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www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Intrasphenoid

septations

inserted

into

the

internal

carotid

arteries:

a

frequent

and

risky

relationship

in

transsphenoidal

surgeries

Clauder

Oliveira

Ramalho

a,b,∗

,

Horacio

Armando

Marenco

a,b

,

Francisco

de

Assis

Vaz

Guimarães

Filho

c

,

Marcos

Devanir

Silva

da

Costa

a

,

Bruno

Fernandes

de

Oliveira

Santos

a

,

Rodrigo

de

Paula

Santos

d

,

Samuel

Tau

Zymberg

a,b

aUniversidadeFederaldeSãoPaulo(UNIFESP),DepartamentodeNeurocirurgia,SãoPaulo,SP,Brazil

bUniversidadeFederaldeSãoPaulo(UNIFESP),ProgramadePós-graduac¸ãodoDepartamentodeOtorrinolaringologiaeCirurgia

deCabec¸aePescoc¸o,SãoPaulo,SP,Brazil

cUniversidadeFederaldeSãoPaulo(UNIFESP),SãoPaulo,SP,Brazil

dUniversidadeFederaldeSãoPaulo(UNIFESP),DepartamentodeOtorrinolaringologia,SãoPaulo,SP,Brazil

Received7January2016;accepted19February2016 Availableonline22April2016

KEYWORDS

Sphenoidsinus; Sphenoidseptations; Skullbase;

Transsphenoidal surgery;

Expandedendonasal approach

Abstract

Introduction:Whenanexpandedendonasaltranssphenoidalsurgicalapproach isperformed, intrasphenoidseptations must be completely resected.If these structures areclose tothe internalcarotidartery(ICA),thentheirmanipulationmightcausevascularinjury.

Objective:Theobjectiveofthisstudyistodescribethefrequencyofintrasphenoidseptations intheinternalcarotidarteryprotuberance(ICAp).

Methods:Computedtomography(CT)scansof421patientswereanalysed.Intrasphenoid septa-tions(classifiedasintersphenoidoraccessory)andtheirrelationshiptotheICApweredescribed. Additionally,asphenoidsinusclassificationwasperformedbasedontheirdegreeof pneuma-tisationtodeterminewhetheradifferenceexistsinthefrequencyofintrasphenoidseptations insertedintoICApwithregardtosinustype.

Results:Thepatientmeanagewas39±21.4years.Overall,219patients(52%)hadseptations intheICAp;359patients(85.3%)hadintersphenoidseptations;ofthelatter,135(37.6%)had septationsintheICAp.Thisfrequencywashigheramongpatientswithsphenoidsinustype4or 5(44.7%and43.5%,respectively).Accessoryseptationswerefoundin255patients(60.6%);140 oftheseseptations(54.9%)wereintheICAp.Among351patientswithtypes3,4or5sphenoid

Pleasecitethisarticleas:RamalhoCO,MarencoHA,GuimarãesFilhoFA,daCostaMD,deOliveiraSantosBF,dePaulaSantosR,etal.

Intrasphenoidseptationsinsertedintotheinternalcarotidarteries:afrequentandriskyrelationshipintranssphenoidalsurgeries.BrazJ Otorhinolaryngol.2017;83:162---7.

Correspondingauthor.

E-mail:[email protected](C.O.Ramalho).

PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.

http://dx.doi.org/10.1016/j.bjorl.2016.02.007

(2)

sinuses(i.e.,onlywell-pneumatisedsphenoidsinuses),219(62.4%)hadseptationsintheICAp. Thesefrequenciesarehigherthanthosereportedinmostpreviousstudies.

Conclusion: Thefrequency ofintrasphenoid septationsinthe ICApfoundis considerable.It ishigheramongpatientswithmorepneumatisedsinuses.Thisfindingjustifiesanappropriate pre-operativestudy,andcarefulattentionmustbepaidduringtranssphenoidalsurgery. © 2016 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/).

PALAVRAS-CHAVE

Seioesfenoidal; Septac¸ões esfenoidais; Basedocrânio; Cirurgia transesfenoidal; Abordagemendonasal ampliada

Septac¸õesintraesfenoidaisinseridasnasartériascarotídeasinternas:umarelac¸ão frequenteearriscadanascirurgiastransesfenoidais

Resumo

Introduc¸ão: Quandoumaabordagemcirúrgicatransesfenoidalendonasalampliadaérealizada, septac¸õesintraesfenoidaisdevemsercompletamenteressecadas.Seestasestruturasestiverem próximasàartériacarótidainterna(ACI),amanipulac¸ãopodecausarlesãovascular.

