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Review

Mucosal

melanoma

of

the

nasal

cavity

and

paranasal

sinuses

L.

Gilain

,

A.

Houette

,

A.

Montalban

,

T.

Mom

,

N.

Saroul

ServiceORLetChirurgieCervico-Faciale,CHU,Universitéd’Auvergne,58,rueMontalembert,63000Clermont-Ferrand,France

a

r

t

i

c

l

e

i

n

f

o

Keywords: Mucosalmelanoma Nasalcavity Paranasalsinuses Nasalobstruction Epistaxis

a

b

s

t

r

a

c

t

Mucosalmelanomaofthenasalcavityandparanasalsinusesisararedisease,butitsincidenceappears tobeincreasing.Themeanageatdiagnosisisbetween65and70years.Unilateralnasalobstruction andepistaxisarethemostcommonpresentingcomplaints.Melanomaarisesintheseptumorlateral wallofthenasalcavityinthegreatmajorityofcases.Thehistologicaldiagnosisisbasedonspecific immunohistochemicallabellingandisusuallyestablishedatanadvancedstageofdisease:stageT3or T4tumoursaccordingtothe7theditionoftheAmericanJointCommitteeonCancer(AJCC)classification oftumours.First-linetreatmentconsistsofsurgery.Theplaceofintranasalendoscopicsurgeryremains controversialduetothedifficultyofcontrollingsurgicalmarginsandshouldbereservedforexperienced teams.Adjuvantradiotherapyisusuallyperformedduetoitsefficacyonlocalandregionaldiseasecontrol. Five-yearoverallsurvivalofmucosalmelanomaofthenasalcavityandparanasalsinusesinthemost recentseriesdoesnotexceed40%.Localrecurrenceisobservedinabout50%ofcasesandmetastatic diseaseiscommon.Thequalityofinitialtumourresectionwithnegativesurgicalmarginsisthemost importantprognosticfactorfortumoursconfinedtothenasalcavity.Hopesforimprovementofsurvival arebasedonearlydiagnosis,progressinradiotherapytechniquesandcellandgenetherapythatare currentlyunderevaluation.

©2014ElsevierMassonSAS.Allrightsreserved.

1. Introduction

Primarymucosalmelanomaofthenasalcavityandparanasal sinusesisararetumour[1,2].Positivediagnosisofthistumouris madedifficultbythenon-specificpresentingcomplaints[3,4].This tumourhasapoorprognosisduetoitsaggressivenatureandthe frequentlydelayeddiagnosis.Itmainlyoccursintheelderlyand thepresenceofcomorbiditiescanlimit theextentof treatment

[4].Treatmentoptionsessentiallyconsistofradicalsurgery and radiotherapy,whilechemotherapyisreservedforadvancedforms. Despiteabetterknowledgeofthistumour,the5-yearoverall sur-vivalremainspooranddoesnotexceed40%inanyofthepublished studies[5–8].

2. Pathogenesisandepidemiology 2.1. Pathogenesis

Melanocytesaredendriticcellsarisingintheneuraltubeand locatedatthedermo-epidermaljunctionofallmucousmembranes.

∗ Correspondingauthor.

E-mailaddress:lgilain@chu-clermontferrand.fr(L.Gilain).

Thepresenceofmelanocytesinthemucosaofthenasalcavityand paranasalsinuseshasbeenknownfor alongtime.Melanocytes are detectedunder normal conditions in about21% of individ-uals[3].Mucosalmelanomaisaneuroectodermaltumourarising fromthesemelanocytes[3,9].Ahigherdensityofmelanocytesin themucosaofthenasalcavityandparanasalsinusescomparedto othersitescouldexplaintherelativefrequencyofprimarymucosal melanomasinthissite[5].Noriskfactorhasbeenclearly identi-fiedtoexplainthedevelopmentofthesetumours.Incontrastwith melanomaoftheskin,inwhichsunexposureisknowntobethe majorriskfactor,theriskfactorsformucosalmelanomashavenot beenidentified.NolinkhasbeendemonstratedbetweenHuman PapillomaVirus(HPV)orHerpesvirusintheaetiopathogenesisof mucosalmelanoma[3].Exposuretoformaldehydehasbeen sus-pectedbutnotconfirmedinseveralstudies[3,10].Smokingmay constituteapredisposingfactoressentiallyformucosalmelanoma oftheoralcavity[3,11].Severalgeneticstudieshavedemonstrated genemutationsaffectingthetyrosinekinasereceptor[3,12].Some authorshavesuspectedtheroleofheredityandenvironmentinthe pathogenesisofmucosalmelanomainordertoexplainthe differ-entprevalenceratesofthesetumoursbetweenCaucasian(1%of melanomas)andAsianpopulations(7.5%ofmelanomas)[1,5].

