Transient Hepatic Parenchymal Enhancement detected at dynamic imaging: A short instruction manual for the clinician.

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ContentslistsavailableatSciVerseScienceDirect

Digestive

and

Liver

Disease

jo u rn a l h om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / d l d

Review

article

Transient

Hepatic

Parenchymal

Enhancement

detected

at

dynamic

imaging:

A

short

instruction

manual

for

the

clinician

夽

Stefano

Colagrande

a,∗

_,

_Silvia

_Pradella

b

_,

_Silvia

_Lucarini

b

_,

_Fabio

_Marra

c,d,∗∗

a_Dipartimento_di_{Fisiopatologia}_{Clinica-Radiodiagnostica,}_University_of_Florence,_Italy

b_Dipartimento_di_Diagnostica_per_Immagini,_Azienda_{Ospedaliero-Universitaria}_Careggi,_Florence,_Italy c_Dipartimento_di_Medicina_Interna,_University_of_Florence,_Italy

d_Centro_di_Ricerca,_{Trasferimento}_ed_Alta_Formazione_DenoTHE,_University_of_Florence,_Italy

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received19April2011 Accepted30October2011 Available online 8 December 2011 Keywords: Biliaryobstruction Bloodperfusion Hepatocellularcarcinoma Hepaticmetastases

a

b

s

t

r

a

c

t

Basicknowledgeintheinterpretationofhepaticimagingisessentialfortheclinicalhepatologist.Inrecent years,theavailabilityofdynamicimagingstudiesoftheliverusingcomputedtomographyormagnetic resonancehasledtoappreciatetheimportanceofearlychangesinarterialperfusionfortheinterpretation ofhepaticlesions.TransientHepaticParenchymalEnhancement(THPE)isdefinedasanormalareaof liverparenchymathatenhancesafterinjectionofcontrastagentduringthearterialphaseofperfusion. Appearanceofthissignismostlyassociatedwithareductioninportalperfusionorwithinflammation, andappearsindifferentmorphologicpatterns.THPEshouldnotbeconsideredaradiologicalartefact, anditsinterpretationisessentialtoavoidmisclassificationofhepaticlesionsthatmayhaveclinical significance,suchashepatocellularcarcinomaorhepaticmetastases.Inthisshortreviewweprovide essentialinformationonthecauses,pathophysiologyandmorphologyofTHPE,anddiscusstherelevance ofthesefindingsinaclinicalperspective.

1. Introduction

Detectionofhepaticnodularlesionsandtheircorrect diagno-sisisaneverydaychallengefortheclinicalhepatologist.Thisisof particularrelevanceinthesettingofacirrhoticliver,where hepa-tocellularcarcinoma(HCC)representsaleadingcomplicationand anincreasinglyobservedcauseofdeath[1].Accordingtothe exist-ingguidelines,imagingplaysacriticalroleinthedeﬁnitionofa nodularlesionasHCCinthecontextofacirrhoticliver[2].These considerationsimplythattheclinicalhepatologistacquiresatleast someknowledgeofthecriteriathatarenecessaryforthe interpre-tationoflivercomputedtomography(CT)ormagneticresonance (MR)dynamicimaging.Infact,correctunderstandingofimaging ﬁndingsoftenneedsclosecooperationbetweenradiologistsand

夽 Grantsupport:WorkinDr.Marra’slaboratoryissupportedbygrantsfromthe IstitutoToscanoTumori(ITT)andAssociazioneItalianaperlaRicercasulCancro (AIRC).

∗ Correspondingauthorat:UniversitàdiFirenze,DipartimentodiFisiopatologia Clinica-UnitàdiRadiodiagnostica,LargoBrambilla3,50134Florence,Italy. Tel.:+390554377673;fax:+39055431970.

∗∗ Correspondingauthorat:DipartimentodiMedicinaInterna,LargoBrambilla3, I-50134Florence,Italy.Tel.:+390554271087;fax:+39055417123.

E-mailaddresses:stefano.colagrande@uniﬁ.it(S.Colagrande),

f.marra@dmi.uniﬁ.it(F.Marra).

clinicians,especiallyinthesettingofcirrhosis,wheresuspicionof malignancyiscommon.

