www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
Carotid
blowout
syndrome
in
patients
treated
by
larynx
cancer
夽
Carlos
Miguel
Chiesa
Estomba
∗,
Frank
Alberto
Betances
Reinoso,
Alejandra
Osorio
Velasquez,
Olalla
Castro
Macia,
Maria
Jesus
Gonzalez
Cortés,
Jesus
Araujo
Nores
UniversityHospitalofVigo,Otorhinolaryngology,HeadandNeckSurgeryDepartment,Pontevedra,Spain
Received31May2016;accepted26August2016 Availableonline29September2016
KEYWORDS
Carotid; Blowout; Larynx; Cancer
Abstract
Introduction:Carotidblowoutsyndromeisanuncommoncomplicationforpatienttreatedby headandnecktumors,andrelatedtoahighmortalityrate.
Objective: Theaimofthisstudywastostudytheriskofcarotidblowoutinalargecohortof patientstreatedonlybylarynxcancer.
Methods:Retrospectiveanalysisofpatientsolderthan18years,treatedbylarynxcancerwho developedacarotidblowoutsyndromeinatertiaryacademiccentre.
Results:197 patients met the inclusion criteria,192 (98.4%)were male and5(1.6%) were female.6(3%)patientsdevelopedacarotidblowoutsyndrome,4patientshadacarotidblowout syndromelocatedintheinternalcarotidarteryand2inthecommoncarotidartery.According tothetypeofrupture,3patientssufferatypeI,2patientsatypeIIIand1patientatypeII. Fiveofthosepatientshadpreviouslyundergoneradiotherapyandallpatientsunderwenttotal laryngectomy.Wefoundastatisticalcorrelationbetweenopensurgicalprocedures(p=0.004) andradiotherapy(p=0.023)andthedevelopmentofacarotidblowoutsyndrome.
Conclusion: Carotidblowoutsyndromeisanuncommoncomplication inpatients treatedby larynxtumours.Accordingtoourresults,patientunderwentradiotherapyandpatientstreated withopensurgicalprocedureswithpharyngealopeninghaveamajorrisktodevelopthiskind ofcomplication.
© 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/).
夽 Pleasecitethisarticleas:ChiesaEstombaCM,BetancesReinosoFA,OsorioVelasquezA,CastroMaciaO,GonzalezCortésMJ,Araujo
NoresJ.Carotidblowoutsyndromeinpatientstreatedbylarynxcancer.BrazJOtorhinolaryngol.2017;83:653---8.
∗Correspondingauthor.
E-mail:[email protected](C.M.ChiesaEstomba).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.
http://dx.doi.org/10.1016/j.bjorl.2016.08.013
PALAVRAS-CHAVE
Carótida; Ruptura; Laringe; Câncer
Síndromedarupturadaartériacarótidaempacientestratadosparacâncerdelaringe
Resumo
Introduc¸ão:A síndromedarupturadacarótidaéumacomplicac¸ãoincomumnopaciente em tratamentoparatumoresdecabec¸aepescoc¸o,relacionadacomumaaltataxademortalidade.
Objetivo:Oobjetivodesteestudofoiestudaroriscoderupturadacarótidaemumagrande coortedepacientessendotratadosisoladamenteporumcâncerdelaringe.
Método: Análiseretrospectivadepacientescommaisde18anos,tratadosporcâncerdelaringe emumcentrodeassistênciaterciária,quedesenvolveramasíndromedarupturadacarótida.
Resultados: Aotodo,197pacientesatenderamaoscritériosdeinclusão,192(98,4%)eramdo sexomasculinoe5(1,6%)eramdosexofeminino.6(3%)pacientesdesenvolveramsíndromeda rupturadacarótida,4tiveramsíndromedarupturadacarótidalocalizadanaartériacarótida internae2naartériacarótidacomum.Deacordocomotipoderuptura, 3pacientes apre-sentaramsíndromedarupturadacarótidatipoI,2pacientes,síndromedarupturadacarótida TipoIIIeumtipoII.Cincodessespacienteshaviamsidopreviamentetratadoscomradioterapia etodos ospacientesforamsubmetidos alaringectomia total. Encontrou-seuma correlac¸ão estatística entre procedimentos cirúrgicosabertos (p=0,004)e radioterapia (p=0,023)e o desenvolvimentodesíndromedarupturadacarótida.