CasiraghiandLefèvreconsideredthatmucosalmelanomasof thenasalcavityandparanasalsinuseswerehistologicallyrelated tothegroupofmalignantroundcelltumours[13].Theysuggested http://dx.doi.org/10.1016/j.anorl.2013.11.004

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a morphologicalcontinuumof thesetumoursbetweenthe two extremesoflife,withsarcomasinchildrenandyoungadultsand mucosalmelanomaintheelderly[13].

2.2. Epidemiology

Primarymucosalmelanomaofthenasalcavityandparanasal sinuses is a rare tumour, representing between 0.7 and 1% of allmelanomasinCaucasian populationsandbetween4and 8% ofmalignant tumoursofthenasalcavityand paranasalsinuses

[3,14].Theincidenceofmucosalmelanomaappearstobe

increas-ing,especiallyinthenasalcavityandparanasalsinuses[2,15].This increasingincidenceappearstobesignificantinwomen[2,14,15]. Despitethisincrease,theprevalencecurrentlyremainsidentical inthetwosexes[4].Thepatient’sageatthetimeofdiagnosisis between60and80yearswithameanagebetween65and70years

[5,16].Primarymucosalmelanomacanariseinvarious

anatomi-calsites,butitpredominantly(55%ofcases)involvestheheadand neck[5],inwhichthenasalcavityandparanasalsinusesisthemost frequentsite,representing70%ofcases(50%inthenasalcavity,20% intheparanasalsinuses)followedbytheoralcavityinabout17% ofcases[2].

3. Diagnosisandassessment 3.1. Clinicalfeatures

Themostcommonpresenting complaintsare nasal obstruc-tionandepistaxis.Nasalobstructionisunilateral,permanentand progressive,eitherisolated orassociated withothersymptoms. Epistaxiscanbeabundantorminimalwiththepresenceofstreaks ofbloodwhenblowingthenose[4,17].Someauthorshavereported epistaxistobethemostcommonpresentingcomplaint[6].These non-specific symptoms are often considered to be responsible for the long interval between first symptoms and diagnosis of melanoma.Thisisparticularlytruewhenthetumourarisesinthe paranasalsinuses[7].Othersymptomsincluderhinorrhoeawhich canbepurulentinthecaseofsuperinfection,painandlacrimation inthecaseofinvasionoftheinferiormeatusandlacrimalduct.More advancedtumoursmaypresentintheformofmalarswelling,nasal deformityorexophthalmos.

3.2. Clinicalexamination

Unilateralsymptomsmustbeconsideredtobesuspiciousand justify thorough fibroscopic or endoscopic investigation of the nasalcavity.Intranasalexaminationdefinestheappearanceofthe tumour (sessile, nodular,polypoid or granulating), its size and implantation.Itmaybeslate-coloured,reddish,crimson,brownish orblack,whichishighlysuggestiveofthediagnosis.Thetumour surfacecanbehomogeneousorheterogeneous,withafriable con-sistencyandthetumourmaybecoveredbyagreyishexudate.An ulceratedappearanceisfrequentlyobserved[3,13].One-thirdof melanomasare achromic[4]. Theexact originofthetumour is sometimesdifficulttodetermineandthetumourisoftenalready extensiveatthetimeofdiagnosiswithameandiameterranging between2 and3cm [14].Tumoursof thenasalcavity predom-inantly involve the septum and lateral wall, while tumours of theparanasalsinusespredominantlyinvolvethemaxillarysinus followed by the ethmoid, frontal and sphenoidal sinuses [4,5]. Thecranialnervesmustbesystematicallyexaminedlookingfor oculomotordisordersandsensorylossoftheface.Complete clini-calstagingassessmentmustincludepalpationofregionallymph nodes. At the time of diagnosis of the primary tumour, cervi-callymphnodemetastasesaredetectedin10to20%ofpatients

[1,13,17]and haematogenous metastases are detectedin 6% of

Fig.1. Infiltrationofthemucosaofthenasalcavitybymelanoma.Thearrow indi-catesthecellularproliferationinvadingthemucosaunderneathanintactsurface epithelium.

patients(lungs,brain,bone,liver)[13].Acompletedermatological andophthalmologicalexaminationmustbeperformedtodetecta possibleprimarytumourinordertoconfirmtheprimaryor sec-ondary natureof thetumour of thenasalcavity and paranasal sinuses.

