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COPYRIGHTEDMATERIAL,DONOTREPRODUCE
June4,2015

Juvenilenasopharyngealangiofibromastaging:An
overview
ByNadaAliAlshaikh,MDAnnaEleftheriadou,MD,PhD

Introduction
Juvenilenasopharyngealangiofibroma(JNA)isararebenignnasopharyngealtumorthataccountsfor0.05to0.5%ofall
headandnecktumors.1Itexclusivelyaffectsadolescentboys.1Itwasfirstdescribedin1906byChauveau,whogaveit
itsname.2However,theoldestrecordedsurgicalprocedureforJNAisattributedtoHippocrates,whoperformeda
longitudinalsplittingofthenasalridgetoremoveaJNA.3
Histologically,JNAsareunencapsulatedtumorsconsistingofabundantvascularchannelsthatlackthenormalmuscular
layerinthechannelwall,whichexplainstheirtendencytowardspontaneousbleeding.Thevascularchannelsare
surroundedbyanetworkoffibrocollagenoustissue.4
Althoughtheyarehistologicallybenign,JNAsarehighlyvascular,locallyaggressive,anddestructiveinnature.They
tendtoexpandintothenose,paranasalsinuses,vidiancanal,andpterygopalatinefossa.5Fromthere,theycaninvade
theinfratemporalfossathroughthepterygomaxillaryfissure,ortheycanextendintotheorbitthroughtheinferiororbital
fissureorintothemiddlecranialfossa,eitherdirectlyorthroughtheforamenlacerum,foramenrotundum,foramenovale
(viaextensionbeyondthesphenoidsinusandvidiancanal),orsuperiororbitalfissure.Erosionthroughtheposteriorwall
ofthesphenoidsinuscanresultinintracranialextension.6
Etiology.TheetiologyofJNAisstillunclear.79Osbornin1959proposedthatthetumorcouldbeeitherahamartomaor
agrowthofresidualfetalerectiletissuesunderhormonalstimulation.9GirgisandFahmyconsideredthetumorasa
paragangliomabasedonthehistologicappearanceofundifferentiatedepithelioidcellsatthemarginsoftheJNA.10
SchicketalsuggestedthatJNArepresentsthegrowthofaresidualvascularplexusfromtheinvolutionofthefirst
branchialartery.11Thisarterycommunicateswiththeinternalcarotidarteryandthemaxillaryarterytemporarilyduring
fetallife,anditspersistencemayleadtothedevelopmentofJNAsecondarytogrowthstimulationatthetimeof
adolescence.Thiscouldexplaintheoccasionalvascularcontributionfromtheinternalcarotidartery.Anothertheoryis
thatJNAdevelopsfromasteroidstimulatedhamartomatousturbinatetissue,whichwouldexplainthenaturalinvolution
ofJNAafterpuberty.10
Todate,themostacceptedtheoryofJNAgenesisisthatitarisesasaresultofrepeatedepisodesofmicrohemorrhages
andrepairbyfibroustissueformationintheareaofthesphenopalatineforamen,whichisrichinvascularerectiletissues
thatdilateinresponsetotheincreaseinsexualhormoneproductionduringadolescence.12Thisprocessisbelievedto
leadtotheformationofJNA,especiallyifthecapillariesweremalformed.
TheexactsiteoforiginofJNAisalsostillunknown.However,thereisaconsensusthatitoriginatesinthesuperior
marginofthesphenopalatineforamenatthepointwherethepterygoidprocessofthesphenoidbonemeetsthe
sphenoidprocessofthepalatineboneandthehorizontalalaofthevomer.13
Diagnosis.PatientswithJNAusuallypresentwithunilateralnasalobstruction,recurrentepistaxis,anda
nasopharyngealmass.Asthediseaseadvances,patientsmaypresentwithfacialswelling,cranialneuropathy,and
proptosis.1Biopsyiscontraindicatedbecauseoftheriskofintractablebleeding.Thediagnosisismadebyconsidering
elementsoftheclinicalpresentationwithradiologicfindingsoncontrastenhancedcomputedtomography(CT),magnetic
resonanceimaging(MRI),and/orangiography.
Treatment.ThereisgeneralagreementthatsurgeryisthebestmodalityoftreatmentavailableforJNA.14Basedonthe
factthatJNAisahighlyvasculartumor,preoperativeangiographyandembolizationofthefeedingvesselsfromthe
externalcarotidarteryarehighlyrecommendedbymanysurgeonsasameansofreducingtheriskofextensive
intraoperativebleeding.Differentsurgicalapproacheshavebeendescribedintheliteraturetheyincludetranspalatal,
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lateralrhinotomy,transantral,midfacedegloving,infratemporalfossa,craniotomy,transnasalmicroscopic,and
transnasalendoscopicapproaches.13OtherdescribedtechniquesforresectionofJNAsincludetheuseoftheKTPlaser
andultrasonicallyactivatedscalpel.15
Othertreatmentmodalitieshavebeenused,mostlyforextensivediseasewithintracranialinvasion,forresidualor
recurrenttumorsatsurgicallyinaccessibleanatomicsites,andwhenahighriskofmajorcomplicationsisanticipated.
Thesealternativesincluderadiotherapy,hormonaltherapy,andembolization.Morerecently,gammakniferadiosurgery
hasbeenusedforthetreatmentofresidualJNAafteraconservativesubtotalresection.16
EventhoughtransnasalendoscopicresectionofJNAshasbeenusedformorethanadecade,clearindicationsforits
useindifferentstagesofJNAhaveyettobeestablished.Mostsurgeonsconsidertheextentandgrowthpatternofthe
tumortodeterminethefeasibilityofendoscopicremoval.Theendoscopicapproachcarriestheadvantagesofminimal
softtissuedissection,avoidanceoffacialincisionsandfacialbonydisruption,theavailabilityofamagnifiedmultiangled
view,andminimalmorbiditywithashorthospitalizationtime.
Nowadays,thereisaconsensusamongmostsurgeonsthattumorsconfinedtothenasopharynx,pterygopalatinefossa,
andparanasalsinusescanbesuccessfullyremovedviaatransnasalendoscopicapproach.17However,thefeasibility
andefficiencyoftheendoscopicmanagementofJNAsthatinvadetheinfratemporalfossaand/ortheskullbaseisstill
problematic.18,19
Stagingsystems.Stagingsystemsforanytumorareimportantbecausetheyusuallystandardizetheguidelinesfor
classificationandmanagementbasedoncumulativefactorsthatinfluencethesurgicaldecision,aswellastheprognosis
aftersurgery,includingtheriskofresidualandrecurrentdisease.Stagingsystemsalsocanservetoeliminateany
confusionthatmightbeengenderedbydifferentreportsintheliterature,andtheyallowforbetterinterinstitutionaldata
comparisons.
ManysystemshavebeenproposedtoclassifythestagesofJNA.FactorsthatinfluencesurgicaldecisionmakinginJNA
includetheextentandsizeofatumor,thetechnicaldifficultiesencounteredinsurgery,andthecommonsitesofresidual
andrecurrentdisease.20Inthisarticle,wereviewtheclassificationsystemsforJNA,andwediscusstheirimpacton
evaluation,management,andprognosis,aswellassomeoftheadvantagesanddisadvantagesofthedifferentsystems.

