Estudo anatômico do forame jugular no pescoço

www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Anatomical

study

of

jugular

foramen

in

the

neck

夽

Carlos

Alberto

Ferreira

de

Freitas

_,

_Luiz

_Roberto

_Medina

_dos

_Santos

_,

Andreza

Negreli

Santos

,

Augusto

Barreto

do

Amaral

Neto

,

Lenine

Garcia

Brandão

a_{UniversidadeFederaldoMatoGrossodoSul(UFMS),FaculdadedeMedicina,CampoGrande,MS,Brazil} b_{CentrodePesquisaOncológica(CEPON),Florianópolis,SC,Brazil}

c_{UniversidadedeSãoPaulo(USP),FaculdadedeMedicina,SãoPaulo,SP,Brazil}

Received17March2018;accepted19September2018 Availableonline9October2018

KEYWORDS Skullbase; Jugularveins; Glossopharyngeal nerve; Vagusnerve; Accessorynerve Abstract

Introduction:Theanatomicalcomplexityofthejugularforamenmakessurgicalproceduresin thisregiondelicateanddifficult.Duetotheadvancesinsurgicaltechniques, approachesto thejugularforamenbecamemorefrequent,requiringimprovementoftheknowledgeofthis regionanatomy.

Objective:Tostudytheanatomyofthejugularforamen,internaljugularveinand glossopharyn-geal, vagusandaccessory nerves,andtoidentify theanatomicalrelationshipsamongthese structuresinthejugularforamenregionandlateral-pharyngealspace.

Methods:A totalof60 sidesof30 non-embalmedcadaverswere examinedfew hoursafter death.Thediametersofthejugularforamenanditsanatomicalrelationshipswereanalyzed.

Results:Thediametersofthejugularforamenandinternaljugularveinweregreateronthe rightsideinmoststudiedspecimens.Theinferiorpetrosalsinusendedintheinternaljugular veinupto40mmbelowthejugularforamen;in5%ofcases.Theglossopharyngealnerve exhi-bitedanintimateanatomicalrelationshipwiththestyloglossusmuscleafterexitingtheskull, andthevagalnervehadasimilarrelationshipwiththehypoglossalnerve.Theaccessorynerve passedaroundtheinternaljugularveinviaitsanteriorwallin71.7%ofcadavers.

Conclusion:Anatomicalvariationswerefoundinthedimensionsofthejugularforamenandthe internaljugularvein,whichwerelargerinsizeontherightsideofmoststudiedbodies; vari-ationsalsooccurredinthetrajectoryandanatomicalrelationshipsofthenerves.Thepetrosal sinuscanjointheinternaljugularveinbelowtheforamen.

© 2018 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Published by Elsevier Editora Ltda. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/).

夽 _{Pleasecitethisarticleas:FreitasCA,SantosLR,SantosAN,AmaralNetoAB,BrandãoLG.Anatomicalstudyofjugularforameninthe}

neck.BrazJOtorhinolaryngol.2020;86:44---8.

∗_{Correspondingauthor.}

E-mail:caff2004@hotmail.com(C.A.Freitas).

PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.

https://doi.org/10.1016/j.bjorl.2018.09.004

1808-8694/©2018Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen

PALAVRAS-CHAVE Basedocrânio; Veiasjugulares; Nervoglossofaríngeo; Nervovago; Nervoacessório

Estudoanatômicodoforamejugularnopescoc¸o Resumo

Introduc¸ão: Acomplexidadeanatômicadoforamejugulartornaarealizac¸ãodeprocedimentos cirúrgicosnessaregiãodelicadaedifícil.Devidoaosavanc¸osobtidosnastécnicascirúrgicas,as abordagensdoforamejugulartêmsidofeitascommaiorfrequência,oquerequerumamelhoria correspondentenoconhecimentodesuaanatomia.

Objetivo: Estudaraanatomiadoforamejugular,daveiajugularinternaedosnervos glossofa-ríngeo,vagoeacessório,assimcomoasrelac¸õesanatômicasentreestasestruturasnaregião doforamejugularenoespac¸oparafaríngeo.

Método: Foramexaminados60ladosde30cadáveresfrescosalgumashorasapósamorte.Os diâmetrosesuasrelac¸õesanatômicasforamanalisados.