3.3. Histology

Thediagnosisisbasedonhistologicalexaminationoftumour biopsies. Histological examination is difficult due to marked cytologicalandarchitecturalpolymorphism[4].Thepresenceof intracytoplasmicmelaninpigmentcanbedetectedbytheaffinity forFontanastain[13,17](Figs.1and2).Severalparametersare evaluatedonhistologicalexamination: morphologyand cellular architecture,pigmentation,presenceofulceration,percentageof necrosis,numberofmitoses,inflammationandbone,perineural, lymphaticandvascularinvasion.Confirmationofthediagnosisis basedonimmunohistochemistryusingapanelofmarkers:protein S100andmelanocyticmarkers(HMB45,Melan-A,tyrosinase,MITF)

[13].Epithelialcellmarkersarenegativebutseveralaberrantcases havebeenreported[13].

3.4. Imaging

Animagingassessmentcomprisingcomputedtomography(CT) ofthefacial bonesand magneticresonanceimaging(MRI)isan

Fig.2. BrownintracytoplasmiclabellingoftumourcellswithHMB45.Thearrow indicatesazoneofintenselabellingintheformofsmallgrains.

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Fig.3. MRI,T1-weightedsequence,coronalsection,showingatumour(define whetheritisahigh-orintermediate-signalintensityandaddarrows)ofthenasal cavityandahomogeneouslow-intensityrightmaxillarysinus.

essentialpartofthelocalstagingofthetumour.Computed tomo-graphyofthefacialbonesandskullbaseisperformedwithaxialand coronalsections,withcontiguous1mmthick(spiralacquisition)or amaximumof3mmthickslicesanddualwindowsettings(bone andsoft tissues).Intravenous iodinated contrastagentinjection allowsenhancementofthetumourwithrespecttosurrounding tissues.Three-dimensional(3D)reconstructionisparticularly use-fulwhenfacial reconstructionisplanned.Theusualappearance isthat ofan aggressiveosteolytictumour.Brain andfacial MRI providesthree-dimensionalsectionsandusuallycomprisesthree sequences:T1,T1post-gadoliniumandT2.Malignantmelanomais characterizedbyheterogeneouscontrastenhancement.According tosomeauthors,aspontaneoushigh-intensitysignalonT1with alow-intensitysignalonT2wouldbecharacteristicofmelanoma. Thisunusualappearance,sometimesobservedwithothertypesof tumours(angiosarcoma,cylindromaandaesthesioneuroblastoma) appearstoberelatedtothehighmelanincontentand/orbleeding insidethetumour[18,19].T2-weightedMRIcandistinguishtumour invasionfromparanasalsinusfluidretention.Finally,MRIis essen-tialtodefinetheanatomicalrelationsofthetumourwiththeorbit andskullbaseandtodetectanybrainmetastases(Figs.3and4). Dis-tantstagingisbasedonchest,abdomenandpelvisCTandpositron

Fig.4.MRI,T1-weightedwithgadoliniumadministrationsequence,axialsection. Heterogeneouscontrastenhancementofthetumour.

Table1

AmericanJointCommitteeoncancerstagingmucosalmelanomaoftheheadand neck,7thedition.

Primarytumor(T)

T3 Mucosaldisease

T4a Moderatelyadvanceddisease;tumorinvolvingdeepsoft tissue,cartilage,bone,oroverlyingskin

T4b Veryadvanceddisease;tumorinvolvingbrain,dura,skull base,lowercranialnerves(IX,X,XI,XII),masticatorspace, carotidartery,prevertebralspace,ormediastinal structures

Regionallymphnodes(N)

NX Regionallymphnodescannotbeassessed N0 Noregionallymphnodemetastases N1 Regionallymphnodemetastasespresent (M)

M0 Nodistantmetastasis M1 Distantmetastasispresent Staging

StageIII T3,N0,M0 StageIVA T4a,N0,M0

T3–T4a,N1,M0 StageIVB T4B,anyN,M0 StageIVC AnyT,anyN,M1

emissiontomography(PET).Thisstagingassessment lookingfor metastasescanbedecisiveinthechoiceoftreatmentandtoassess thevalueofcertaincosmeticallyandfunctionallydestructiveforms ofradicalsurgery(orbitalexenteration).