Conclusão:Asíndromederupturadacarótidaéumacomplicac¸ãoraraempacientestratados paratumoresdelaringe.Deacordocomnossosresultados,pacientessubmetidosaradioterapia epacientestratadoscomprocedimentoscirúrgicosabertoscomaberturadafaringeapresentam umriscomaiordedesenvolveressacomplicac¸ão.
© 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
Carotidblowoutsyndrome(CBS)isanuncommon complica-tionforpatientstreatedbyheadandnecktumours(HNT).1 Theincidenceofcarotidblowoutinpatientswhounderwent surgicalproceduresinvolvingheadandneckcancersranged from2.9% to4.3%.2---5In thosewhoreceivedre-irradiation becauseofrecurrentheadandneckcancers,theincidences ofcarotidblowoutvariedfrom2.6%to10%.6,7Inthisway, CBSismorefrequentinpatientswithHNTandthosecases whenradiationinducednecrosis,recurrenttumours,wound complicationsfromneckdissection,orvesselerosionfrom pharyngocutaneousfistulas.8
The mortality rateof carotid blowoutwasreported to rangefrom3%toover50% inthe literature.3---5,7---10 There-fore,inarecentmeta-analysis,themortalityrateofcarotid blowout after re-irradiation in those patients treated by headandnecktumourswasashighas76%.6On theother hand,the neurologicalsequela reportedin thosepatients whosurvivedanacuteepisodeofcarotidblowout,wasfrom 16%to50%.9
Inthepast,thetraditionalapproachtotreatthiskindof complicationwasthesurgical revisionor ligation.4,5 How-ever, these tendencies have changed in recent years into a less aggressive approach, and nowadays, endovascular techniques, includingballoons, destructive(embolization) andconstructive(stentgrafting)techniques,performedby interventionalneuroradiologistsaregainingpopularityand havingpromisingresults.1,9,10
Few studieshave discussed therelevant risk factorsof carotidblowoutoccurredin patients treatedby headand neckcanceringeneral.However,theaimof thisresearch
wastostudytheriskofcarotidblowoutinalargecohortof patientstreatedonlybylarynxcancer.
Methods
A retrospective analysis was performed on previously untreated patients, diagnosed with squamous cell carci-noma(SCC)ofthelarynx(cT1-cT4),N−/+,M−/+according to criteria of the Union Internationale Contre le Cancer (UICC)andtheAmericanJointCommitteeonCancer(AJCC) between Januaryof 2009and Januaryof 2012. Identifica-tion of caseswasachieved by informaticresearch onthe medical records of our database, using the International ClassificationofDiseases (ICD-9).Thisstudywasapproved by the ethics committee of our centre. The demographic data(age,sex),pastmedicalhistory,comorbidities,stage, typeofsurgery,CBSasacomplication,wereobtainedbya reviewofmedicalhistory.
withchemotherapy(QT),inthosecaseswheremalignancy waspresent.
Additionalpostoperativeradiotherapywasadministered to some patients with advanced neck disease (N2a/b/c, N3), when the histopathological examination revealed extracapsular spread or, in thosepatients withlymphatic micrometastases.Patientswithhistologicallyclosesurgical margins, mainly at the base of the tongue, also received post-surgicalradiotherapy4weekspostoperativelyfollowed byweeklydosestoreachatotaldoseof60Gy.
