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Brazilian

Journal

of

OTORHINOLARYNGOLOGY

www.bjorl.org

ORIGINAL

ARTICLE

Repeated

fine-needle

aspiration

cytology

for

the

diagnosis

and

follow-up

of

thyroid

nodules

Agnaldo

José

Graciano

a,∗

,

Carlos

Takahiro

Chone

b

,

Carlos

Augusto

Fischer

c

,

Giuliano

Stefanello

Bublitz

d

,

Ana

Jacinta

de

Aquino

Peixoto

a

aHospitalSãoJosé,Joinville,SC,Brazil

bDisciplinadeOtorrinolaringologiaCabec¸aePescoc¸o,UniversidadeEstadualdeCampinas(UNICAMP),Campinas,SP,Brazil cSetordeOtorrinolaringologiaeCirurgiadeCabec¸aePescoc¸o,HospitalSãoJosé,Joinville,SC,Brazil

dServic¸osIntegradosdePatologia,Joinville,SC,Brazil

Received30September2013;accepted28December2013 Availableonline22July2014

KEYWORDS

Thyroidgland; Thyroidneoplasms; Fineneedlebiopsy; Headandneck neoplasms

Abstract

Introduction:Therecently-proposedBethesdareportingsystemhasofferedclinical recommen-dationsforeachcategoryofreportedthyroidcytology,includingrepeatedfine-needleaspiration (FNA)fornon-diagnosticandatypia/follicularlesionsofundeterminedsignificance,butthere arenosoundindicationsforrepeatedexaminationafteraninitialbenignexam.

Objective:ToinvestigatetheclinicalvalidityofrepeatedFNAinthemanagementofpatients withthyroidnodules.

Method: Thepresentstudyevaluated412consecutivepatientswhohadrepeatedaspiration biopsiesofthyroidnodulesafteraninitialnon-diagnostic,atypia/follicularlesionof undeter-minedsignificance,orbenigncytology.

Results:The majorityof patients were female (93.5%) ranging from 13 to 83 years. Non-diagnosticcytologywasthemostcommonindicationforarepeatedexaminationin237patients (57.5%), followed by benign (36.8%), and A/FLUS(5.6%) cytology.A repeated examination altered theinitial diagnosis in70.5%and78.3% ofthenon-diagnostic andA/FLUSpatients, respectively,whereasonly28.9%ofpatientswithabenigncytologypresentedwithadifferent diagnosisonasequentialFNA.

Conclusions:RepeatFNAisavaluableprocedureincaseswithinitialnon-diagnosticorA/FLUS cytology,but itsroutine usefor patients withaninitial benignexamination appears tonot increasetheexpectedlikelihoodofamalignantfinding.

© 2014Associac¸ãoBrasileira de Otorrinolaringologiae CirurgiaCérvico-Facial. Publishedby ElsevierEditoraLtda.Allrightsreserved.

Pleasecitethisarticleas:GracianoAJ,ChoneCT,FischerCA,BublitzGS,PeixotoAJ.Repeatedfine-needleaspirationcytologyforthe diagnosisandfollow-upofthyroidnodules.BrazJOtorhinolaryngol.2014;80:422---7.

Correspondingauthor.

E-mail:entbrazil@gmail.com(A.J.Graciano).

http://dx.doi.org/10.1016/j.bjorl.2014.07.002

1808-8694/©2014Associac¸ãoBrasileiradeOtorrinolaringologia eCirurgiaCérvico-Facial. PublishedbyElsevierEditoraLtda.All rights

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PALAVRAS-CHAVE

Glândulatireoide; Neoplasiasda glândulatireoide; Biópsiaporagulha fina;

Neoplasiasdecabec¸a epescoc¸o

Repetic¸ãodapunc¸ãoporagulhafinaparaodiagnósticoeseguimentodenódulosde tireoide

Resumo

Introduc¸ão: A classificac¸ão de Bethesda para relatórios citológicos de tireoide oferece recomendac¸ões clínicasparacadacategoriadiagnóstica,incluindoarepetic¸ãodoexamede punc¸ãopara examescitológicosnão diagnósticos(ND) eatipia/lesãofoliculardesignificado indeterminado(A/FLUS).Todavia,arepetic¸ãodapunc¸ãoparapacientescomexamecitológico inicialbenignoaindaédiscutida.

Objetivo: Investigaravalidadedapunc¸ãorepetidaparaomanejodepacientescomnódulos tireoidianos.

Método: Estudolongitudinalhistóricoavaliando412pacientesconsecutivoscombiópsias aspi-rativasrepetidasdenódulosdatireoideapósexameinicialND,A/FLUS,oubenigno.

Resultados: Acitologianãodiagnósticafoiaindicac¸ãomaiscomumparaumexamerepetido em 237pacientes(57,5%),seguidaporcitologiainicial benigna(36,8%)eA/FLUS(5,6%).Um examerepetidoalterouodiagnósticoinicialde70,5%e78,3%dospacientescomcitologiainicial não diagnósticaeA/FLUS,respectivamente,enquantoapenas28,9%dospacientescomuma citologiainicialbenignaapresentaramumdiagnósticodiferenteemumapunc¸ãosequencial.

Conclusões: Repetirapunc¸ãoaspirativaéumprocedimentoválidoparapacientescom citolo-giainicialnãodiagnósticaouatipia/lesãofoliculardesignificadoindeterminado,masseuuso rotineiroem pacientescomexameinicial benignoparecenão aumentaraprobabilidadede malignidadeparaestegrupo.

©2014Associac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.Publicado por ElsevierEditoraLtda.Todososdireitosreservados.

Introduction

Thyroid nodules are common. Current data suggest that nodules are present in 5% to 10% of women and 1% to 2%of adultmen.1---3 Furthermore,nodules havebeen inci-dentally diagnosed via ultrasound scans in up to 67% of elderly females.4,5 It is believed that 5% to 15% of these nodulesaremalignant.6Clinicalanddiagnosticfindingsare warranted todifferentiatepatients at risk for malignancy whorequirefurtherworkup.Thisenhanceddiagnosislikely contributestotheincreaseinsurgicallytreatedthyroid can-cersover the last decades,which affect 3.5---8.5/100,000 of womenand 2.3/100,000 of men.7,8 Fine-needle aspira-tion(FNA)biopsyhasproved tobeavaluabletoolfor the evaluation of these nodules, with a diagnostic accuracy of approximately97% and pivotal clinical implications.9,10 In general, FNA biopsy is recommended for solid hypoe-choicnodulesgreaterthan1cminlargestdimension,mixed solid/cysticnodulesgreaterthan2cm,andmicrocentimeter nodules with suspect ultrasound features, such as micro-calcifications and irregular borders. In addition, FNA is warrantedforpatientsathighriskforthyroidcancer, includ-ingthosewithafamilialhistoryforthiscancerormultiple endocrine neoplasia, and exposure to ionizing radiation in early life. The recently described Bethesda system for reportingthyroidcytopathologyoutlinessixcategorieswith correlatingclinical recommendations for each category.A repeatedFNA,withinthreetosixmonths,issuggestedfor initial non-diagnostic examinations and also for patients withatypia/folicullarlesionsof undeterminedsignificance (A/FLUS).11---13 A sequential exam is not routinely recom-mendedforpatientswithinitialbenigncytology,asmostare judiciouslyfollowed-upwithsequentialclinicalexamination

andimaging.Despitethispractice,somedatasuggestthat repeatedFNAshouldalso beconsidered for patients with aninitial benign cytology inordertodecrease therisk of false negatives and confirm the benign features of these nodules.14---20 Therefore,the present studysought to eval-uate the indications and validity of repeated FNA in the managementofpatientswiththyroidnodules.

Materials

and

methods

This was a retrospective cohort study of 568 consecutive patients who had repeated aspiration biopsies of thyroid nodules evaluated in a single center between January of 1998andDecemberof2010. Duetodifferencesinthyroid cytology reporting over the study period, all cytological resultswereupdatedaccording tothe2010Bethesda sys-temforreportingthyroidcytology.Allpatientshadaninitial examinationclassifiedasnon-diagnostic,benign,orA/FLUS, and at least one more repeated FNA within a maximum intervalof 36 monthsbetween aspirations, in addition to nosignificant clinical orradiological changesinthe previ-ouslyevaluateddominantorsinglenodule.Patientswitha repeatedFNAwithin a timeframe greater the previously mentioned, and those with a cytology report of follicu-lar neoplasm, suspected for malignancy or confirmed as malignant, were excluded. Descriptive and comparative statistical analyses were performed using SPSS 13.0 for Windows® andsoughttoassessthe possibilityof repeated

aspiration toalter the initial diagnosis, with a particular interestin the rate ofsuspect/malignant findings on sub-sequentFNAstratifiedbyinitial cytologicaldiagnosis. The results were expressed as frequencies and percentages,

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Table1 Cytologyresultsfor initialversusrepeated fine-needleaspiration(FNA).

FNA2 FNA1

Non-diagnosticbenignA/FLUS

ND 70 19 5 29.5% 12.5% 21.7% B 106 108 10 44.7% 71.1% 43.5% A/FLUS 25 13 5 10.5% 8.6% 21.7% FN 24 7 2 10.1% 4.6% 8.7% S/M 12 5 1 5.1% 3.3% 4.3% =FNA1 70 108 5 29.5% 71.1% 21.7% /= FNA1 167 44 18 70.5% 28.9% 78.3% Total 237 152 23

FNA1,initial;FNA2,repeated;ND,nondiagnostic;B,benign; A/FLUS,atypiaorfollicularlesionofundeterminedsignificance; FN,follicularneoplasia;S/M,suspicious/malignantcytology;=, similarFNA1; /=,differentFNA1.

and Fisher’s exact test was used to compare the ratings of observed results between categories. This study was approvedby the ethicscommittee of the institution (CEP 100046).

Results

Thefinalanalysisincluded412patientsrangingfrom13to 83yearsofage(mean49.3years).Themajorityofpatients were female (93.5%). The mean interval between initial andsequentialexaminationswas10.8monthsfortheentire cohort.However,this intervalvariedfrom6.3months for non-diagnosticcytologyto18.1monthsand13.8monthsfor benignandA/FLUScytology,respectively.Anon-diagnostic cytology wasthe most common indicationfor a repeated FNAin237patients(57.5%),followedbybenign(36.8%),and A/FLUS(5.6%)atinitialFNA(Table1).Arepeated examina-tionalteredtheinitialdiagnosis in70.5%and78.3%ofthe non-diagnosticandA/FLUSpatients,respectively, whereas only 28.9% of patients with a benign cytology presented with a different diagnosis on a sequential FNA. This dif-ference between groups was significant, aspatients with initial benign cytology had a much higher chance of a similar result on a sequential examination (Table 2). No significantdifferencewasobservedin theoccurrenceofa repeatedFNAshowinga suspect/malignantcytology for a non-diagnostic(5.1%),benign(3.3%),orA/FLUS(4.3%)initial exam(Table3).

Table2 Probabilityofdifferentrepeatedfine-needle aspi-rationcytologyreportbetweengroups.

FNA1 pa

ND×B <0.001

ND×A/FLUS 0.630

B×A/FLUS <0.001

ND,Nondiagnostic;A/FLUS,atypiaorfollicularlesionof

unde-terminedsignificance;B,benign.

a Fisher’sexacttest;p<0.008.

Table3 Comparisonoftheriskofmalignancyforarepeat fine-needleaspirationbetweengroups.

Malignancyratescompared pa

ND×B 0.457

ND×A/FLUS 1.000

B×A/FLUS 0.576

ND,nondiagnostic;A/FLUS,atypiaorfollicularlesionof

unde-terminedsignificance;B,benign.

a Fisher’sexacttest;p<0.008.

Surgical treatment outcome data was obtained from 26.6% (63/237) of patients with an initial non-diagnostic FNA,andfor21.7%(5/23)ofpatientswithanA/FLUS cytol-ogy,whereasonly14.5%(22/152)ofpatientswithaninitial benign diagnosis had surgery. Histologic data are summa-rizedinTable4.

Discussion

Clinical and incidental findings of thyroid nodules have becomecommon,mainlyduetoincreasedawarenessofthis condition and readily-available high resolution ultrasound diagnostic techniques. Most of these nodules are benign, withlimitedsurgicalindications.Obviously,itwouldbeideal tooperateonly thosepatientswithmalignanttumorsand those whose clinical symptoms required surgical manage-ment. The use of FNA for thyroid cytology datesback to the early1950s,withthe goalof identifyingnoduleswith anincreasedriskformalignancy.FNAhasgraduallyevolved asakeydiagnostictoolandis responsiblefor an increase of surgically treated thyroid cancers; at present, 50% of thyroidectomiesareduetomalignanttumors,whereasthis ratewaslessthan14%.21FNAcytologyreportsbasedonthe recentlyproposedBethesdasystemareassociatedwith sen-sitivity, specificity, and diagnostic accuracy rates of 97%, 50.7%,and68.8%,respectively.22Despitethesefigures, thy-roidcytologymaybeaffectedbynon-diagnosticspecimens inapproximately10%ofcases,23andisparticularly challeng-ingA/FLUScases.

Non-diagnosticFNAwasthemostcommonindicationfor a repeated examination in this series, with 70.5% result-ing in a different diagnosis from the first cytology. It is interestingtonotethat44.7%oftheinitialnon-diagnostic FNA were re-classified as a Bethesda 2 (benign cytol-ogy), allowing for non-surgical management and clinical follow-up whenappropriate,whereasonly5.1%presented with a second exam that was suspect/malignant. Furlan etal.24alsoobservedthat100%oftheirpatientswithinitial

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Table4 Histologicaloutcomeaccordingtoinitialfine-needleaspirationcytology. Outcome

P1 Benign Malignant

Non-diagnostic Nodularhyperplasia---40 Papillarycarcinoma---9 Hashimoto’sthyroiditis---6 Hurthlecellcarcinoma---2 Hurthlecelladenoma---4 (17.5%)

Follicularadenoma---2 (82.5%)

Benign Nodularhyperplasia---14 Papillarycarcinoma---5 Hashimoto’sthyroiditis--- 3 (22.7%)

(77.3%)

A/FLUS Follicularadenoma---1 Papillarycarcinoma---2 Nodularhyperplasia---2 (40%)

(60%)

P1,initialfine-needleaspirationcytology;A/FLUS,atypiaorfollicularlesionofundeterminedsignificance.

non-diagnosticcytology were re-classifiedintoa different Bethesdacategory in asequential FNA.A decreasein the percentageofnon-diagnosticresults wasalsoobservedby Orija et al.,25 who found that sequential FNA provided a diagnosis in up to 60% of these cases. Therefore, the Bethesda recommendation for a repeat exam after three to six months after the first FNA is supported. Coorough etal.26 also observed that a repeatFNA yielding another non-diagnosticfindinghadtwice thechance ofpresenting withcarcinomaatfinalhistology,comparedtoa5%riskof malignancyinpatientswhohadadiagnosticcytologypriorto surgicalintervention.Thepresentstudyincluded63patients withaninitialnon-diagnosticcytologywhounderwent sur-gical resection, and observed that 17.5% of them had a malignanttumoratfinalpathology.Theseresultsaresimilar tothoseof Joetal.,27 whoevaluatedagroup of57 non-diagnosticthyroid aspiratesfollowed bysurgical resection andobserveda20%riskofmalignancyafteranon-diagnostic FNA,whichwouldfavortheneedforarepeatedFNAforthis groupofpatients.TheBethesdareportingsystemstatesthat arepeatFNAmightalsobeconsideredforA/FLUSlesions, butthebenefitofthisapproachisyettobefullycaptured. In the present study, it wasobserved that 5.6% of the repeatedFNAwereduetoaA/FLUScytology,whichis con-sistent with an expected 7% rate of A/FLUS,13 and43.5% of these patients were classifiedas a Bethesda 2 (benign cytology)inasequentialFNA,whereasonly21.7%persisted asA/FLUS. Thesefigures aresimilartothosereportedby Chenetal.28 whoexamined26 patientswithA/FLUS nod-ules andhada repeatedFNAthat wasbenignin 42.3%of cases,whereas23.07%persistedasA/FLUS.Althoughtheir incidenceof suspicious for malignancywas 15.38%,which is three times higher than the 4.3% rate observed in the presentstudy,thesedifferencesarereasonableasthetrue incidence of malignancy for A/FLUS is stillunknown, and a5%to15%malignantrateisanacceptablerangeof vari-ability. The useof repeatFNAforA/FLUS lesionshasalso proved tobe a cost-effectivestrategy when comparedto a standarddiagnostic lobectomy.29 Despitethese findings, roughly 60% ofpatients whohave an initialA/FLUS cytol-ogyarestillreferredforsurgerywithoutasequentialFNA,24 and this approach is expected to change with increased

compliancewiththeBethesdareportingsystem recommen-dations.In thepresent study,itwasobservedthat 40%of surgicallytreatedpatientswithan initialA/FLUS cytology hadamalignanttumordiagnosedathistology.Thesefigures correlatewiththoseofVanderLaannetal.,30 whofounda malignantdiagnosisin41%to43%ofpatientsafterasingle orconsecutiveA/FUSFNA,respectively.However,any fur-therconsiderationregardingtherelativeriskofmalignancy ofpatientswithA/FLUScytologyanditscorrelationto his-tologicalfindingswasbeyondtheobjectiveofthisstudyand wouldbelimitedbythesmallnumberofpatientsincluded. Thereis alsoan ongoing debate whetherpatients with benigncytologymayalsobenefitfromroutinerepeatFNAto reducetheriskoffalsenegativeresults.Someauthorshave shownthat approximately90% to98% of patients withan initialbenigndiagnosiswillnotchangeaftermultipleFNAs, andconcludedthat routinerepeatedexaminationsshould notbeconsideredfor allpatients.17,31---33Ithasbeenfound thattheratesofchangeforsuspicious/malignantlesionsfor repeatedFNA after an initial benign cytology range from 0.5%to5%.Orlandietal.34evaluatedpatientswithbenign nodulardisease andsuggestedthatat leastthree sequen-tialFNAswouldberequiredforthediagnosistochange to malignantin2.25% ofcases,considering that97.7%ofthe examinationsmaintainedthesamebenigncytological pat-tern aftertwo tosix repeatedFNAs. These findings were similartothoseofIllouzetal.,35 in which86%ofpatients whopresented with suspicious/malignantchanges after a repeatedFNAfor benign cytology required at least three sequential exams for that change to be observed. These observationshaveledsomeauthorstofavorrepeatFNAfor allpatientswithbenignnodulargoiters.36---38Inthepresent study,itwasobservedthat3.3%oftheinitially-benignFNAs werereportedassuspicious/malignantcytologyaftera sin-gle sequential exam and these were the only patients to presentapositivehistologicfindingfor malignancyat sur-gical histology. Furthermore, the projected likelihood of malignancyforpatientswithaninitialbenignFNA, consid-eringtheobservedriskofmalignancyaftersurgeryforeach cytologicalreportonsequential exam, wouldincrease for 8.5%. These figures are not significantly higher than the expected5%to15%rateofmalignancyforanysolidnodule.

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Itisinterestingtonotethatatleast91.5%ofpatientswith aninitialbenigncytologic reportwouldavoidunnecessary diagnosticsurgeryasasequentialFNAalonewouldnot sig-nificantly increase the likelihood of a malignancy report. This is also supported by the findings of Rosario et al.39 suggestingthat suspicious ultrasonographiccharacteristics (suchasmicrocalcification,hypoechogenicity,irregular mar-gins, and predominantly central flow) could beused asa criteriontoselectthosepatientswithaninitialbenign cytol-ogythat wouldbenefit froma repeatexam, since17% of patientswiththesefindingswouldpresentwithamalignant changeinasequential FNAcomparedto0.5%to5% malig-nantchangeswhetheraroutinerepeatFNAwasofferedto allpatientswithabenigncytology.

Conclusion

RepeatFNAisavaluableprocedureincaseswithinitial non-diagnostic or A/FLUS cytology, providing informationthat mighthaveimplicationsregardingclinicalfollow-upversus surgicalintervention.

Itsroutineuseforthefollow-upofallpatientswithan ini-tialbenignexaminationseemsnottoincreasetheexpected likelihoodofamalignantlesionandshouldlikelybeusedfor selectedcases.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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