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www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Translation

and

adaptation

of

the

Radiotherapy

Edema

Rating

Scale

to

Brazilian

Portuguese

Débora

dos

Santos

Queija

a,∗

,

Lica

Arakawa-Sugueno

b

,

Bruna

Mello

Chamma

c

,

Marco

Aurélio

Vamondes

Kulcsar

d,e

,

Rogério

Aparecido

Dedivitis

d,f

aUniversidadedeSãoPaulo(USP),FaculdadedeMedicina,CursodePós-Graduac¸ãoemFisiopatologiaExperimental,SãoPaulo,

SP,Brazil

bUniversidadedeSãoPaulo(USP),FaculdadedeMedicina,Ciências,SãoPaulo,SP,Brazil cUniversidadeBrazCubas,MogidasCruzes,SP,Brazil

dUniversidadedeSãoPaulo(USP),FaculdadedeMedicina,DepartamentodeCirurgia,SãoPaulo,SP,Brazil eInstitutodoCâncerdoEstadodeSãoPaulo(ICESP),Servic¸odeCirurgiadeCabec¸aePescoc¸o,SãoPaulo,SP,Brazil

fUniversidadedeSãoPaulo(USP),FaculdadedeMedicina,GrupodeTumoresdeLaringeeHipofaringedoServic¸odeCirurgiade

Cabec¸aePescoc¸o,SãoPaulo,SP,Brazil

Received5January2017;accepted28March2017 Availableonline9May2017

KEYWORDS

Edema; Headandneck neoplasms; Radiotherapy; Pharynx; Larynx

Abstract

Introduction:Internallymphedemaisoneofthesequelaeofheadandneckcancertreatment thatcanleadtovaryingdegreesofswallowing,speech,andrespirationalterations.The Radio-therapyEdemaRatingScale,developedbyPattersonetal.,isatoolusedtoevaluatepharyngeal andlaryngealedema.

Objective:To translateinto Brazilian Portuguese, toculturally adaptand test thisscalein patientsundergoingtreatmentforheadandneckcancer.

Methods:Theprocessfollowedtheinternationalguidelinesandtranslationstepsbytwohead and neck surgeons and back-translation performed independently by two North-American natives.Thefinalversionofthetestwasevaluatedbasedontheassessmentof18patientsby twoheadandnecksurgeonsandtwospeechtherapistsusingthescalesinBrazilianPortuguese. Results:Thetranslationandculturaladaptationweresatisfactorilyperformedbythemembers ofthecommitteeincharge.

Pleasecitethisarticleas:QueijaDS, Arakawa-SuguenoL, ChammaBM,KulcsarMA,DedivitisRA.Translationand adaptationofthe

RadiotherapyEdemaRatingScaletoBrazilianPortuguese.BrazJOtorhinolaryngol.2018;84:344---50.

Correspondingauthor.

E-mails:dqueija@uol.com.br,queijad@gmail.com(D.S.Queija).

PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.

https://doi.org/10.1016/j.bjorl.2017.03.014

1808-8694/©2017Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen

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Conclusion: The translation and adaptation into Brazilian Portuguese of the Radiotherapy EdemaRatingScalewassuccessfullyperformedandshowedtobeeasytoapply.

© 2017 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

Edema;

Neoplasiasdecabec¸a epescoc¸o;

Radioterapia; Faringe; Laringe

Traduc¸ãoeadaptac¸ãoparaoportuguêsbrasileirodaEscaladeClassificac¸ãodoEdema daRadioterapia

Resumo

Introduc¸ão: Olinfedemainternoéumadassequelasdotratamentoparaocâncerdecabec¸ae pescoc¸o,podendolevaraalterac¸õesdegrauvariadonadeglutic¸ão,vozerespirac¸ão.AEscala doEdemadaRadioterapia(RadiotherapyEdemaRatingScale),elaboradaporPattersonetal., éumaferramentadeavaliac¸ãodoedemadefaringeelaringe.

Objetivo: Traduzir,paraoportuguêsbrasileiro,adaptarculturalmenteetestarestaescalaem pacientessubmetidosaotratamentoparaocâncerdecabec¸aepescoc¸o.

