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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

    4# Gaet9 M6 T"e neurop"ysiology o3 $rain in%ury,

    Clin Neurophysiol*??B= ++56B"4# +ubMed Abstract+ublisher $ull Tet

    *# ,ivision of Knjury Resonse= >ational %enter for Knjury +revention and %ontrol %enters for ,isease

    %ontrol and +revention= ;#S ,eartment of Health and Human Services6

    Traumatic Brain Injury in the United States: Emerency !epartment "isits# $ospitali%ations# and

    !eaths# ''('')# *tlanta# *?4?#

    .# Maegele M= Engel ,= 0ouillon 0= Lefering R= $ach H= Raum M= 0uchheister 0= Schaefer ;= /lug >=

    >eugebauer E6 /ncidence and outcome o3 traumatic $rain in%ury in an ur$an area in

    'estern Europe o#er +7 years,

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    +ubMed %entral $ull Tet

    @# %hiu !T= Huang S= Tsai SH= Lin != Tsai M,= Lin T= Huang !%6 T"e impact o3 time=? Bra@ilian patients 3rom Florianopolis City,

    , Trauma*??O= A>6N"O?#+ubMed Abstract +ublisher $ull Tet

    # 3iong U= Mahmood A= %ho M6 Emerging treatments 3or traumatic $rain in%ury,

    Expert -pin Emer !rus*??O= +=6@C"B# +ubMed Abstract+ublisher $ull Tet

    +ubMed %entral $ull Tet

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    3uture,

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    Neurosurery4O= **6NO"@.# +ubMed Abstract+ublisher $ull Tet

    4B# Shaira U= Shohami E= Sidi A= Soer ,= $reeman S= %otev S6 Experimental closed "ead in%ury

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    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

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    Nat /rotoc*??O= =64.*"4..C#+ubMed Abstract +ublisher $ull Tet

    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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    , 0orean Neurosur Soc*?4?= =>6C"4?# +ubMed Abstract +ublisher $ull Tet

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    , Neurosur4OO@= ?56CC"B#+ubMed Abstract +ublisher $ull Tet

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    , Neurotrauma4OO@= +86NNC"N@# +ubMed Abstract +ublisher $ull Tet

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    in%ury,

    Brain +es4O4= *++6CO"O#+ubMed Abstract +ublisher $ull Tet

    **# $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

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    , Neurotrauma4OOB= ++6.?.".4N# +ubMed Abstract +ublisher $ull Tet

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    .?# ,e/os'y ST= Goss R= Miller +,= Styren S,= /ochane' +M= Marion ,6 pregulation o3 ner#e

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    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

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    *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

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    , 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

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    .@# 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

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    N# Mc>amara /%= Lisembee AM= Lifshit9 6 T"e '"isker uisance Task /denti4es a (ate 1nset6@ON"C?@# +ubMed Abstract +ublisher $ull Tet

    NO# Myer ,= Gur'o GG= Lee SM= Hovda ,A= Sofroniew M)6 Essential protecti#e roles o3 reacti#e

    astrocytes in traumatic $rain in%ury,

    Brain*??@= +*96*C@4"*CC*# +ubMed Abstract+ublisher $ull Tet

    @?# Mura'ami >= Uama'i T= Kwamoto U= Sa'a'ibara T= /obori >= $ushi'i S= ;eda S6Experimental

    $rain in%ury induces expression o3 amyloid precursor protein< w"ic" may $e related to

    neuronal loss in t"e "ippocampus,

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    @4# Hoshino S= Tamao'a A= Ta'ahashi M= /obayashi S= $uru'awa T= &a'i U= Mori &= Matsuno S= Shoji S=

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    amyloid$eta protein in c"ronic stage o3 Duid percussion in%ury in rat $rain,

    Neuroreport4OO= 964CO"4.#+ubMed Abstract +ublisher $ull Tet

    @*# Miya9a'i S= /atayama U= Lyeth 0G= en'ins L!= ,e!itt ,S= Goldberg S= >ewlon +G= Hayes

    RL6 Enduring suppression o3 "ippocampal longterm potentiation 3ollowing traumatic

