Comparison of the results from simple radiography, from before to after Salter osteotomy, in patients with Legg-Calvé-Perthes disease

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

Original

Article

Comparison

of

the

results

from

simple

radiography,

from

before

to

after

Salter

osteotomy,

in

patients

with

Legg-Calvé-Perthes

disease

夽

,

夽夽

Hugo

Futoshi

Toma

_,

_Thiago

_de

_Almeida

_Oliveira

_Felippe

_Viana

_,

Rostanda

Mart

Meireles

_,

_Isabel

_Moreira

_Borelli

_,

_Francesco

_Camara

_Blumetti

_,

Eduardo

Shoiti

Takimoto

_,

_Eiffel

_Tsuyoshi

_Dobashi

a_{UniversidadeFederaldeSãoPaulo(UNIFESP),SãoPaulo,SP,Brazil}

b_{DepartmentofOrthopedicsandTraumatology,UniversidadeFederaldeSãoPaulo(UNIFESP),SãoPaulo,SP,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received13June2013 Accepted12August2013

Availableonline16September2014

Keywords:

Legg-Calvé-Perthesdisease Radiography

Classification Child

a

b

s

t

r

a

c

t

Objectives:Todeterminewhethertheclinicalvariablesandpreoperativeclassificationof patientswithLegg-Calvé-Perthesdisease(LCPD)whoundergoSalterosteotomycorrelate withtheradiographicresultatthetimeofskeletalmaturity.

Methods:Inthisretrospectivecohortstudy,47individualswithLCPDwhoweretreatedusing Salterosteotomy(1984–2004)wereevaluated.Thepatientswereevaluatedaccordingto sex,skincolor,sideaffectedandageatwhichosteotomywasperformed.Thepreoperative radiographswereanalyzedinaccordancewiththeclassificationsofWaldenström, Catter-all,LaredoandHerring.Theradiographsobtainedatthetimeofskeletalmaturitywere classifiedusingtheStulbergmethod.

Results:Themeanageatthetimeofsurgicaltreatmentwas82.87months(6.9years).Theage presentedastatisticallysignificantcorrelationwiththeStulberggradesatskeletalmaturity (p<0.001).Patientsovertheageof6.12yearstendedtopresentlessfavorableresults.The variablesofsex,skincolorandsideaffecteddidnotpresentanystatisticallysignificant correlationwiththeprognosis(p=0.425;p=0.467;p=0.551,respectively).OnlytheLaredo classificationpresentedastatisticallysignificantcorrelationwiththefinalresultgivenbythe Stulbergclassification(p=0.001).Theotherclassificationsused(Waldenström,Catteralland Herring)didnotpresentanycorrelationbetweenthetimeatwhichsurgerywasindicated andthepostoperativeresult.

Conclusions:TheageatwhichthepatientsunderwentsurgicaltreatmentandtheLaredo classificationgroupsweretheonlyvariablesthatpresentedsignificantcorrelationswith theStulbergclassification.

©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.Allrightsreserved.

夽

Please cite this article as: TomaHF, de Almeida Oliveira FelippeViana T, Meireles RM,Borelli IM, BlumettiFC, Takimoto ES, etal.Comparac¸ãoentreresultados deradiografiasimples,pré epós-osteotomiadeSalter, em pacientesportadores da doenc¸ade Legg-Calvé-Perthes.RevBrasOrtop.2014;49(5):488–93.

夽夽

WorkdevelopedintheDisciplineofPediatricOrthopedics,DepartmentofOrthopedicsandTraumatology,PaulistaMedicalSchool, UniversidadeFederaldeSãoPaulo(UNIFESP-EPM),SãoPaulo,SP,Brazil.