Método: O processo seguiu as diretrizes internacionais e as etapas de traduc¸ão por dois cirurgiões de cabec¸a e pescoc¸o e aretrotraduc¸ãode forma independente pordois nativos norte-americanos.Otestedaversãofinalparaavaliac¸ãofoirealizadoapartirdaavaliac¸ãode 18pacientespordoismédicoscirurgiõesdecabec¸aepescoc¸oeduasfonoaudiólogaspormeio daaplicac¸ãodasescalasemportuguês.

Resultados: Atraduc¸ãoeadaptac¸ãoculturalforamexecutadassatisfatoriamentepelos mem-brosdocomitêresponsável.

Conclusão:Atraduc¸ãoeadaptac¸ãodaEscaladoEdemadaRadioterapiaparaoportuguêsfoi bemsucedidaedefácilaplicac¸ão.

© 2017 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

The head and neck encompasses an extensive lymphatic networkandmorethan300lymphnodes(one-thirdofthe lymphnodesinthebody).1Thetreatmentforheadandneck cancer involves multimodal therapies that result in increasedsurvivalrates;however,theyareaccompaniedby theriskofsecondarycomplications,suchassecondary lym-phedema.The tumor,surgery,andradiotherapy canbreak downlymphaticstructuresandblocklymphflow,resulting in soft tissue edema. Muscle contraction and soft tissue compression facilitate lymphatic flow throughmovement. However, the damage caused by surgery and radiothe-rapyadverselymodifiesthismechanism,leadingtoreduced movementandlymphflow.1---4

Lymphaticdysfunctionoccurswhenanylymphatic struc-tureorthatsurroundingsofttissueisdamagedbycancerand itstreatment,limitingthecapacityofthelymphaticsystem totransportthelymphvolumecarriedtothetissues. Lym-phedemais aswellingthatdevelopsduring aperiodofat leastthreemonthsafterheadandneckcancertreatment, beyondtheperiodwhenacuteedemaoccurs.5---7

When thelymphedemadevelops,the lymphaticsystem maybeabletorepairorcompensateforthedamagedone, resulting in visible swelling reduction. If the damage is severeorthereisnointervention,theaccumulated protein-rich lymphatic fluid can trigger a chronic inflammatory

response,resultinginafibroscleroticprocesswhereinfatty orfibroustissuesmaydevelop.1,7

Headandneckcancerlymphedemamayaffectexternal (face,submental andneck)andinternal structures(upper aerodigestivetract,tongue,epiglottis)orboth(compound). Internal lymphedema may impair chewing, swallowing, speech,andvoice.8Bothtypescanprogressovertimeand, whenidentifiedandtreatedearly,swellingregressionand prevention of late effects, such as fibrosis, may be the result.9Therefore,itisimportanttoassessforlymphedema aspartoftheclinicalroutineoftheevaluationofheadand neckcancerpatients.1,3,6,8,10,11

Fewmeasurestoevaluateedemaandlymphedemahave beendevelopedoverthelastfewyears.Concernaboutthese aspectshasbeen increasing inthe lastdecade, aiming to identify,andmonitortheevolutionofalterationsand treat-mentresults.11---14

The Radiotherapy Edema Rating Scale, developed by Patterson et al.,15 is the most comprehensive tool that evaluates and stages, in a simple and objective man-ner, 11 structures and two spaces of the pharynx and larynx through endoscopy. The scale showed good intra-rater(Kappa=0.84)andmoderateinter-rater(Kappa=0.54) reliability.

Theaimofthisstudyistocarryoutthetranslationofthe RadiotherapyEdemaRatingScaleintoBrazilianPortuguese anditscross-culturaladaptation.

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Methods

Thisstudyrepresentstheinitialphaseoftheclinicalstudy project,approvedbytheEthicsCommitteeoftheinstitution whereitwasperformed,undernumber528/14.Todevelop the work using the scale, permission was granted by the author,whoauthorizedthetranslation.