    $rain in%ury in rat,

    Brain +es4OO*= 5?56..N"..O#+ubMed Abstract +ublisher $ull Tet

    @.# +it'anen A= Kmmonen R= Grohn &H= /haratishvili K6 From traumatic $rain in%ury to

    posttraumatic epilepsy6 w"at animal models tell us a$out t"e process and treatment

    options,

    Epilepsia*??O= 57-Sul *16*4"*O# +ubMed Abstract +ublisher $ull Tet

    @B# Smith ,H= &'iyama /= Thomas M= %laussen 0= McKntosh T/6 E#aluation o3 memory

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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

    c"aracteri@ation o3 alterations in t"e distri$ution o3 amyloid precursor proteins and

    $etaamyloid peptide a3ter experimental $rain in%ury in t"e rat,

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    @C# Smith ,H= Lowenstein ,H= Gennarelli TA= McKntosh T/6 :ersistent memory dys3unction is

    associated wit" $ilateral "ippocampal damage 3ollowing experimental $rain in%ury,

    Neurosci 8ett4OOB= +A?64N4"4NB#+ubMed Abstract+ublisher $ull Tet

    @# )in' R= Mullins +G= Temle M,= 0ao != $aden AK6 Small s"i3ts in craniotomy position in t"e

    lateral Duid percussion in%ury model are associated wit" di2erential lesion

    de#elopment,

    , Neurotrauma*??4= +?6.O"BC# +ubMed Abstract +ublisher $ull Tet

    @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,

    , Neurotrauma*??*= +96.?.".4@# +ubMed Abstract +ublisher $ull Tet

    C?# %arbonell !S= Grady MS6 !egional and temporal c"aracteri@ation o3 neuronal< glial< and

    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,

    , Neurotrauma*?4?#+ubMed Abstract +ublisher $ull Tet

    C*# ,ion %E= %lifton GL= Lighthall != Uaghmai AA= Hayes RL6 controlled cortical impact model

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    C.# Smith ,H= Soares H,= +ierce S= +erlman /G= Saatman /E= Meaney ,$= ,ion %E= McKntosh T/6

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    "istopat"ologic e2ects,

    , Neurotrauma4OON= +*64@O"4C# +ubMed Abstract +ublisher $ull Tet

    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,

    , Neurosci +es*??O= ?>6CON"?N#+ubMed Abstract +ublisher $ull Tet+ubMed %entral $ull Tet

    C@# Adelson +,= !halen M= /ochane' +M= Robichaud += %arlos TM6 Blood $rain $arrier

    permea$ility and acute inDammation in two models o3 traumatic $rain in%ury in t"e

    immature rat6 a preliminary report,

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    @# 0as'aya M/= Rao AM= ,ogan A= ,onaldson ,= ,emsey R6 T"e $ip"asic opening o3 t"e

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    Neurosci 8ett4OOC= **A6..".@#+ubMed Abstract +ublisher $ull Tet

    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,

    *cta Neurochir Suppl4OO= >+6.?.".?N# +ubMed Abstract

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    $rain edema 3ollowing Icontrolled cortical impact in%uryI in rats,

    *cta Neurochir Suppl4OOC= >764?@"4?# +ubMed Abstract

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    pediatric posttraumatic epilepsy,

    Epilepsy +es*??O= ?A6**4"**.# +ubMed Abstract +ublisher $ull Tet+ubMed %entral $ull Tet

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    Exp Neurol*??O= *+56*B."*N*#+ubMed Abstract +ublisher $ull Tet

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    *cta Neuropathol4O*= 5>6*.."*.N# +ubMed Abstract+ublisher $ull Tet

    OB# Ra'os G= /is V= >agy ,= Lur G= $ar'as T= Hortobagyi T= )ecsei L= Toldi 6 E#ans Blue

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    19/22

    , Cere4 Blood 5lo6 Meta4*?4?= 8764BCC"4B@#+ubMed Abstract+ublisher $ull Tet

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    OC# Giralt M= +en'owa M= Lago >= Molinero A= Hidalgo 6 Metallot"ionein+* protect t"e CS

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    , Neurotrauma*??B= *+6C.."CB?# +ubMed Abstract +ublisher $ull Tet

    4??# 0ordey A= Hablit9 = Sontheimer H6 !eacti#e astrocytes s"ow en"anced inwardly

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    4?4# +en'owa M= Giralt M= Lago >= %amats = %arrasco = Hernande9 = Molinero A= %ambell KL=

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    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

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    4?B# Siren AL= Radyush'in /= 0oretius S= /ammer ,= Riechers %%= >att &= Sargin ,= !atanabe T=

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