∗ _{Correspondingauthor.}

E-mail:eiffeldobashi@uol.com.br(E.T.Dobashi).

http://dx.doi.org/10.1016/j.rboe.2014.09.003

Comparac¸ão

entre

resultados

de

radiografia

simples,

pré

e

pós-osteotomia

de

Salter,

em

pacientes

portadores

da

doenc¸a

de

Legg-Calvé-Perthes

Palavras-chave:

Doenc¸adeLegg-Calvé-Perthes Radiografia

Classificac¸ão Crianc¸a

r

e

s

u

m

o

Objetivos: Determinarempacientescomdoenc¸adeLegg-Calvé-Perthes(DLCP) submeti-dosàosteotomiadeSalterseasvariáveisclínicaseasclassificac¸õespré-operatóriasse correlacionamcomoresultadoradiográficonamaturidadeesquelética.

Métodos: Nesteestudodecoorteretrospectivoforamavaliados47indivíduosportadoresda DLCPtratadoscomosteotomiadeSalter(1984-2004).Ospacientesforamavaliadosdeacordo comsexo,cor,ladoacometidoeidadeemquefoifeitaaosteotomia.Asradiografias pré-operatóriasforamanalisadasdeacordocomasclassificac¸õesdeWaldenström,Catterall, LaredoeHerring.Asradiografiasobtidasnamaturidadeesqueléticaforamclassificadas segundoométododeStulberg.

Resultados: Amédiadaidadenomomentodotratamentocirúrgicofoide82,87meses(6,9 anos).Aidadeapresentoucorrelac¸ãoestatisticamentesignificativacomosgrausdeStulberg namaturidadeesquelética(p<0,001).Pacientesacimade6,12anostendemaapresentar resultadosmenosfavoráveis.Asvariáveissexo,coreladoacometidonãoapresentaram correlac¸ãoestatisticamentesignificativacomoprognóstico(p=0,425;p=0,467;p=0,551, respectivamente).Apenasaclassificac¸ãodeLaredoapresentoucorrelac¸ãoestatisticamente significantecomoresultadofinaldadopelaclassificac¸ãodeStulberg(p=0,001).Asdemais classificac¸õesusadas,Waldenström,CateralleHerring,nãoapresentaramcorrelac¸ãoentre omomentoemquefoiindicadaacirurgiaeoresultadopós-operatório.

Conclusões: Aidadeemqueospacientesforamsubmetidosaotratamentocirúrgicoeos gruposdaclassificac¸ãodeLaredoforamasúnicasvariáveisqueapresentaramcorrelac¸ão significativacomaclassificac¸ãodeStulberg.

©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Todososdireitosreservados.

Introduction

SinceLegg-Calvé-Perthes disease(LCPD)was firstdescribed in1910,ithasalwaysbeenamatterofgreatinterestamong researchersandhasbecomeoneofthemost-debatedtopics inthe orthopedicliterature.Several aspectsofthis clinical entitystillremainunclear,especiallyregardingitsetiologyand treatment.

Foralongtime,almostallauthorsconcentratedon ana-lyzingthe radiographicaspectsofthe disease.Itsphaseof evolutionwerefirstdescribedbyWaldenström,1_whose clas-sification was subsequently simplified and correlated with theanatomopathologicalfindingsbyJonsäter.2_{Evaluationson} impairmentoftheossificationnucleusofthefemoralhead weresystematizedbyCatterall3_{basedonanalysisofsimple} radiographsdone during the phaseofmaximum fragmen-tation.Withthe aimofdeterminingtheproportionsofthe lesionduringtheinitialphaseandduringnecrosis,Salterand Thompson4 _{demonstrated thatthe sizeofthesubchondral} fracture in the lateral view ofthe head precisely reflected thedegreetowhichtheproximalfemoralepiphysishadbeen affectedbythedisease.Morerecently,Herringetal.5_proposed anewclassificationbasedontheheightofthelateralcolumn ofthefemoralepiphysis.