Literaturereview
WeconductedastructuredreviewofthePubMed,Embase,andCochraneCollaborationdatabases(theCochrane
CentralRegisterofControlledTrialsandtheCochraneDatabaseofSystematicReviews)usingthefollowingMeSH
terms:juvenilenasopharyngealangiofibroma,nasopharyngealtumor,nasopharyngealdisease,juvenileangiofibroma,
angiofibromastaging,tumorclassification,andtumorstaging.Wefoundnorandomizedcontrolledtrialsorsystematic
reviewsintheentireEnglishlanguageliteratureregardingtheuseofdifferentstagingsystemsforJNAandtheir
influenceinmanagementdecisionsandpredictionsofresidualandrecurrentdisease.Therefore,weconductedourown
reviewofpublishedstagingsystems.Thedetailsofsomeofthesesystemsareshownintable1.Asummaryofreportson
thetreatmentofJNAisshownintable2.

Table1.SelectedclassificationsystemsforJNA

StageI

StageII

StageIII

StageIV

StageV

Sessions,21
1981

A.Minimalextension
intothepterygo
A.Involvement palatinefossa
ofthenoseor
nasopharyngeal B.Fulloccupationof
thepterygopalatine
vault
fossa
B.Extension
intooneormore C.Infratemporal
extensionw/orw/o
sinuses
involvementofthe
cheek

Intracranialextension

Chandler,22
1984

Involvementof
Extensionintothe
the
nasalcavityor
nasopharyngeal
sphenoidsinus
vault

Extensionintothe
maxillarysinuses,
ethmoidsinuses,
Intracranial
pterygopalatinefossa,
extension
infratemporalfossa,orbit,
orcheek

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Juvenilenasopharyngealangiofibromastaging:Anoverview

Extensionintooneor
Confinementto
Extensionintothe
moreofthefollowing:
thenasalfossa
Intracranial
sphenoidsinusand/or maxillarysinus,ethmoid
and/or
extension
pterygomaxillaryfossa sinus,orbit,infratemporal
nasopharynx
fossa,cheek,andpalate

Invasionofthe
Confinementto
pterygopalatinefossa
Andrews
thenoseor
ormaxillary,ethmoid,
Fisch,241989 nasopharyngeal
orsphenoidsinus
vault
w/bonedestruction