Resultados: Osdiâmetrosdoforamejugularedaveiajugularinternaforammaioresnolado direitonamaioriadosespécimesestudados.Oseiopetrosoinferiorterminavanaveiajugular internaaté40mmabaixodoforamejugular,em5%doscasos.Onervoglossofaríngeoexibiu umarelac¸ãoíntimaanatômicacomomúsculoestiloglossoapósasuasaídadocrânioeonervo vagoexibiuumarelac¸ãosemelhantecomonervohipoglosso.Onervoacessóriopassouemtorno daveiajugularinternaviasuaparedeanteriorem71,7%doscadáveres.

Conclusão:Foram encontradasvariac¸ões anatômicas nasdimensões doforamejugular e da veiajugularinterna,queapresentaramtamanhosmaioresàdireitanamaioriadosespécimes estudados;variac¸õestambémocorreramnatrajetóriaenasrelac¸õesanatômicasdosnervos.O seiopetrosopodeseuniràveiajugularinternaabaixodoforame.

© 2018 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Publicado por Elsevier Editora Ltda. Este ´e um artigo Open Access sob uma licenc¸a CC BY (http:// creativecommons.org/licenses/by/4.0/).

Introduction

Thejugularforamenisanopeninginthepetro-occipital fis-sure formedby thejunctionofthe petrousportionof the temporalboneandthelateralborderoftheoccipitalbone. Itislocatedattheskullbase,lateraltotheforamen mag-num,posteriorandmedialtothebaseofthestyloidprocess ofthetemporalbone,slightly lateralandposteriortothe carotidcanalandlateraltothehypoglossalnervecanal.1,2

The internal jugular vein, the main venous drainage pathway of thebrain, andthree cranial nerves, the glos-sopharyngealnerveorcranialnerveIX,thevagalnerveor cranialnerveX andtheaccessoryorcranialnerveXI,pass throughthejugularforamen,alsocalledtheposteriorlace rum,3_{toreachtheneck.Theinferiorpetrosalsinus,which}

drainsbloodfromthecavernoussinustothejugularbulbor totheinternaljugularveinitself,andoneormorebranches of theascendingpharyngeal arteryor theoccipital artery tothemeninges,1,2,4_{arealsofoundinthejugularforamen}

region.

This anatomical complexity makes performing surgical proceduresin thisregiondelicate anddifficult.5 _The

ana-tomical relationshipsof the structuresemergingfrom the loweropeningofthejugularforamenandtheirrelationships inthelateral-pharyngealspaceareofgreatinterestinthe fieldsof head andneck andskullbase surgery.This study wasperformedwiththeobjectiveofstudyingtheanatomy of the jugularforamen, the internal jugularvein and the glossopharyngeal,vagalandaccessorynervesinthejugular foramenregionandlateral-pharyngealspace.

Methods

A total of 60 dissections were performed on 30 non-embalmedadultcadavers,priortoautopsy.Thisstudywas approved by the institution’s research committee and is in accordance with the ethical and methodological stan-dards.

The groupconsisted of36 (60%)dissections of18 male corpses and 24 (40%) dissections of 12 female corpses. The age distribution ranged from 34 to 87 years, with a medianof 58 years,mean of60 yearsand standard devi-ationof 17.34 years. With regard tothe studied side, 30 (50%) were leftside dissections, and 30 (50%) were right sidedissections.Regardingskincolor,28(46.7%)dissections were performed on white cadavers, and 32 (53.3%) were performed on non-whitecadavers. The physical type was alsoobserved, with16 longilineal(26.7%)and44 normoli-neal(73.3%) bodies.None ofthebodieswereclassified as brevilineal.

The study included only cadavers without diseases of the neck that could interfere with the anatomy of the analyzed structures, such as those with tumors, those in whichdeathhad been due totraumaticcauses andthose with gross deformities of the cervical region. The study was performed on non-embalmed cadavers a few hours after death so that the results would reflect realistic conditions asclosely as possible. After careful dissection of the area and exposure of the studied structures, the dimensions, trajectory and anatomical relationships were noted.

Figure 1 Right jugular foramen(JF) after internal jugular veinremotion, accessory nerve (AC), glossopharyngealnerve (G),vagusnerve(VG),styloidprocess(ST).

Results

Theloweropening ofthejugularforamen hadthelargest diameter,rangingfrom2.8mmto13mm,withamedianof 9.0mm,meanof8.5mmandstandarddeviationof2.53mm (Fig.1).In73.3%ofthestudiedcadavers,therightsidewas largerthantheleft.

