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SOCIEDADE BRASILEIRA DE ORTOPEDIA E TRAUMATOLOGIA

w w w . r b o . o r g . b r

Original

Article

Amputation

risk

after

the

revascularization

procedures

in

sarcoma

resections

Luiz

Eduardo

Moreira

Teixeira

a,b,∗

,

Thiago

Marques

Leão

c

,

Daniel

Barbosa

Regazzi

c

,

Cláudio

Beling

Gonc¸alves

Soares

b

aUniversidadeFederaldeMinasGerais(UFMG),FaculdadedeMedicina,BeloHorizonte,MG,Brazil

bHospitalMadreTeresa,Servic¸odeOrtopediaeTraumatologia,BeloHorizonte,MG,Brazil

cUniversidadeFederaldeMinasGerais(UFMG),HospitaldasClínicas,BeloHorizonte,MG,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received2May2016 Accepted30August2016 Availableonline21October2017

Keywords:

Softtissuesarcoma Osteosarcoma Limbsalvage Amputation

Reconstructivesurgicalprocedures

a

b

s

t

r

a

c

t

Objective:Theobjectiveofthisstudyistoevaluatetheefficacyofvascularreconstructive surgeryafterresectionofboneandsofttissuetumorsinextremitiesandtheriskof progres-siontoamputation.

Methods:This is a retrospective, observationaldata collection frommedical recordsof patientswhounderwentresectionofboneandsofttissuetumorsintheperiodof2002–2015. Thirteenpatientsmettheinclusioncriteria,whichevaluatedthecorrelationsbetween cer-tainfactors(gender,tumortype,location,reconstruction,revascularizationandpatency, infection)withamputationinthepostoperativeperiod.

Results:Inthisstudy,ofthe13patientsundergoingreconstruction,five(38.46%)evolved toamputation.Allpatientswhoprogressedtoamputationhadthefollowingincommon: presenceofbonesarcoma(p=0.005),havingundergonereconstructionwithanorthopedic prosthesis(p=0.005),lackofvascularpatencyintherevascularizationsiteinthe postopera-tiveperiod(p=0.032),andsurgicalsiteinfection(p=0.001).Noneofthepatientswithsoft tissuesarcomaunderwentamputation,andtheonlypatientwithbonesarcomawhodid notundergoamputationhadnoinfectionandmaintainedvascularpatencyofthegraft. Conclusion:Theoccurrenceofinfectionappearstobeoneofthemainriskfactorsforfailure ofrevascularization,especiallyincasesofbonesarcomainwhichvascularreconstruction isperformedwithplacementofanon-conventionaljointprosthesis.

©2016SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

StudyconductedatHospitalMadreTeresa,Servic¸odeOrtopediaOncológica;andUniversidadeFederaldeMinasGerais,Hospitaldas Clínicas,BeloHorizonte,MG,Brazil.

Correspondingauthor.

E-mail:[email protected](L.E.Teixeira). http://dx.doi.org/10.1016/j.rboe.2017.10.005

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Risco

de

amputac¸ão

após

procedimento

de

revascularizac¸ão

nas

ressecc¸ões

de

sarcoma

Palavras-chave:

Sarcomadetecidosmoles Osteossarcoma

Salvamentodemembro Amputac¸ão

Procedimentoscirúrgicos reconstrutivos

r

e

s

u

m

o

Objetivo: Oobjetivodesteestudoéavaliaraeficáciadacirurgiadereconstruc¸ãovascular apósressecc¸ãodetumoresósseosetecidosmolesemextremidadeseoriscodeevoluc¸ão paraamputac¸ão.

Métodos: Estudoretrospectivo,observacional,decoletadedadosemprontuáriomédicode pacientessubmetidosaressecc¸ãodetumoresósseosedetecidosmolesde2002a2015;13 pacientespreencheramocritériodeinclusão,foramavaliadasascorrelac¸õesde determina-dosfatores(gênero,tipodetumor,localizac¸ão,reconstruc¸ão,revascularizac¸ãoepatência, infecc¸ão)comamputac¸ãonopós-operatório.