Duetoitshightemporalresolution(speed),multi-detectorCT allowstoacquireimagesoflargeportionsofthebodyinasingle breath-hold.Inatypicaldynamicstudyoftheabdomen,and partic-ularlyoftheliver,theunenhancedscanisusuallyfollowedbytwo (orthree)additionalscansacquiredduringthearterialandportal venousphases(approximately30and70sfollowing administra-tionofcontrastmedium,respectively),toobtaininformationabout arterialandportalperfusionofthehepaticparenchyma.Dynamic imaging techniqueshave identifieda newphenomenon related tochangesinarterialperfusionoftheliver,whichoccursrather frequentlyinCTimaging(between9.3%and15%ofallexams per-formedontheabdomen)[3].Thisphenomenonwasfirstdescribed byItaietal.[4]whonamedit“TransientHepaticAttenuation Dif-ference”(THAD);itrepresentsaverycommoncauseofdiagnostic uncertainty,oftenleadingtoadditionalimagingstudiesand possi-blyeventoliverbiopsy.Inthispaperwereviewthebiologicaland clinicalsignificanceofthesehepaticarterialphenomena,focusing onthepossiblediagnosticpitfalls.

2. Deﬁnition

Since the ﬁrst description by Itai in CT scans, a THAD has beendeﬁnedas‘anormalareaofliverparenchymathatenhances after injection of contrast agent during the arterial phase of

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364 S.Colagrandeetal./DigestiveandLiverDisease44 (2012) 363–368

perfusion’.ThesamephenomenonisdeﬁnedasTransientHepatic IntensityDifference(THID)in MRimaging[5,6].ThetermTHPE (TransientHepaticParenchymalEnhancement)hasthereforebeen createdtoencompassbothTHAD and THID[7]. TPHEindicates anincrease in arterialperfusion, dueto a variationof the nor-malhepaticbloodsupply.THPEisgenerallyobservedasanareaof hyperdensity/hyperintensity(thenwithappearancebrighterthan surroundingareas)intheparenchymainthearterialphase,which tendstodisappearduringtheportalphase[8,9].

TounderstandthebasisofTHPE,itisimportanttoconsiderthe peculiarityofthehepaticvascularsystem.Theliverreceivesadual bloodsupplyfromtheportalvein(about75%)andthehepatic arter-ies(about25%).Thesetwosystemsareinterconnectedthroughthe trans-sinusoidal,thetransvasalandtheperibiliaryplexus,which provideacompensatorysystemtoensureaconstantflowofblood throughthehepaticparenchyma,regardlessofvariationsthatmay occurineitherthearterialorvenoussupplies[10,11].The auto-nomicnervoussystemandsolublefactorsregulateflowthrough thesevessels.ItshouldbeunderscoredthatTHPEcanbeseenas theimagingequivalentofaphenomenonknownas“arterialbuffer response”,whichisactivatedbytheliverbasedontherequirement ofoxygenandmetabolites.Asaconsequenceofadecreasein por-talsupply,anincreaseinarterialflowisgeneratedandbecomes detectableinthearterialphaseofCTimaging[11,12].

3. Pathophysiologyandimagingﬁndings

Fromapathogeneticpointofview,THPEcanbedividedintotwo majorcategories:(1)thosebasedonarterialhyperperfusion sec-ondarytoareductionofportalperfusionand(2)thoseinwhichthe arterialhyperperfusionisprimary,independentlyoftheoccurrence ofaportalhypoperfusion.

Portalhypoperfusionmaybecausedbyobstruction,thrombosis, compressionorinfiltrationofabranchoftheportalvein,asoccurs incaseofcompressionabextrinseco,e.g.byanodularlesionora haematoma.Hypoperfusionmayalsobecausedbyflowdiversion asoccursinarterio-portalshunts(APS),causedbysmall arterio-portalfistulasorbythepresenceofanabnormalafferentblood asinthecaseofvenousorarterialanatomicalvariations.Inthese latterconditionsarterialblood, withhigherpressure,flowsinto theportalbed,withlowerpressure,andblocksportalflow,thus triggeringthearterialreactionandthengeneratingtheTHPE.