3.5. Classification

The clinical and imaging assessment allows staging of the melanomainordertoproposeadaptedtreatmentand toassess theprognosis.Ballantyne’sclassificationistheoldestclassification, butdoesnottaketumoursize,tumourhistologyandlocal exten-sionintoaccount[20],asstageIisdefinedastumourconfinedtothe originalsite,stageIIisdefinedastumourwithregionallymphnode metastasesandstageIIIisdefinedastumourwithdistant metas-tases.Useofthisoldclassificationallowscomparisonofvarious series[1],butitisnowpreferabletorefertotheclassification estab-lishedbytheAmericanJointCommitteeonCancer(AJCC)[21,22]. The7theditionoftheAJCCclassificationdoesnotcomprisestage T1andT2inviewofthesystematicallyaggressivenatureofthese melanomas.TheproposedclassificationcomprisingstageT3andT4 tumoursismoreconsistentwiththelocalextensionandthepoor prognosisofthisdisease(Table1).

4. Treatment 4.1. Surgicaltreatment

Ageneralconsensushasbeenreachedtoconsidersurgeryas first-linetreatment[1,5,23].Theindicationforsurgerymusttake intoaccountthepatient’squality oflife,duetothepoorglobal prognosisofthesetumours.Thetreatmentdecisionisgenerally takenbyanoncologymultidisciplinaryconsultationbasedonthe stagingassessment.Surgeryisindicatedasfirst-linetreatmentand inthecase oflocalrecurrence.Thechoicebetweenanexternal or an intranasal incisiondepends on thetumour size and site. Thechoiceof intranasalendoscopicsurgery remains controver-sialduetothedifficultyofcontrollingsurgicalmarginsandshould bereservedforexperiencedteams[16].Itisindicatedforstrictly intranasaltumoursandunderconditionsoftumourresectionthat areabletoachievethesamecancercontrolresultsasviaan exter-nalapproach.Craniofacialresectionisthereferencetechniquefor tumourssituatedincontactwithorinvadingtheskullbase[16].The tumourmustbewidelyresectedwith1.5to2cmnegativesurgical

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margins[17].Marginsareconsideredtobenegativewhentheyare greaterthanorequalto5mmondefinitivehistological examina-tionoftheoperativespecimen.Systematiclymphnodedissection isnotpartofconventionalsurgicalmanagementandisonly per-formedinthepresenceofclinicallyorradiologicallypathological lymphnodes[1].Thesentinellymphnodebiopsytechnique,used incutaneousmelanoma,iscurrentlyunderevaluationinmucosal melanoma.

4.2. Radiotherapy

Mucosal melanomas are generally considered to be poorly radiosensitive. Melanomas are composed of cells with a high post-irradiationregenerativecapacity.Radiotherapyisclassically indicated in the presence of positive surgical margins, local recurrence, locally advanced tumour, or sometimes for pallia-tivepurposesorwhenthepatientrefusessurgery.Themajority of authors consider that adjuvant radiotherapy increases local andregionalcontrolwithoutincreasingsurvivalindependentlyof tumourstage[8,24–27].Theredoesnotappeartobeanysignificant survivaldifferencebetweenpatientstreatedbysurgeryaloneand patientstreatedbysurgeryandadjuvantradiotherapy[3,28]. How-ever,thefindingsofthesestudiesarecontroversial,asotherteams havedemonstratedtheefficacyofsurgeryandadjuvant radiothe-rapyonsurvival[1].

In particular, the development of new radiotherapy tech-niques,suchasintensity-modulatedradiationtherapy(IMRT)has improved the results obtained with conventional radiotherapy especiallyonlocalandregionalcontrolwithgoodlocalsafetyand lowmorbidity[29–31].Asaresultofthisprogress,radiotherapy isincreasinglyproposedsystematicallyaspartoftheinitialphase oftreatmentasanadjuvanttosurgerywhetherornotthesurgical marginsareinvaded[29,31].