Because thisscale evaluates structuresstrictly related toanatomy,thetranslationwasperformedbytwoheadand necksurgeonswithexperienceinheadandneckedemaand lymphedema,whowereproficientintheEnglishlanguage, basedontheNomina Anatomica.16 The processwasbased oninternationalguidelines.

Subsequently, a consensus developed between the translators regarding a Brazilian Portuguese version and subsequentback-translationperformedbytwonative speak-ersoftheEnglishlanguage,independently.Followingthat, the comparison of the back-translation with the original scalewasperformed,analyzingaspectsrelatedto concep-tual,semanticandcontentequivalence andlatercreation ofatranslatedversionbythecommittee,whichconsisted ofthetranslatorsandback-translators.

Eighteen patients submitted to surgical and/or radio-chemotherapytreatmentwereevaluatedbynasoendoscopy, which wasrecorded onDVD for furtherevaluation by the committee.

Thefinalversionwasappliedbyfourhealth profession-als(twoheadandnecksurgeonsandtwospeechtherapists, withbroadexperienceinheadandneckcancerand interpre-tationofvideoendoscopicimagesofthepharynxandlarynx). Due to similar interpretations, the evaluators achieved consensus.

Results

The translation of the Radiotherapy Edema Rating Scale (Table 1) was performed independently by twohead and necksurgeonsproficientintheEnglishlanguage.15

The two translations (Tables 2 and 3) were analyzed jointlybythetwotranslators,whoreachedaconsensusfor itsfinalversioninBrazilianPortuguese(Table4).Therewas aquestionregardingthetermcricopharyngealprominence, which in Portuguese referstothe cricopharyngealbar,an alterationrelatedtotheanatomyofpatientssubmittedto Table1 RadiotherapyEdemaRatingScale(originaltoolintheEnglishlanguage).

Ratingofedema

Structures Normal Mild Moderate Severe

Baseoftongue

Posteriorpharyngealwall Epiglottis Pharyngoepiglotticfolds Aryepiglotticfolds Interarytenoidspace Cricopharyngealprominence Arytenoids

Falsevocalfolds Truevocalfolds Anteriorcommissure

Spaces Normal Mildlyreduced Moderatelyreduced Severelyreduced Vallecullae

Pyriformsinus

Table2 RadiotherapyEdemaRatingScale(TranslatorA).

Classificac¸ãodoedema

Estruturas Normal Discreto Moderado Intenso

Basedalíngua

Paredeposteriordefaringe Epiglote Pregasfaringo-epiglóticas Pregasariepiglóticas Membranainteraritenóidea Áreapós-cricóide Aritenóides Bandasventriculares Pregasvocais Comissuraanterior

Espac¸os Normal Reduc¸ãodiscreta Reduc¸ãomoderada Reduc¸ãointensa Valécula

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Table3 RadiotherapyEdemaRatingScale(TranslatorB).

Classificac¸ãodoedema

Estruturas Normal Discreto Moderado Severo

Basedalíngua

Paredeposteriordefaringe Epiglote

Pregasfaringo-epiglóticas Pregasariepiglóticas Espac¸ointeraritenóideo Árearetrocricóidea Aritenóides Pregasvestibulares Pregasvocais Comissuraanterior

Espac¸os Normal Discretamentereduzida Moderadamentereduzida Severamentereduzida Valécula

Seiospiriformes

Table4 FinalversionoftheRadiotherapyEdemaRatingScale(consensusbetweentranslatorsAandB). Classificac¸ãodoedema

Estruturas Normal Discreto Moderado Severo

Basedalíngua

Paredeposteriordefaringe Epiglote

Pregasfaringo-epiglóticas Pregasariepiglóticas Espac¸ointeraritenóideo Árearetrocricóidea Aritenóides Pregasvestibulares Pregasvocais Comissuraanterior

Espac¸os Normal Discretamentereduzida Moderadamentereduzida Severamentereduzida Valécula

Seiospiriformes

Table5 Radiotherapyedemarating(independentback-translation).

