Rev. bras. ortop. vol.50 número1

r e v b r a s o r t o p . 2015;50(1):68–71

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

Original

article

Bone

mineral

density

evaluation

among

patients

with

neuromuscular

scoliosis

secondary

to

cerebral

palsy

夽

Rodrigo

Rezende

_,

_Igor

_Machado

_Cardoso

_,

_Rayana

_Bomfim

_Leonel

_,

Larissa

Grobério

Lopes

Perim

_,

_Tarcísio

_Guimarães

_Silva

_Oliveira

_,

Charbel

Jacob

Júnior

_,

_José

_Lucas

_Batista

_Júnior

_,

_Rafael

_Burgomeister

_Lourenc¸o

a_{HospitalSantaCasadeMisericórdia,Vitória,ES,Brazil} b_{DiagnosticImagingCenter,Vitória,ES,Brazil}

a

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t

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c

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e

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n

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o

Articlehistory:

Received3October2013 Accepted25November2013 Availableonline30December2014

Keywords: Scoliosis Neuromuscular Osteoporosis

a

b

s

t

r

a

c

t

Objective:Toevaluatebonemineraldensityamongpatientswithneuromuscularscoliosis secondarytoquadriplegiccerebralpalsy.

Methods:Thiswasadescriptiveprospectivestudyinwhichbothbonedensitometricand anthropometricdatawereevaluated.Theinclusioncriteriausedwerethatthepatients shouldpresentquadriplegiccerebralpalsy,beconfinedtoawheelchair,bebetween10and 20yearsofageandpresentneuromuscularscoliosis.

Results:Weevaluated31patients(20females)withameanageof14.2years.Theirmean bicepscircumference,calfcircumferenceandbodymassindexwere19.4cm,18.6cmand 16.9kg/m2_{,respectively.Themeanstandarddeviationfrombonedensitometrywas−3.2}

(z-score),whichcharacterizesosteoporosis.

Conclusion:Thereishighincidenceofosteoporosisinpatientswithneuromuscularscoliosis secondarytoquadriplegiccerebralpalsy.

©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.Allrightsreserved.

Avaliac¸ão

da

densidade

mineral

óssea

em

pacientes

portadores

de

escoliose

neuromuscular

secundária

a

paralisia

cerebral

Palavras-chave: Escoliose Neuromuscular Osteoporose

r

e

s

u

m

o

Objetivo:avaliaradensidademineralósseaempacientesportadoresdeescoliose neuro-muscularsecundáriaàparalisiacerebraltetraespástica.

Métodos:estudoprospectivo,descritivo,emqueseavaliaram,alémdadensitometriaóssea, dadosantropométricos.Comocritériodeinclusão,adotamospacientescomparalisia cere-braltetraespástica,cadeirantes,entre10e20anosecomescolioseneuromuscular.

夽

WorkdevelopedatHospitalSantaCasadeMisericórdiadeVitória,ES,Brazil. ∗ _{Correspondingauthor.}

E-mail:jcharbel@gmail.com(C.JacobJúnior).

http://dx.doi.org/10.1016/j.rboe.2014.12.003

rev bras ortop.2015;50(1):68–71

69

Resultados: avaliamos31pacientes,20dosexofeminino,cujamédiadeidadefoide14,2 anos.Amédiadacircunferênciabicipital,dapanturrilhaedoIMCfoide19,4cm,18,6cm e16,9Kg/m2_{,respectivamente.Odesviopadrãomédioencontradonadensitometriaóssea}

foide–3,2(z-score),oquecaracterizaosteoporose.

Conclusão: existeelevadaincidênciadeosteoporoseempacientesportadoresdeescoliose neuromuscularsecundáriaàparalisiacerebraltetraespástica.

©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Todososdireitosreservados.

Introduction

Manyneuromusculardiseasesleadtodevelopmentofspinal

deformities.Amongthese,cerebralpalsyisthemostfrequent: itsincidencemayrangefrom25%to100%ofsuchpatients, dependingonthedegreeofneuromuscularinvolvement.1_Its etiologicaloriginissecondarytoimbalancebetweenthe mus-cle forces in the axial skeleton,2 _{caused by lesions in the} upperandlowermotorneurons.3 _{Scoliosisusuallypresents} aC-shapedformat,inassociationwithpelvicobliquity,and itfrequentlyprogressesevenafterskeletalmaturityhasbeen reached.4

Thus,incasesofseveredeformity,orinthoseinwhich pro-gressionofthecurveisdetected,surgicaltreatmentbecomes necessary,withtheaimsofavoidingprogressionand restor-ingormaintainingthesagittalandcoronalbalanceandthe capacitytosit,therebyleadingtoagreatimprovementofthe patients’qualityoflife.