4.3. Chemotherapy

Chemotherapyisclassicallyindicatedforpalliativetreatment orinmetastatic patients[7].However,someauthorshave pro-posedmultimodalfirst-linetreatmentcomprisingchemotherapy and/orimmunotherapyforthemanagementoflocallyaggressive forms[28,32].A recentstudyhighlightedthevalue ofselective intraarterialchemotherapy [33]. Immunotherapy by interleukin 2 or interferon alpha (IFN␣) either alone or in combination withchemotherapyandvaccinationiscurrentlyunderevaluation

[34,35].Inmetastaticdiseaseorunresectableformsofcutaneous

melanoma,thechemotherapystrategyisdesignedaccordingtothe presenceorabsenceofV600mutation[31,36].Vemurafenib,aBRAF proteinkinaseinhibitor,isthereforereservedforthetreatmentof advancedmelanomaassociatedwithBRAFV600mutation[31,37]. Trialsofvemurafenibandipilimumabcombinationtherapyare cur-rentlyunderwayinpatientswithBRAFmutation.Intheabsence ofBRAFV600mutation,treatmentoftheseadvanced, treatment-refractoryforms isbasedontheuseofipilimumabeitheralone orincombinationwithstandardchemotherapy(dacarbazine).The transpositionoftheserecentdatatothemanagementofstage4 mucosalmelanomaofthenasalcavityandparanasalsinusesmust beconsideredin the light ofprogress of oncogeneticsin these mucosalforms.

However,theadverseeffects ofthesetreatmentsrepresenta considerablelimitingfactorforthemanagementofpatientswith mucosalmelanomaofthenasalcavityandparanasalsinuses,who aregenerallyelderlywithcomorbiditiescontraindicatinganyform ofchemotherapyorimmunotherapy.

5. Survivalandprognosis

The5-yearoverallsurvivalofmucosalmelanomaofthenasal cavityand paranasalsinusesinthemostrecentseriesdoesnot exceed40%(20%–40%)[5–8]andmeansurvivaldoesnotexceed 28months(17–28months)[4,27].Localrecurrencesoccurinabout 50%ofcases[3,27].Thishighrecurrencerateappearstobedueto themultifocalnatureofthelesions,submucosallymphaticspread andthehighrateofvascularinvasion.Localrecurrencesarealso relatedtoinadequatefirst-linesurgicalresection.Localrecurrences arepredictiveofthepresenceofdistantmetastases[3,27].Themost commonmetastaticsitesarelungs,liver,boneand,morerarely, brainandadrenalglands. Metastasesarefoundinabout50%of cases,sometimesduringthecourseofthedisease[27],whilelymph nodemetastasesarefoundin20to40%ofcases[13,27].

Prognosticfactorshavebeenextensivelystudiedinthe litera-turebymeansofmultivariateanalyses.Thequalityoftheinitial tumour resection with negative resection margins is the most importantprognosticcriterionfortumoursconfinedtothenasal cavity[6,17].

Anadvancedageatthetimeofdiagnosisisafactorofpoor prog-nosis.Theunfavourableagelimithasbeenestimatedtobe70years accordingtosomeauthors[38]and60yearsaccordingtoothers

[1,3],whileagelessthan50yearsappearstobeassociatedwitha

betterprognosis[3].Tumoursizegreaterthan3–4cmisconsidered tobeafactorofpoorprognosis[13,38].Anisolatedseptaltumour isassociatedwithgoodprognosis[6]incontrastwithtumoursof theparanasalsinusesthathaveaverypoorprognosis.

Ballantyne’sstageIhasabetterprognosis[1].Ahighmitotic index and a pseudopapillary and sarcomatoid architecture on histologicalexaminationarefactorsofpoorprognosis[4,13,39]. Someauthorsconsiderthepresenceofmelaninandthelevelof pigmentationtobefactorsofpoorprognosis[4],whileachromic melanomasareusuallyconsideredtobeassociatedwithapoorer prognosis[40].

6. Conclusion

Earlydiagnosisofmucosalmelanomaofthenasalcavityisan essentialprognosticfactor.Thepresenceofunilateralsymptoms, suchasepistaxisornasalobstruction,inapatientovertheageof 60yearsmustbeconsideredtobesuspicious.Thediagnosisisbased onhistologicalandimmunohistochemicalexaminationofabiopsy. First-linetreatmentisbasedonwidesurgicalresection,possibly completedbyadjuvantradiotherapy.Aninitialcompleteresection withhealthymarginsisadecisivefactorforsurvival.Theoverall prognosisofthesetumoursisverypoor.Hopesforimprovementof survivalarebasedonprogressinradiotherapytechniquesandcell andgenetherapythatarecurrentlyunderevaluation.

Disclosureofinterest

Theauthorsdeclarethattheyhavenoconflictsofinterest con-cerningthisarticle.

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