Objetivo: Oobjetivodesteestudofoidescreverafrequênciadeseptac¸õesintraesfenoidaisna protuberânciadaartériacarótidainterna(pACI).

Método: Examesdetomografiacomputadorizada(TC)de421pacientesforamanalisados.As septac¸ões intraesfenoidais (classificadas como interesfenoidais ouacessórias) e suarelac¸ão comapACIforamdescritas.Alémdisso,umaclassificac¸ãodoseioesfenoidalfoirealizadacom basenoseugraudepneumatizac¸ãoparadeterminarseexisteumadiferenc¸anafrequênciade septac¸õesintraesfenoidaisinseridasempACIemrelac¸ãoaotipodeseio.

Resultados: Pacientes com idade média de 39±21,4 anos foram incluídos. No geral, 219 pacientes (52%) apresentavam septac¸ões na pACI; 359 (85,3%) tinham septac¸ões interes-fenoidais; 135(37,6%)comseptac¸õesnapACI. Estafrequênciafoimaiorentreospacientes comseioesfenoidaltipo4ou5(44,7e43,5%,respectivamente).Asseptac¸õesacessóriasforam encontradas em 255doentes (60,6%);140 dessasseptac¸ões(54,9%)estavam napACI. Entre 351 pacientescom seiosesfenoidaistipos 3, 4ou 5(isto é,apenas seios esfenoidais bem-pneumatizados),219 (62,4%)tinhamseptac¸ões napACI.Estasfrequências sãosuperiores às relatadasnamaioriadosestudos.

Conclusão:A frequência de septac¸ões intraesfenoidais na pACI encontrada é considerável, sendomaiorentrepacientescomseiosmaispneumatizados.Esteachadojustificaumestudo pré-operatório adequado euma atenc¸ãoespecial deve serdada duranteacirurgia transes-fenoidal.

© 2016 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

Transnasal transsphenoidal surgery has developed

sig-nificantly over recent decades. The cooperative work

betweenneurosurgeonsandear,neckandthroatsurgeons

has been essential for this development. The

introduc-tion of the endoscope was another landmark. Compared

with the microscope, the endoscope enabled additional

expansion of this surgical technique, thereby increasing

the possibility of resecting lesions not otherwise eligible

for transnasal transsphenoidal surgery.1 With the

emer-gence of the endoscopic expanded endonasal approach,

areas such as the clivus, the petrous bone, the

mid-dle cranial fossa and the infratemporal fossa became

accessible.2 An extensive sphenoidotomy with septation

resection is necessary to create an adequate surgical

corridor.3

Intrasphenoid septations are bony structures found in

thesphenoidsinuswithseveralanatomicalconformations.

Because they are located in the sinus walls, they are

often adjacent to surrounding structures, especially the

internal carotid artery (ICA), which can increase the risk

of expanded transsphenoidal surgeries during septation

resection(Fig.1).

ICA injury is one of the most dramatic intraoperative

complications. This injury can lead to a challenging

sur-gical scenario featuring rapid blood loss that can result

in patient exsanguination.4 An appropriate pre-operative

radiologicevaluationofthesphenoidsinusanditsseptations

isnecessarytopreventthiscomplication.

Previousarticleshavedescribedthefrequencyof

intras-phenoidseptationsinthe ICAprotuberance(ICAp).1---5 The

majorityof thesearticleshave found fewerintrasphenoid

(3)

Figure1 (a)CTscanaxialview ofanintersphenoidseptationintheleft internalcarotid arteryprotuberance(ICAp)and(b) intraoperativeview(0◦endoscope)showingthesameseptationintheleftICAp.

currentarticledescribesthefrequencyofintrasphenoid

sep-tationsintheICApamongasampleof421patientsanalysed

usingcomputedtomography(CT)scansandcomparesthese

findingswiththoseofpreviousstudies.

Methods

Sampleandselectioncriteria

We searched the database of the department of

radiol-ogy of a hospital institution from January 2010 to April

2013 for patients who underwent CT scans of the skull

base. Individuals with a previous history of paranasal

sinusdisease orendonasal surgerywereexcluded. Atotal

of 421 patients were selected. Informed consent was

obtained from all individual participants included in the

study.

AllpatientsunderwentaCTscanwithskullbasesections

usingtheBrillianceCT64system(Philips,2004).The scan

wasperformedwith20×0.625collimation,apitchof0.348,

amatrixof512;200mmoffieldofview.Sectionthickness

ranged from0.6 to 1mm. The obtained data were

trans-ferredtotheExtendedBrillianceWorkspace(PhilipsMedical

System),wheretheimageswerereconstructedintheaxial,

coronal,andsagittalplanes.

