of injury# Thus= models solely mimic'ing focal or diuse injury are needed#
Kn conclusion= there are numerous rodent models of T0K available= widely varying in their ability to model
athomechanisms associated with human T0K# They rovide the eerimental bac'bone for investigating T0K
athomechanisms and for the initial testing of neurorotective comounds#
Competing interests
The authors declare that they have no cometing interests#
ut"ors- contri$utions
%A! drafted the manuscrit# ALS corrected and wrote the Inal manuscrit# 0oth authors read and aroved
the Inal manuscrit#
cknowledgements
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This wor' received Inancial suort from the !ilhelm Sander $oundation -Munich= Germany1#
!e3erences
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4?# Maas AK6 europrotecti#e agents in traumatic $rain in%ury,
Expert -pin In.esti !rus*??4= +76CN."C@C#+ubMed Abstract +ublisher $ull Tet
44# $aden AK6 europrotection and traumatic $rain in%ury6 t"eoretical option or realistic
proposition,
Curr -pin Neurol*??*= +56C?C"C4*#+ubMed Abstract +ublisher $ull Tet
4*# Statler /,= en'ins L!= ,ion %E= %lar' RS= Marion ,!= /ochane' +M6 T"e simple model
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t"e $edside,
, Neurotrauma*??4= +?644ON"4*?@#+ubMed Abstract +ublisher $ull Tet
4.# Shohami E= Shaira U= %otev S6 Experimental closed "ead in%ury in rats6 prostaglandin
production in a nonin%ured @one,
Neurosurery4O= **6NO"@.# +ubMed Abstract+ublisher $ull Tet
4B# Shaira U= Shohami E= Sidi A= Soer ,= $reeman S= %otev S6 Experimental closed "ead in%ury
in rats6 mec"anical< pat"op"ysiologic< and neurologic properties,
Crit Care Med4O= +A6*N"*@N#+ubMed Abstract+ublisher $ull Tet
4N# $lierl MA= Stahel +$= 0eaucham /M= Morgan S= Smith !R= Shohami E6 Mouse closed "ead
in%ury model induced $y a weig"tdrop de#ice,
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4@# $oda MA= Marmarou A6 new model o3 di2use $rain in%ury in rats, :art //6 Morp"ological
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, Neurosur4OOB= ?76*O4".??#+ubMed Abstract +ublisher $ull Tet
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experimental model o3 di2use $rain in%ury in rats,
, 0orean Neurosur Soc*?4?= =>6C"4?# +ubMed Abstract +ublisher $ull Tet
+ubMed %entral $ull Tet
4O# Adelson +,= Robichaud += Hamilton RL= /ochane' +M6 model o3 di2use traumatic $rain
in%ury in t"e immature rat,
, Neurosur4OO@= ?56CC"B#+ubMed Abstract +ublisher $ull Tet
*?# %hen U= %onstantini S= Trembovler )= !einstoc' M= Shohami E6 n experimental model o3
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'idespread depression o3 t"e acti#ity o3 an en@yme in cortex remote 3rom a 3ocal
in%ury,
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**# $eeney ,M= 0oyeson MG= Linn RT= Murray HM= ,ail !G6 !esponses to cortical in%ury6 /,
Met"odology and local e2ects o3 contusions in t"e rat,
Brain +es4O4= *++6@C"CC#+ubMed Abstract +ublisher $ull Tet
*.# Morales ,M= Mar'lund >= Lebold ,= Thomson H= +it'anen A= Mawell !L= Longhi L= Laurer H=
Maegele M= >eugebauer E= Graham ,= Stocchetti >= McKntosh T/6 Experimental models o3
traumatic $rain in%ury6 do we really need to $uild a $etter mousetrap
Neuroscience*??N= +8A6OC4"OO#+ubMed Abstract +ublisher $ull Tet
*B# Mi'awa S= /inouchi H= /amii H= Gobbel GT= %hen S$= %arlson E= Estein %= %han +H6ttenuation
o3 acute and c"ronic damage 3ollowing traumatic $rain in%ury in copper< @inc
superoxide dismutase transgenic mice,
, Neurosur4OO@= ?56N"O4#+ubMed Abstract +ublisher $ull Tet
*N# 0ellander 0M= von Holst H= $redman += Svensson M6 cti#ation o3 t"e complement cascade
and increase o3 clusterin in t"e $rain 3ollowing a cortical contusion in t"e adult rat,
, Neurosur4OO@= ?56B@"BCN#+ubMed Abstract +ublisher $ull Tet
*@# %erna' K6 nimal models o3 "ead trauma,