Resultados: Nopresenteestudo,dos13pacientessubmetidosàreconstruc¸ão,cinco(38,46%) evoluíram comamputac¸ão.Todos ospacientesqueevoluíram comamputac¸ãotinham emcomumofatodeserportadoresdesarcomaósseo(p=0,005),tersidosubmetidosa reconstruc¸ãocompróteseortopédica(p=0,005)enãoapresentarpatênciavascularnolocal darevascularizac¸ãonoperíodopós-operatório(p=0,032),alémdeapresentarinfecc¸ãono localdacirurgia(p=0,001).Nenhumdospacientesportadoresdesarcomadepartesmoles foisubmetidoàamputac¸ãoeoúnicopacientedogrupocomsarcomaósseoquenãosofreu amputac¸ãonãoapresentavainfecc¸ãoemantinhapatênciavascularnoenxerto.

Conclusão:Aocorrênciadeinfecc¸ãopareceserumdosprincipaisfatoresderiscoparaa falên-ciadarevascularizac¸ão,especialmentenoscasosdesarcomaósseoemqueareconstruc¸ão vascularéfeitajuntamentecomcolocac¸ãodeprótesesarticularesnãoconvencionais.

©2016SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Este ´eumartigoOpenAccesssobumalicenc¸aCCBY-NC-ND(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Primarymalignanttumorsofthemusculoskeletalsystemare rare, accountingfor1%ofall typesofcancer1–9;surgery is

the primary method of treatment. Currently, limb preser-vation is possible in 80% of cases. A few decades ago, involvement of large vessels by tumors was an indica-tionforamputation.1,2,7,10,11However,withtheimprovement

of imaging techniques and adjuvant treatment, it has becomepossibletouse vascular reconstructiontechniques without harm regarding relapse or metastatic dissemina-tion ofthe disease,which increases the limbpreservation rate without compromising survival or recurrence of the disease.2,8–10

Vascularreconstructioninpatientsundergoingsurgeryfor resectionofsarcomashasproventobeaviablemethodinlimb salvageprocedures;autologousgraftsorvascularprostheses madeofsyntheticmaterials,suchaspolytetrafluoroethylene (PTFE),canbeused.1,3–9,11,12

Umezawaet al.1 assessed23 patientswithbone orsoft

tissuetumorsinthelowerlimbswhounderwentextensive resectionswithvascularstructureresection;totalamputation wasavoidedinallpatients.Emorietal.3 evaluatedpatients

withsofttissuesarcomaslocatedintheinguinalregionwho underwenttumorresectionandrequiredvascular reconstruc-tion;innineofthetenpatientsintheirstudy,preservation oftheaffectedlimbwaspossible.Otherauthorshaveshown good results of vascular reconstruction as a limb salvage technique.4,6,8

Basedonthesedata,thisstudy aimedtoassesstherisk ofamputationafterarterialreconstructioninboneandsoft tissuesarcomasattheextremities,andthefactorsassociated withfailureofthesalvageprocedure.

Material

and

methods

Thisisaretrospective,observationalstudyofdatacollection inmedicalrecordsofpatientswhounderwentboneandsoft tissuetumorresectionfrom2002to2015.

Thestudyincludedpatientswho,duringtumorresection, requiredinterventionbythevascularsurgeryteamfora vas-cularreconstructionprocedure;theprocedurewasindicated priortoorduringsurgery.Patientsinwhomthevascular pro-ceduredidnotrequirereconstruction(suchasarteriorrhaphy), thosewithincompletedatainthemedicalrecord,thosewith lessthansixmonthsoffollow-up,andthosewhodidnotagree toparticipatewereexcludedfromthestudy.