Becausethe hips have a cartilaginous mold during the growthstagethatisnotvisibleonsimpleradiographs,Laredo6 and Milani and Dobashi7 _{demonstrated that arthrography}

wouldmakeitpossibletodetectalterationstotheshapeofthe headandfemoralextrusionbeforeconventionalradiographic examinationwouldbeabletorecognizethesefeatures.These authorsproposedanarthrographicclassificationcomposedof fivegroups.Amongthese,itwouldbepossibletotreatgroupsI andIIusingclosedtechniques,whilearthrographicriskwould beshown bythe othergroups, withthepresenceof extru-sionandmorphologicalalterationsofthehead,andsurgical containmentwouldbenecessary.

AlthoughLCPDtreatmenthasforyearsbeenthesubject ofexhaustivediscussionsamongorthopedists,thereisstill noclearevidenceregardingthebesttherapeuticmethod.In relation to surgical treatment, the methods mostused for providingimprovementsintherelationshipbetweenthe prox-imalfemoralepiphysisandtheacetabulumaretheso-called containmentprocedures,whichcanbedividedintotwomajor groups:(1)osteotomyoftheproximalfemur8,9_{; and(2)} pro-cedures involving theiliac bone. Thelatter groupincludes “shelf”surgery,medialdisplacementosteotomy10_andSalter osteotomy,11,12_{whichcanbeusedduringtheactivephaseof} thedisease.Inadditiontothebiomechanicalaspectsofthe improvementthroughcontainment,itisbelievedthatthere isalsoabiologicaleffectthatgivesrisetoaccelerationofthe reossificationprocess.13–16

Laredocorrelatedwiththeradiographicresultatthetimeof skeletalmaturityandwhetherthesemightindicatethe prog-nosis.

Materials

and

methods

Thepresentstudywassubmittedtoevaluationbyour insti-tution’sresearchethicscommitteeandwasapprovedunder reportno.0795/11.

Weevaluatedaretrospectivecohortconsistingofallthe individualswithLCPDwhoweretreatedinourinstitution’s departmentoforthopedicsand traumatologybetween1984 and 2004.Patients who fulfilledthe followingcriteria were included: (1) individuals with LCPD who underwent Salter osteotomytoachievecontainmentofthe femoralhead;(2) whohadreachedskeletalmaturitybythetimeofthelast clin-icalassessment;and(3)forwhomradiographsfrombeforethe operationandafterreachingskeletalmaturitywereavailable. Individualspresentingnecrosisoftheproximalfemurwith definedetiologyandthosewithLCPDwhounderwentother typesoftreatmentwereexcluded.

Forty-sevenpatientsfulfilledtheinclusioncriteria.The fol-lowingdatawere evaluatedandextractedfrom theclinical medicalfiles:sex,skincolor,sideaffectedandageatwhich osteotomywasperformed.

Thepreoperativeradiographswereclassifiedinaccordance withthefollowingmethodsthathavebeendescribedinthe literature: (1) Waldenström,1 _{as modified by Jonsäter}2_{; (2)} Catterall3_{;(3) Laredo}6,7_{;and (4)the lateral pillarmethodof} Herringetal.5_{Theradiographsobtainedafterskeletal} matu-rityhadbeenreachedwereclassifiedinaccordancewiththe methodofStulbergetal.17

Theradiographsfromthepreoperativeexaminationsand thosefromthetimeofskeletalmaturitywereclassifiedbythe seniorauthoratdifferenttimes.Thisauthoralsodidnothave accesstotheclinicaldata,soastominimizetheriskofbias.

Thenominalvariableswerecorrelatedusingabsoluteand relativefrequenciesandthecontinuousvariables,bymeansof summarymeasurements(mean,standarddeviation,median, minimumandmaximum).

TheStulberggradeswereevaluatedaccordingtosex,skin colorandsideaffected,usingtheMann–Whitneytest.18 Spear-man’scorrelationtestwasusedtoinvestigatewhetherthere were anyrelationships betweenthe Stulberg scaleand the gradesshownbytheotherscales,andwithageandlength offollow-up.18

Thevariablesthatpresentedsomestatisticallysignificant relationshipwiththegradesontheStulbergscalewerefitted intoamultiplelogisticregressionmodel,19_{withgroupingof} gradesIandIIandgradesIIIandIV.Onlythevariablesthat togetherhadaninfluenceonthegradeontheStulbergscale were keptinthefinal model.All thetests wereperformed takingthesignificancelevelof5%.