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*C# Ksa'sson = Hillered L= &lsson U6 Cogniti#e and "istopat"ological outcome a3ter weig"t
drop $rain in%ury in t"e rat6 inDuence o3 systemic administration o3 monoclonal
anti$odies to /CM+,
*cta Neuropathol*??4= +7*6*B@"*N@# +ubMed Abstract+ublisher $ull Tet
*# Allen G)= Gerami ,= Esser M6 Conditioning e2ects o3 repetiti#e mild neurotrauma on
motor 3unction in an animal model o3 3ocal $rain in%ury,
Neuroscience*???= 996O."4?N# +ubMed Abstract+ublisher $ull Tet
*O# ;hl M!= 0iagas /)= Grundl +,= 0armada MA= Schiding /= >emoto EM= /ochane' +M6E2ects o3
neutropenia on edema< "istology< and cere$ral $lood Dow a3ter traumatic $rain in%ury
in rats,
, Neurotrauma4OOB= ++6.?.".4N# +ubMed Abstract +ublisher $ull Tet
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growt" 3actor 3ollowing cortical trauma,
Exp Neurol4OOB= +8764C."4CC#+ubMed Abstract +ublisher $ull Tet
.4# Holmin S= Schalling M= Hojeberg 0= >ordPvist A%= S'eftruna A/= Mathiesen T6 elayed cytokine
expression in rat $rain 3ollowing experimental contusion,
, Neurosur4OOC= ?A6BO."N?B#+ubMed Abstract +ublisher $ull Tet
.*# >ilsson += Ga9elius 0= %arlson H= Hillered L6 Continuous measurement o3 c"anges in
regional cere$ral $lood Dow 3ollowing cortical compression contusion trauma in t"e
rat,
, Neurotrauma4OO@= +86*?4"*?C# +ubMed Abstract
..# Lindh %= !ennersten A= Arnberg $= Holmin S= Mathiesen T6 i2erences in cell deat" $etween
"ig" and low energy $rain in%ury in adult rats,
*cta Neurochir 12ien3*??= +5764*@O"4*CN# +ubMed Abstract +ublisher $ull Tet
.B# ;mschwief G= Shein >A= Aleandrovich AG= Trembovler )= Horowit9 M= Shohami E6 eat
acclimation pro#ides sustained impro#ement in 3unctional reco#ery and attenuates
apoptosis a3ter traumatic $rain in%ury,
, Cere4 Blood 5lo6 Meta4*?4?= 876@4@"@*C#+ubMed Abstract +ublisher $ull Tet
.N# Shohami E= >ovi'ov M= Horowit9 M6 (ong term exposure to "eat reduces edema 3ormation
a3ter closed "ead in%ury in t"e rat,
*cta Neurochir Suppl 12ien34OOB= A76BB."BBN#+ubMed Abstract
.@# Leinhase K= Ro9ans'i M= Harhausen ,= Thurman M= Schmidt &K= Hossini AM= Taha ME= Rittirsch ,=
!ard +A= Holers )M= Ertel != Stahel +$6 /n"i$ition o3 t"e alternati#e complement acti#ation
pat"way in traumatic $rain in%ury $y a monoclonal anti3actor B anti$ody6 a
randomi@ed place$ocontrolled study in mice,
, Neuroin7ammation*??C= =64.#+ubMed Abstract 0ioMed %entral $ull Tet
+ubMed %entral $ull Tet
.C# Leinhase K= Holers )M= Thurman M= Harhausen ,= Schmidt &K= +iet9c'er M= Taha ME= Rittirsch ,=
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$rain in%ury induces expression o3 amyloid precursor protein< w"ic" may $e related to
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amyloid$eta protein in c"ronic stage o3 Duid percussion in%ury in rat $rain,
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@*# Miya9a'i S= /atayama U= Lyeth 0G= en'ins L!= ,e!itt ,S= Goldberg S= >ewlon +G= Hayes
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@.# +it'anen A= Kmmonen R= Grohn &H= /haratishvili K6 From traumatic $rain in%ury to
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@B# Smith ,H= &'iyama /= Thomas M= %laussen 0= McKntosh T/6 E#aluation o3 memory
dys3unction 3ollowing experimental $rain in%ury using t"e Morris water ma@e,
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@N# Soares H,= Thomas M= %loherty /= McKntosh T/6 e#elopment o3 prolonged 3ocal cere$ral
edema and regional cation c"anges 3ollowing experimental $rain in%ury in t"e rat,
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@@# +ierce E= Trojanows'i W= Graham ,K= Smith ,H= McKntosh T/6 /mmuno"istoc"emical
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lateral Duid percussion in%ury model are associated wit" di2erential lesion
de#elopment,
