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Toloneetal.BMCSurgery2013,13(Suppl2):S11http://www.biomedcentral.com/1471-2482/13/S2/S11

RESEARCHARTICLEOpenAccessTheimpactofageandoralcalciumandvitaminDsupplements

onpostoperativehypocalcemiaaftertotalthyroidectomy.Aprospectivestudy

SalvatoreTolone*,

RuggieroRoberto,GianmattiadelGenio,LuigiBrusciano,DomenicoParmeggiani,VincenzoAmoroso,GiuseppinaCasalino,

IgnazioVerde,AlfonsoBosco,AntonioDAlessandro,RaffaelePirozzi,GianlucaRossetti,



PaoloLimongelli,LudovicoDocimo

From26thNationalCongressoftheItalianSocietyofGeriatricSurgeryNaples,Italy.19-22June2013

Abstract

Background:Hypocalcemiacausedbytransientordefinitivehypoparathyroidismis

themostfrequentcomplicationaftertotalthyroidectomy(TT).Weaimedtocomparethe

impactofageandtheclinicalusefulnessoforalcalcium



andvitaminDsupplementsonpostoperativehypocalcemiaafterTT,andtodeterminewhichriskfactorsareimportantforhypocalcemiaincidence.

Methods:Two

hundredconsecutivepatientstreatedbyTTwereincludedprospectivelyinthepresentstudy.

AllpatientssupplementedoralcalciumandvitaminDinthepost-operativetime.The

dataconcerningsymptomaticandlaboratoristichypocalcemiawerecollected.Patientswereevaluated



accordingtoage,sex,postoperativeserumcalciumlevels,andpreoperativeserumalkalinephosphatasislevels.

Results:Symptomatichypocalcemiadevelopedonlyin19patients

(9.5%),whereaslaboratoryhypocalcemiadevelopedin36patients(18%).Theriskforpostoperative

hypocalcemiawasincreate20-foldforpatientsolderthan50years.

Conclusions:

Ageissignificantlyassociatedwithpostoperativehypocalcemia.Implementingoralcalcium



andvitaminDaftertotalthyroidectomycanreducetheincidenceofhypocalcemiarelatedtosurgery.

Background

Totalthyroidectomy(TT)

isnowthepreferredoptionforthemanagementofbenignmultinodulargoiter.Postoperative

hypocalcemiaisobservedinuptoonethirdoftotalorcompletionthyroidectomy

patientsandisthemostcommoncomplication,duetoparathyroid



glandinsufficiency,anditcontinuestochallengeevenexperiencedsurgeonssinceitoftenextendsthedurationofhospitalstayandincreasestheneedfor

biochemicaltests[1-5].Surgicaltechniquehasevolvedtopreserveparathyroidfunctionwhereverpossible.

However,

*Correspondence:[email protected],Department

ofSurgery,SecondUniversityofNaples,ViaS.Pansini5,



80131,Naples,Italytransienthypoparathyroidismstilloccursowingtoparathyroidmanipulation,devascularization,venousengorgementorinadvertentremovaloftheparathyroidglandswiththethyroid

specimen.

Hypocalcemiaaftertotalthyroidectomyisusuallytransient,andtheincidence

ofpermanenthypoparathyroidismis3%orlessaccordingtotheexperienceofmost

ofthesurgicalunitsstudied[6-8].Despitebeingself-limitingin



mostpatients,symptomatichypocalcemiaisofparticularconcernbecauseofadelayinitsmanifestationandtheconsequentneedforprolongedpatienthospitalizationor

readmission.Followingtotalthyroidectomy,patientsarecloselyobservedforbleedinginthefirst

24h.Themaindischarge-limitingfactorthereafteristhedevelopmentof

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Toloneetal.BMCSurgery2013,13(Suppl2):S11Page2of6http://www.biomedcentral.com/1471-2482/13/S2/S11

hypocalcaemiaaspatientsnotatriskofhypocalcaemia

maybedischargedonday1followingsurgery.