Results

Table1summarizesthedemographicdataandallthe vari-ablesgathered,withtheirrespectivedistributions,including:

Table1–Distributionoffrequenciesofthepatients included,accordingtothevariablesofsex,skincolor, sideandtheWaldenström,Catterall,Herring,Laredo andStulbergclassifications.

Variable Frequency(n) %Total %Valid

Sex

Female 10 21.3 21.3

Male 37 78.7 78.7

Subtotal 47 100 100

Color

White 40 85.1 95.2

Others 2 4.3 4.8

Subtotal 42 89.4 100

Noinformation 5 10.6

Side

Right 21 44.7 44.7

Left 26 55.3 55.3

Waldenströmclassification

I 16 34.0 34.0

II 24 51.1 51.1

III 5 10.6 10.6

IV 2 4.3 4.3

Catterallclassification

II 2 4.3 4.3

III 23 48.9 50

IV 21 44.7 45.7

Subtotal 46 97.9 100

Unclassifiable 1 2.1

Herringlateralpillarclassification

A 5 10.6 10.9

B 22 46.8 48

C 19 40.4 41.3

Subtotal 46 97.9 100

Unclassifiablea _{1 2.1}

Laredoclassification

III 25 53.2 56.8

IV 15 31.9 34

V 4 8.5 9.1

Subtotal 44 93.6 100

Unclassifiablea _{3 6.4}

Stulbergclassification

I 11 23.4 24.4

II 6 12.8 13.3

III 18 38.3 40.0

IV 10 21.3 22.2

Subtotal 45 95.7 100

Unclassifiablea _{2 4.3}

Total 47 100

a _{Patientswereconsideredtobeunclassifiablewhenthe}

radio-graphsavailablewereonlyfromtheremodelingphase,inwhich mostofthemethodscannotbeapplied.

sex,skincolor,sideaffected,preoperativeclassification1–7_and postoperativeclassification(Stulberg).17

Themean ageatwhichthesurgicaltreatmentwas per-formedwas82.87months(range:48–152)andthemeanlength offollow-upwas118.07months(9.84years)(Table2).

Table2–Summarymeasurementsforageandlengthoffollow-upamongthepatientsincluded.

Variable Mean SD Median Minimum Maximum N

Age(months) 82.87 24.82 77 48 152 47

Lengthoffollow-up(months) 118.07 22.76 119 67 158 47

SD,standarddeviation.

0.0 0.0 0.2 0.4 0.6 0.8 1.0

0.6 0.4 0.2

1 – Specificity

Sensitivity

1.0 0.8

Fig.1–ROCcurverelatingtosensitivityandspecificityof ageindeterminingaworsefinalresultcharacterizedby StulbergIIIorIV.

According to the analysis on the curve,73.5 months(6.12 years)wastheagethatbestdistinguishedbetweenStulberg IIIandIV,andthisageshowedsensitivityof78.6%and speci-ficityof70.6%.Thismeansthatwhentreatmentisinstituted aroundthisage,theprognosisisbest.Ageasaseparate fac-toralsoshowedastatisticallysignificantcorrelation(p<0.001) andindicatedthattheyoungertheageatwhichthepatient undergoescorrectivesurgeryis,thebettertheprognosisalso is.

Thevariablesofsex,skincolorandsideaffected,as eval-uated using the Mann–Whitney test, did not present any statistically significant difference regarding the prognosis (p=0.425;p=0.467;andp=0.551,respectively).