ThetypeofrupturewasclassifiedaccordingtoPowitzky et al.11 Type I: ‘‘Threatened’’ include all those CBS who occurswhenthecarotidarteryisexposedthroughsofttissue breakdown,secondarytomucocutaneousfistula,infection, tissuenecrosis,recurrenttumouroracombinationofthese. TypeII:‘‘Impeding’’,whentherupturewaslimited,itcould betemporarilysolvedwithpressureandwoundpackingand precedingtheultimatehaemorrhagebyaperiodofmonths, andtypeIII‘‘ActiveorRupture’’isconsideredrapidlyfatal. AllpatientswithsuspectofCBSwereevaluatedand sev-eral patients with type I and II CBS lesionswere treated byneuro-radiologist,andtypeIIIwastreatedwithsurgery. Carotidblowoutwasconfirmedbypossiblecausativelesions, including endoluminal irregularityor disruption, pseudoa-neurysmformation, andextravasation.11 Patientswhohad an acute bleeding but who did not receive angiographic examinations were not considered to have had a carotid blowout.Riskforcerebralischaemiawasdeterminedby bal-loonocclusiontestunderwentembolization.Thosepatients who could not tolerate this were considered for carotid stenting.
In ourdepartment,patients treatedfor headand neck malignanttumoursarefollowedduring5yearsatleast. How-ever,forthisstudy,weconsideredagroupofpatientsthat havebeenfollowedforaminimumof36months.
Statistical analysis was run in SPSS program for Win-dows,Version20.0(SPSS,INc.Illinois,EE.UU).Quantitative variables in the study were expressed as media±typical deviation.Thedifferentvariableswerecorrelatedby Pear-son Chi-squaretest andfor the comparison of continuous variables.Valuesofp<0.05wereconsideredtobe statisti-callysignificantinalltests.
Results
197 patients met the inclusion criteria, 192 (98.4%) were male and 5 (1.6%) were female. The mean age was 63.8±10.13 (Min: 40/Max: 88). Of these 37 (18.5%) were diabetics and 69 (34.5%) were hyperten-sive.The patients hadamean postoperativehaemoglobin level of 12.7±1.89g/dL and a mean albumin level of 41.0±2.98g/L. Tumoural stage of patients included 39 (19.7%) as stage I, 39 (19.7%) as stage II, 53 (26.9%) as stage 3 and 66 (33.5%) asstage IV.138 (70.05%) patients were classified asN0,14 (7.1%) as N1,13 (6.5%) asN2A, 16 (8.1%) as N2b, 13 (6.5%) as N2c and 3 (1.5%) as N3. Therewere4(2.03%)casesofdistantmetastases(M1).The mean follow-up was 46.1±12 months (Min: 11/Max: 72). Regarding thetype of surgery, themost commonwas the transorallasermicrosurgeryforglottistumours(58=29.44%)
Table1 Demographicdataofpatientswithlarynxcancer withandwithoutcarotidblowout.
Variable Totals(%) CBScases
Age 63.8±10.13(Min:
40/Max:88)
Sex M:192/F:5
Meanfollow-upwas 46.1±12months(Min: 11/Max:72)
Post-OpHgBlevel 12.7±1.89g/dL
Albuminlevel 41.0±2.98g/L
Tstage
I 39(19.7%)
II 39(19.7%) 1
III 53(26.9%) 1
IV 66(33.5%) 4
Nstage
N0 138(70.05%)
N1 14(7.1%)
N2a 13(6.5%)
N2b 16(8.1%)
N2c 13(6.5%)
N3 3(1.5%)
Mstage
M0 193(98%)
M1 4(2%)
CBS,carotidblowoutsyndrome.
and total laryngectomy without chemo-radiation therapy (23=11.6%)(Table1).
Six(3%)patientstreatedbylaryngealcancerdeveloped aCBS(Table2),4patientshadaCBSlocatedintheinternal carotidartery (ICA)and 2had a CBS located inthe com-moncarotidartery(CCA).Accordingtothetypeofrupture, 3patients suffer atypeI, 2patients suffer atype IIIand 1patient suffersa typeII. 5 of thosepatients had previ-ouslyundergone radiotherapy and all patients underwent totallaryngectomy.However,anyone underwenta radical neckdissection(Table2).
About the cause of CBS, 3 patients suffered radiation induced necrosisproved by pathologicaland image study, 2patients presentvessel erosionfrompharyngocutaneous fistulasandtumourrecurrencewasprovedbypathological examinationin1patient.Nonetheless,2caseswere man-agedwithembolization,1casewasmanagedwithsurgery andonepatientwastreatedwithastent(Fig.1).Theother 2 patients died due tosevere bleedingin the emergency room.Neurologicalsequelaewereevidentin2patientsdue
Table2 Demographicdataofpatientswithlarynxcancer andcarotidblowout.
