Rev. bras. ortop. vol.51 número1

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

Original

Article

Use

of

superficial

peroneal

nerve

graft

for

treating

peripheral

nerve

injuries

夽

Samuel

Ribak

a,b,∗

,

Paulo

Roberto

Ferreira

da

Silva

Filho

a,b

,

Alexandre

Tietzmann

a

,

Helton

Hiroshi

Hirata

a,b

,

Carlos

Augusto

de

Mattos

a

,

Sérgio

Augusto

Machado

da

Gama

a

a_Pontifícia_Universidade_Católica_de_Campinas,_Campinas,_SP,_Brazil

b_Hospital_Nossa_Senhora_do_Pari,_São_Paulo,_SP,_Brazil

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Articlehistory:

Received1March2015 Accepted6April2015

Availableonline13January2016

Keywords:

Peripheralnerve Nerve/transplantation Peronealneuropathies

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b

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t

Objective:Toevaluatetheclinicalresultsfromtreatingchronicperipheralnerveinjuries usingthesuperficialperonealnerveasagraftdonorsource.

Methods:Thiswasastudyonelevenpatientswithperipheralnerveinjuriesintheupper limbsthatweretreatedwithgraftsfromthesensitivebranchofthesuperficialperoneal nerve.Themeantimeintervalbetweenthedatesoftheinjuryandsurgerywas93days.The ulnarnervewasinjuredineightcasesandthemediannerveinsix.Therewerethreecases ofinjurytobothnerves.Inthesurgery,alongitudinalincisionwasmadeontheanterolateral faceoftheankle,thusviewingthesuperficialperonealnerve,whichwaslocatedanteriorly totheextensordigitorumlongusmuscle.Proximally,thedeepfasciabetweentheextensor digitorumlongusandtheperoneallongusmuscleswasdissected.Next,themotorbranch oftheshortperonealmuscle(oneofthebranchesofthesuperficialperonealnerve)was identified.Theproximallimitofthesensitivebranchwasfoundatthispoint.

Results:Theaveragespacebetweenthenervestumpswas3.8cm.Theaveragelengthofthe graftswas16.44cm.Thenumberofsegmentsusedwastwotofourcables.Inevaluatingthe recoveryofsensitivity,27.2%evolvedtoS2+,54.5%toS3and18.1%toS3+.Regardingmotor recovery,72.7%presentedgrade4and27.2%grade3.Therewasnomotordeficitinthedonor area.Asensitivedeficitinthelateraldorsalregionoftheankleandthedorsalregionofthe footwasobserved.Noneofthepatientspresentedcomplaintsinrelationtowalking.

Conclusions: Useofthesuperficialperonealnerveasagraftsourcefortreatingperipheral nerveinjuriesissafeandprovidesgoodclinicalresultssimilartothosefromothernerve graftsources.

夽

WorkdevelopedintheHandSurgeryandMicrosurgeryGroup,PontifíciaUniversidadeCatólicadeCampinas,Campinas,SP,Brazil, andHospitalNossaSenhoradoPari,SãoPaulo,SP,Brazil.

∗ _{Corresponding}_author_.

E-mail:ribaksamuel@yahoo.com.br(S.Ribak).

http://dx.doi.org/10.1016/j.rboe.2015.04.010

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Emprego

do

enxerto

do

nervo

fibular

superficial

para

tratamento

de

lesões

de

nervos

periféricos

Palavras-chave:

Nervosperiféricos Nervo/transplante Neuropatiasfibulares

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e

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Objetivo:Avaliarresultadosclínicosdotratamentodaslesõescrônicasdenervosperiféricos comonervofibularsuperficialcomofontedoadoradeenxerto.