OnlytheLaredoclassificationpresentedastatistically sig-nificantcorrelationwiththefinalresultgivenbytheStulberg classification(p=0.001),accordingtoSpearman’scorrelation test. The other classifications (Waldenström,Catterall and Herring)didnotpresentanycorrelationbetweenthetimeat whichsurgicaltreatmentwasindicatedandthepostoperative result,andwerethereforenotpredictorsregardingthe treat-mentandprognosis.ThesedataaresummarizedinTable3.

Discussion

Salterosteotomy11,12_{hasbeenusedinourinstitutionfor} sur-gicaltreatmentofLCPDsince1979.Thisindicationismadein caseswithextensiveimpairmentandespeciallyincaseswith alterationstotheshapeandsizeofthefemoralheadthatare

shownbyarthrographicassessmentofthehipinaccordance withtheLaredoclassification.6,7

Theclassificationmethodsthataremostwidely dissemi-natedintheliteraturewereusedinthisstudy.Itwassought to establishwhich ofthem mighthave greatestprognostic valueinrelationtothefinalresultafterthediseasehadrunits course.AccordingtotheWaldenströmclassification,mostof thepatientswereinthephasesofnecrosis(34%)and fragmen-tation(51.1%),giventhatthesearethebesttimesforsurgical intervention,beforetheremodelingprocessgetsunderwayor isconcluded.20 _{Becausethiswas asampleofpatientswho} underwentsurgicaltreatmentconsistingofSalterosteotomy, mostofthe individualsincludedpresentedhipswith mod-erate tosevere involvement,according to the radiographic classificationsofCatterall3_{andHerringetal.}5

Preoperativearthrographywasperformedon44patients. Inallofthesecases,therewereimportantmorphological alter-ationsofthefemoralhead,especiallyintermsofextrusion andincreasedsize.Thus,allofthese44hipswereincludedin thethreearthrographicriskgroupsofLaredo,with predomi-nanceofgroupsIIIandIV.

Few studiesin theliteraturehave correlatedthe results from Salter osteotomy fortreating LCPD withthe Stulberg classificationforgradingtheradiographicresults.21–23

Ishidaetal.23_{studiedtheresultsfromSalterosteotomyfor} treating32patients(37hips)atskeletalmaturityandobserved thatthehipsclassifiedbyLaredoasbelongingtogroupIII pre-sentedbetterresultsthanthoseofhipsingroupsIVand V. Thisobservationcorroboratestheconceptthatadequate cov-erageofthefemoralheadbeforeseveredeformitybecomes established provides animprovement inhip biomechanics andfavorstheremodelingprocessoverthecourseofLCPD.15,16 Likewise,inourstudy,weobservedthat47.8%ofthepatients classifiedinLaredogroupIIIevolvedtoStulbergtypeIorII.On theotherhand,inthegroupofpatientsclassifiedasLaredo groupsIVandV,only13.4%and25%ofthepatientsevolvedto StulbergtypeIorII,respectively.

Theseobservationsvalidatetwofacts:firstly,hip radiogra-phyinLCPDcasesdoesnotmirrortheanatomicalrealityof thefemoralheadaffectedbythedisease;secondly,itis pre-ciselywhenahipisclassifiedasbelongingtoLaredogroupIII6 thattheheadisconsideredtobeleavingitsprotectionzoneat theacetabularbonerim.Insuchcases,ifnocoverisprovided intime,theheadwilldeform.24

Table3–CorrelationoftheStulbergclassificationwiththevariablesofsex,color,side,age,lengthoffollow-upandthe Waldenström,Catterall,HerringandLaredoclassifications.