Ratingofedema

Structures Normal Mild Moderate Severe

Baseofthetongue Posteriorpharyngealwall Epiglottis Pharyngoepiglotticfolds Aryepiglotticfolds Interarytenoidspace Cricopharyngealprominence Arytenoids

Falsevocalfolds Vocalfolds

Anteriorcommissure

Spaces Normal Slightlyreduced Moderatelyreduced Severelyreduced Valleculla

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totallaryngectomy.Toclarifythisdoubt,wecontactedthe authorand asked whether the term would correspond to thecricopharyngealprominence.Theauthorconfirmedour hypothesis.

Basedonthislastversion,theback-translationwas car-riedoutindependently bytwobilingualtranslators.Inthe case of the term that raised doubts in the translators,it wasunderstoodintheback-translationaspost-cricoidarea. Thus,theversionsweresimilartoeachother withoutany impairmenttotheoriginalversion.Thecommitteechoseto retainthe originalversion, withthetermcricopharyngeal prominence(Table5).

Theauthorschosetotranslatethepyriformsinus struc-ture as seio piriforme because, although the Nomina indicates the term ‘‘pyriformrecess,’’ the term piriform sinusiswidelyused.

The examinationswere then performed by ahead and necksurgeoninthe18patientsrecruitedforthestudy.

Thetoolwasappliedbythegroupconsistingoftwohead andnecksurgeonsandtwospeechtherapists(whohad expe-rienceininterpretingnasoendoscopyresults)inaconsensus, tothe18 patients at the institutionwhere the study was carriedout (Tables 6 and 7). Because this is a scale that evaluates anatomical structures, we did not observe any difficultiesinunderstandingandapplyingthetool.

Discussion

The techniques of edema and lymphedema assessment throughimagesaretoolsthatofferamoreaccuratechoice of the structures involved both with the disease and the treatment. The evaluation of internal edema secondary to treatment in head and neck cancer is a tool that can contribute not only to its diagnosis but also to its evolution.

Other modalitiessuch aslymphoscintigraphy, magnetic resonanceimaging,computedtomography,ultrasonography, andfluorescenceimaging,scarcelymentionedinthe litera-tureoftheheadandneckregion,arealsousedinadditionto thelaryngologicalevaluationusingtheRadiotherapyEdema RatingScale. ThePatterson Scalecan beeasilyappliedin clinicalpractice,sincelaryngologicalexaminationispartof theroutineevaluationandfollow-upofpatientswithhead andneckcancer.1,14,17---22

Anotherpossibilityistoverifytheassociationof swallow-ingandvoicealterations withthepresenceof pharyngeal and laryngeal edema, which can be better quantified usingthe Radiotherapy Edema Rating Scale. The associa-tionbetweeninternaledemaandswallowingandbreathing alterations and their impact on quality of life using this scaleidentifiedastrongcorrelationbetweenedema sever-ity, especially in the region of the aryepiglottic folds, pharyngoepiglottic folds, epiglottis, arytenoids, and pyri-form sinus with swallowing symptoms, mainly of solid consistency.When compared to patients without internal edema,theimpactonfunctionandqualityoflifewasmore evident.10,22

Damagetothelymphatictissuescanleadtolymphedema and fibrosis, which may manifest as early or late effects of head and neck cancer treatment. Lymphedema and fibrosisarenotstaticprocesses.Lymphedemaisassociated

Table 6 Demographic, clinical and treatment characteristics. Variable Category n Age Min.---max. 36---82 Median 60 Mean±standard deviation 61.22±11.39 Gender Female 6 Male 12

Tumorlocation Mouth 7

Oropharynx 5

Larynx 1

Infraglottic 1

Thyroid 1

Face 2

Occultprimarytumor 1

Staging Tx 1 T1b 1 T2 10 T3 2 T4 2 N0 10 N1 2 N2 1 N2a 2 N2b 1 Treatment Surgery 8 Surgery+radiotherapy 4 Surgery+radio-chemo 5 Radio-chemotherapy 1 Neckdissection No 3 Yes 15 Typeofneck dissection Supraomohyoid 9 Radical 3 Modifiedradical 1 Jugular 1 Selective 1 Radiotherapy Min.---max. 3150---7000 Median 1575 Mean±standard deviation 3186±3292.57 Timeuntiltheend

oftreatment (months) Min.---max. 3---40 Median 6.5 Mean±standard deviation 11.94±12.12 Alcoholism No 18 Yes ---Smoking No 16 Yes 2 Tracheostomy No 17 Yes 1 Nasogastrictube No 17 Yes 1

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Table7 Distributionofradiotherapyedemaclassification.