Bagatella
Mazzoni,26
1995

StageIfeaturesplus
extensiontooneor
moreofthefollowing
Confinementto
w/bonedestruction:
the
thecontralateralnaso
nasopharynx
pharynxandnasal
andipsilateral
fossa,sinuses,
nasalfossa
parapharyngeal
w/nobone
space,
destruction
pterygomaxillary
fossa,andinfraspheno
temporalfossa

A.Extensionintothe
infratemporalfossaor
orbit
B.Intracranialextension
intotheextradural
parasellararea

StageIIfeaturesplus
extensionintothe
temporalandzygomatic
fossaeorintraorbitalor
intracranialextradural
extention

A.Minimalextension
intothe
A.Minimalskullbase
A.Involvement pterygopalatinefossa involvement,including
ofthenoseor
themiddlecranialfossa
nasopharyngeal B.Fulloccupationof and/orbaseofthe
thepterygopalatine
pterygoidplates
Radkowski,27 vault
fossa
1996
B.Extension
B.Extensiveintracranial
intooneormore C.Infratemporalfossa involvementw/orw/o
extensionorextension invasionintothe
sinuses
posteriortothe
cavernoussinus
pterygoidplates

Onerci,28
2006

Deepextensionintothe
cancellousboneatthe
Extensionintothe
baseofthepterygoid
Extensioninto
maxillarysinusorthe musclesorthebodyand
thenose,
anteriorcranialfossa, greaterwingofthe
nasopharyngeal
fulloccupationofthe sphenoidbone,signifcant
vault,and
pterygomaxillary
extensiontothe
ethmoidand
fossa,andlimited
infratemporalfossaor
sphenoid
extensiontothe
pterygoidplates
sinuses
infratemporalfossa
posteriorlyortheorbital
region,andobliterationof
thecavernoussinus

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A.Intracranial
extension
intradural
extensionw/o
infiltrationofthe
cavernoussinus,
pituitaryfossa,or
opticchiasma

B.Intracranial
intradural
extension
w/infiltrationofthe
cavernoussinus,
pituitaryfossa,or
opticchiasma

Intracranial
intradural

Intracranial
extensionbetween
thepituitarygland
andinternal
carotidartery,
tumorextension
posterolateralto
theinternalcarotid
artery,middle
fossaextension
andextensive
intracranial
extension

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INCan,31
2008

Juvenilenasopharyngealangiofibromastaging:Anoverview

A.Involvementofthe
nasopharynx,nasal
fossa,maxillary
antrum,anterior
ethmoidcells,and
sphenoidsinus
Involvementof
invasionintothe
the
pterygomaxillary
nasopharynx,
fossaornfratemporal
nasalfossae,
fossaanteriortothe
maxillary
pterygoidplates,with
antrum,anterior
itsgreatestdiameter
ethmoidcells,
andsphenoid <6cm
sinus
B.Invasionintothe

Invasionintothe
infratemporalfossa
posteriortothepterygoid
platesorintothe
posteriorethmoidcells

Extensiveskull
baseinvasion>2

cmorintracranial
invasion

pterygomaxillaryfossa
orinfratemporalfossa
anteriortothe
pterygoidplates,with
itsgreatestdiameter
6cm

UPMC,32
2010

V(M):Medial
intracranial
extension
Skullbaseerosion w/residual
w/involvementof vascularityfrom
Involvementof Involvementofthe
theinternal
Skullbaseerosionw/
theorbitand
thenasalcavity paranasalsinusesand
involvementoftheorbit infratemporalfossa carotidartery
and
lateralpterygopalatine
V(L):Lateral
andinfratemporalfossa w/residual
pterygopalatine fossaw/noresidual
intracranial
w/noresidualvascularity vascularityfrom
fossa
vascularity
theinternalcarotid extension
w/residual
artery
vascularityfrom
theinternal
carotidartery

Table2.SummaryofreportsonthetreatmentofJNA

Author

Staging
N
system

CT/MRI Embolization Surgicalapproach

Residual
or
recurrent
tumor,%

Snyderman
etal,32
35 UPMC
2010

All/NA

30

27endoscopic,6combinedendoscopicopenapproach,2
23
openapproach

Andrews
Nicolaiet
46 Fisch,
al,292010
Onerci

All/all

40

Allendoscopic

Midilliet
al,42009

42 Radkowski All/none 25

Khalifaand
Andrews
Ragab,19 32
Fisch
2008
Guptaet

All/all

16

28 Radkowski All/none 21

8.7

12endoscopic,10lateralrhinotomy,7midfacedegloving,
17
6transpalatalapproach,6craniotomy,1midfacesplitting

16endoscopIcallyassistedantralwindowapproach,16
endoscopIcallyassistedmidfacedegloving