Thistypeofdiversioncanalsotakeplaceintheterritoriesof the“thirdhepaticinﬂow”whichconsistsofthecapsularveins,the Sappeyparaumbilicalveins,hilarandepiploicveins,suspensory ligamentanddiaphragmaticveinsandtheaccessorycysticvein. Theseanomalousaccessoryveinsentertheliverseparatelyfrom

theportalvenoussystemand mayact,accordinglytothe pres-suregradient,asanomaloussupplyordrainagevessels,providing someareasoftheparenchyma,mainlylocatedinsegmentsI–IV. Asaconsequence,thesevenoussystemsworkasashuntbetween thesystemicvenouscirculationandthesinusoids.In physiologi-calconditionstheyrepresentahepatopetalsystem,contributing nomorethan2–3%ofthehepaticbloodﬂow.Inthepresenceof portalhypertension,theintraportalpressurebecomeshigherthan thatofthesystemicveins,andthe“third”hepaticsystembecomes hepatofugal,allowingforthedevelopmentofshuntingsystemsin acirrhoticliver[13–15].

AsecondtypeofTHPEisindependentofportalhypoperfusion andismainlyrelatedtoinflammation,asinthecaseof cholecys-titis,abscessesorcholangitis.Inflammatorymediatorsmaycause vasodilatationandincreasedvascularpermeabilityinthenearby normalparenchyma.Oncetheinflammationisresolved,theTHPE phenomenaalsodisappear.AnothertypeofprimaryTHPEmaybe relatedtothepresenceofhypervascularbenigntumours(‘sump effect’,seebelow).

IdentificationofTHPEandincreasedknowledgeoftheir differ-enttypesisamajorchallengefortheclinicianwhohastointerpret thesefindings.Intheclinicalsetting,itisparticularlyimportant toevaluatethepossibilitythatsomeofthesepicturesmaybethe expressionof proliferative lesionsorthat heraldtheir eventual appearance.Apivotalaspectisthataradiologistmustdescribethe presenceofaTHPE,eventhoughhe/sheisunabletodetermineits cause.Ontheotherhand,theclinicianshouldneverconsiderTHPE asanartefact,andthesefindingsneedtobeplacedinthe frame-workoftheclinicalhistoryandcurrentconditionsofthepatient.In anycase,acloseinteractionbetweentheradiologistandthe clini-cianisessential,inordertoreducethenumberofmissedorwrong diagnosesandtowarrantanappropriatefollow-uptothepatient. Ideally,THPEshouldbeclassifiedaccordingtotheir etiopatho-genesis.However,thisapproachisimpracticalbecausemorphology isthemostappreciablecharacteristicofthesearterialphenomena. Thus,thisreviewisorganizedaccordingtotheimaging appear-anceofTHPEs,distinguishinglocalizedanddiffuseformsofTHPE (Table1andFig.1).

3.1. LocalizedTHPEs

Thesearegenerallyassociatedwithportalhypoperfusion,and particularlywithportalveinthrombosis.Theyappearmostlyas tri-angularareas,andmayalsobeassociatedwithmalignantorbenign lesions,suchashaemangiomaorabscess[16,17].Depending on thepositionofthelesion,thearterialareamaybedifferentlysized. Especiallyincaseoftriangular-shapedTHPE,theradiologistshould Table1

ClassiﬁcationofthedifferenttypesofTransientHepaticParenchymalEnhancement.