Inthesecases,despitetheneedtoperformsurgical treat-ment,thecomplicationrateisveryhighandisdirectlyrelated totheimpairmentofcardiorespiratory andgastrointestinal function and the nutritional gradeshown by the patient.5 Amongallthe possiblecomplicationsarising fromsurgery, infectionandlooseningofthesynthesismaterialusedfor cor-rectingthedeformityaretheonesmostfrequentlyobserved.6 Failureoffixationofthepediclescrewsinthespinemay occurduetoosteoporosisofthevertebra,causedbyfactors suchastheseverityoftheneurologicalimpairment, increas-ingdifficultyineatinganduseofanticonvulsants.7

Veryfewstudieshaveanalyzedthebonemassofpatients

with tetraspastic cerebral palsy. Many complications can

result from loosening of the synthesis material in such

patients.Thiscanbepreventedthroughcorrectanalysisof bonemetabolismandearlytreatmentofpatientswhopresent

low bonemass. Weconducted the present study with the

objectiveofanalyzingthebonemassofpatientswith

cere-bralpalsy who also had neuromuscularscoliosis. Through

this,itmightbecomepossibletoadoptappropriate preven-tivemeasuresforavoidingthedevelopmentofosteoporosis andconsequentlytoachieveimprovementoftheirqualityof life.

Sample

and

method

Thiswasaprospectivestudyofdescriptivenatureforwhich datacoveringtheperiodfromFebruary2012toJanuary2013

weregathered.Theinclusioncriteriawerethatthepatients

needed topresent neuromuscular scoliosisdue tocerebral

palsy, with a tetraspastic component, and were using a

wheelchair.Patientsagedlessthan10yearsandover20years andpatientswhosescoliosiswasnotofneuromuscularorigin duetocerebralpalsywereexcluded.

Aconveniencesamplewasused,whichwasformedasthe patientscametotheorthopedicoutpatientclinicofa philan-thropichospitalinVitória.Intotal,31patientswereevaluated (20 females), withamean age of14.2 years.Subsequently,

eachpatient’sbonemasswasdeterminedbymeansofbone

densitometry on the lumbar spine, on the Lunar Prodigy

Advancedensitometer,modelPA+41606,whichproduces

dig-itizeddensitometryscansbymeansofX-rays,fromaspecial constant76kVsourcewithanefficientk-edgedosefilter.The

densitometrywas alsocomputer-assisted,bymeans ofthe

Windows-basedProdigyBissoftware.

The results were represented numerically by means of

absolute values and percentages and were documented in

accordancewithprotocols.Thedataanalysiswasperformed usingthesoftwareMicrosoftOffice/Excel2007®_andGraphPad Prism®_{(SanDiego,CA,USA).}

Inadditiontobonemass,anthropometricdatawere evalu-ated,suchasmeasurementsofestimatedheight,weight,body massindex(BMI), bicepscircumferenceandcalf circumfer-ence.Specificdatasuchaswhetherthepatienthadundergone

gastrostomy, was doing physiotherapy or was using an

adaptedwheelchairwerealsoascertained.Furthermore,

lab-oratory testssuch as hemogram, TSH, freeT4, potassium,

calcium,serum iron,ferritin,transferrin,C-reactiveprotein (CRP),totalproteinsandalbuminwereperformed.

To calculate BMI, the formula used was BMI=W/H2_{, in}

which W=weight and H=estimated height. Theestimated

height was calculated bymeans of the following formula:

H=(2.69×KH)+24.2,inwhichKHwasthedistancefromthe kneetotheheel.8

Results

Among the 31 patients analyzed, 11 were constantly

doing motor physiotherapy. Only 11 were using adapted

wheelchairs; the remaining 20 were using conventional

wheelchairs.

The anthropometric measurements were: weight, 28kg;

70

Table1–Meanvaluesfromlaboratorytests.