NA

Allendoscopic

3.6

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al,332008
19lateralrhinotomy,4transpalatalapproach,4midface
degloving,4anterolateralosteoplasticmaxillotomy,3
medialosteoplasticmaxillotomy,2endoscopic,2
craniofacialresection,2notmentioned,14radiotherapy

Yiotakiset
20 Radkowski All/some 12
al,172008

9endoscopic,6transpalatalapproach,5midface
degloving

90

Danesiet
Andrews
85
al,342008
Fisch

All/33

44midfacedegloving,41lateralrhinotomy

Andradeet
Andrews
12
al,52007
Fisch

All/none None

Allendoscopic

Allendoscopic

17

Borgheiet
23 Radkowski All/some None
al,352006

Allendoscopic

61

El
Banhawyet 20 Fisch
al,362006

All/some None

Midfacedegloving

Tyagiet
Andrews
95
al,302006
Fisch

All/some 25

65combinedtranspalatalandtransantralapproach,15
transpalatalapproach,10infratemporalfossaapproach,5 2
craniotomy

Onerciet
36 Onerci
al,282006

NA

NA

24openapproach,12endoscopic

33

Tosunet
24 Radkowski All/5
al,372006

All

10transpalatalapproach,9endoscopic,4lateral
rhinotomy,1midfacedegloving

17

Cansizet
22 Fisch
al,382006

All/9

13

16midfacedegloving,4endoscopic,2combinedmidface
59
deglovingandinfratemporalfossaapproach

Hofmannet
21 Fisch
al,392005

NA

19

Allendoscopic

9.5

Kaniaet
20 Radkowski All/some All
al,402005

8endoscopic,5midfacedegloving,3endoscopically
assistedmidfacedegloving,2lateralrhinotomy,2
endoscopicallyassistedcraniotomy

15

Andrews
Pasquiniet
6 Fisch,
All/all
al,412004
Radkowski

Allendoscopic

16.7

AllendoscopIcallyassistedmidfacedegloving

Carrilloet
54 INCan
al,312008

All/none 8

Eloyet
6 Radkowski All/all
al,202007

El
Banhawyet 15 Fisch
al,422004

35

All

All

All/some 2

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Mannet
30 Fisch
al,132004
Onerciet
al,72003