Extension Pathogenesis Appearance Predominantcauses

Localized Portalhypoperfusion Triangular •Benignormalignantfocallesion(rarelyhiddennodule) •Arterio-portalshunt

•Portalthrombosis Inﬂammation Polymorphous •Cholecystitis,pleuritis

•Othercauses:parenchymalinjury,extrinsiccompression,percutaneous biopsyortreatments.Intheselattercasestheypresentinvariousshapes, includingtriangular

Primaryhyperperfusionnotlinkedto portalﬂowblockade(‘sumpeffect’)

Lobarormulti-segmental •Largeandbenignfocallesions

•Vascularvariants(whichcanalsoinducepolymorphousTransient HepaticParenchymalEnhancement)

Diffuse Post-sinusoidalﬂowblockade Patchypattern •Rightheartfailure •Budd–Chiarisyndrome Pre-sinusoidalﬂowblockade Central–peripheralpattern •Thrombosisofportaltrunk

•Cirrhosis Peribiliaryplexusimpairment,frequently

associatedwithinﬂammation

Peribiliarypattern •Biliarytreedilationwithorwithoutinﬂammation(e.g.

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Fig.1.AppearanceofTransientHepaticParenchymalEnhancement.Toppanel:examplesofdifferenttypesoflocalizedTransientHepaticParenchymalEnhancement (THPE).Upperimage:triangularTHPEcausedbyanodularlesion(notvisibleintheimageprovided);middleimage:polymorphousTHPE(arrows)associatedwithextrinsic compressionoftherighthepaticlobecausedbyﬂuidcollection;lowerimage:lobarTHPE(arrow)causedbyahepaticabscess(arrowhead).Bottompanel:examplesof differenttypesofdiffuseTHPE.Upperimage:patchyTHPEinapatientwithBudd–Chiarisyndrome;middleimage:central–peripheralphenomenonassociatedwithportal veinthrombosis(notvisibleintheimageprovided);lowerimage:peribiliarypatterninapatientwithbiliarytreeobstructionduetocholedocholitiasis.

carefullylookforthepresenceofanodularlesion,whichisusually

placedwithintheTHPEoratitsapex.Infact,insomecases,the

focallesionmaybeverysmallorisodensetotheareaofTHPE,and

thereforedifﬁculttoidentify.Inthisoccurrence,a“hidden

nod-ule”shouldbesuspected,causingaportalcompression,butnot

detectablebecauseofbeingtoosmallordevoidofasufﬁcient

con-trastdifferencewithrespecttothesurroundingstructures[18,19].

Inallthesecasesafollow-upisstronglyrecommended,asitis pos-siblethatthefocallesionwillappearwithtime(Fig.2).Acommon conditionthatneedsparticularattentionistheappearanceofa tri-angularTHPEinthecontextofacirrhoticliver,especiallywhenin proximityofthehepaticcapsulewhereitcanmimicanoduledue totheincidenceoftheX-raybeam(Fig.3).Incontrasttothe typ-icalCTappearanceofHCCincirrhosis(hyperinthearterialphase withportalwashout),THPEdonotshowanywashoutduringthe portalphase.Alsointhiscase,ifaTHPEisdetectedbyCTscan, addi-tionalimagingstudiessuchasMRIwithliver-speciﬁcgadolinium chelatesarenecessary.Infact,typicalHCCusuallydonotenhance

inthehepatobiliaryphase,whilstTHPEshowsadelayed enhance-mentequaltothatofthesurroundingparenchyma.Thisbehaviour of THPEcouldmimic a well-differentiatedHCC andtherefore a closefollow-upismandatory.Thus,whena nodulewithoutthe typicalHCCpatternis detectedin acirrhoticliver,the possibil-ityofapseudonodularTHPEshouldbekeptinmind[20].THPE withpseudonodularappearancecanbemainlyfoundin subcapsu-larareasandinthedistrictofthe“thirdhepaticsupply”.Itshould beunderscored thatin these areas,arterialphenomena can be observedalsoinnon-cirrhoticlivers,especiallyafter chemother-apy,whichcandamageminorportalvesselsandfacilitateblood inﬂow through systemic veins (i.e. the “thirdinﬂow”) (Fig. 4). Clearly,appearanceof thesepseudonodularlesionsin apatient undergoingchemotherapymaybechallengingastheymayraise thesuspicionofalivermetastasis.