Métodos: Estudode11pacientescomlesõesdenervosperiféricosnosmembrossuperiores tratadoscomenxertodoramosensitivodonervofibularsuperficial,comintervalomédiode 93diasentreadataderegistrodalesãoeacirurgia.Foramobservadaslesõesdonervoulnar emoitopacientesedonervomedianoemseis.Emtrêsambososnervosforamlesados. Nacirurgiafaz-seincisãolongitudinalnafaceanterolateralnotornozelo,visualiza-seo nervofibularsuperficial,situadoanteriormenteaomúsculoextensorlongodosartelhos. Proximalmentedisseca-seafásciaprofundaentreosmúsculosextensorlongodosartelhos eofibularlongo.Aseguir,identifica-seoramomotordomúsculofibularcurto,umdos ramosdonervofibularsuperficial.Olimiteproximaldoramosensitivoencontra-senesse ponto.

Resultados: Amédiadoespaçoentreoscotosnervososfoide3,8cm,comprimentomédio dosenxertosde16,44cm,númerodesegmentosusadosdedoisaquatrocabos.Naavaliação darecuperaçãodasensibilidade,27,2%evoluíramparaS2+,54,5%paraS3e18,1%paraS3+. Quantoàrecuperaçãomotora,72,7%apresentavamgrau4e27,2%,grau3.Nãohouvedéficit motordaáreadoadora,observou-sedéficitsensitivonaregiãodorsolateraldotornozeloe dorsaldopé.Nenhumpacienteapresentouqueixasàdeambulação.

Conclusões:Ousodonervofibularsuperficialnotratamentodaslesõesdenervosperiféricos comofontedeenxertoéseguro eproporcionaresultadosclínicossemelhantesaoutras fontesdeenxertodenervos.

Introduction

Intreatingperipheralnerveinjuries,theobjectiveistoachieve primaryrepairwithouttensiononthesuture.Situationsin whichthereisnopossibilityofsuturing,orincasesoflossof nervesegments,suchaslateinjuries,orincomplexcases,the treatmentconsistsofreconstructionofthenerve.1

Overrecentdecades,avarietyofexperimentalstudieshave beendevelopedtodeterminethebestmethodsforfillingthe gapbetweenthestumpsofinjurednerves.2

Althoughresearchusingautogenoustubes(frommuscles orvessels)3,4_and_synthetic_{(non-autogenous)}_tubes5_has_been developed,graftsfromautogenousnervesarestillthematerial mostindicatedandused.1,2

Inchoosingthenervegraft,themattersthatneedtobe takenintoconsiderationincludewhetheritissufficientlylong toensuretension-freeanastomosis;whetherthenumberof fasciculiiscoincidentwiththoseofthereceptornerve;and whetherthesequelaeinthedonorareaareminimal.6

Giventhesecharacteristics,thedonornervesaregenerally limitedtothecutaneousnervesoftheextremities.

In the upper limbs, the nerves that are used most are themedialcutaneousnerve oftheforearm andthe lateral cutaneousnerveoftheforearm.1,2,6_The_advantage_of_these nervesistheirlocation(inthesamelimbthatistobe oper-ated),whiletheirdisadvantageistheirsmall diameterand limitedlength,whichisofteninsufficienttoadequatelyfillthe gap.6

Thesuralnerve,inthelowerlimbs,isconsideredtobethe standardfornervegrafts.7,8_It_is_the_one_most_used_because_of itsmoresuitablediameterandlength(upto30cminlength). However,despitetheabovecharacteristics,eventhismaynot alwaysbesufficientwhenlargergapsneedtobefilledorin casesofmultipleinjuries.Italsohastheinconvenienceof sen-sorylossonthelateralfaceofthefootorothercomplications inherenttothesurgicalprocedure.