Meanvalue Referencerange

Hemoglobin 13.52 12–14g/dL

Hematocrit 39.94 38–42%

Totalproteins 7.21 6.0–8.0g/dL

Albumin 4.42 3.5–5.5g/dL

TSH 2.38 0.350–5.50UI/mL

FreeT4 1.16 0.70–2.0ng/dL

Serumcalcium 8.89 8.4–10.6mg/dL

Potassium 4.26 3.5–5.2mEq/L

Ferritin 34.01 10–140ng/mL

Serumiron 92.15 Men:60–150mcg/dL

Women:40–145mcg/dL

Transferrin 218.19 200–360mg/dL

CRP 5.29 <6mg/L

Table2–Bonedensityanalysis.

Bonedensity Normal Osteopenia Osteoporosis Total

No.ofpatients 1(3.3%) 5(16%) 25(80.7%) 31

Themeanvaluesfromthelaboratorytestswerewithinthe normalranges,asshowninTable1.

On analyzing the bone densitometry results, we found

thatthe mean Z-score inthelumbarspine was−3.2, with

a minimum of−6.0 and a maximum of 2.1. Thus, among

the31patientsanalyzed,25presentedosteoporosis,fivehad osteopeniaandonehadnormaldensity,asshowninTable2. Regardingthesepatients’BMI,wefoundastrong

relation-shipbetweenlowBMIandlowbonemineraldensity,which

wasa statisticallysignificant result(p=0.005, i.e. <0.05),as showninFig.1.Weobservedthatthepatients’degreeof mal-nutritionwasdirectlyrelatedtolowbonemass.

Discussion

Surgicaltreatmentforneuromuscularscoliosisisoften diffi-cultbecauseofthevariouscomplicationsthatarepossibleand becauseoftheconstantneedforamultidisciplinaryteam.9 Therefore,whensurgicaltreatmentisindicated,theutmost cautionisrequiredinordertoavoidthesepossible complica-tions.

Themalnutrition observedamongthesepatients,which

is due to difficulty in eating, use of anticonvulsants and

40.0 30.0

20.0 10.0

0.0 –1

–2

–3

–4

–5

–6

–7 0 1 2 3

BMI

Score

Fig.1–RelationshipbetweenBMIandZ-score.

neurologicalimpairment,mayleadtodiminishedbonemass,

which implies a higher rate of loosening of the

synthe-sismaterial.6_{Inthesecases,newsurgicalinterventionsare} neededinordertodecreasethepseudarthrosisrate.

Althoughthe possibilityoflowbonemassamongthese

patients isalreadyknown,thereisnopreoperativeroutine forassessingit.Wedidnotfindanystudiesintheliterature

thatdiscriminateamongthesepatients’meanbonemineral

density(BMD)values.

ToevaluateBMDanddiagnoseosteoporosisinchildrenand

adolescents, weused the Z-score, which isthe number of

standarddeviationsresultingfromcomparingachild’sBMD

valuewiththemeanBMDvalueofastandardpopulationof

thesamesexandage.Thevaluesareconsideredtobe abnor-mal whenthe Z-score isless than −1. Inthese cases, the thresholdsforosteopeniaandosteoporosisarenotverywell definedorvalidated,butitisconsideredthatchildrenpresent osteoporosiswhentheirZ-scoreislowerthan−2.7

InastudybyHenderson,LinandGreene,whichincluded 139childrenandadolescentswithvaryingseveritiesof

cere-bral palsy, BMDwas evaluated in the proximal femur and

lumbarspine,andthemeanZ-scoreforthelumbarspinewas

−0.92±0.14.10_{However,inthatstudy,aheterogenousgroup} ofpatientswasused,andthefactorthatbestcorrelatedwith

lowBMDwasthecapacitytowalk.Inourstudy,a

homoge-nousgroupinwhichallthepatientswerenon-walkerswas

evaluated,andweonlyusedtheBMDofthelumbarspine.In thismanner,weobservedthattherewasgreaterlossofbone mass.ThemeanZ-scorewas−3.19.