Thestudiedvariableswere:

1. Age 2. Gender

3. Reconstruction level (iliofemoral, femoropopliteal, poplitealtibial,brachial)

4. Typeoftumor(bone,softtissue) 5. Typeofreconstruction(prosthesis,graft) 6. Postoperativeinfection

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Fig.1–(A)Vascularprosthesis;(B)invertedsaphenousveingraft.

The statistical analysis was performed initially by a descriptive study of frequencies, expressed as mean and standard deviation (SD). The comparative study was con-ductedinitiallybyunivariateanalysisusingthechi-squared testwithorwithoutcorrectionbyFischer’sexacttestfor qual-itativevariables.Continuous variableswere analyzedusing Student’s t-test. The multivariate analysis was performed using multiple logistic regression, including variables with p<0.25.ThestudywasperformedusingSPSS® software ver-sion21.0(Chicago,USA),consideringassignificantp-values ≤0.05.

Results

Atotalof279patientsunderwentresectionofboneandsoft tissuesarcomasduringthestudyperiod.Ofthese,13required vascularreconstruction(12withinvertedsaphenousveingraft andonewithsyntheticgraft);allwereincludedinthestudy. Fig.1AandBpresentsimagesofvascularreconstructions.

Thepatient’s age variedfrom 12 to 68 years;the mean agewas36.46yearsandthemedian,35years.Nine(69.23%) patients were male and four (30.77%), female. Six (46.15%) patientshadbonesarcoma(onefibrosarcoma,one pleomor-phicsarcoma,onechondrosarcoma,andthreeosteosarcomas) and seven (53.85%) had soft tissue sarcomas (four malig-nantfibroushistiocytomas,onesofttissueEwing’ssarcoma, onesynovialsarcoma,andonehemangiopericytoma).Seven (53.85%)patientsunderwentradiationtherapy(oneinthe pre-operative periodand six in the postoperative period), and seven(53.85%)chemotherapy(threeinthesofttissuesarcoma groupandfourinthebonesarcomagroup).Epidemiological dataaresummarizedinTable1.

Amputation was required in five (38.46%) of the 13 patientsthathadrevascularizationproceduresaftersarcoma resection.Sevenpatients(53.85%) hadsoft tissuesarcomas andsix(46.15%)hadbonesarcomas.Allpatientswhoevolved toamputationhadbonesarcoma(p=0.005).Regardinggender, althoughthefivepatientswhounderwentamputationwere male,theresultwasnotstatisticallysignificant(p=0.98).

Reconstructionwithosteoarticularprosthesisofthe oper-atedsegmentwasperformedinsix(46.15%)patients,allwith bonesarcoma;ofthese,five(83.33%)evolvedwithexigencyfor amputation,astatisticallysignificantresult(p=0.005).

Regardingthelevelofrevascularization,inthree(23.08%) patients, it was performed at the iliofemoral level, in two (15.38%) at the femoropopliteal, in seven (53.85%) at the popliteal tibial, and in one (7.69%) at the brachial level. Five casesrequired amputation, one(20%) casewith revascularization at the iliofemoral level, one (20%) at the femoropopliteal,andthree(60%)atthepoplitealtibiallevel (p=0.843).

Five (38.46%) ofthe 13(100%) casesoperated,developed postoperative infection and eight (61.54%) had no infec-tion. A statistically significant association (p=0.001) was observedbetweentheoccurrenceofpostoperativeinfection andexigencyforamputation;ofthefiveinfectedpatients,all underwentamputation,whereasinthegroupwithout infec-tion,noneofthepatientsrequiredamputation.

Seven (53.85%) of the 13 patients had undergone prior chemotherapy and six (46.15%) had not. Ofthe cases that receivedchemotherapy,three(42.86%)evolvedwithexigency for amputation, whereas among the cases that did not receivechemotherapy,two(33.33%)progressedwithexigency for amputation. Nostatistically significant correlation was observedbetweenneedforamputationandprior chemother-apy(p=0.587).