All/NA

All

15transnasalapproach,8midfacedegloving,6lateral
rhinotomy,1transpalatalapproach

NA

All

8endoscopic,4endoscopicallyassistedmidface
degloving

NA

Wormald
andVan
7 Radkowski All/NA
Hasselt,43
2003

All

Allendoscopic

29

Senneset
33 Sessions
al,142003

All/NA

NA

NA

NA

Nicolaiet
Andrews
15
al,442003
Fisch

NA/all

All

Allendoscopic

13

Mairet
5 Fisch
al,452003

NA/all

All

AllendoscopicwiththeNd:YAGlaser

NA

Rogeret
20 Radkowski All/some 19
al,462002

Allendoscopic

40

Petrusonet
32 Chandler
al,472002

16lateralrhinotomy,13transantralapproach,2
radiotherapy,1embolization

NA

Allendoscopic

12 Radkowski NA

22/some 17

Jorissenet
13 Radkowski NA
al,482000

All

NA=
information
not
available.
Sessionssystem.Introducedin1981,theSessionsclassificationsystemisregardedasthefirststandardizedJNA
stagingsystem(table1).21Sessionsandcolleaguesproposedthisradiologicstagingsystemwiththegoalofeliminating
confusionamongdifferentinstitutionswithregardtosurgicalapproaches,morbidity,andcurerates.TheyusedCTscans
todefinetheanatomiclocationofthedisease,andtheyusednasopharyngealcarcinomaasastagingmodel.They
believedthatitistumorextensionratherthantumorsizethatdeterminesthestageandthesurgicalapproachtotumor
clearance.However,Sessionsetalfailedtoincorporatesurgicalchallenges,treatmentoutcomes,andsitesofresidualor
recurrentdiseaseintotheirclassificationsystem.Furthermore,atthattime,intracranialextensionwasageneralterm
thatdidnotspecifywhetherthedurahadbeenpenetrated.Inouropinion,thisisofgreatimportanceinsurgicalplanning
andprognosis,butthemajorpitfalloftheSessionssystemisthatitisbasedonthestagingofnasopharyngeal
carcinoma.Basingthestagingsystemofabenignprocessonthatofamalignantprocessislikelytoresultingenerally
inaccuratefindings,sincethepathophysiology,nature,andbehaviorofthesetwoprocessesiscompletelydifferent.
Chandlersystem.ThesystemdevisedbyChandleretalin1984wasbasedontheclinicalevaluationoftumor
extensionandsizecombinedwithradiologicfindingsonCTand/orMRI(table1).22Theirsystemintegratedknown
tumorextensionandrationalplanningwiththetherapeuticapproachesavailableatthattime.
Thissystemhasbeenadoptedbysomesurgeonsandfoundtobeusefulinmakingdecisionsaboutthesurgical
approachandmanagementofdifferentJNApatients.However,Chandleretalstagednasalcavityinvolvementhigher
thannasopharyngealinvolvement,suggestingthattheformerrequiresdifferentandmoreextensivesurgery,whichisnot
thecase.Inaddition,theyfailedtoconsiderthecomplexityofintracranialextension,andthustheirsystemachievedless
popularitythandidsomeoftheothersystems.Ultimately,theirsystemisunreliablebecauseitwasbasedonthe
AmericanJointCommitteeonCancersystemasnoted,angiofibromaisabenignlesionthatfollowsadifferentcourse
frommalignantlesions.
Antonellisystem.AninterestingclassificationsystemwasintroducedbyAntonellietalin1987(table1).23Theybased
theirsystemontheirexperienceinmanaging19casesofJNA.Theirsystemwasbasedentirelyonclinicoradiologicdata
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ontumorsizeandextension.However,thissystemdidnotgainpopularity,probablybecauseitdidnotcorrelatewellwith
surgicalapproachesandoutcomes.Forexample,stageIIIinthissystemincludedmaxillaryandethmoidsinusextension
alongwithinfratemporalfossainvolvement,eventhoughinfratemporalinvolvementrequiresmoreextensivesurgery
thandoesextensionintothemaxillaryorethmoidsinuses.
AndrewsFischsystem.Basedonhiswideexperienceinskullbasesurgery,FischintroducedastagingsystemforJNA,
whichhe,Andrews,andothersmodifiedin1989themodificationiscalledtheAndrewsFischsystem(table1).24This
systemhasbecomeoneofthemostpopularinusetoday.Infact,mostsurgeonsworldwideconsiderittobethe
standard.
Intheirreport,Andrews,Fisch,andcolleaguesdescribedindetailthegrowthpatternofJNAasitoriginatesinthe
superiormarginofthesphenopalatineforamenatthejunctionofthesphenoidprocessofthepalatineboneandthe
pterygoidprocessofthesphenoidbone.24Fromthere,thetumorgrowsintothenasopharyngealandnasalspaces
anteriorlyandposteriorlybeforeiterodesthebonesofthemaxillary,ethmoid,andsphenoidsinuses.Itcanalsospread
tothepterygopalatinefossa,andfromthereitcanerodethepterygoidplatesandspreadintotheinfratemporalfossaor
throughtheinferiororbitalfissureintotheorbit.Fromthebaseofthepterygoidplates,thetumorcanexpandthrough
threeforamina(lacerum,rotundum,andovale)intothemiddlecranialfossa,whereitcanfurtherinvadetheparasellar
areawithoutintraduralinvasion.Inveryrareandveryadvancedstages,thetumorcanerodetheposteriorwallofthe
sphenoidsinusandinfiltratethepituitaryfossa,opticchiasm,and/orthecavernoussinus.
Thisanalysisofgrowthcharacteristicsandthecomplexityoftumorextensions,especiallyattheskullbase,madethis
classificationsystemwellrecognizedinternationallyasthefirstcomprehensive,practical,andapplicableguidetothe
surgicalapproachandpredictionofoutcomeinthemanagementofJNA.
Forexample,thissystemclassifieserosionintotheskullbasewithoutintraduralextensionasstageIII,whileintradural
growthisclassifiedasstageIV.Thisdistinctionisverywellexplainedbythefactthatextraduralinvasionoftheskullbase
isoperableandcanbeextirpatedcompletelywithoutmajorcomplications,whileintraduralinvasionisassociatedwitha
highriskofmajorcomplicationsand,ifitisextensive,shouldbetreatedwithtumordebulkingandpostoperative
radiotherapy.