In seekingalternatives,the superficial fibular nervehas emergedasaninterestingoption.Thisisalateralbranchof thecommonfibularnervethatinnervatesthelongandshort fibularmuscles.Itsuppliessensitivitytothelateraland infe-riorfacesoftheskinofthelowerleganddorsumofthefoot.9 In the lower third of the lower leg, it perforatesthe deep fascia andpenetrates into thesubcutaneouscellulartissue atthejunctionofthemiddleandlowerthirds.Atthislevel (i.e.themalleolusoftheankle),itdividesintotwobranches (medialandintermediatedorsalcutaneousbranches),which arebothresponsibleforthesensitivityofthedorsalsurface ofthefoot.10_This_is_the_commonest_branching_pattern_that hasbeendescribed.Inalesscommontype,thesebranches passindependentlythroughthedeepfascia,whichindicates thestartingpointforbranchingthatismoreproximal,2_but_it presentsthesameareaofsensitivityonthefoot.

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Table1–Dataonthe11patients:patientnumber,sex, age,timebetweentheoriginalinjuryandthesurgical treatment,andnerveaffected.

Patient Sex Age

(years)

Timeelapsedsince originalinjury

(months)

Nerve affected

1 Male 19 9 Medianand

ulnar

2 Male 58 2 Ulnar

3 Male 39 7 Ulnar

ulnar

5 Male 36 4 Ulnar

6 Male 35 1 Median

7 Male 41 1 Median

8 Male 31 1 Ulnar

9 Male 35 1 Ulnar

ulnar

11 Male 30 3 Median

Theobjective ofthe present study was to evaluatethe resultsfromclinicaluseofthesuperficialfibularnerveasa graftsourcefortreatingperipheralnerveinjuries.

Materials

and

methods

InthisretrospectivestudyconductedbetweenJune2011and January2013,11patientswithdiagnosesofperipheralnerve injuriesunderwentoperations.Directrepairstotheseinjuries duringtheoperationwerenotpossible.Inallofthesecases, thesensorybranchofthesuperficialfibularnervewasusedas agraftdonorsource.

Allthepatientsweregivenexplanationsandsigneda state-mentoflegalresponsibility,forthestudytobeconducted.The studyreceivedpriorapprovalfromtheethicscommitteefor researchonhumanbeings.

Allthepatientsweremale,withameanof4.7years(range: 19–58), and the time that had elapsed between the initial injuryand thesurgical treatmentrangedfrom onetonine months(meanof2.9).Theupperlimbswereaffectedinall cases,withwoundsinthevolarregionoftheforearm:seven ontheleftsideandfourontherightside,andthedominant sidewasaffectedinfivecases.Theulnarnervewasinjuredin eightcasesandthemediannerveinsixcases.Inthreecases (Table1),therewasconcomitantinjurytobothofthesenerves.

Surgicaltechnique

Generalanesthesiawasusedinallthecases.Thepatientwas positionedinsupinedecubitus,ahandtablewasusedand exsanguinationwasperformedusingapneumaticcuff.The elbowandforearmwerekeptextendedinordertomarkout theincision.

Afterthenerveinjuryhadbeenidentified,thetechnique consistedofresectingthedamagednervetissueuntilhealthy tissue was encountered. The fascicles of this tissue were identified.Atthispoint,thegapbetweenthestumpswas mea-sured,alongwiththesizeofthegraftthatwastobeharvested (Fig.1).

Fig.1–Measurementincentimetersofthespacebetween thestumpsinacaseofulnarnerveinjury.

With the limb positioned, the anterior subcutaneous courseofthesuperficialfibularnervetothelateral malleo-luscouldbeviewed(Fig.2).Thesubcutaneouscourseofthis nervecouldbeviewedinninepatientsbeforetheoperation.

Withthepatientinthesamedecubituspositionandwith atourniquetonthelowerlimbthatwastobeoperated,a lon-gitudinalincisionwasmadeinthelateralfaceoftheankle, 4cmanteriorlytothemidlineofthemalleolus.

Afterthesubcutaneoustissuehadbeenopened,the super-ficialfibularnervecouldbeviewed.Thiswaslocatedanteriorly tothelongextensormusclesofthetoes.Atthislocation, prox-imal dissectionwasperformedbymeans oflongitudinalor continuousincisions,whichfollowedthesubcutaneouspath ofthenerveasfarasthelowerthirdofthelowerleg,whereit perforatedthedeepfascia(Fig.3).