Septationtypedefinitionanditsrelationshipwith ICAp

Intrasphenoid septations were classified as intersphenoid

whenthey(1) werelongitudinal andina medianor

para-median location and (2) separated the cavity into two

non-communicatingcompartmentsfromtheanteriortothe

posteriorsinuswall.Aseptationwasdefinedasanaccessory

whenitdidnotfollowalloftheintersphenoidsinuspatterns

(Fig.2).

Toconsiderthetruerelationshipbetweenseptationand

ICAp, aCTsection hadtoclearlyshowa septationin this

structure(Fig.2).

Sinusclassification

Sphenoidsinuses were classifiedbased ontheir degree of

pneumatisation,whichwasestablishedbythespatial

rela-tionship of the sinus posterior wall and the anterior and

posteriorwallsofthesellaturcica.Sinuseswereclassifiedas

follows:thosewithanabsenceofaerationorminimal

aera-tionwereclassifiedastype1;thosewiththeirposteriorwall

inapositionrostraltothesellaanteriorwallwereclassified

astype2;thosewiththeirposteriorwallbetweenthesella

anteriorandposteriorwallswereclassifiedastype3;those

withtheirposteriorwallreachingtheposteriorwallofthe

(4)

Figure3 Sinusclassification.MidsagittalreformattedimagesobtainedfromCTscans.(a---e)Types1through5sphenoidsinuses, respectively.

sellawereclassifiedastype4;andthosewithposterior

cli-noidaerationwereclassifiedastype5.Thepurposeofthis

analysiswastoassesswhetherthefrequencyofseptationin

theICApdifferedacrosspatientswithdisparatesinustypes

(Fig.3).

Statisticalanalyses

Categorical variableswere described bynumbers of cases

and percentages. Groups were comparedusing the z-test

for proportions and either the chi-square test or Fisher’s

exacttest,asappropriate.Continuousvariableswere

char-acterised as either the mean±standard deviation or the

median and interquartile range depending on normality;

between-group comparisonswere madeusingStudent’s t

-test or the Kruskal---Wallis test, respectively. A resultwas

considered significant when p<0.05. Statistical analyses

wereconductedwiththeSPSS17(Chicago,IL,USA).

Researchprotocol

Theethicscommitteeapprovedtheresearchprotocol

(doc-umentnumber186.717).

Results

Weidentified189maleand232femalepatients(meanage:

39±21.4years).Themostfrequenttypeofsinuswastype

4(61%ofcases)(Table1).

Atotalof359patients(85.3%)hadintersphenoid

septa-tions.Outoftheseseptations,135(37.6%)werefoundinthe

ICAp.Totalsof44.7%and43.5%ofpatientswithtype4and

5sinuseshadintersphenoidseptationsintheICAp,

respec-tively;only14.1%ofpatientswithtype3sinuseshadthese

septationsintheICAp.Patientswithtypes1or2sinusesdid

nothaveICAp-adjacentseptations.

Accessoryseptationswerefoundin255patients(60.6%).

These septations were present in only one-quarter of

patientswith type2 sinuses, whereasmost of those with

types 3, 4 or 5 sinuses had septations. Septations were

located in the ICAp of 140 patients (54.9% of those with

accessoryseptations;25.4%,42.8% and52.2% for types3,

4and5,respectively).Themaximumnumbersfoundwere

2,3,5,and4fortypes2,3,4,and5,respectively,whereas

themaximum numbersfoundintheICApwere2,3,and3

fortypes3,4,and5,respectively.

The number of patients with septation in the ICAp,

regardless of type, was 219 (52%). Those patients were

older than those without septations (43±18 vs. 34±23;

p<0.0001); no significant difference was observed with

regardtosex(femalescomprised 55%of allcasesin both

groups, p=0.963). Patients with types 4 and 5 sphenoid

sinusesweremorecommonthanthosewithtype3(Table2).

Ofthe351patientswithtype3,4or5sphenoidsinuses,

219 (62.4%) had septations in the ICAp. A total of 322

patients (91.7%) had intersphenoid septations; of these

patients,135(41.9%)hadseptationsintheICAp.Ofthe244

patientswithatleastoneaccessoryseptation,140(57.4%)

(5)

Table1 Intersphenoidandaccessoryseptationsbysinustype.