Patients Structures Spaces

BT PPW E PEF AEF IS CPP A FVF VF AC V PS 1 1 0 2 0 1 2 2 3 2 0 0 2 1 2 0 0 0 0 0 0 0 0 0 0 0 1 0 3 0 0 0 0 1 2 0 2 0 0 0 0 0 4 0 0 0 0 0 1 0 1 0 1 0 0 0 5 0 1 1 0 2 2 2 3 1 0 0 0 2 6 0 0 0 0 0 2 2 0 0 0 0 0 0 7 0 0 0 0 0 0 0 0 0 0 0 0 0 8 1 0 1 1 0 2 2 2 0 0 0 1 0 9 0 1 0 0 0 0 0 0 0 0 0 0 0 10 0 0 1 0 2 2 2 2 0 0 0 0 0 11 0 0 1 0 0 1 2 1 0 0 0 0 0 12 0 0 0 0 0 0 0 0 0 0 0 0 0 13 1 2 1 0 2 2 1 2 0 0 0 1 1 14 1 0 1 0 2 2 2 2 0 0 0 1 0 15 0 2 1 2 1 2 2 2 0 0 0 0 1 16 0 0 0 0 0 0 0 0 0 0 0 0 0 17 0 0 1 2 2 2 2 2 0 0 0 0 2 18 2 2 2 2 3 3 3 3 0 0 0 0 3

BT,baseofthetongue;PPW,posteriorpharyngealwall;E,epiglottis;PEF,pharyngoepiglotticfolds;AEF,aryepiglotticfolds;IS, Inter-arytenoidspace;CPP,cricopharyngealprominence;A,arytenoids;FVF,falsevocalfolds;VF,vocalfolds;AC,anteriorcommissure;V, valleculla;PS,pyriformsinus;degreeofedemaofstructures:0,normal;1,mildedema;2,moderateedema;3,severeedema;degree ofspacereduction:0,normal;1,mildlyreduced;2,moderatelyreduced;3,severelyreduced.

withongoing inflammationresultingin progressivefibrosis and adipose tissue deposition. With the development of fibrofatty tissue, manual lymphatic drainage and compressiontherapymaybelesseffective.Therefore,the evaluation of treatment effects may facilitate an earlier approachaimingtoavoidorminimizethesealterations.23

TheRadiotherapyEdemaRatingScaleisindicatedby sev-eralauthorsasavalidtoolforthecharacterizationofedema afterheadandneckcancertreatment.1,2,12,18,22

Conclusions

ThetranslationoftheRadiotherapyEdemaRatingScaleinto BrazilianPortuguesewascompatiblewiththeoriginal.The toolisaccessibleandeasytointerpretforhealth profession-alsexperiencedintheevaluationandtreatmentofheadand neckcancer.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

References

1.DengJ,RidnerSH,AulinoJM,MurphyBA.Assessmentand mea-surementofheadandnecklymphedema:state-of-the-science andfuturedirections.OralOncol.2015;51:431---7.

2.Murphy BA, Gilbert J. Dysphagia in head and neck cancer patients treated with radiation: assessment, sequelae, and rehabilitation.SeminRadiatOncol.2009;19:35---42.

3.MurphyBA,GilbertJ,CmelakA,RidnerSH.Symptomcontrol issuesandsupportivecareofpatientswithheadandneck can-cers.ClinAdvHematolOncol.2007;5:807---22.

4.McGarveyAC,OsmotherlyPG,HoffmanGR,ChiarelliPE. Lym-phoedema following treatment for head and neck cancer: impactonpatients,andbeliefsofhealthprofessionals.EurJ CancerCare(Engl).2014;23:317---27.

5.BentzenSM,DörrW,AnscherMS,DenhamJW,Hauer-JensenM, MarksLB,etal.Normaltissueeffects:reportingandanalysis. SeminRadiatOncol.2003;13:189---202.