Children with mental deficiencies may present difficul-tiesincommunication,oromotorandposturaldysfunctions, foodintolerancesandalterationsofappetitecausedbytheir

medication, which frequently interferes qualitatively and

quantitatively withnutrientintakeand isreflectedintheir nutritional status.11 _{Most of the studies available present} loweranthropometricindicatorsthanthoseofchildren

with-out deficiencies. They alsoshow that adequate macro and

micronutrient intake is rare, including calcium and iron

intake.12

Sullivanetal.12 _{reportedthatthesechildrenhaveadiet}

consisting ofmilk-baseddrinks and milkproducts, mainly

because the liquid or pasty consistency of these

prod-ucts makes them easier to consume.The low variety and

quantity of nutrients may contribute towards a situation

of malnutrition and consequent spoliation of electrolytes,

thereby comprising the water-electrolyte balance. Another

importantfactorthatmayberelatedtomalnutritionamong thesepatientsischronictreatmentwithcertain anticonvul-sants thatareconsidered tobehepatic enzymeinducers.13 TheseactontheenzymaticactivityoftheP450systemand thus decreasetheavailability ofvitaminDintheorganism

and consequently interfere with calcium and phosphorus

absorption.14_{However,inourstudy,themeanserum} potas-sium,calcium,ironandalbuminvaluesremainedwithinthe limitsofnormality,eventhoughthepatientspresentedlow

bonemass.

rev bras ortop.2015;50(1):68–71

71

patients,which makesthe surgicaltreatmentsafer,with a lowercomplicationrate.

Conclusions

Thereishighincidenceofosteoporosisamongpatientswith neuromuscular scoliosis secondary to tetraspastic cerebral palsy.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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f

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r

e

n

c

e

s

1. OlafssonY,SarasteH,Al-DabbaghZ.Bracetreatmentin

neuromuscularspinedeformity.JPediatrOrthop.

1999;19(3):376–9.

2. EricksonMA,BauleshDM.Pathwaysthatdistinguishsimple

fromcomplexscoliosisrepair.CurrOpinPediatr.

2011;23(3):339–45.

3. WeinsteinSL.Thepediatricspine:principlesandpractice.

2nded.NewYork:LippincottWilliams&Wilkins;2001.

4. DaherMT,CavaliPTM,SantoMAS,RossatoAJ,LehoczkiMA,

LandimE.Correlac¸ãoentreonúmerodeparafusoseo

percentualdecorrec¸ãonotratamentocirúrgicodaescoliose

neuromuscular.Coluna/Columna.2009;8(2):105–9.

5. MulpuriK,PerdiosA,ReillyCW.Evidence-basedmedicine

analysisofallpediclescrewconstructsinadolescent

idiopathicscoliosis.Spine(PhilaPA1976).2007;

32(19Suppl):S109–14.

6.HendersonRC,LarkRK,GurkaMJ,WorleyG,FungEB,

ConawayM,etal.Bonedensityandmetabolisminchildren

andadolescentswithmoderatetoseverecerebralpalsy.

Pediatrics.2002;1101Pt1:e5.

7.CanhãoH,FonsecaJE,QueirozMV.Diagnósticoeterapêutica

daosteoporosenaidadepediátrica.ActaMedPortuguesa.

2004;17:385–90.

8.SouzaKE,SankakoNA,CarvalhoSM,BraccialliLM.

Classificac¸ãodograudecomprometimentomotoredoíndice

demassacorpóreaemcrianc¸ascomparalisiacerebral.Rev

BrasCrescDesenvHum.2011;21(1):11–20.

9.MasterDL,Son-HingJP,Poe-KochertC,ArmstrongDG,

ThompsonGH.Riskfactorsformajorcomplicationsafter

surgeryforneuromuscularscoliosis.Spine(PhilaPA1976).

2011;36(7):564–71.

10.HendersonRC,LinPP,GreeneWB.Bone-mineraldensityin

childrenandadolescentswhohavespasticcerebralpalsy.J

BoneJointSurgAm.1995;77(11):1671–81.

11.FungEB,Samson-FangL,StallingsVA,ConawayM,LiptakG,

HendersonRC,etal.Feedingdysfunctionisassociatedwith

poorgrowthandhealthstatusinchildrenwithcerebralpalsy.

JAmDietAssoc.2002;102(3):361–73.

12.SullivanPB,JuszczakE,LambertBR,RoseM,Ford-AdamsME,

JohnsonA.Impactoffeedingproblemsonnutritionalintake

andgrowth:OxfordFeedingStudyII.DevMedChildNeurol.

2002;44(7):461–7.

13.FarhatG,YamoutB,MikatiMA,DemirjianS,SawayaR,El-Hajj

FuleihanG.Effectofantiepilepticdrugsonbonedensityin

ambulatorypatients.Neurology.2002;14(9):1348–53.

14.GoodmanSB,JiranekW,PetrowE,YaskoAW.Theeffectsof

medicationsonbone.JAmAcadOrthopSurg.