Similarly, no statistically significant correlation was observedbetweentheneedforamputationandtumor loca-tion(p=0.80).Inthepresentstudy,three(23.08%)tumorswere locatedinthepoplitealregion,two(15.38%)inthefemur,four (30.78%)inthetibia,one(7.69%)inthethigh,one(7.69%)in thearm,andtwo(15.38%)intheinguinalregion.Ofthefive amputations,two(40%)weretumorslocatedinthefemurand three(60%)tumorslocatedinthetibia.Table2summarizes theseresults.

Discussion

Vascularreconstructionassociatedwithresectionofsarcomas thataffectlargevesselsofalimbhasbeenshowntobeaviable methodforaffectedlimbpreservation.1,3–9,11,12

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Table1–Epidemiologicaldata.

Name Age/gender Diagnosis Location RTX QTX

1 26/F Malignantfibroushistiocytoma Popliteal Postop No

2 38/M Fibrosarcoma Femur No No

3 27/M Ewing’ssarcoma(softtissue) Thigh Postop Yes

4 47/F Synovialsarcoma Inguinal Postop Yes

5 65/F Pleomorphicsarcoma Tibia Preop Yes

6 63/M Chondrosarcoma Proximalfemur No No

7 35/M Malignantfibroushistiocytoma Inguinal Postop No

8 12/M Osteosarcoma Tibia No Yes

9 24/M Hemangiopericytoma Popliteal No No

10 39/F Malignantfibroushistiocytoma Popliteal Postop No

11 14/M Osteosarcoma Proximaltibia No Yes

12 68/M Malignantfibroushistiocytoma Arm Postop Yes

13 16/M Osteosarcoma Tibia No Yes

Postop,postoperative;Preop,preoperative;QTX,chemotherapy;RTX,radiotherapy.

Table2–Dataanalysisresults.

Amputation Total p

No Yes

Gender

Male 4(44.44%) 5(55.56%) 9(100%) 0.098

Female 4(100%) 0(0%) 4(100%)

Diagnosis

Softtissue 7(100%) 0(0%) 7(100%) 0.005

Bone 1(16.66%) 5(83.34%) 6(100%)

Location

Popliteal 3(100%) 0(0%) 3(100%) 0.080

Femur 0(0%) 2(100%) 2(100%)

Tibia 1(25%) 3(75%) 4(100%)

Thigh 1(100%) 0(0%) 1(100%)

Arm 1(100%) 0(0%) 1(100%)

Inguinal 2(100%) 0(0%) 2(100%)

Reconstruction

Yes 7(100%) 0(0%) 7(100%) 0.005

No 1(16.67%) 5(83.33%) 6(100%)

Revascularization

Iliofemoral 2(66.67%) 1(33.33%) 3(100%) 0.843

Femoropopliteal 1(50%) 1(50%) 2(100%)

Poplitealtibial 4(57.14%) 3(42.86%) 7(100%)

Brachial 1(100%) 0(0%) 1(100%)

Infection

Yes 0(0%) 5(100%) 5(100%) 0.001

No 8(100%) 0(0%) 8(100%)

Chemotherapy

Yes 4(57.14%) 3(42.86%) 7(100%) 0.587

No 4(66.67%) 2(33.33%) 6(100%)

Patency

Yes 7(87.5%) 1(12.5%) 8(100%) 0.032

No 1(20%) 4(80%) 5(100%)

no vascular patency atthe postoperative revascularization site (p=0.032), and presentedinfection atthe surgical site (p=0.001).Noneofthesofttissuesarcomapatientsunderwent amputation;theonlypatientinthenon-amputatedbone sar-comagroupdidnotpresentinfectionandmaintainedvascular patencyinthegraft.

In their study, Emori et al.3 reported limb

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Muramatsuetal.4reportedthatonlyonepatientrequired

amputationseven monthsaftersurgerydue toprogressive deteriorationwithischemiclimbpain;nonetheless,nopatient presentedvascular insufficiency inthe immediate postop-erative period. Furthermore, three cases of infection were identified;intwoofthem,asyntheticgrafthadbeenusedfor revascularization,whichledtheauthorstorecommendthe useofautologousveingraftasfirstchoice,inanattemptto reducetheriskofinfection.