Sinustype

1 2 3 4 5

Total(%) 26(6.2) 44(10.5) 71(16.9) 257(61) 23(5.5)

Meanage(interquartile range)

4(8)a 35(51) 43(34) 42(30) 46(28)

Males 14(53.8) 24(54.5) 33(46.5) 104(40.5) 14(60.9)

Intersphenoidseptation --- 37(84.1) 66(93) 237(92.2) 19(82.6)

Intersphenoidseptation intheinternalcarotid arteryprotuberance (ICAp)

--- --- 10(14.1) 115(44.7) 10(43.5)

Accessoryseptation --- 11(25) 45(63.4) 181(70.4) 18(78.3)

Accessoryseptationin theICAp

--- --- 18(25.4) 110(42.8) 12(52.2)

aMediansignificantlydiffersfromtheothers(p<0.05).

Table2 Sphenoidseptationintheinternalcarotidartery protuberancebysinustype.

Total %

Type1 ---

---Type2 ---

---Type3 23 32.4% a

Type4 179 69.6% b

Type5 17 73.9% b

Proportionsidentifiedwithdifferentlettersaresignificantly dif-ferentaccordingtothez-testforproportions(p<0.05).

Discussion

Theexpandedendonasaltranssphenoidalapproachmarked a breakthrough in skull base surgery. With its develop-ment,lesionspreviouslyinaccessibleusingtheconventional endonasal route (e.g., those in the cavernous sinus, the planum sphenoidale, the middle cranial fossa, Meckel’s cave, the suprasellar region and the clivus) could be accessed.2 To obtain appropriate exposure and

accommo-datethesurgicalendoscopicinstruments,awidesphenoid

sinus opening is required with intrasphenoid septation

resection.3

Intrasphenoid septations are naturally occurring bony

structures inside the sphenoid sinus that divide it into

compartments. They are divided into intersphenoid and

accessory septations. The association with fusion lines

between ossification centres(synchondrosis)and the

sep-tationpositionsmightexplaintheirorigin.6,7Ingeneral,one

or more intersphenoidseptations are present. They show

greatvariability;therefore,theytypicallycreatetwo

asym-metriccompartments:rightandleft.Accessoryseptations

occur in different positions and are also common. Both

canbefound instructuresadjacent tothesphenoidsinus

increasingtheriskofneurovasculardamageduringsurgery,

especiallywhentheyarelocated intheICAp. Cope

previ-ouslydescribedthiscomplicationin1917.6

Inourstudy,CTscansrevealedthat 219patients(52%)

hadseptationsintheICAp.Amongpatientswithtype3,4,

or5sinuses(i.e.,well-pneumatisedsphenoidsinuses),this

prevalencewasevenhigher(62.4%).

Ourdatacontrastwiththoseofpreviouspapersshowinga

smallerprevalence.5,8---12However,Fernandez-Mirandaetal.

showedradiologicprevalenceof85%amongpatientswithat

leastoneseptationintheICAp.3

RennandRhotonfoundintersphenoidseptationsnextto

theICAchannelin32%ofcadavers.5Sethidescribed

inter-sphenoid septations in the ICAp in 40% of 30 cadavers in

an endoscopic study in 1995.8 Unal et al. and Abdullah

etal.reported30%and31% ofseptationsofthesphenoid

sinusattachedtothewalloftheICA,respectively,usingCT

scans.10,12

Elwany et al. found that 12.9% of patients had

septa-tions in the bone surrounding the ICAp in an endoscopic

studywith93cadavers.9Hamidetal.showedfrequenciesof

4.7%and6.75%forintersphenoidandaccessoryseptations

intheICAp,respectively.11 Bothofthesestudiesrepresent

thelowestfrequenciesintheliterature.

Thecurrentfindingssupporttheneedforapre-operative

radiologic study on intrasphenoid septations. Appropriate

knowledgeconcerningtheirpositionandtheirrelationship

tosurrounding structuresmight significantly decrease the

riskofsurgerycatastrophesduetovascularinjuries.

Pre-operativeCTscansaretheradiologicalevaluationof

choicebecausetheyadequatelyvisualise bonestructures.

Theanalysisoftheaxial,coronal,andsagittalplanesaswell

astheir3dimensionalreconstructionabilityallow

radiolo-giststoaccuratelydeterminewhetheraseptation isclose

tothestructuressurroundingthesphenoidsinus(e.g.,the

ICA).3,13---16

With regard to sinus classification, patients with type

4 or 5 sinuses weremore likelytohave septations in the

ICAp than patientswithtype 3sinuses. The aeration

pro-cessthatthesphenoidbodyundergoesexplainsthisresult.