TheAndrewsFischsystemwasdesignedduringatimewhentheonlysurgicalapproachesavailablefortumorsatthis
regionwereopenprocedures.Therefore,itsmajordrawbackintermsofcurrentapplicationinouropinionisthatitdoes
nottakeintoaccountrecentadvancesinbothradiologicimagingandsurgicaltechniques.Asaresult,itisdifficultto
predictcurerates,risksofcomplications,andsitesofresidualandrecurrentdiseasewiththeAndrewsFischsystem.
Mishrasystem.Thatsameyear,Mishraetalproposedtheirsystem,butitdidnotbecomewidelyaccepted.25Their
systemwasbasedontheirexperiencewith100casesofJNA.TheynoticedthatthegrowthpatternofJNAdiffers
accordingtothepatient'sageatpresentationinthatitismoreextensiveinadolescentsthaninpatientsyoungerthan10
years.Theyalsoclassifiedtumorextensionchronologicallyasprimary,secondary,andtertiary.Theyproposedthat(1)
primaryextensionsgrowinananterior,posterior,ormedialdirection,(2)secondaryextensionsstartgrowinglaterallyor
tothecontralateralnostril,and(3)tertiaryextensionsinvadethecheek,orbit,infratemporalfossa,andskullbase.
Mishraetalbasedtheirsystemontheirearlieranalysesofpatternsofgrowthandextensionandtheavailablesurgical
approachesandmodalities.However,despitethefactthattheygavegreatconsiderationtothedifferentcategoriesof
extensionandsubclassifiedskullbaseextensionaccordingtothepresenceorabsenceofduralinvolvement,theydid
notgivedueconsiderationtoallofthesurgicaloptionsthatwereavailableatthetime.
AnothershortcomingoftheMishrasystemisthatonly25%ofthecasestheauthorsreviewedhadbeenwellevaluated
preoperativelybyCT.Finally,theyreportedanoticeablyhighsurgicalfailurerate(27%).Alloftheseissuesputthe
validityandapplicabilityoftheMishrasystemintoquestion.
BagatellaMazzonisystem.In1995,BagatellaandMazzonisuggestedamodificationoftheoriginalFischstaging
system(table1).26Thenewsystemtookintoaccounttheprogressivedegreesoftumorextensionandthesurgical
difficultiesencounteredinattackingthem.Theauthorsbasedtheirclassificationon34consecutivelypresentingcasesof
JNAthatwereallmanagedwithasimilarmicroscopictransmaxillarysurgicalapproach.Inouropinion,theBagatella
Mazzonisystemwashardtoadoptbecauseitfailedtoguidesurgicaldecisionmakingortocorrelatewiththeprognosis.
Radkowskisystem.In1996,RadkowskietalsuggestedsomemodificationstotheSessionssystembasedontheir
experiencewith23cases(table1).27Theycontendedthatpreoperativetumorstageistheprimaryfactoraffectingtumor
recurrence.TheRadkowskisystemcombinedtheadvantagesofsomeoftheothersystemsandcorrelatedeachstage
withthebestsurgicalapproachthatwouldminimizetheriskofresidualorrecurrenttumor.Theirsystemhasbecomeone
ofthemostwidelyusedtoday.
OnemodificationoftheSessionssysteminvolvedstageIIRadkowskietaladdedtumorextensionposteriortothe
pterygoidplatestostageIIC.TheyalsomodifiedstageIIIbysubdividingitintosubstagesIIIAandIIIB.StageIIIAwas
definedasminimalskullbaseinvolvement,includingthemiddlecranialfossaand/orbaseofthepterygoidplatesstage
IIIBwasdefinedasextensiveintracranialinvolvementwithorwithoutinvasionintothecavernoussinus.Basedontheir
newsystem,Radkowskietalgraded9oftheir23caseshigherthantheywouldhavebeengradedwiththeSessions
system4caseswereupgradedtostageIICand5tostageIIIB.23
ThepopularityoftheRadkowskisystemnotwithstanding,theanalysisbyRadkowskietalshowedthattherewassome
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confusionabouttheSessionssystemRadkowskietalthoughtthatSessionshadclassifiedminimalintracranial
extensionasstageIICwheninfactSessionslistedintracranialextensioningeneralasstageIII.Moreover,theupgrading
ofsomecasesdidnotchangethewaytheyweremanaged,nordidithaveaneffectonrecurrencerecurrencesafter
primarysurgerywereseenin5ofthe23cases(22%),3ofwhichhadbeenupgraded.
Onercisystem.By2006,advancesinendoscopicandmicroscopicsurgeryandtheevolutionofnewtechniquesin
preoperativeevaluationandembolizationpromptedadesireforanewclassificationsystembasedonthesitesof
residualandrecurrentdisease.Tothatend,Onercietalsuggestedamodificationofexistingstagingsystemsbasedon
theirretrospectiveanalysisof36patientstheytreated(table1).28Basedondiseaseextent,theirsystemtookinto
accountthenewsurgicalapproachesthathadevolvedandthesurgicaldifficultiesthathadbeenencountered,aswellas
thesitesofresidualdisease.Theiraimwastoachieveabetterevaluationofthetumorandareductionintheriskof
residualandrecurrentdisease.
IntheOnercisystem,involvementoftheethmoidandsphenoidsinuseswasconsideredstageIdiseasebecausein
thesecases,thetumorcanbecompletelyremovedviaanendoscopicendonasalapproachwithoutadditionalsurgical
challenges.
MaxillarysinusextensionandtotalinvolvementofthepterygopalatinefossawerebothclassifiedasstageII,sinceboth
situationsindicatethepresenceofalargetumorthatwillrequiresomemodificationsofthesurgicalapproachand
technique.Minimalinvolvementoftheinfratemporalfossa,definedasnoextensionbeyondthelateralborderofthe
posteriormaxillarysinuswall,wasalsoclassifiedasstageIIdisease,sincetheauthorsbelievedthatsuchanextension
couldberemovedendoscopically.
InfratemporalfossainvolvementbeyondthelateralborderoftheposteriormaxillarysinuswallwasclassifiedasstageIII
disease,sinceitnecessitatesanexternalsurgicalapproachforcompletetumorclearance.
Despitethefactthatsomereportsintheliteraturehadrevealedthatthemostcommonsiteofdiseaserecurrencewasthe
baseofthepterygoidplates(75to93%ofcases),28Onercietalwerethefirsttoaddressthisissue.Theybelievedthat