Thecausesof

hypocalcemiaafterTTaremultifactorial,andsomeofthesefactorsincludeiatrogenicsurgical

traumatotheparathyroidglands,incidentalparathyroidectomy,thenumberof



functioningglandsleftbehind,extentofsurgery,experienceofthesurgeon,hyperthyroidism,retrosternalgoiter,concomitantneckdissection,andthyroidcarcinoma[9,10].Severalauthorshave

attemptedtoidentifyriskfactorsinthedevelopmentofhypocalcemia.Declinesinserum

calcium[7]orintactparathyroidhormone(iPTH)levels[11,12]aftersurgeryhavebeen

suggestedasbeingreliablepredictorsofpostoperativehypocalcemia.Althoughmeasurements



ofserumcalciumoriPTHallowtheidentificationofpatientswhohavenoriskofhypocalcemiaaftertotalthyroidectomy,itisnotalwayseasy

topredictwhichpatientscanbedischargedearlyfromthehospitalorto

identifythoserequiringclosemonitoringofserumcalciumlevelsorthosethatshould

receivecalciumandvitaminDsupplements.Implementationofprotocolsusing



postoperativePTHmeasurementhasbeenshowntofacilitateday1dischargeafterthyroidectomy[13].However,rapidPTHmeasurementisnotreadilyavailableinmany

hospitals.

RoutineoralcalciumandvitaminDsupplementshavebeenproposed

topreventthedevelopmentofsymptomatichypocalcemiaandtoincreasethelikelihoodof

earlyhospitaldischargeafterbilateralsurgicaltreatmentofthethyroid



glandorexplorationoftheparathyroidglands[14,15].VitaminDplaysacriticalroleincalciumhomeostasis[16].Insufficiencyincalciumabsorptiondueto

lowvitaminDconcentrationleadstoanincreaseinparathyroidhormone(PTH)secretion.

IncreasedPTHstimulatesthesynthesisofcalcitriolandtherebyimprovescalciumabsorptionefficiency.

However,eveninpatientswhopracticedapostoperativeimplementationwith



oralcalciumandvitaminD,theriskofpostoperativehypocalcemiccrisisisnotavoided,suggestingaroleforotherriskfactors.Identifyingsomeof

thisriskfactorscanled,inturn,toareductionincostsassociated

withmultiplebloodsamplingsinmonitoringthedevelopmentofhypocalcemiaaswellas

costsassociatedwithprolongedhospitalization.

Theaimsof



thisprospectiveclinicalstudyare:(1)tocomparetheimpactofageandtheclinicalusefulnessoforalcalciumandvitaminDsupplementson

postoperativehypocalcemiaafterTT,and(2)todeterminewhichriskfactorsareimportant

forhypocalcemiaincidence.

Methods

Inthesettingofaprospectivestudy,

200consecutivepatients[44men(22%,meanage45±



14years),156women(78%,meanage43±18years)],undergoingtotal

thyroidectomyintheDivisionofGeneralandBariatricSurgeryatUniversity

ofNaplesS.U.N.betweenMarch2011andFebruary2013,wereenrolled.Allof

thepatientshadnohistoryofpriorthyroidornecksurgery.Patientsrequiring

unilaterallobectomyorsubtotalorcompletionthyroidectomywereexcluded,and



onlypatientsundergoingtotalthyroidectomywereenrolledintothestudy.Allpatientshadnormalrenalfunctionatthetimeofsurgery.Noneofthepatientshadsignsorsymptomsindicating

metabolicbonedisease,andnoneofthepatientswereonmedications,suchas

oralcalcium/vitaminDsupplementation,anti-resorptiveagents,hormonereplacementtherapyforpostmenopausalwomen,

anabolicagents,thiazidetypediuretics,orantiepilepticagents,knownto



affectserumcalciummetabolism.IndicationsforsurgeryarelistedinTable1;eachsubjectprovidedaspecificinformedconsent,beforebeingpartofthe

study.Thestudyplanwasreviewedandapprovedbylocalinstitutionalethicalcommittee.