Depending onthe size ofgraft required, dissectionwas thenperformedintheproximaldirectionatadeeperlevel, inwhichthedeepfasciawassectionedalongthelongaxisof theincisionandthelayerbetweenthelongextensormuscle ofthetoesand thelong fibularmuscleswasseparatedout laterally(Fig.4).

Followingthis,thebranchtotheshortfibularmusclewas identified.Theproximallimitofthesensitivebranchwasset atthispoint.Thedistaldissection,atthelevelofthelateral malleolus,followedthemedialandintermediatedorsal cuta-neousbranches(Fig.5).

Toharvestthenerve,sectioningoftheproximalportionof thenervewaspreferred.Followingthis,thenervewasraised

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Fig.3–Viewingofthefibularnerveanditsanatomical references:4cmanteriorlytothelateralmalleolusand dissectionmoreproximallyalongitssubcutaneouscourse.

Fig.4–Identificationofthesuperficialfibularnerveina moreproximaldissection,throughopeningthefascia.

proximallyandalongitsentirelength,includingthetwodistal branches(Fig.6).

Independentofthebranchingpatternobserved,themain trunk of the superficial fibular nerve penetrated into the deepfascia,orthemedialandintermediatedorsalcutaneous branchespenetrateditseparately.Thedissectionwassimilar towhatwasdescribedabove,sinceinidentifyingthebranches, theywerefollowedtothestartofthemostproximalbranching, alongthedeepfascia(Fig.7).

Inthereceptorarea,thelengthanddiameterofthe inter-fascicular grafts that would be necessary in order both to

Fig.5–Identificationofthemedialandintermediatedorsal cutaneousbranchesafterdistaldissection.

Fig.6–Viewoftheproximalharvestingofthenerveand itselevationalongitsentirecourse.

Fig.7–Identificationofthemostproximalbranchingofthe sensoryfibularnerve.

fill the gap between the stumps and to cover the entire cross-sectional area ofthe injured nervewere ascertained. Inpreparingthe finalgraft,cablesofappropriatesizewere arrangedinparallelandwerejoinedusingfibringlue(Fig.8).

Followingthis,thegraftwassuturedbothproximallyand distally (Fig. 9)usingfibrin gluetogether withthesuturing (Ethilon 8 or 9-0 nylon thread). In cases in which associ-atedtendoninjurieswerepresent,thetendonsweresutured first.

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Fig.9–Nervegraftpositionedbetweenthenervestumpsin anappropriatepositionforsuturingwithouttension.

Criteriaforassessingtheresults

- Measurementofthegapbetweenthenervestumpsafter excisionoftheneuroma,usingarulerwithascalein mil-limeters,withthejointsadjacenttotheinjurymaintained intheneutralposition.

- Identificationoftheanatomicalpatternofthebranchingof thefibularnerve,definedastype1,whenthemaintrunkof thesuperficialfibularnervepenetratedintothedeepfascia; ortype2,withseparatepenetrationofthemedialand inter-mediatedorsalcutaneousbranchesintothedeepfascia.11 - Lengthofthesuperficialfibularnerveharvested.

- Numberofcablesneededtoachieveadequatethicknessfor thecross-sectionalareaoftheinjurednerve.

- Evaluation oftherecoveryofsensitivity(measuredusing thescaleoftheBritishMedicalCouncilSystemof Assess-ment), inwhichS0represented lackofsensory recovery; S1, recoveryregardingdeep cutaneouspain; S2, recovery regardingsuperficialcutaneouspain;S2+,exacerbationof theresponse;S3,recoveryregardingpainandtouchwithout exacerbationanddiscriminationoftwopoints>15mm,S3+, goodlocalizationofstimulianddiscriminationoftwopoints at7–12mm;andS4,completerecoveryanddiscrimination oftwopointsat2–6mm.