Variable Total(%)
Age 62.5±13.48(Min:49/Max:79)
Sex M:5/F:1
Meanfollowup 17.8±20months(Min:1/Max:56) Post-OpHgBlevel 10.2±1.68g/dL
Figure1 Leftcarotidarterystentinapatientwhosuffera carotidblowoutsyndrome.
tocerebralstroke,1patientafterligationandtheotherone afterICAembolization(Table3).
Discussion
CBScanbeconsideredasaniatrogeniccomplicationofHNT treatment. The syndrome was described at first in 1962, since then, several surgical and endovascular treatment optionshavebeenattempted.12Atthebeginning,CBScould betreatedonly withsurgicalligation orsurgicalbypassof the carotidartery. However,these techniques were asso-ciatedtohigh mortalityand tohigh neurologic morbidity withratesabout40%and60%,respectively.13Inthemidof 80s,endovascular techniquestomanaged acuteCBSwere introduced.14 Then, this treatment has gradually gained popularityduetheeaseoftheapproachandlowermorbidity andmortalityratescomparedtothesurgicalapproach.1,13,15 Short and long term effects of radiation over arteries havebeen reported.Atotal radiation dosesof40Gyover a10daydurationcouldinducedamagetothevasavasorum oflargearteriesanditmight berelatedtotheruptureof greatarteriesindogsaccording toMcCreadyetal.16 Free radicals produced by radiation were also found to cause
Table4 Statisticalanalysisoffactorscommonlyassociated withcarotidblowout.
Variable p=0.05
RT 0.023
Neckdissection 0.151
Opensurgery 0.004
Fistula 0.842
thrombosis and obliteration of vasa-vasorum, adventitial fibrosis, premature atherosclerosis, andthe weakening of thearterialwallinthehistologicalexaminationofresected carotidarteries.10,11,17 Wealsofound a significant statisti-caldifferencein theappearance ofCBS,inthosepatients who received RT treatment before surgery (5/6=83.3%) (p=0.023)(Table4).
Furthermore,someauthorssuggesttheunderestimated roleofinfectionsinCBS(tissuenecrosisorfistula),andthe relationofbacterialinflammationasacauseofvasavasorum thrombosis, andsecondary arterial wall damage.18 This is whysummarizingtheeffectsovervasa-vasorumofradiation andinfection,itisnecessarytotakeintoconsiderationthe importanceof these factors,due tothe adventitial layer, whichcarriesabout80%ofthebloodsupplytotheremaining wallsofthecarotidartery.Inourseriesofpatientsaffected byCBS,2(2/6=33%)patientssufferedapharyngo-cutaneous fistulaintheearlypost-operativeperiod,and3(3/6=50%) otherpatientssufferedradiationinducingtissuenecrosis.
NecksurgeryisanothersignificantfactorrelatedtoCBS, becausethistypeofsurgeriescouldcompromisethe nutri-tionof thecarotidarteryduringcervical nodesresection, resulting in injury to the adventitial layer, and this dele-terious effectoccursindependently of radiation.9 Radical neck dissections render the carotid artery more vulnera-ble to rupture because of the lack of supporting healthy tissues.11 Moreover, in those patients with accompanying pharyngealsurgery,thereisahigherrisktodevelopaCBS due tomajorproportionofsalivaryfistula formation6 and whena hemithyroidectomyhasalsobeen carriedout,the carotidartery liesveryclosetotheskin andthe tracheal stomaincreasingtheriskofdamageovertheartery.In rela-tiontolarynx tumours,Chenetal. found anincidence of 0.9%ofCBSinpatientstreatedbylarynxtumours,alower percentagecomparedwithourresults.19However,previous literaturereviewreportsthelarynxasthemostcommon pri-marytumoursiteinalmost23%ofpatientswhosuffereda CBS.11
Table3 Patienttreatedbycarotidblowoutsyndromeatourinstitution.