TheTTprocedureconsistsofa3-to5-cmskinincision1

to1.5cmabovethesternalnotch.Afterdivisionof



theplatysma,thecervicallineaalbaisopenedwithoutdivisionofthestrapmuscles.Thethyroidlobeisdissectedprogressivelyfromthestrapmuscles.After

identificationoftherecurrentlaringeanerveandparathyroidglands,thevascularpediclesof

thethyroidlobeareligatedwiththeHarmonicAce/Focusscalpel(EthiconEndo-SurgeryInc.,

Cincinnati,OH,USA),andthethyroidlobeisremoved[17-20].



Afteracheckforhemostasis,adrainisplacedinthethyroidbed.Thecervicallineaalbaandplatysmaaresuturedwithabsorbablesutures,and

theskinisclosedbyanintracutaneousrunningsuture.

Patientswere

askedtotakeoralcalcium2g/dtakentwice(1gevery12hours)andvitaminD1g/dtakentwice

(0.5gevery12hours)fromthenightofoperation



topost-operativeday14.Intravenouscalciumgluconatewasadministeredifsignificantsymptomatichypocalcemiapersistedaftersurgerydespiteoralsupplementation.

Themedicaland

nursingnoteswerecarefullyexaminedfordocumentationofsymptomsofhypocalcaemia.Thetime

ofadministrationofcalcium,vitaminDanaloguesandintravenousfluidsinrelationto

serumcalciumandhypocalcaemicsymptomswasalsonoted.Serumcalcium,



albumin,creatinine,andalkalinephosphatase

Table1Preoperativediagnosis

DiseaseTOTALN=200Multinodulargoiter168(84%)Carcinoma20

(10%)Basedow12(6%)




levelsweredeterminedthedaybeforesurgery,on

theeveningofsurgery(day0),onthemorningofday1and

thenevery24hoursuntilpatientdischarge.Serumcalciumconcentrationwascorrectedfor

changesinserumalbumin.Serumcalcium,creatinine,albumin,andalkaline



phosphataseweremeasuredusingautomatedassays.Thereferencerangesforserumcalciuminourlaboratorywere8.5to10.5mg/dL.

Allpatients

wereseenintheoutpatientsdepartment2weeksaftersurgery.Thereportedsymptoms

ofhypocalcaemiaandthetreatmentrequiredtocontrolthesesymptomswerenoted.

Postoperativehypocalcemiawasdefinedaseithersymptomaticorlaboratory.



Hypocalcemicsymptomsandsigns,fromperioraltinglingandnumbnesstocarpopedalspasmsandtetany,wereregisteredindetail.Laboratoryhypocalcemiawasdefined

asserumtotalcalciumconcentrationsof<8.0mg/dL,evenifrecordedonlyin

asinglemeasurement.

Statistics

DatawereanalyzedusingSPSS

15.0forWindows(SPSSInc,Chicago,IL).Resultswereexpressed



asmean±SD.ComparisonsofdatausedtheWilcoxonsigned-ranktest,chi-squaretest,andlogisticregressionanalysis.Resultswereconsideredstatisticallysignificantwhen

the2-tailedPvaluewaslessthan0.05.

Results

All

patientsrespectedtheoralsupplementprotocol.Thethyroiddiseasesofthepatientsincluded

inthestudyareshowninTable1.Theoperative



procedureswerealltotalthyroidectomy.Nomajorcomplicationoccurred

(e.g.persistentvocalcordparalysisandhypoparathyroidism,bleedingrequiringreintervention).Incidentalparathyroidectomywas

foundin3patients(1.5%).Themeans(±SD)forserumalbumin,creatinine,calcium

andalkalinephosphataselevelswere3.8±0.09g/dL,

0.8±

0.1mg/dL,8.9±0.2mg/dl,and162±74



U/L,respectively.Thepostoperativeserumcalciumlevelwaslowerthanthepreoperativeserumcalciumlevel(8.9±0.2mg/dLvs8.2±0.9mg/dL,P<0.001).