Spark et al.6 reported a case of exigency for

amputa-tionten monthsaftersurgeryduetolocalocclusionofthe vascular graft,secondary to compression caused bytumor recurrence.Intheirstudy,theauthorsreportedtheuseofa distalfemoralprosthesisinonecaseandatotalfemoral pros-thesisinanothercase;intheformer,earlyreassessmentwas necessary,asthepatientevolvedwithtwoepisodesofgraft occlusioninthefirst24h(oneduetocompressionbetween theprosthesisandtheremnantsofmuscleandtheotherdue tothrombusformation).Inthatstudy,nocasesofprogression toamputationorinfectionwerereportedinpatientswithtotal anddistalfemoralprosthesis.

Nishinariet al.8 reportedthat, at18 months

postopera-tively, nine oftheir patients who had undergone resection with venous reconstruction in the lower limbswere alive; onepatientevolvedtoabove-the-kneeamputation,11months aftersurgery,due torelapse. Amongpostoperative compli-cations,thoseauthorsobservedonecaseofsurgicalwound infection,whichevolvedtovasculargraftruptureat21days aftersurgery,butdidnotrequireanamputation.

Adelanietal.9 assessedrevascularizationafterresection

ofsoft tissuesarcomas inthe lower limbs;onlyone of14 patientsunderwentamputationduetoanacutearterial occlu-sion.However,theauthorsreportedthepresenceofsurgical woundinfectioninfourcases(ofthese,twoofthemevolved withinfectionofthevasculargraft,bothmadefromsynthetic material)andthepresenceofthrombosisinfivecases.Two patientspresentedboththrombosisandinfection; nonethe-less,itwasnotpossibletoestimatethecause/effect relation-shipbetweenthetwo.Ithasbeen reportedthattheriskof infectionwithsyntheticvasculargraftsappearstobegreater. Nishinarietal.11evaluatedpatientswithmalignanttumors

involving large vessels of the lower limbs; only one case evolved with the exigency for amputation due to relapse. Nocasesofarterialreconstructionocclusionwereobserved. However,onecaseofruptureofanarterialreconstruction sec-ondary toinfection ina surgical woundwas reported; the graft wasligatedand satisfactorycollateral circulationwas observed.

Hohenbergeretal.12reportedacaseofamputationdueto

occlusionoftherevascularizationgraftonthe17th postopera-tiveday.Intheirstudy,aninfectionrateof21%wasobserved; inonecaseofinfection,occlusionofthesyntheticgraftthat replacedthefemoralveinwasreported.

Inturn,McKayetal.7reportedfourcasesofpatientswith

softtissue neoplasias inthe groinarea, who were submit-tedtoresectionandvascular reconstruction;theprocedure wassuccessfulinpreservingthelimbinallcases.No post-operativeamputationwasrequiredduringthatstudyandno arterialocclusionoranastomoticfailurewereobservedinthe reconstructions.

Intheassessedstudies,themainriskfactorsfor amputa-tionaftertumorresectionsurgeryandvascularreconstruction for limbpreservationappear tobelocal tumorrecurrence, occlusion,andlossofgraftpatency.

However, in the present study, it was observed that, in additiontolossofpatency,thereappearstobeastatistical significancebetweenlocalinfectionandamputation.Ofthe five casesthat evolved withexigencyfor amputation, four (80%)presentedinfectionandlossofpatency;onecase(20%) presentedinfectionwithpreservedpatency.Therefore,inthe presentstudy,infectionwasariskfactorfortheneedof ampu-tation. Inadequate vascularizationmayincrease theriskof infection;infectionmayalsocompromisegraftviability.