suchinvolvementwasnotonlyassociatedwithahighrateofrecurrence,butitalsomightindicatethepresenceofmiddle
cranialfossaextensionbecauseitisconsideredtobethemostlikelyrouteofintracranialinvolvement.Therefore,
extensionintothecancellousboneofthepterygoidplatesandinvolvementofthepterygoidmuscleswereclassifiedas
stageIIIdisease.
Intracranialextensionwasclassifiedaccordingtothesiteofinvolvement.Anteriorcranialfossaextensionwasclassified
asstageIIdiseasesinceitisapproachableendoscopically,whilemiddlecranialfossaextensionwasclassifiedasstage
IVdiseasebecauseitrequiresanexternalapproachforitsclearance.AccordingtoOnercietal,allstageIVtumorsare
extensiveandshouldbemanagedviaacombinedendoscopicandexternalapproach,althoughcompleteclearance
occasionallymaynotbepossible.
TheOnercistagingsystemisrelativelynew,andithasbeentestedinonlyonestudyof46casesofJNAreportedby
Nicolaietalin2010(table2).29However,thesetumorshadbeenresectedentirelythroughanendoscopicapproach,
despitethefactthat26ofthesecaseswereOnercistageIIItumors.AlthoughwebelievethattheOnercistagingsystemis
quitecomprehensiveandbasedonlongexperiencewiththemanagementofJNAviabothopenandendoscopic
approaches,thepossibilitythatitwouldfailtoguidethesurgeontothebestresectionmodalityisasignificantdrawback.
FurtherreportsareneededtoevaluatethevalidityoftheOnercistagingsystem.
Tyagisystem.Laterin2006,TyagietalproposedsomemodificationstostagesII,III,andIVoftheAndrewsFisch
system.30Theybasedtheirclassificationofintracranialextraduralextensiononthesizeofthetumorandthesurgical
approachnecessaryforitsexcision.SmallextraduralextensionswereclassifiedasstageIIIB,andtherecommended
surgicalapproachwasacombinedtranspalatalandtransmaxillaryprocedure.Largeextraduralextensionwasclassified
stageIVA,andfrontotemporalcraniotomywastherecommendedapproach.
Intheirreportof95casesofJNArangingbetweenstageIIandIV,theyindicatedthatmostcaseswereresectedviaan
openapproach(table2).30However,theirmodificationhasnotbeenadvocatedbyotherauthorswhosubsequently
reportedtheirownseries.Webelievethattheirmodificationdidnotaddressadvancementsinendoscopicsinusand
skullbasesurgery.
INCansystem.In2008,CarrilloetalattheInstitutoNacionaldeCancerologia(INCan)inMexicoCityintroduceda
promisingnewstagingsystemthatwasbasedoncorrelatingtumorsize,tumorlocation,thebestsurgicalapproach,and
therecurrencerate(table1).31Theyhadretrospectivelyreviewed54casesofJNAandcomparedrecurrenceratesand
diseasefreesurvival(DFS)betweentheAndrewsFischandRadkowskisystems(table2).WiththeRadkowskisystem,
theyfoundthatDFSforstageIIIBpatientswasbetterthanthatforstageIIIApatients.AccordingtotheAndrewsFisch
system,patientswithstageIIIBdiseasehadashorterDFSthandidthosewithstageIVAandIVBdisease.
CarrilloetalalsofoundthattumorsizewasasignificantfactorinrecurrenceandDFSintheearlystages(stageIandII).
OtherfactorsthatcontributedtohighrecurrenceratesandshorterDFSwereextensionofthetumorintothe
pterygomaxillaryfissure,intracranialinvasion,skullbaseinvasion,andinfratemporalfossainvasion.Basedonthese
findings,theauthorssubclassifiedinfratemporalfossainvasionasanteriorandposteriorinrelationtothepterygoid
plates.Theyalsoclassifiedskullbaseinvasionaccordingtothedegreeofduralpenetration.
AccordingtotheINCansystem,stageIandstageIIAdiseasecanbemanagedexclusivelyviaanendoscopicapproach,
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stageIIBandstageIIIviaacombinedendoscopicandopenapproach(preferablyfacialdegloving),andstageIVviaa
combinedanterolateralorlateralskullbaseapproach.CarrilloetalconcludedthattheINCansystemhasabetterimpact
onthepredictionofrecurrenceandDFSforpatientswithadvanceddisease.Assuch,itservesasagoodguidetothe
bestsurgicalapproachineachstageofdisease.However,sincethisclassificationisrelativelynew,itsapplicabilityand
successhaveyettobedetermined.
UPMCsystem.Finally,in2010,SnydermanandcolleaguesattheUniversityofPittsburghMedicalCenter(UPMC)
introducedthemostrecentendoscopicstagingsystemforJNA(table1).32Theytookintoconsiderationthecurrent
advancementsinendonasalsurgicalapproaches,theroutesforintracranialextensionofthetumor,andtheextentof
vascularsupplyfromtheinternalcarotidartery(ICA)theybelievedthatthesizeofthetumoranditsextensionintothe
sinusesarelesspredictiveofoutcomeafterendonasalresection.Intheirseries,74%ofcasesinvolvedskullbase
erosion,and51%involvedresidualvascularityfromtheICAafterembolizationoftheexternalcarotidarterytributaries
(table2).Theyconsideredthesetobethemostimportantpredictivefactorsforprognosisintermsofbloodloss,the
numberofoperationsrequiredtoresectthetumorcompletely,andtumorrecurrence.Assuch,thestagingsystemthey
proposedclassifiedthepresenceofresidualvascularityfromtheICAasstageIV,whileintracranialextensionwas
classifiedasstageV.
TheUPMCsystemisverycomprehensive,andittakesintoconsiderationthenatureofthetumorandcurrentsurgical
approaches.Inaddition,itcorrelateswellwithprognosis.Finally,itgivessurgeonsthechoicetotakethesurgical
approachoftheirpreference.However,surgeonscanstageJNAwiththeUPMCsystemonlyafterembolizationofthe
tumor.Inotherwords,ifnoembolizationisperformedbeforesurgery,theUMPCstagingsystemisnotapplicable.In
addition,thisstagingsystemisnotaguidetodeterminingwhichapproachshouldbeusedforeachJNAstage.Finally,
becauseitisanewsystem,itneedstobeadoptedbymoresurgeonsbeforeitsvaliditycanbeascertained.