Sometimes localizedTHPEs are not triangular but polymor-phousand/orround-shaped.Theselatterareusuallynotassociated withfocal lesions and are mainlycaused by APS,parenchymal

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366 S.Colagrandeetal./DigestiveandLiverDisease44 (2012) 363–368

Fig.2.Exampleofa‘hiddennodule’.(A)PresenceofmultipleTransientHepaticParenchymalEnhancements(THPE)(arrowforanexample)inapatientwithoutevidenceof nodularlesions.(B)Inafollow-upcomputedtomographyscanafter6months,thereisclearevidenceofmultiplemetastasesinareaswhereTHPEwerepreviouslydetected (arrow).

Fig.3.DiagramofthenodularappearanceofaTransientHepaticParenchymal Enhancement.ThedrawingshowshowinaxialimagestheshapeofaTransient HepaticParenchymalEnhancement(THPE)dependsontheplaneorientationwith respecttothearterializedarea.Thismaymimicanodularlesion.

injury, extrinsic compression or inﬂammation (Fig. 1) [21]. A particularconditionwheremultipleAPSmaybepresentis hered-itaryhaemorrhagictelangiectasia(Rendu–Osler–Weber disease) [7].Anomalousarteriesoraccessoryveins,asinthe“third hep-aticsupply”(seeabove)areanothercauseofalteredbloodsupply thatmayleadtoappearanceofthistypeofTHPE.

TherearepolymorphousTHPEswhicharenotcloselyrelatedto portalhypoperfusion.TheseformsofTHPEareprevalentlylinked

Fig.5. Exampleof a localized,polymorphous Transient HepaticParenchymal Enhancement.Arterialphase-computedtomographyimageshowinganarterial phenomenonwithapolymorphouspattern(arrow)inapatientwithcholecystitis (inﬂammatorypathogenesis).

toinflammationofbileductsand/oradjacentorgans(cholecystitis, pancreatis,abscesses)[6](Fig.5).Theseincludeconditionsdefined inotherstudiesas“inflammatoryhepaticarteryhyperaemia”and increasedbloodflow fromadilatedaberrantcysticvein[22].In thesecases,arterialphenomenaarelocatedaroundtheinflamed area.Theirmorphogenesisisrelatedtothespreadofinflammatory mediatorstotheparenchyma,bycontiguity,althoughincreased

Fig.4. TransientHepaticParenchymalEnhancementinthedistrictofthe‘thirdhepaticsupply’.Arterialphasesofmagneticresonanceimaging(A)andcomputedtomography scan(B)showthepresenceofanodularTransientHepaticParenchymalEnhancementneartothegallbladder(arrows)asatypicalareaof‘thirdinﬂow’.

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arterialﬂowmayalsobesecondarytoportalinﬂowreductiondue tointerstitialoedema[10].

A third,less common type of localizedTHPE, notrelated to portalhypoperfusion,istheso-called“sumpeffect”,alsoknown as“syphoningphenomenon”,whichisassociated with haeman-giomas, focal nodular hyperplasia, or hypervascular tumours, usually larger than 3cm and benign [23]. These tumours can markedlyincreasethearterialbloodsupplytothelobeorsegment whereitiscontained,resultinginatransientlyhigherarterial atten-uationinthelobarareasurroundingthetumour.Incontrast,the contralaterallobereceivesalessabundantarterialbloodsupplyand showslowerarterialattenuation.Anotherrelatedphenomenon, althoughrarelyoccurring,isthe‘stealphenomenon’,the explana-tionofwhichexceedsthescopesofthisreview[7].

3.2. DiffuseTHPEs

ThesetypesofTHPEinvolvetheentiretyorthemostpartof theliverwithapatchy,central–peripheralorperibiliarypattern (Table1).Theyareusuallyassociated withportal and/orbiliary obstruction,andtheimagingappearancedependsonboththelevel andthetypeofobstruction[5,6,18,24].Apatchypatternis usu-allyduetopost-sinusoidalobstructionoftheportalﬂow,which canoccuratthelevelofthehepaticveins,suchasincaseofheart failure,Budd–Chiarisyndromeor inferiorvena cavaobstruction syndrome.Intheseconditions,occlusionofthehepaticveinsresults inincreasedsinusoidalpressureandreversesthepressure gradi-entbetweenthesinusoidalandportalveins.Theportalveinthen becomesadrainingvein,causinganincreaseinarterialbloodﬂow, and resulting in a functional APS [25,26]. At dynamic imaging, thisappearsasanenhancementofthecentralpartofthehepatic parenchyma(centrilobularenhancement)withamottled/marbled appearance.Thispattern isevident inthearterialphase, but is typicallymaintainedintheportalphase(Fig.1).