Anotherriskfactorobservedinthepresentstudywasthe presenceofbonesarcoma,necessitatinganunconventional osteoarticularprosthesistoreplacetheresectedbone.Ofthe sixcasestreatedwithprosthesis,onlyone(16.67%) didnot undergoamputation;thispatientpresentedvascularpatency anddidnotevolvewithinfection.Moreover,allcases requir-ing amputationhad incommonthe useofunconventional osteoarticularprosthesisduetoresectionofbonesarcomaand infection.Inthegroupofpatientswithsofttissuesarcoma, noneevolvedwithamputationorinfection;theonlycase with-out graftpatency didnotrequire amputation,astherewas satisfactorycollateralcirculation.

Lossofpatencyandinfectionareriskfactorsfor amputa-tion,aswellastumorrecurrence,thatwereobservedincases ofamputationreportedinotherstudies.3,6,8,11 Thefactthat

theuseofunconventionalosteoarticularprosthesisincaseof bonesarcomasappearstobeariskfactor,maybeassociated withprolongedsurgerytimeandthepresenceofmoreinert biomaterials,withthepossibilityofinfectionassociatedwith theimplant.

Conclusion

Inthepresentstudy,theriskofamputationwas38.46%. Theoccurrenceofinfectionappearstobeoneofthemain riskfactorforrevascularizationfailure,especiallyincasesof bonesarcomainwhichvascularreconstructionisperformed togetherwiththeuseofunconventionaljointprostheses.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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1.UmezawaH,SakurabaM,MiyamotoS,NagamatsuS,Kayano S,TajiM.Analysisofimmediatevascularreconstructionfor lower-limbsalvageinpatientswithlower-limbboneand soft-tissuesarcoma.JPlastReconstrAesthetSurg. 2013;66(5):608–16.

2.SawaizumiM,ImaiT,MatsumotoS.Recentadvancesin reconstructivesurgeryforboneandsofttissuesarcomas.IntJ ClinOncol.2013;18(4):566–73.

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sarcomasintheinguinalregion:oncologicandfunctional outcomes.AnnVascSurg.2012;26(5):693–9.

4. MuramatsuK,IharaK,MiyoshiT,YoshidaK,TaguchiT. Clinicaloutcomeoflimb-salvagesurgeryafterwideresection ofsarcomaandfemoralvesselreconstruction.AnnVascSurg. 2011;25(8):1070–7.

5. KarakousisCP,KarmpaliotisC,DriscollDL.Majorvessel resectionduringlimb-preservingsurgeryforsofttissue sarcomas.WorldJSurg.1996;20(3):345–9.

6. SparkJI,CharalabidisP,LawsP,SebenR,ClayerM.Vascular reconstructioninlowerlimbmusculoskeletaltumours.ANZJ Surg.2009;79(9):619–23.

7. McKayA,MotamediM,TempleW,MackL,MooreR.Vascular reconstructionwiththesuperficialfemoralveinfollowing majoroncologicresection.JSurgOncol.2007;96(2):151–9. 8. NishinariK,WoloskerN,YazbekG,ZeratiAE,NishimotoIN.

Venousreconstructionsinlowerlimbsassociatedwith

resectionofmalignancies.JVascSurg.2006;44(5): 1046–50.

9.AdelaniMA,HoltGE,DittusRS,PassmanMA,SchwartzHS. Revascularizationaftersegmentalresectionoflower extremitysofttissuesarcomas.JSurgOncol. 2007;95(6):455–60.

10.FergusonPC.Surgicalconsiderationsformanagementof distalextremitysofttissuesarcomas.CurrOpinOncol. 2005;17(4):366–9.

11.NishinariK,WoloskerN,YazbekG,ZeratiAE,NishimotoIN, PennaV,etal.Vascularreconstructioninlimbswith malignanttumors.VascEndovascSurg.2004;38(5): 423–9.

Imagem

Fig. 1 – (A) Vascular prosthesis; (B) inverted saphenous vein graft.
Table 2 – Data analysis results.

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