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@O# $loyd %L= Golden /M= 0lac' RT= Hamm R= Lyeth 0G6 Craniectomy position a2ects morris
water ma@e per3ormance and "ippocampal cell loss a3ter parasagittal Duid percussion,
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axonal response a3ter traumatic $rain in%ury in t"e mouse,
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C4# Sain A= ,aumas S= Lifshit9 = Rhodes = Andrews += Horsburgh /= $owler H6 Mild Fluid
:ercussion /n%ury in Mice :roduces E#ol#ing Selecti#e xonal :at"ology and Cogniti#e
e4cits !ele#ant to uman Brain /n%ury,
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C*# ,ion %E= %lifton GL= Lighthall != Uaghmai AA= Hayes RL6 controlled cortical impact model
o3 traumatic $rain in%ury in t"e rat,
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C.# Smith ,H= Soares H,= +ierce S= +erlman /G= Saatman /E= Meaney ,$= ,ion %E= McKntosh T/6
model o3 parasagittal controlled cortical impact in t"e mouse6 cogniti#e and
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CB# ,hillon HS= ,onaldson ,= ,emsey R= +rasad MR6 !egional le#els o3 3ree 3atty acids and
E#ans $lue extra#asation a3ter experimental $rain in%ury,
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CN# Griesbach GS= Sutton RL= Hovda ,A= Uing V= Gome9"+inilla $6 Controlled contusion in%ury
alters molecular systems associated wit" cogniti#e per3ormance,
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C@# Adelson +,= !halen M= /ochane' +M= Robichaud += %arlos TM6 Blood $rain $arrier
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C# 0as'aya M/= ,ogan A= Temi9 %= ,emsey R6 pplication o3 *6O."OO# +ubMed Abstract+ublisher $ull Tet
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$rain edema a3ter controlled cortical impact in%ury .CC//0,
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$rain edema 3ollowing Icontrolled cortical impact in%uryI in rats,
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pediatric posttraumatic epilepsy,
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Exp Neurol*??O= *+56*B."*N*#+ubMed Abstract +ublisher $ull Tet
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cere$ral edema and su$seHuent axonal spread to ot"er $rain regions, preliminary
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Duorescence permits t"e rapid #isuali@ation o3 nonintact cells in t"e perilesional rim
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/leinschnit9 %6 /n"i$ition o3 $radykinin receptor B+ protects mice 3rom 3ocal $rain in%ury
$y reducing $lood$rain $arrier leakage and inDammation,
http://www.etsmjournal.com/pubmed/9153635http://www.etsmjournal.com/pubmed/9153635http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=9153635http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=9153635http://www.etsmjournal.com/pubmed/10674761http://dx.doi.org/10.1089/neu.2000.17.93http://dx.doi.org/10.1089/neu.2000.17.93http://dx.doi.org/10.1089/neu.2000.17.93http://dx.doi.org/10.1089/neu.2000.17.93http://www.etsmjournal.com/pubmed/9779214http://www.etsmjournal.com/pubmed/9416293http://www.etsmjournal.com/pubmed/19520549http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19520549http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19520549http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19520549http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=19520549http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=19520549http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=19520549http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=19520549http://www.etsmjournal.com/pubmed/19013458http://www.etsmjournal.com/pubmed/19013458http://www.etsmjournal.com/pubmed/19013458http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19013458http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