Conclusion
WhenlookingatsomeoftheseriesofJNAcasesthathavebeenpublishedintheliteratureoverthepast15years,itis
clearthattheRadkowskisystemandeithertheoriginalFischsystemortheAndrewsFischsystemwerethemost
frequentlyusedbysurgeons(table2).4,5,7,13,14,17,19,20,2848Itappearsthatsurgeonshavefoundthatthesesystems
correlateaccuratelyandsignificantlywiththeirdecisionsonsurgicalapproachestoJNAwithdifferentdegreesof
extensionandthattheyaregoodindicatorsofdiseaserecurrenceandprognosis.Inaddition,itisimportanttoconsider
theOnerci,INCan,andUPMCsystems,whichseemtocorrelatebetterwithcurrentadvancesindiagnosticimagingand
surgicaltechniques.However,sincethesethreesystemsarerelativelynew,moreexperiencewiththemisencouraged
beforeweadvocateanyoneofthemasthenewstandarduponwhichtostageJNA.
Inthisreview,wehavehighlightedtheexistingcontroversiesregardingthestagingofJNA.Nowadays,withthe
significantadvancesinourunderstandingoftransnasalendoscopicapproaches,instrumentation,andimaging
technologysuchasintraoperativeMRIandimageguidednavigationsystemstherehasbeenanoticeablechangeinthe
expectedratesofresidualandrecurrentdisease,aswellastheoverallprognosisforpatientswithJNA.
TherehaslongbeenasubstantialneedforauniversalstandardizedJNAstagingsystemthattakesintoconsiderationall
thefactorsthatplayaroleinJNA.Inouropinion,onlyonesystemtheUPMCsystemmeetsthisneed.However,since
thissystemisstillnewandhasnotbeenclinicallyappliedbysurgeonsotherthanSnydermanetal,32thereisaneedfor
anintegratedmultidisciplinaryeffortbyexperiencedsurgeonstousetheUPMCsystemandtosharetheirexperiences
withitintermsofitscredibilityandfeasibilityasabalanced,informative,andguidingstagingsystem.Oncethathappens,
perhapsitcanbeuniversallyadoptedastheidealstandardizedstagingsystemforJNA.

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FromtheDepartmentofOtolaryngology,DammamMedicalComplex,Dammam,KingdomofSaudiArabia(Dr.Alshaikh)
andtheENTDepartment,GeneralHospitalofRethymnon,Rethymnon,Greece(Dr.Eleftheriadou).
Correspondingauthor:NadaAliAlshaikh,MD,DepartmentofOtolaryngology,DammamMedicalComplex,POBox
2471,Dammam31451,SaudiArabia.Email:nadaats@yahoo.com
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