The internal jugular vein exhibited diameters of 2.5---9.0mmwithamedianof6.0mm,meanof6.2mmand standarddeviationof1.81mm.In66.6%ofthespecimens, theveinwaslargerontherightside,10%hadequal diame-ters,andin23.4%,theinternal jugularvein waslargeron theleftside(Fig.2).

The inferior petrosal sinus wasfound below thelower openingofthejugularforamenin5%ofthestudied speci-mens(3casesfromatotalof60).Itwaslocatedontheright side,occupyingtheanteriorandmedialportionofthe fora-menbetweentheglossopharyngealandvagalnerves(Fig.3) and ending in a distance varying between 23 and 40mm below the foramen, witha diameter of between 2.0 and 4.0mm.

The glossopharyngeal nerve exhibited diameters of 0.6---2.0mm,withamedianof1.0mm,meanof1.1mmand standarddeviationof0.3mm.Thenerveemergedfromthe jugularforamen in all cases studied via the anteriorand medialportion,infrontofthevagalnerve,andcurved medi-ally,neartheposteriorandinferiorfaceofthestyloglossus muscleandtheanteriorwalloftheinternalcarotidartery (Fig.2).

Thevagusnerveexhibiteddiametersof1.2---3.8mm,with a median of 2.4mm, mean of 2.4mm and standard

devi-Figure2 Leftaccessorynerve(AC)crossingposteriorlytothe internaljugularvein(IJV).JF,jugularforamen;G, glossopharyn-gealnerve;HPG,hypoglossalnerve;VG,vagusnerve.

Figure3 Rightinferiorpetrosalsinus(IPS)intheneck, acces-sory nerve(AC) crossing infront ofthe internaljugular vein (IJV).HPG,hypoglossalnerve.

ationof0.45mm.Inall casesstudied,thenerveemerged fromthejugularforamenviatheanteriorandmedial por-tion,between theglossopharyngealand accessorynerves. Inall specimens,thevagusnerveexhibitedaclose relati-onshipwiththehypoglossalnerve,which,afterexitingthe skull,continuedaroundthevagusnerveviaitsinferior gan-glion,betweentheinternaljugularveinandinternalcarotid artery,followingitstrajectorytowardthebaseofthetongue (Fig.2).

Theaccessorynerveexhibiteddiametersof0.9---2.0mm, withamedianof1.2mm,meanof1.3mmandstandard devi-ationof0.34mm.Inall casesstudied,thenerveemerged fromthejugularforamenviatheanteriorandmedial por-tion,posterior tothevagal nerve.Afterexiting theskull, itfollowedadifferenttrajectoryinrelationtotheinternal jugularvein.In71.7%ofcases,theaccessorynervepassed aroundtheanteriorwall(Fig.3),andin28.3%ofcases,it passedaroundtheposteriorwall(Fig.2).

Discussion

Thediameterofthejugularforamenwasgreaterontheright sidein73.3%ofthecadaversanalyzedinthisstudy.Others authorshavefoundsimilarresults.2,4---9

Themostimportantconclusionofthisstudywasthe fin-dingofaPetrosalLowerSinusintheneck.Thismalformation canbeanimportantcauseofbleedingduringsurgical pro-ceduresintheregion.

Extracranial extension of the inferior petrosal sinus endingintheinternaljugularveinbelowthejugular fora-menisuncommon.SuchasituationwasobservedbyGailloud et al.10 _{in 5 of 101 patients studied. According to these}

authors,thisstructureshouldbecalledtheaccessoryjugular vein.ForMilleretal.,11_{in10%ofcasesstudied,theinferior}

petrosal sinus joined theinternal jugular veinvia asmall vein in theregion correspondingtothemiddle portion of theatlastransverseprocess.

Inturn,Katsutaetal.4_{notedthatthelowerpetrosalsinus}

drainsbloodintothejugularbulbthroughmultiplechannels; thelargesthasadiameterofbetween2.0and3.0mmand passesbetweentheglossopharyngealnerve,anteriorly,and thevagal nerve,posteriorly.Theyalsostatedthat,rarely, thismainsinuschanneldrainsintotheinternaljugularvein belowtheextracranialopeningofthejugularforamen.

Rubinsteinetal.12 _{confirmedthat,asreportedinother}

studies, the area where the inferior petrosal sinus drains thebloodintothejugularvenoussystemisvariableandcan

occurwithintheforamen, intheloweropening, or below theopening.