19013458http://www.etsmjournal.com/pubmed/7271242http://www.etsmjournal.com/pubmed/7271242http://www.etsmjournal.com/pubmed/7271242http://dx.doi.org/10.1002/ana.410090511http://dx.doi.org/10.1002/ana.410090511http://dx.doi.org/10.1002/ana.410090511http://www.etsmjournal.com/pubmed/6181647http://www.etsmjournal.com/pubmed/6181647http://dx.doi.org/10.1007/BF00685395http://dx.doi.org/10.1007/BF00685395http://dx.doi.org/10.1007/BF00685395http://www.etsmjournal.com/pubmed/17691222http://www.etsmjournal.com/pubmed/17691222http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=17691222http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=17691222http://www.etsmjournal.com/pubmed/9153635http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=9153635http://www.etsmjournal.com/pubmed/10674761http://dx.doi.org/10.1089/neu.2000.17.93http://www.etsmjournal.com/pubmed/9779214http://www.etsmjournal.com/pubmed/9416293http://www.etsmjournal.com/pubmed/19520549http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19520549http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pubmed&pubmedid=19520549http://www.etsmjournal.com/pubmed/19013458http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=19013458http://www.etsmjournal.com/pubmed/7271242http://dx.doi.org/10.1002/ana.410090511http://www.etsmjournal.com/pubmed/6181647http://dx.doi.org/10.1007/BF00685395http://www.etsmjournal.com/pubmed/17691222http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&cmd=prlinks&retmode=ref&id=17691222 -
8/9/2019 bg hasan a1
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, Cere4 Blood 5lo6 Meta4*?4?= 8764BCC"4B@#+ubMed Abstract+ublisher $ull Tet
O@# +ifarre += +rado = Giralt M= Molinero A= Hidalgo = Garcia A6 Cyclic GM: p"osp"odiesterase
in"i$ition alters t"e glial inDammatory response< reduces oxidati#e stress and cell
deat" and increases angiogenesis 3ollowing 3ocal $rain in%ury,
, Neurochem*?4?= ++*6?C"4C#+ubMed Abstract+ublisher $ull Tet
OC# Giralt M= +en'owa M= Lago >= Molinero A= Hidalgo 6 Metallot"ionein+* protect t"e CS
a3ter a 3ocal $rain in%ury,
Exp Neurol*??*= +>8644B"4*#+ubMed Abstract +ublisher $ull Tet
O# Eris'at = $urst M= Stoel M= 0aethmann A6 Correlation o3 lesion #olume and $rain swelling
3rom a 3ocal $rain trauma,
*cta Neurochir Suppl*??.= ?A6*@N"*@@# +ubMed Abstract
OO# Stoel M= 0lau %= Reinl H= 0reidt = Gersonde /= 0aethmann A= +lesnila >6 /denti4cation o3 $rain
tissue necrosis $y M!/6 #alidation $y "istomorp"ometry,
, Neurotrauma*??B= *+6C.."CB?# +ubMed Abstract +ublisher $ull Tet
4??# 0ordey A= Hablit9 = Sontheimer H6 !eacti#e astrocytes s"ow en"anced inwardly
recti3ying ; currents in situ,
Neuroreport*???= ++6.4N4".4NN#+ubMed Abstract +ublisher $ull Tet
4?4# +en'owa M= Giralt M= Lago >= %amats = %arrasco = Hernande9 = Molinero A= %ambell KL=
Hidalgo 6 strocytetargeted expression o3 /(A protects t"e CS against a 3ocal $rain
in%ury,
Exp Neurol*??.= +?+64.?"4B#+ubMed Abstract +ublisher $ull Tet
4?*# +en'owa M= Giralt M= %arrasco = Hadberg H= Hidalgo 6 /mpaired inDammatory response
and increased oxidati#e stress and neurodegeneration a3ter $rain in%ury in
interleukinAde4cient mice,
9lia*???= 8*6*C4"*N#+ubMed Abstract +ublisher $ull Tet
4?.# Wuintana A= Giralt M= Rojas S= +en'owa M= %ambell KL= Hidalgo = Molinero A6 i2erential
role o3 tumor necrosis 3actor receptors in mouse $rain inDammatory responses in
cryolesion $rain in%ury,
, Neurosci +es*??N= ?*6C?4"C4@#+ubMed Abstract +ublisher $ull Tet
4?B# Siren AL= Radyush'in /= 0oretius S= /ammer ,= Riechers %%= >att &= Sargin ,= !atanabe T=
Serling S= Michaelis T= +rice = Meyer 0= $rahm = Ehrenreich H6 Glo$al $rain atrop"y a3ter
unilateral parietal lesion and its pre#ention $y eryt"ropoietin,
Brain*??@= +*96B?"BO# +ubMed Abstract+ublisher $ull Tet
http://www.etsmjournal.com/pubmed/20197781http: