www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
Fine
needle
non-aspiration
cytology
for
the
diagnosis
of
cervical
lymph
node
tuberculosis:
a
single
center
experience
夽
Moncef
Sellami
a,∗,
Slim
Charfi
b,
Mohamed
Amine
Chaabouni
a,
Salma
Mrabet
a,
Ilhem
Charfeddine
a,
Lobna
Ayadi
b,
Souha
Kallel
a,
Abdelmonem
Ghorbel
aaHabibBourguibaUniversityHospital,DepartmentofOtorhinolaryngology-HeadandNeckSurgery,Sfax,Tunisia bHabibBourguibaUniversityHospital,DepartmentofAnatomopathology,Sfax,Tunisia
Received28March2018;accepted13May2018 Availableonline28June2018
KEYWORDS Cervical; Lymphadenopathy; Cytology; Non-aspiration technique; Tuberculosis Abstract
Introduction:Thefine-needlecytologyisbeingusedasafirstlineofinvestigationinthe diag-nosisofheadandneckswellings,asitissimple,costeffectiveandlessinvasiveascompared tobiopsy.
Objective: Theaimsofthisstudyweretoevaluatetheresultsofthefine-needlenon-aspiration cytologyofcervicallymphadenopathy andtostudy thefactorsinfluencing therateof non-diagnosisresults.
Methods:This retrospective study was conducted on selected patients with cervical lym-phadenopathy that had undergone a fine-needle non-aspiration cytology followed by a histologicalbiopsy.Thesensitivity,specificity,positive predictivevalue andnegative predic-tivevalueoffine-needlenon-aspirationcytologyfordiagnosingtuberculosiswereestimated. Theriskfactorsofnon-diagnosisresultswereevaluated.
Results:Thesensitivity,specificity,positivepredictivevalueratesoffine-needlenon-aspiration cytologyfortuberculosiswere83.3%,83.3%,78.9%and86.9%respectively.Intotal,47outof the131samples(35.8%)wereconsiderednon-diagnosis.Ofthenon-diagnosissamples,84.2% (38outof47)werebenignmostlyduetotuberculosis(30cases).Amongthestudiedfactors, onlytuberculosis(confirmedbyhistopathologicalexamination)wassignificantlyassociatedwith non-diagnosiscytology(p=0.02,Odds-Ratio=2.35).
夽 Pleasecitethisarticleas:SellamiM,CharfiS,ChaabouniMA,MrabetS,CharfeddineI,AyadiL,etal.Fineneedlenon-aspirationcytology
forthediagnosisofcervicallymphnodetuberculosis:asinglecenterexperience.BrazJOtorhinolaryngol.2019;85:617---22.
∗Correspondingauthor.
E-mail:sellamimoncef@yahoo.fr(M.Sellami).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.
https://doi.org/10.1016/j.bjorl.2018.05.009
1808-8694/©2018Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen
Conclusion:Tuberculosis is currently the commonest cause ofcervical lymphadenopathyin North Africa. Fine-needle non-aspiration cytology is safe and accurate in the diagnosis of cervicaltuberculouslymphnodethatisassociatedwiththeriskofnon-diagnosiscytology. © 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/). PALAVRAS-CHAVE Cervical; Linfadenopatia; Citologia; Técnica não-aspirativa; Tuberculose
Punc¸ãonãoaspirativacomagulhafinaparaodiagnósticodetuberculoselinfonodal cervical:experiênciadecentroúnico
Resumo
Introduc¸ão: Apunc¸ãonão aspirativacomagulhafinatem sidoutilizadacomo primeiralinha deinvestigac¸ãonodiagnósticodetumoresdecabec¸aepescoc¸o,porserumatécnicasimples, custo-efetivaemenosinvasivaquandocomparadaàbiópsia.
Objetivo:Osobjetivosdesteestudoforamavaliarosresultadosdecitologiaporpunc¸ão não-aspirativacomagulhafinadelinfadenopatiascervicaiseestudarosfatoresqueinfluenciama taxadefalhadiagnóstica.
Método: Esteestudoretrospectivofoirealizadoempacientesselecionadoscomlinfadenopatia cervicalsubmetidosapunc¸ãonãoaspirativacomagulhafina,seguidaporbiópsiahistológica. Foramestimadasasensibilidade,especificidade,ovalor preditivopositivo evalor preditivo negativodapunc¸ãonãoaspirativacomagulhafinaparaodiagnósticodetuberculose.Osfatores deriscodosresultadoscomfalhadiagnósticaforamavaliados.
Resultados: Astaxasdesensibilidade,especificidade,ovalorpreditivopositivoevalor pred-itivo negativoda punc¸ãonão aspirativacomagulha finapara tuberculose foramde 83,3%, 83,3%,78,9%e86,9%,respectivamente.Das131amostras,47(35,8%)foramconsideradascomo falhadiagnóstica.Dasamostrasnãodiagnosticadas,84,2%(38de47)erambenignas, princi-palmentedevidoàtuberculose(30casos). Entreosfatoresestudados,apenas atuberculose (confirmadapeloexamehistopatológico)estavasignificativamenteassociadaàcitologiacom falhadiagnóstica(p=0,02,oddsratio=2,35).
Conclusão:Atuberculoseéatualmenteacausamaiscomumdelinfadenopatiacervicalnonorte daÁfrica.Apunc¸ãonãoaspirativacomagulhafinaéumatécnicaseguraeprecisanodiagnóstico delinfonodoscervicaisassociadosaoriscodecitologiacomfalhadiagnóstica.
© 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
According to the 2015 World Health Organization report, theprevalenceandincidenceofTuberculosis(TB)inTunisia were42/100,000and33/100,000,respectively.1
Lymphadenopathiesarethemostcommonformof extra-pulmonarytuberculosisandtuberculouslymphadenitisisthe most common cause of peripheral lymphadenopathy in a developingcountry.2
Thegold-standardprocedureforthediagnosisofa cer-vical lymphadenopathy is open biopsy with histological examinationoftheexcisedtissue.2
The fine-needlecytology isbeingusedasafirstline of investigationinthediagnosisofheadandneckswellings,as itissimple,costeffectiveandlessinvasiveascomparedto biopsy.3Thisprocedurehasnotbeencommonlydeveloped inNorthAfrica,asmostcliniciansstilluseprimarysurgical excisionbiopsies.
Theobjectivesofthisretrospectivestudywereto eval-uate the results of fine-needle non-aspiration cytology
(FNNAC)ofcervicallymphadenopathyandtostudythe fac-torsinfluencingtherateofnon-diagnosis(ND)results.
Methods
Thepresentstudywasconductedonselectedpatients pre-senting an enlarged cervical lymphadenopathy.This study was limited to the selected cases that had undergone a FNNACfromthecervicallymphadenopathyandfollowedby asubsequentexcisionalbiopsyofthesame lymphadenopa-thyorabiopsyofthesuspectedprimarysiteforadefinitive histopathological diagnosis. Patients with missing FNNAC reportsor thosecaseswhocouldnotundergobiopsywere excluded.
In each case detailed history, clinical presentation of cervical lymphadenopathy and clinical examination were carriedout.
An ENT surgeon performed the FNNAC. The lesion is immobilizedwithonehand,andafterdisinfectingtheskin,
a 25 gauge needle is introduced into the lymphadenopa-thywiththeotherhand.Theneedleispassedthroughthe lesioninthesamewayasinFine-NeedleAspiration Cytol-ogy(FNAC),butnosuctionisapplied.Thematerialentering thehuboftheneedlebycapillaryactionisthenexpressed ontocleanglassslidesafterattachinganair-filledsyringeto it.Multiplesmears(3---5)areprepared.Theair-driedsmears (10min)arestainedwiththeMay-Grünwald-Giemsa(MGG) stainforroutinecytodiagnosis.
Cytologyreportswerecategorizedintofourmainresults (a)‘‘benigndiagnosiswithrecommendationoffollowup’’; (b) ‘‘Malignantmetastaticdiagnosiswithrecommendation of searching for the primary tumors’’3,4; (c) ‘‘Malignant primarylymphoma(non-HodgkinlymphomaorHodgkin lym-phoma)withrecommendationofexcision forconfirmation andimmunophenotyping’’;(d)‘‘Inadequatesmearsor non-diagnosis(ND)’’becauseofscanty/acellularsamples.
Suggestive orsuspiciouscaseswere consideredas posi-tiveformalignancyasallthesecaseswereinvestigatedand managedseriously.
Cytomorphologically tuberculouslesionswere classified intothreegroupsasdescribedbyDasetal.5Thecytologic features oftuberculous lesionsweregrouped underthree majorcytologicresponsetypesasfollows:
• TypeI---Epithelioidgranulomawithoutnecrosis; • TypeII---Epithelioidgranulomawithnecrosis; • TypeIII---Necrosiswithoutepithelioidgranuloma.
Statistics
Thedatawereenteredtostatisticalsoftware(version20.0, SPSS,IBMCompany,Armonk,NewYork).
Forthe qualitative variables,the percentagewasused asthedescriptiveindexandforthequantitativevariables, meanandStandardDeviation(SD)ormedianand Interquar-tileRange(ICR)wasused.
AfterrulingouttheNDresults,theSensitivity(Se), Speci-ficity (Sp), Positive Predictive Value (PPV) and Negative Predictive Value (NPV) of FNNAC to diagnose tuberculosis werecalculated.
NDresultswerestudiedaccordingtoage,size,location ofthe nodeand histologicalresult.Thecut-off valuesfor quantitative variables (age, timeto the first consultation andsize)werecalculatedbyROCcurveanalysis.
Wheneverrequired,thevalueswerecomparedusingthe Chi-squaredtesttodeterminethesignificanceinthe differ-encebetweenthevariables.WeestimatedtheOddsRatio (OR) with 95% Confidence Interval (95% CI) of ND results associatedwitheachriskfactor.
Ap-value<0.05wasusedasthelevelofsignificance.
Results
FNNAC was done for 131 patients with palpable lym-phadenopathy in the cervical neck region. The main characteristicsofthepatientsaregiveninTable1.The com-monestsiteoftheinvolvedcervicallymphadenopathywas the upperdeepcervical lymph nodes(66.4%) followedby theinferiordeepcervical lymphnodes(29%).Themedian sizeofthelymphadenopathywas3cm(ICR=2).
Table1 Demographicandclinicalcharacteristicsof stud-iedpatients.
Characteristics Patients,n◦ Values
Gender Male 54 41.2 Female 77 58.8 Age(years) 35.3±18.5 Medicalhistory Tuberculosis 1 0.7 Alcoholism 8 6
Tuberculosisinthefamily 2 1.5 Timetofirstconsultation
(months)
2(5)
Numberoflymphnodes
Single 61 46
Multiple 70 54
Size(cm) 3(2)
Values given as % or mean±standard deviation or median (interquartilerange).
Table2 Cytologicalresultsofthe131studiedpatients. Cytologicaldiagnosis Noofcases Percentage
Benign 47 35.8
Tuberculous lymphadenitis
38 29.7
Reactivelymphnodes 9 6.8
Metastatictumoror suspiciouscases 17 12.9 Metastatic 11 8.3 Suspiciousofmetastasis 6 4.5 Lymphoma 20 15.2 Lymphoma 6 4.5 Suspiciousoflymphoma 14 10.7 Non-diagnosis 47 35.8
Table2 shows the distributionof FNNACresults; 35.8% werebenign.Mostweretuberculouslymphadenitis(38out of47).Amongthelymphadenopathyaspirateswith tubercu-louslesions(39cases),theTypeI,II,andIIIreactionswere observedin50%,24%and26%,respectively(Fig.1).
Diagnosisbyhistologyshowed;50.4%tuberculosis,20.6% reactive lymph node, 17.55% lymphoma and 11.45% sec-ondarymetastaticcarcinoma.
The cytopathological results were compared with the histopathological diagnoses of the corresponding excised lymphadenopathyor biopsy of the suspected primarysite (Table3).
Intotal,84(64%)sampleswereconsideredadequate. Overall, 70% (59 out of 84) of the adequate samples wereinagreementwiththehistologyresultsforthesame patients.
TheSe,Sp,PPVandNPVratesofFNNACfortuberculosis were83.3%,83.3%,78.9%and86.9%respectively.
Intotal,47outofthe131samples(35.8%)were consid-eredNonDiagnosis(ND).OftheNDsamples,84.2%(38out of47)werebenignmostlyduetotuberculosis(30cases).
Figure1 CytomorphologicalTypeIItuberculosis.A,Caseousnecrosis(arrow)andanepithelioidgranuloma(MGG×100).
Table3 Comparativeanalysisofcytologicaldiagnosesandhistopathologicaldiagnoses.
Cytopathologicaldiagnoses Histopathologicaldiagnoses Total
Tuberculosis Reactivelymphnodes Metastasis Lymphoma
Tuberculosis 30 5 1 2 38
Reactivelymphnodes 1 5 --- 3 9
Metastasis --- 1 10 --- 11 Suspiciousofmetastasis 1 3 2 6 Lymphoma 1 --- --- 5 6 Suspiciousoflymphoma 3 4 --- 7 14 Non-diagnosis 30 9 2 6 47 Total 66 27 15 23 131
Dataarepresentedasnumberofpatients.
Based onROC curve analysis thecut-off valuesfor ND resultswereanageof25years,atimetothefirst consul-tation of 7 weeks and a size of the lymphadenopathy of 2cm.
Among the studied factors, only tuberculosis (con-firmedby histopathological examination) wassignificantly associated with ND cytology (p=0.02, OR=2.3 and 95% CI=1.1---4.9)(Table4).
Discussion
Tuberculosis continues to be a major problem of public healthinterestinNorthAfrica.Ourstudyfound tuberculo-sistobethecommonestcauseofcervicallymphadenopathy followedbyreactivelymphadenitisandlymphoma.
Lymph node lesionscould befound in patients ranging fromanearlytoadvancedage.4 Inourstudytheyoungest patientinthepresentstudywas3yearsoldandtheoldest onewas83yearsold.
In1981,fineneedlesamplingwithoutaspiration,called as Fine Needle Non-Aspiration Cytology (FNNAC) was introduced.6 Thistechnique(non-aspiration)allowsbetter controlofthehand duringtheprocedure andagood per-ceptionoftheconsistencyofthelesion.7
Srikanthetal.comparedFNACandtheFNNACtechniques inheadandneckswellingsandfoundsthatFNNACtechnique providesanadequate cellularyieldforadefinitediagnosis in all head and neck swellings with a statistically signifi-cantbetterretentionofarchitectureinFNNACsmearsfrom lymphnodelesions.6
Diagnosisof tuberculosisdependsupon the demonstra-tionofepithelioidgranulomawithorwithoutnecrosis.Other reactivecomponents,suchaslymphocytes,polymorphs,and Langhan’s giant cells, mayor may notbe present.5 Cases in which FNAC smears contain necrotic material without epithelioidgranulomahavealsobeen consideredas tuber-culouslesions,aswedointhisstudy.8
Inourstudy,mostcommoncytologicalpatternof tuber-culosiswaspresenceofepithelioidcellgranuloma(TypeI), whichwasobservedin50%ofcases(19samples).However, tuberculosiswasconfirmedinonly12cases(truepositives). FNNACwasfoundtobeahighlyaccuratemethodinthe diag-nosisoftuberculosis;withasensitivityandspecificityofover 80%.Thiscomparesfavorablywithotherstudiesdone else-whereinthedevelopingworldwheretuberculosisisendemic (Table5).
Thesefindingsweredifferentfromaretrospective,5year studyfromapublichospitalintheUnitedStates,whereFNA wasfoundtohavealowsensitivityof53%inthediagnosisof
Table4 Studyofriskfactorfornon-diagnosiscytology.
Non-diagnosiscytology Diagnosiscytology p Odds-ratio(95%CI)
Age≥25years 31 58 0.7 0.8 (0.4---1.8) Age<25years 16 26 Timetofirstconsultation <7weeks 14 36 0.1 1.7 (0.8---3.7) ≥7weeks 33 48
Sizeofthelymphnode
<2cm 7 16 0.3 0.6
(0.3---1.4)
≥2cm 40 68
Superiorlymphnode 32 55 0.7 0.8
(0.4---1.9)
Inferiorlymphnode 15 29
Diagnosis Tuberculosis+ 30 36 0.02 2.3 (1.1---4,9) Tuberculosis− 17 48 Metastasis+ 2 13 0.053 0.2(0.05---1.1) Metastasis− 45 71
Reactivelymphnode+ 9 18 0.7 0.8(0.3---2,1)
Reactivelymphnode− 38 66
Lymphoma+ 6 17 0.3 0.6(0.2---1.7)
Lymphoma− 41 67
95%CI,95%ConfidenceInterval.
Table5 Resultsoffine-needleaspirationforthediagnosisoftuberculosis.
Diagnosis Origin Sensitivity(%) Specificity(%) PPV(%) NPV(%)
Muyanja9 Uganda 93.1 100 100 78.9
ElHag10 SaudiArabia 97 100 100 93
Prasad11 India 83 94
Adhikari2 Nepal 80 100 100 82
Abdissa12 Ethiopia 88.4 48.8 86.1 54.1
Ourstudy Tunisia 83.3 83.3 78.9 86.9
PPV,PositivePredictiveValue;NPV,NegativePredictiveValue.
tuberculosis.13Wefoundsixfalsenegativesdiagnosesmade onFNNACforthediagnosisoftuberculosiswhencompared withhistology.Thisiscomparablewithpreviousstudies.9,10 Failure to establish an accurate diagnosis may due to samplingerrorandinthesecircumstances,repeataspiration orexcisionalbiopsymaybeconsidered.14Inourexperience, theNDratewas35.8%.Thenon-diagnosticrateforNDFNA accordingtotheliteraturerangesfrom0.9%to48%.9,15
Rammehetal.studiedthefactorsinfluencingtherateof non-diagnosisFNAandfoundthatthisratedependsonthe size<1cm,submandibularlocationofthelymphnode,and theexperienceoftheaspirator.14
The fibrosisor theextensivenecrosisfound in tubercu-losismay alsoexplainthe rateof NDassociated withthis conditioninourstudy(30outof47).Thus,wefound that tuberculosisconfirmedbyhistologywassignificantly associ-atedwithanon-diagnosisFNNAC.
The experience ofthe aspirator is an importantfactor determining the quality of FNA. Singh et al. investigated 5226FNACsamplesfromthesixcommonestsitesand com-pared the inadequate rates.16 The authors observed that
therateofNDwerelowest whenFNACwasperformed by acytopathologist (12%) andhighest whendone bya non-cytopathologist(32%).
AhnD.statedthatwithtrainingandexperience manag-ingatleast100ultrasound-guidedFNACcases,surgeonscan ensurealowinadequatesamplingrateandgooddiagnostic accuracy.17
Theimprovedefficiencyofultrasound-guidedFNACover palpation-guidedFNACintheheadandneckmasseshasbeen welldocumented,leadingtoitsacceptanceasthestandard ofcare amongradiologistsand manycytopathologists.18,19 The addition of ultrasound guidance reduces the non-diagnosticrate.20Itishoweveramoreexpensivetechnique thannon-ultrasoundguided FNAandshouldbe performed for lymphadenopathy that aresmallin sizeor in difficult locations.20Inourstudy,weusedthepalpation-guided tech-niqueinallcases.
Repeating cytology is useful and should be considered especiallyinthecaseofnon-diagnosiscases.Inthestudyof Shykhonetal.,NDwas48%inthefirstcytologyanddropped to32%afterthesecond.15
Conclusion
Insummary,ourstudyshows thattuberculosisiscurrently thecommonestcauseofcervicallymphadenopathyinNorth Africa.This condition wassignificantly associatedwithND cytology
FNNACis safeandaccurateinthediagnosis ofcervical tuberculouslymphnodethatisassociatedwithriskof non-diagnosiscytology.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
References
1.WorldHealthOrganization. GlobalTuberculosisReport,2015;
2015,http://dx.doi.org/10.1007/s13398-014-0173-7.2.
2.Adhikari P, Sinha B, Baskota D. Comparison of fine needle aspiration cytologyand histopathology in diagnosingcervical lymphadenopathies.AustralasMedJ.2011;4:97---9.
3.DukareSR,JadhavDS,GaikwadAL,RankaSN,KalePB,D’Costa G.Fineneedleaspirationcytologyofcervicallymphadenopathy ---astudyof510cases.AsianJSciTechnol.2014;5:537---40.
4.Hafez NH, Tahoun NS. Reliability of fine needle aspiration cytology(FNAC)asadiagnostictoolincasesofcervical lym-phadenopathy.JEgyptNatlCancInst.2011;23:105---14.
5.Das DK,BhambhaniS,PantJN,ParkashS,MurthyNS,Hedau ST, et al. Superficial and deep-seated tuberculous lesions: fine-needleaspiration cytologydiagnosis of574cases. Diagn Cytopathol.1992;8:211---5.
6.SrikanthS,AnandamG,KashifM.Acomparativestudyof fine-needleaspirationandfine-needlenon-aspirationtechniquesin headandneckswellings.IndianJCancer.2014;51:98---9.
7.ZajdelaA,ZillhardtP,VoillemotN.Cytologicaldiagnosisbyfine needlesamplingwithoutaspiration.Cancer.1987;59:1201---5.
8.Das DK, Pant JN, Chachra KL, Murthy NS, Satyanarayan L, ThankammaTC,etal.Tuberculouslymphadenitis:correlation ofcellularcomponentsandnecrosisinlymph-nodeaspiratewith A.F.B.positivityandbacillarycount.IndianJPatholMicrobiol. 1990;33:1---10.
9.MuyanjaD,KalyesubulaR,NamukwayaE,OthienoE, Mayanja-KizzaH.Diagnosticaccuracyoffineneedleaspirationcytology
inproviding a diagnosis ofcervical lymphadenopathy among HIV-infectedpatients.AfrHealthSci.2015;15:107---16.
10.el Hag IA, Chiedozi LC,al Reyees FA, Kollur SM. Fine nee-dle aspiration cytology of head and neck masses. Seven years’experience in a secondary care hospital. Acta Cytol. 2003;47:387---92.
11.Prasad RR, Narasimhan R, Sankaran V, Veliath AJ. Fine-needle aspiration cytology in the diagnosis of superficial lymphadenopathy:ananalysisof2,418cases.DiagnCytopathol. 1996;15:382---6.
12.AbdissaK,TadesseM,BezabihM,BekeleA,ApersL,RigoutsL, etal.Bacteriologicalmethodsasaddonteststofine-needle aspiration cytology in diagnosis of tuberculous lymphadeni-tis:cantheyreducethediagnosticdilemma?BMCInfect Dis. 2014;14:720.
13.EllisonE,LapuertaP,MartinSE.Fineneedleaspiration diagno-sisofmycobacteriallymphadenitis.Sensitivityandpredictive valueintheUnitedStates.ActaCytol.1999;43:153---7.
14.RammehS,BenRejebH,M’farrejMK,ZnaidiN,FarahF,Ferjaoui M,et al. Cervical nodefine needle aspiration:factors influ-encingthefailurerate.RevStomatolChirMaxillo-FacialeChir Orale.2014;115:85---7.
15.ShykhonM,MacnamaraM,El-AssyA,WarfieldAT.Roleofrepeat fineneedleaspirationcytologyinheadandnecklesions: pre-liminarystudy.JLaryngolOtol.2004;118:294---8.
16.SinghN,RyanD,BerneyD,CalaminiciM,SheaffMT,WellsCA. Inadequateratesare lowerwhen FNACsamplesaretakenby cytopathologists.Cytopathology.2003;14:327---31.
17.AhnD,Kim H,Sohn JH,ChoiJH, NaKJ. Surgeon-performed ultrasound-guidedfine-needleaspirationcytologyofheadand neckmasslesions:samplingadequacyanddiagnosticaccuracy. AnnSurgOncol.2015;22:1360---5.
18.Boland GW,Lee MJ,Mueller PR, Mayo-SmithW, Dawson SL, SimeoneJF.Efficacyofsonographicallyguidedbiopsyof thy-roid masses and cervical lymph nodes. Am J Roentgenol. 1993;161:1053---6.
19.RobitschekJ,StraubM,Wirtz E,KlemC,Sniezek J. Diagnos-ticefficacyofsurgeon-performedultrasound-guidedfineneedle aspiration: a randomized controlled trial. Otolaryngology ---HeadNeckSurgOffJAmAcadOtolaryngol---HeadNeckSurg. 2010;142:306---9.
20.Addams-Williams J, Watkins D, Owen S, Williams N, Fielder C. Non-thyroid neck lumps: appraisal of the role of fine needle aspiration cytology. Eur Arch Otorhinolaryngol. 2009;266:411---5.