- Evaluationofmotorrecovery,usingthescaleoftheBritish MedicalCouncilSystemofAssessment,inwhichgrade5 representednormalstrengthagainsttotalresistance;grade 4,musclestrengthisreduced,butthereismuscle contrac-tion against resistance; grade3, joint movement is only achievedagainstgravityand withoutresistancefromthe examiner;grade2,thereismusclestrengthandjoint move-mentonlywithoutresistancefromgravity;grade1,muscle contractionwithoutmovementisseenorfelt,or fascicula-tionisobservedinthemuscle;andgrade0,nomovement isobserved.

- Sensoryandmotordeficitsinthedonorarea. - Complaintsaboutabnormalitiesofwalking. - Complaintsaboutthehealinginthedonorarea.

Results

Themeandurationofthepostoperativefollow-upwas11.18 months(range:sixto18).

Fig.10–Areaofresidualanesthesia,sixmonthsafterthe operation.

Themeandistancebetweenthenervestumpsafter exci-sion oftheneuroma was 3.8cm (range: 3–5.5cm). Incases ofinjuryonlytotheulnarnerve,itwas3.57cm;andtothe mediannerve,4.08cm.Whenbothnerveswereinjured,the meansizeofthegraftneededwas4.13cm.

Regardingtheanatomicalpatternoffibularnerve branch-ing,90.9%(tencases)presentedthetype1patternandonly onecaseshowedtype2(9.09%).Themaximumlengthofthe graftharvestedwas26cmandtheminimumwas9cm(mean of16.9cm).

Themeannumberofcablesusedinordertoachieve ade-quatethicknessofthecross-sectionalareawasthreetofour cablesforthemediannerveandtwotothreefortheulnar nerve.

Inevaluatingtherecoveryofsensitivity,27.2%presented S2+ (three cases),54.5% S3 (six cases) and 18.1% S3+ (two cases). Regarding motor recovery, 72.7% (eight cases) pre-sentedgrade4and27.2%(threecases),grade3.

Innocasewasmotorlossinthedonorlimbobserved. Sensorydeficitinthedonorareawasobservedinthe dor-solateral region of the ankle and the dorsal region of the foot (Fig. 10). There was no sensory deficit in the plantar region.Noneofthepatientspresentedcomplaintsinrelation towalking.Regardingthedonorarea,therewerenocaseson complaintsabouthealing,eveninthecasesinwhichalarge quantityofgraftwasnecessary,withagreaternumberof inci-sionstoharvestit.

Onlyonecasepresentedsuperficial infectious complica-tionsoftheskininthedonorarea,whichwasseenoneweek afterthesurgery.Itwastreatedwithoralantibiotic,withgood evolution.

Discussion

Despitedecadesofadvancesinnerveresearch,12 _treatment ofperipheralnerveinjuriescontinuestobeasignificant chal-lenge.

For filling the space between the nerve stumps, grafts fromautogenousnervesremainthegoldstandardfornerve reconstruction,sincetheyprovidesupportarchitecture, neu-ralgrowthguides,neurotrophicfactorsandSchwanncells.13

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ofthelocationsofthemedialandlateralcutaneousnervesof theforearm,thesenervesareoflimitedthicknessandlength.6 Thesuralnerveistheonemostused,anditisconsidered tobethestandardasagraftdonorsource.7,8 _However, har-vestingthisnervepresentssomeinconveniencesintermsof itspositioning,theneedtochangedecubitusandtheareaof lossofsensitivityinthelateralregion.Thissourceislimited whenalargequantityofgraftisneeded.

Theidealwouldbeto haveanoptionalgraft sourcefor whenthisisnecessary,orevenasthefirstchoicetobeused. Thesuperficialfibular nerve hasbeen shownto beagood optionasadonorsource,sinceitsuppliesalonggraftofgood caliberthatisanatomicallypredictable.Itcanbeharvested withthepatientindorsaldecubitusandiseasilyaccessible, withouttheneedforchangesofdecubitus.