LvandWu13_{describedaduplicationoftheupperpartof}

theinternaljugularvein,separatedbytheaccessorynerve, in0.4%ofcases.Mitsuhashi14_{foundtheendoftheinferior}

petrosal sinus below the jugular foramen in 37.3% of the studiedcases.Zhangetal.15 _{foundthischangein34.6%of}

cases,withameandiameterof2.51mmandending40mm fromthejugularforamen.

In our sample, this anatomical change was found in 5% of cases, all onthe right side, with a cervical exten-sion of 23.0---40.0mm and a diameter ranging between 2.0 and 4.0mm. The vein exited the skullvia the region medial and anterior to the jugular foramen, posterior to theglossopharyngealnerveandinfrontofthevagusnerve, confirmingthefindingsofotherstudies.

Call and Pullec,16 _Petriglieri17 _{and Rhoton and Buza}7

reportedananatomicalvariationinwhichthe glossopharyn-geal nerve exits the skull via a channel of its own. This variationwasnotfoundinanyofthecadaverswestudied. Tubbsetal.18_{foundameningealseptumseparatingthe}

glos-sopharyngealnervefromthevagalandaccessorynervesin 36%ofcases,andofthese,7.2%wereossified.Wefounda meanglossopharyngealnervediameterof1.1mm.Tekdemir etal.19_{foundameandiameterof2.3mm.}

After exiting the skull, the accessory nerve exhibits a variabletrajectoryinrelationtotheinternaljugularvein. Thisnervecurveslaterallyatalevelcorrespondingtothe transverseapophysisoftheatlasandcrossingtheinternal jugularveinmostoftenviaitsfrontwall.Wefoundthis rela-tionshipin71.7%ofthecasesstudied.Intheremaining28.3% ofcases,thenervepassedbehindthevein.Katsutaetal.4

andCock20_{havefoundsimilarresults.}

Parsons and Keith, cited by Cock,20 _{obtained a similar}

result,althoughtheyobserveda modificationinwhich,in 3.2% of the 415 skullsides studied, cranial nerve XI pas-sedthroughthejugularvein.Hinsley21_{alsofoundonecase}

out of 116 in which the accessory nerve passed through the jugular vein at the height of the posterior belly of the digastrics muscle. We found no such variationin our sample.

Caliot et al.22 _{found a higherfrequency (90%) of cases}

withthenerveinfrontofthevein.Theyalsoreportedthat the accessory nervewas posterior to the internal jugular vein on both sides in only one case. Some other studies, however, have found a slightpredominance of the acces-sorynervecrossingtheveinlaterallyviaitsanteriorwall. Diopetal.23_{foundarateof57.6%,andSalehetal.}24_52.5%.

Thisoccursatalevelcorrespondingtotheatlastransverse process,aswealsoconfirmedinourstudy.

A similarresultwasobtainedby Sooetal.,25 _with56%

and44%ofnervespassinganteriorlyandposteriorly, respec-tively.Berroneetal.26_{alsofoundanaccessorynervewitha}

‘‘pre-venous’’trajectoryinslightlymorethan50%ofcases anda‘‘retro-venous’’trajectoryintheremainingcases.

Leeetal.27_{studiedtherelationshipbetweenthe}

acces-sory nerve and the internal jugular vein in 181 patients undergoing neck dissection and found a slightly different result,withthe nervein a positiondorsal to theinternal jugularvein in 57.4%of cases andwiththe nervepassing through the internal jugular vein in 2.8% of cases. Piffer

etal.28_{analyzed32cadaversidesandalsoreportedfinding}

theaccessorynerveinadorsalpositionin81.2%ofcases.

Conclusion

Theresultsofthisstudyshowedthatimportantanatomical variations existin the loweropening of the jugular fora-men. The diameters of the jugular foramen and internal jugularvein were variableand were greater on the right sideinmostofthe studiedspecimens.The inferior petro-salsinusmayendintheinternaljugularveinupto40mm belowthejugularforameninupto5%ofcases.Thevagus nerveisclosely relatedtothehypoglossalnerve,withthe latterhavingitsownchannelforexitingtheskull.The glos-sopharyngealnervehasanintimateanatomicalrelationship withthe styloglossus muscle after it exits the skull. The accessorynervemorefrequentlypassed aroundthe inter-naljugularvein viaitsanteriorwall andlessoften via its posteriorwall.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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