Variable Stulberg Total p

I II III IV

n % n % n % n %

Sex 0.425a

Female 3 25.0 0 0.0 5 41.7 4 33.3 12

Male 8 22.8 6 17.2 14 40.0 7 20.0 35

Color 0.467a

White 8 21.1 5 13.2 16 42.1 9 23.7 38

Others 1 50.0 0 0.0 1 50.0 0 0.0 2

Side 0.551a

Right 5 23.8 2 9.5 12 57.1 2 9.5 21

Left 6 25.0 4 16.7 6 25.0 8 33.3 24

Waldenströmclassification 0.052b

I 5 35.7 1 7.1 6 42.9 2 14.3 14

II 6 25.0 5 20.8 9 37.5 4 16.7 24

III 0 0.0 0 0.0 1 20.0 4 80.0 5

IV 0 0.0 0 0.0 2 100.0 0 0.0 2

Catterallclassification 0.260b

II 2 100.0 0 0.0 0 0.0 0 0.0 2

III 4 19.0 4 19.0 9 42.9 4 19.0 21

IV 5 23.8 2 9.5 8 38.1 6 28.6 21

Herringlateralpillarclassification 0.243b

A 2 40.0 0 0.0 2 40.0 1 20.0 5

B 6 30.0 4 20.0 6 30.0 4 20.0 20

C 3 15.8 2 10.5 9 47.4 5 26.3 19

Laredoclassification 0.001b

III 7 30.4 4 17.4 11 47.8 1 4.3 23

IV 1 6.7 1 6.7 7 46.7 6 40.0 15

V 0 0.0 1 25.0 0 0.0 3 75.0 4

Meanage±SD 62.91±19.32 80.5±17.55 87.94±21.4 97.8±28.91 83.02±25.08 <0.001b MeanLF±SD 121.55±19.82 106±18.01 120.17±22.55 117.7±28.88 118.07±22.76 0.802b

LF,lengthoffollow-up;SD,standarddeviation.

a _{ResultfromMann–Whitneytest.}

b _{ResultfromSpearman’scorrelationtest.}

treatmentprovided,patientsovertheageofsixyearstendto evolvewithgreaterincidenceofunsatisfactoryresults.25,26

TheCatterallandHerringclassificationshavebeenwidely usedintheliteratureandinclinical practiceforindicating treatment forLCPD.However, it has been reported in sev-eralstudiesthatbothmethodspresentdeficienciesintheir capacitytopredictthefinalclinicalresult.27,28 _Ourdataare concordantwiththeseobservations, sincewefoundinour samplethatwasasignificantdissociationbetweenthe grad-ingsgivenbytheseclassificationsbeforethe operationand theresultsatthetimeofskeletalmaturity.Forexample,more thanhalf(n=3;60%)ofthepatientsclassifiedasHerringtype AevolvedwithhipsofStulbergclassesIIIorIV.Attheother extreme,five ofthe patients classified asCatterall type IV (23.8%)evolvedwithhipsofStulbergclassI.

Several authors have pointed out that oneof the prob-lemsofthe radiographicclassificationsforPerthesdisease, and notably in relation to Catterall, is the low to moder-ateinterandintra-observerconcordance.29–31_{Thestabilityof} theHerringclassificationhasalsobeenquestionedrecently

by Park et al., who noted changes from the initial grad-ing in 40% of the patients with LCPD that they evaluated usingserialradiographs.32_{Theseobservationshaveimportant} implicationswhensomeofthesemethodsareusedinclinical practice,giventhattheclassificationsshouldideallydictate thetreatmentandprognosis.

Basedonthedataobservedinthisstudy,webelievethat the Laredo classification6,7 _{may provide thebest substrate,} in a systematized manner, for determining the prognosis ofpatients inwhom surgical treatmentisindicated. Thus, ourdataconfirmtheobservationsofIngman33_andPaterson etal.,34_{whofoundacloserelationshipbetweenthepresence} ofmarkedflatteningofthefemoralheadonarthrographyand occurrencesofpoorresultsfromSaltersurgery.

Conclusion

Laredoclassificationweretheonlyvariablesthatpresenteda significantcorrelationwhichtheStulbergclassification.Thus, we conclude that the Laredo classification showed higher prognosticvaluethantheCatterallandHerringclassifications fortreatingLCPDbymeansofSalterosteotomy.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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