Sex Treatment Stage Causeofrupture Side Site Type Neurologicalcomplaints CBStreatment
Male TL+CND+QT+RT T4aN0M0 Necrosis Right ICA I No Embolization
Male TL+CND+QT+RT T2N2cM0 Fistula Left ICA III Die Die
Male TL+CND+RT T4aN2bM0 Necrosis Left CCA I No Stent
Female TL+CND+RT T3N1M0 Necrosis Right ICA III Die Surgery
Male TL+CND T4aN2cM0 Fistula Right CCA II Yes Embolization
In our series, we only included all those patients who came tothe emergency room due toa CBS, treated pre-viously bya larynx tumour.In thisway, it isimportant to emphasizethatallofthemunderwentatotallaryngectomy withbilateral cervicalneckdissection(6/6=100%).Thisis why,according tothetypeoflarynxprocedure, wefound astatistical correlationbetween opensurgical procedures andthedevelopmentofaCBS(p=0.004).However,wedid notfindstatisticalcorrelationbetweenneckdissectionand CBS(p=0.151)whenweincludeallofourpatients(openand endoscopiclaryngealprocedures).Furthermore,itis impor-tanttounderlinethatanypatientinourseries,underwent aradicalneckdissectiondevelopingaCBS,inthisway,we can suggest that selective neck dissectioncan be related withtheappearanceofCBStoo,maybenotasamainfactor, butitcouldbeassociatedwithothertreatment strategies orcomplications(Table4).
AnotherfactorrelatedtoCBSinpreviousstudiesis the presence of mobile foreign bodies in the head and neck like tracheostomy tube, nasogastric tubes, or the pres-ence of wet gauzes. In this case wound healing can be interruptedbecauseofchronicirritationandinflammatory response.According toChen etal.thiscould explainwhy thosepatientswithopenwoundsintheneckrequirewound care with wet dressing having a 4-fold increased risk of developingcarotidblowout.19 Nutritionalfactorshavealso beenrelatedtotherisk ofCBS,andthiscanbeexplained bythe lesssoft tissuecoverage,causing the carotid arte-rial walls to weaken in the cervical region.20 Moreover, in their study Chen et al. found a 2-fold increased risk of developing carotid blowout in patients with a BMI of <22.5kg/M2.19
The incidence of cerebral complications in patients affected by CBS, up to 87% when hypotensionis present at the time of ligation comparedto 28% in normotensive patients.21 Furthermore,inthosepatientswhosurvivedan acuteepisodeofcarotidblowout,theneurologicalsequela reported was from 16% to 50%.9 Moreover, in a recent study,authorsfoundoutthatpatientswithcarotidblowout underwent surgical intervention had a higher neurologic complicationrateandmortalityratewhencomparedwith thoseofpatientsreceivedendovascularprocedures.19Inour series 2 (33.3%) patients showed up neurological sequela afterbleeding,oneofthemdiedinthefirst10daysafterthe initialepisodeduetoare-bleeding,andtheotherpatient sufferedandhemiparesisasalongtermsequela.
About the best option to treat this complication on these days, there exists a trend in favour of endovascu-lar techniques. However,recent studies shows that there is no statistical significant difference in technical and hemostatic outcomes between reconstructive and decon-structive endovascular techniques.8,22,23 Moreover, other authorssuggestthat permanentvesselocclusionresultsin higherimmediately cerebralischaemia, butstentgrafting induces potentially delayed complications, such as infec-tions,rebleedingorstentthrombosis.8,11
Finally, our study has anumber of limitations. Primar-ily, its retrospective nature and the small sample size can limit the validity of our results. Moreover, we only includedpatientstreatedbylarynxtumours,andthiskind of complications can affect all those patients treated by head and neck tumours. In this way, a prospective study
comparing the results of different types of treatments couldbenecessary.
Conclusion
Carotid blowoutsyndrome (CBS) is an uncommon compli-cationinpatientstreatedbylarynxtumours.Accordingto ourresults,patientsunderwentradiotherapy andpatients treated with open surgical procedures with pharyngeal opening,haveamajorrisktodevelopaCBS.Inthiswayis necessarytotryingtopredicttheriskinallofourpatients and take the appropriate actions to prevent this kind of complications.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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