Insinusoidalandpre-sinusoidalobstruction,the interconnect-ingshunts betweenthearterialand theportalsystems playan importantrole,inparticulartheopeningoftheperibiliaryplexus, whichdeterminesthecentral–peripheralpattern, i.e.anarterial enhancementoftheperipheralsubcapsularparenchymawith rel-ativehypodensityoftheperihilararea.Theblockoccurseitherat theportaltrunk(beforethesinusoids),asinportalveinthrombosis, oratsinusoidallevel,asincirrhosis[7].Portalflowusuallyremains adequateinthecentralareaoftheliver(segmentsIandIV),and insegmentsIIandIII,whilstintheperipheryitsrelativedeficiency leadstoanincreaseinarterialflow,withopeningofshuntsatthe leveloftheperibiliaryplexus.

A pattern intermediate between the patchy and the central–peripheral phenomenon, with variable expression, may be noted during veno-occlusive disease, more recently named sinusoidal obstruction syndrome. This describesa non-thromboticobstructionofthehepaticsinusoidswithorwithout venularinvolvement,basedonendothelialtoxicitymainlydueto chemotherapy and/or radiotherapy. The consequent congestion oftheliverparenchymamayleadtoalightpatchypatternwith linearhypodensitydue tosinusoidal walloedema. Nonetheless, thediagnosisofthisconditionisbasedonliverbiopsy[27].

A peribiliary pattern may be observed in the case of long-standing bile duct dilation (e.g. due to choledocholithiasis, pancreaticcancerorampulloma).Increasedpressurecauses com-pressionoftheperibiliaryplexus,whichsurroundsthebileductand lacksamuscularwall.Thismaycauseareductionofbloodﬂowfrom theportalveintothesinusoids,resultinginanarterial compen-sationandadiffuseandirregularenhancementoftheperibiliary parenchyma(Fig.6).Ifthecauseofobstructionisnotremoved, persistenceofcholestasisleadstoparenchymalatrophy,especially inthepresenceofportalveinobstruction[28]whilstiftheblock

Fig.6. Exampleofadiffuse,peribiliary.TransientHepaticParenchymal Enhance-ment.Arterialphase-computedtomographyimageshowingaTransientHepatic ParenchymalEnhancementwithperibiliarypattern(arrow)inapatientwith dilata-tionoftheintrahepaticbranchesofthebiliarytree(star)associatedwithstenosis ofthedistaltractofthecommonbileduct.

isremoved,theTHPEphenomenadisappear[18,29].Thispattern maybepresentalsointhecaseofcholangitis,whentheperibiliary plexusisblockedbecauseoftheinvolvementbytheinﬂammation. Thiscanbeofclinicalutility,supportingthediagnosisofcholangitis, thatmaybedifﬁcultintheabsenceofbileductdilation.

ThistypeofTHPEusuallypresentsinadiffuseform,butitmay beappearingalsoinatriangularshapeifonlyabranchofthe bil-iarytreeisinvolved.Intheselattercases,ifCTscanisnotsufﬁcient todetectthecauseofobstruction,additionalinvestigationwith ultrasoundand/orMRIshouldbeperformed.Afterremovalofthe obstruction(suchasincaseofbiliarystones),follow-upis manda-torybecauseTHPEtendtodisappearinthesecases.Incontrast,in thecaseofmalignantdisease,THPEtendtopersistandadditional effortsmustbeputtoidentifyitscause.