6.Deng J, Ridner SH, Dietrich MS, Wells N, Wallston KA, Sinard RJ, et al. Prevalence of secondary lymphedema in patientswithheadandneckcancer.JPainSymptomManage. 2012;43:244---52.

7.AvrahamT,ZampellJC,YanA,ElhadadS,WeitmanES,Rockson SG,etal.Thedifferentiationisnecessaryforsofttissuefibrosis andlymphaticdysfunctionresultingfromlymphedema.FASEB J.2013;27:1114---26.

8.DengJ,MurphyBA,DietrichMS,WellsN,WallstonKA,Sinard RJ,etal.Impactofsecondarylymphedemaafterheadandneck cancertreatmentonsymptoms,functionalstatus,andquality oflife.HeadNeck.2013;35:1026---35.

9.Stout Gergich NL, PfalzerLA, McGarveyC, Springer B, Ger-berLH,SoballeP.Preoperativeassessmentenablestheearly diagnosis and successful treatment of lymphedema. Cancer. 2008;112:2809---19.

10.Deng J, MurphyBA, Dietrich MS,Sinard RJ,Mannion K, Rid-ner SH. Differences of symptoms in head and neck cancer patientswithandwithoutlymphedema.SupportCareCancer. 2016;24:1305---16.

11.SmithBG,HutchesonKA,LittleLG,SkorackiRJ,RosenthalDI, LaiSY,etal.Lymphedemaoutcomesinpatientswithheadand neckcancer.OtolaryngolHeadNeckSurg.2015;152:284---91.

12.Smith BG, Lewin JS. Lymphedemamanagement in head and neckcancer.CurrOpinOtolaryngolHeadNeckSurg.2010;18: 153---8.

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13.DengJ,RidnerSH,DietrichMS,WellsN,MurphyBA.Assessment ofexternallymphedemainpatientswithheadandneck can-cer:acomparisonoffourscales.OncolNursForum.2013;40: 501---6.

14.DengJ,DietrichMS,RidnerSH,FleischerAC,WellsN,Murphy BA.Preliminaryevaluationofreliabilityandvalidityofheadand neckexternallymphedemaandfibrosisassessmentcriteria.Eur JOncolNurs.2016;22:63---70.

15.PattersonJM,HildrethA,WilsonJA.Measuringedemain irradi-atedheadandneckcancerpatients.AnnOtolRhinolLaryngol. 2007;116:559---64.

16.SociedadeBrasileiradeAnatomia.TerminologiaAnatômica.São Paulo:Manole;2001.

17.Maus EA,Tan IC,Rasmussen JC,Marshall MV,Fife CE,Smith LA, et al. Near-infrared fluorescence imaging of lympha-tics in head and neck lymphedema. Head Neck. 2012;34: 448---53.

18.InternationalSocietyofLymphology.Thediagnosis and treat-ment of peripheral lymphedema: 2013 Consensus document of the international society of lymphology. Lymphology. 2013;46:1---11.

19.TassenoyA, DeMeyJ,DeRidder F,Van SchuerbeeckP, Van-derhasseltT,LamoteJ,etal.Postmastectomylymphoedema: differentpatternsoffluiddistributionvisualisedbyultrasound imagingcomparedwithmagneticresonance imaging. Physio-therapy.2011;97:234---43.

20.LeeJH,Shin BW,Jeong HJ,KimGC,KimDK,SimYJ. Ultra-sonographic evaluation of therapeutic effects of complex decongestive therapy in breast cancer-related lymphedema. AnnRehabilMed.2013;37:683---9.

21.SuehiroK,MorikageN,MurakamiM,YamashitaO, SamuraM, HamanoK.Significanceofultrasoundexaminationofskinand subcutaneoustissueinsecondarylowerextremitylymphedema. AnnVascDis.2013;6:180---8.

22.JacksonLK, Ridner SH,Deng J,Bartow C,Mannion K, Nier-mannK,etal.Internallymphedemacorrelateswithsubjective andobjectivemeasuresofdysphagiainheadandneckcancer patients.PalliatMed.2016;19:949---56.

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