In an anatomical study, Buntic et al.6 _reported _that _in theirsample,themeanlengthharvestedwas14.7cm(range: 3–25cm),andthat40cmwouldbepossible.Inourstudy,we achievedasimilarmean,of16.44cm(range:9–26cm),which wascomparabletothesizesusedwhenthesuralnervewas chosen.7,13

Lossofsensitivityintheregionsuppliedbythedonornerve isa formofmorbidity common toany graft source.What maydifferentiatethe sourcesisthe extentofthe areaand itslocation,whichmightbeclosetoaninconvenientregion. Inthisregard,useofthelateralcutaneousnervecanbecited, whichgivesrisetolossofsensitivityalongthelateralfaceof theforearmthatmayextendoverthethenarregion,whichis undesirableincasesofinjuriestothemediannerveorfinger nerves.

Inthecaseoftheradialsensorynerve,compromisingthe dorsolateralregionofthehandisalsoundesirable.

Inthelowerlimbs,preservationoflateralandplantar sen-sitivityisextremelyimportantforpreventingulcersandother wounds.Inthisregard,useofagraftfromthesuperficial fibu-larnervehasanadvantagebecause onlyanareaofdorsal anesthesiaoccurs.

Inrelationtopossiblecomplicationsinthedonorarea, for-mationofapainfulneuromawouldbeoneofthese.Buntic etal.6 _observed_the _presence_of_a_case_of_painful_neuroma ofthesuperficialfibular nervethathad tobeoperated. No presenceof neuromas was observed in our series. Forma-tionofneuromasuponharvestingthesuralnervehasbeen reportedintheliteratureatratesrangingfrom22%to42%of thecases.14,15

Inourseries,noinjuriestomotorbranchestothefibular musclesweredetectedinanyofourcases.

Knowledgeoftheanatomicalvariationsofbranchingofthe fibularnerveisofprimeimportanceforsurgeonswhowish tousethisnerveasagraftsource,sothatinjurywhile rais-ingitsdistalbranchescanbeavoided.Inthepresentstudy, thetype1anatomicalpatternofbranchingwasmore preva-lent.Themaintrunkofthesuperficialfibularnervepenetrated thedeepfascia,asalsoseeninotherstudiesintheliterature, whichconfirmstheeaseofharvestingofthisnerve.However, itshouldbenotedthatoccurrencesoftype2arepossible.

Thepossibilityofsubcutaneousviewingofthefibularnerve inmostpatientsmakesiteasiertomaketheinitial identifi-cationandtoperformthedissection.Intheliterature,some methodsfor viewingthis nerve havebeen described, such

asplantarflexionoftheanklecombinedwithinversion.Its courseinthedistalsegmentofthelowerlegcanbemarked outbeforetheoperation,evenifitslocationmaychangewith differentpositionsofthefootandankle.16_This_is_an_advantage indissectingit.

Accurate and reproducible assessment of the evolution iftreatmentsfornerveinjuriesisdifficult,giventhatmany variables are involved, in relation to both the patient’s comorbiditiesandthesurgicaltechnique,typeoflesionand postoperativerehabilitationprotocols.

Theresultsfromthisstudyonclinicaluseofgraftsfrom the superficialfibularnervewerecomparablewiththosein theliterature.Useofthisnerveremainslow,buttheoverall resultsweresimilartothosefromseriesthatusedothernerves asgraftdonorsources.6,7

Thesuperficialfibularnervethereforeemerges asasafe and valuabledonornerve source,particularlyincasesthat require long grafts.Not onlydoesit constitute anoptional source,butalsoitcould formthe firstchoiceforuseasan autologousnervegraft,becauseofitsadvantages.

Conclusions

Useofthesuperficialfibularnerveasanervegraftsourcefor treatingperipheralnerveinjuriesissafeand providesgood clinicalresults.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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