WhentheICAispronounced,itcansubstantiallybulgeinto

thepneumatisedsinus,therebyincreasingtheareathatis

susceptibletoaseptationattachment.13

Thefactthatsinusesaremorepneumatisedinolder

peo-plemightexplainthehighermeanageofthepatientswho

(6)

The present study describes the anatomicalfindingsof

alarge,multiracialpopulation.Toourknowledge,itisthe

largestseriesregardingthisissue.

Conclusion

The high frequency of intrasphenoid septations in the

ICAprequiresanappropriatepre-operativeradiologicstudy.

Furthermore, careful attention should be paid during

transsphenoidal surgeryto reduce potentially serious

vas-cularinjuries.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

References

1.FelisatiG,Lenzi R,PipoloC,MaccariA, MessinaF,RevayM, etal.Endoscopicexpandedendonasalapproach---preliminary experiencewiththenew3Dendoscope.ActaOtorhinolaryngol Ital.2013;33:102---6.

2.Kassam AB, Gardner P, Snyderman C, Mintz A, Carrau R. Expanded endonasal approach fully endoscopic, completely transnasalapproachtothemiddlethirdoftheclivus,petrous bone,middlecranialfossa,andinfratemporalfossa.Neurosurg Focus.2005;19:E6.

3.Fernandez-Miranda JC, Prevedello DM, Madhok R, Morera V, Barges-Coll J, Reineman K, et al. Sphenoid septations and theirrelationshipwithinternalcarotidarteries:anatomicaland radiologicalstudy.Laryngoscope.2009;119:1893---6.

4.Valentine R, Wormald PJ. Controlling the surgical field during a large endoscopic vascular injury. Laryngoscope. 2011;121:562---6.

5.Renn W, Rhoton AL Jr. Microsurgical anatomy of the sellar region.JNeurosurg.1975;43:288---98.

6.CopeVZ.Theinternalstructureofthesphenoidalsinus.JAnat. 1917;51:127---36.

7.HaetingerRG,NavarroJA,LibertiEA.Basilarexpansionofthe humansphenoidalsinus:anintegratedanatomicaland comput-erizedtomographystudy.EurRadiol.2006;16:2092---9.

8.Sethi DS, Stanley RE, Pillay PK. Endoscopic anatomy of the sphenoidsinus and sellaturcica. JLaryngol Otol. 1995;109: 951---5.

9.ElwanyS,ElsaeidI,ThabetH.Endoscopicanatomyofthe sphe-noidsinus.JLaryngolOtol.1999;113:122---6.

10.UnalB,BademciG,BilgiliYK,BatayF,AvciE.Riskyanatomic variations of sphenoid sinus for surgery. Surg Radiol Anat. 2006;28:195---201.

11.HamidO,ElFikyL,HassanO,KotbA,ElFikyS.Anatomic varia-tionsofthesphenoidsinusandtheirimpactontrans-sphenoid pituitarysurgery.SkullBase.2008;18:9---15.

12.Abdullah BJ,Arasaratnam S,Kumar G, Gopala K. The sphe-noidsinuses:computedtomographicassessmentofseptation, relationshiptotheinternalcarotidarteries,andsidewall thick-nessintheMalaysianpopulation.HongKongJRadiol.2001;4: 185---8.

13.GuldnerC,PistoriusSM,DiogoI,BienS,SesterhennA,Werner JA.Analysisofpneumatizationandneurovascularstructuresof thesphenoidsinus usingcone-beam tomography(CBT).Acta Radiol.2012;253:214---9.

14.HewaidiG,OmamiG.Anatomicvariationofsphenoidsinusand relatedstructuresinLibyanpopulation:CTscanstudy.LibyanJ Med.2008;3:128---33.

15.Meloni F,Mini R, Rovasio S, Stomeo F,Teatini GP. Anatomic variationsofsurgicalimportanceinethmoidlabyrinthand sphe-noidsinus.Astudyofradiologicalanatomy.SurgRadiolAnat. 1992;14:65---70.

16.DavoodiM,Saki N,SakiG,RahimF.Anatomicalvariationsof neurovascularstructuresadjacentsphenoidsinusbyusingCT scan.PakJBiolSci.2009;12:522---5.

Imagem

Figure 1 (a) CT scan axial view of an intersphenoid septation in the left internal carotid artery protuberance (ICAp) and (b) intraoperative view (0 ◦ endoscope) showing the same septation in the left ICAp.
Figure 3 Sinus classification. Midsagittal reformatted images obtained from CT scans. (a---e) Types 1 through 5 sphenoid sinuses, respectively.
Table 1 Intersphenoid and accessory septations by sinus type.

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