4. EvolutionofTHPE

Ingeneral,ifthecauseofTHPEisremoved,arterial phenom-enarapidlydisappear.However,evenifthecausepersists,imaging alterations tend tobecomeless evident withtime and eventu-allydisappearwithinmonths.Thismaybeexplainedbythefact thatinnormalconditionstheliverneedslowoxygentensionand highlevelsofnutrients.Whentheseconditionsarenotmet,asin thecase ofapersistentlyincreasedarterialbloodﬂow,theliver parenchymaundergoesmetabolicchangesthatpresentasanarea ofhypodensityonimaging.Thisislikelyduetothepresenceof oedema,ﬁbrosisand/ordepletionofhepatocytesintheunderlying parenchyma[7,25,30].

5. Conclusion

Severalstudiesinrecentyearshavehighlightedthepotential relevanceofTHPEphenomenaobservedbyhepaticimaging per-formedbyCTscanorMRimaging.Theclinicalrelevanceofthese formsisbasedonthepossibilitytobemisdiagnosedascancerous lesions,tohideanunderlyingcancer,ortobeexpressionofsevere hepaticdiseases.Inallthesecases,incorrectrecognitionand clas-siﬁcationofaTHPEwillpromptcostlyandpossiblyunnecessary testsandwillbeasourceofconsiderabledistressforthepatient. Thus,aclosecollaborationbetweentheradiologistandthe clin-icianisnecessarytodiscusstheclinicalandimagingﬁndingsof eachcontroversialcase,thusincreasingthepossibilitytoreacha correctdiagnosis.

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368 S.Colagrandeetal./DigestiveandLiverDisease44 (2012) 363–368 Conﬂictofintereststatement

Theauthorshavenoconﬂictsofinteresttodisclose.

Listofabbreviations

APS,arterio-portalshunt;CT,computedtomography;HCC, hepatocellularcarcinoma;MR,magneticresonance;THAD, Transient Hepatic Attenuation Difference; THID, Tran-sientHepaticIntensityDifference;THPE,TransientHepatic ParenchymalEnhancement.

References

[1]YangJD,RobertsLR.Hepatocellularcarcinoma:aglobalview.NatRev Gas-troenterolHepatol2010;7:448–58.

[2]BruixJ,ShermanM,AmericanAssociationfortheStudyofLiverDiseases. Man-agementofhepatocellularcarcinoma:anupdate.Hepatology2011;53:1020–2. [3]GolfieriR,CentiN,FuscoF,etal.Pseudolesionidaflussoeverelesioni nodu-lariflusso-dipendenti.In:StrambiniT,editor.Diagnosticaperimmaginidelle malattiedelfegatoedelleviebiliari.Milano:Masson;2005.p.373–402. [4]ItaiY,MossAA,GoldbergHI.Transienthepaticattenuationdifferencesoflobar

orsegmentaldistributiondetectedbydynamiccomputedtomography. Radi-ology1982;144:835–9.

[5] Colagrande S,Centi N,Galdiero R, etal. Transient hepatic intensity dif-ferences.PartI.Thoseassociatedwithfocallesions.AJRAmJRoentgenol 2007;188:154–9.

[6]ColagrandeS,CentiN,GaldieroR,etal.Transienthepaticintensity differ-ences.PartII.Thosenotassociatedwithfocallesions.AJRAmJRoentgenol 2006;188:160–6.

[7]QuirogaS,SebastiàC,PallisaE,etal.Improveddiagnosisofhepaticperfusion disorders:valueofhepaticarterialphaseimagingduringhelicalCT. Radio-graphics2001;21:65–81.

[8]ChenWP,ChenJH,HwangJI,etal.Spectrumoftransienthepaticattenuation differencesinbiphasichelicalCT.AJRAmJRoentgenol1999;172:419–24. [9]GryspeerdtS,VanHoeL,MarchalG,etal.Evaluationofhepaticperfusion

disorderswithdouble-phasespiralCT.Radiographics1997;17:337–48. [10] ColagrandeS,CarmignaniL,RoselliG,etal.Arterialhepaticsectorial

enhance-ment[ASE]asasignofacuteportalthrombosisthreecasereports.RadiolMed 1998;96:639–41.

[11] KawasakiT,CarmichaelFJ, SaldiviaV,etal. Relationshipbetweenportal venousandhepaticarterialbloodﬂows.Spectrumofresponse.AmJPhysiol 1990;259:G1010–8.

[12]GulbergV,HaagK,RoessleM,etal.Hepaticarterialbufferresponseinpatients withadvancedcirrhosis.Hepatology2002;35:630–4.

[13]HashimotoM,HeiannaJ,TateE,etal.Smallveinsenteringtheliver.EurRadiol 2002;12:2000–5.

[14]BreenD,RutherfordE,StedmannB,etal.Intrahepaticarterioportalshunting andanomalousvenousdrainage:understandingtheCTfeaturesintheliver. EurRadiol2004;14:2249–60.

[15] GallegoC,VelascoM,MarcuelloP,etal.Congenitalandacquiredanomaliesof theportalvenoussystem.Radiographics2002;22:141–59.

[16] GiovagnoniA,TerilliF, ErcolaniP,et al.MR imagingof hepaticmasses: diagnosticsigniﬁcanceofwedge-shapedareasofincreasedsignalintensity surroundingthelesion.AJRAmJRoentgenol1994Nov;163:1093–7. [17]YamasakiM,FurukawaA,MurataK,etal.Transienthepaticattenuation

differ-ence(THAD)inpatientswithoutneoplasm:frequency,shape,distribution,and causes.RadiatMed1999;17:91–6.

[18] ColagrandeS,CarmagniniL,PagliariA,etal.Transienthepaticattenuation differences(THAD)notconnectedtofocallesions.RadiolMed2002;104:25–43. [19] BrinkJA,IncreasedCT.Contrastenhancementof“normal”hepaticparenchyma

mayheraldoccult“metastases”.Radiology1997;205:37–8.

[20] ColagrandeS,LaVillaG,BartolucciM,etal.Spiralcomputedtomographyversus ultrasoundinthefollow-upofcirrhoticpatientspreviouslytreatedfor hepa-tocellularcarcinoma:aprospectivestudy.JHepatol2003;39:93–8. [21]AhnJH,YuJS,HwangSH,etal. Nontumorousarterioportalshuntsinthe

liver: CTandMRIﬁndings considering mechanisms andfate.EurRadiol 2010;20:385–94.

[22]ItoK,AwayaH,MitchellDG,etal.Gallbladderdisease:appearanceof associ-atedtransientincreasedattenuationintheliveratbiphasic,contrast-enhanced dynamicCT.Radiology1997;204:723–8.

[23]Colagrande S, Centi M, Pradella S, et al. Transient hepatic attenuation differencesandfocalliverlesions:sumpeffectduetoprimaryarterial hyper-perfusion.JCAT2009;33:259–65.

[24] KobayashiS,NgCS,KazamaT,etal.Hemodynamicandmorphologicchanges afterportalveinembolization:differentialeffectsincentralandperipheral zonesintheliveronmultiphasiccomputedtomography.JComput Assist Tomogr2004;28:804–10.

[25] ItaiY,MatsuiO.Bloodﬂowandliverimaging.Radiology1997;202:306–14. [26]KimTK,ChoiBI,HanJK,etal.Nontumorousarterioportalshuntmimicking

hypervasculartumorincirrhoticliver:two-phasespiralCTﬁndings.Radiology 1998;208:597–603.

[27] MahgereftehSY,SosnaJ,BogotN,etal.Radiologicimagingandinterventionfor gastrointestinalandhepaticcomplicationsofhematopoieticstemcell trans-plantation.Radiology2011;258:660–71.

[28]Hann LE, GetrajdmanGI, Brown KT, etal. Hepatic lobaratrophy: asso-ciation with ipsilateral portal vein obstruction. AJR Am J Roentgenol 1996;167:1017–21.

[29]ColagrandeS,CentiN,LaVillaG,VillariN.Transienthepaticattenuation differ-ences.AJRAmJRoentgenol2004;183:459–64.

[30] GolﬁeriR,GavelliG.Liverhemodynamicchanges,pseudolesionsandbenign nodularﬂow-dependentlesionstheirpathogenesisandspiralcomputed tomo-graphicradiologicalaspects.RadiolMed2000;99:233–49.