Symptomatichypocalcemiadevelopedonlyin19patients(9.5%),whereaslaboratoryhypocalcemiadevelopedin

36patients(18%).Hypocalcemicsymptomswereminimalin12patients.Intravenouscalciumwas

administeredto7patientswithseverehypocalcemicsymptoms(Table2).



Regardingtheselattercasesonly,inthesubsequenthystopathologicalanalysisonremovedthyroidtissue,incidentalparathyroidtissueswerefoundinthree.Permanenthypocalcemiadeveloped

innoneofpatients.Hypercalcemiaorothersideeffectsdidnotdevelopin

anyofthepatientsreceivingroutineoralsupplements.

Table2Patients

developinghypocalcemia

HypocalcemiaTotalN=200LaboratoryHypocalcemia



36(18%)SymptomaticHypocalcemia19(9.5%)RequiringE.V.Calcium7(3.5%)

Ageandserumalkalinephosphataselevelsweresignificantlyhigherinpatientswho

developedhypocalcemiathaninothers(56.7±8yearsand242.21±72

U/Lvs

42.1±9yearsand123.21±41U/L,

P<0.001).Postoperativeserumcalciumlevelsweresignificantlylowerin



hypocalcemicpatients(7.3±0.4mg/dLvs8.6±0.3mg/dL,P<0.001).Hospitalstaywassignificantlylongerinhypocalcemicpatients(4±1days,range

2-5days)thanothers(2±

0.5days,range1-3days)

(P<0.001).Infemalepatients,theratioofpostoperativehypocalcemiawasfoundto

besignificantlyhigherwhencomparedtomalepatients(24%vs



8%,P<0.01).Therewasanegativecorrelationbetweenserumcalciumlevelandage(rs-0.501,P<0.001)andfemalegender(rs-0.203,P<0.01)andserumalkalinephosphatase

level(rs-0.498,P<0.001).

Patientageandpreoperativeserumalkalinephosphatase

level,wereindependentsignificantvariablesinthedevelopmentofhypocalcemiaafterthyroidectomy.The

riskforpostoperativehypocalcemiawasincreased20foldforpatientsolder



than50years(oddsratio[OR]20.2;95%confidenceinterval[CI]10.4-58.3).

Discussion

Thepresentstudyshowsthatpost-operativeoral

calciumandvitaminDsupplementscanreducetheincidenceofhypocalcemiaaftertotal

thyroidectomy.Also,weinvestigatedthepredictionvalueofage,preoperativeserumcalciumand

alkalinephosphataseonpostoperativehypocalcemiaaftertotalthyroidectomy.



Wefoundthatagewassignificantlyassociatedwithpostoperativehypocalcemia.Negativecorrelationswereobservedbetweentheserumcalciumlevelandage,andserumalkaline

phosphataselevel.Accordingtoalogisticregressionanalysis,agewasasignificantindependent

variableassociatedwithpostoperativehypocalcemia.

Postoperativehypocalcemiaisoneofthe

mostfrequentcomplicationsafterTT[21].Inseveralstudies,the



incidenceofhypoparathyroidismvariedfrom1.6%toabove50%[7,22].

ThecausesofhypocalcemiaafterTTaremultifactorial,andsomeofthese

causesincludeinjury,devascularization,andunintentionalexcisionofparathyroidglands,thenumberof

functioningglandsleftbehind,theextentofsurgery,theexperienceofthesurgeon,

hyperthyroidism,




retrosternalgoiter,concomitantneckdissection,andthyroidcarcinoma

[22-27].

However,theroleofimplementationoforalcalciumandvitamin

Disnotnew,anditisconsideredaneffectiveapproachtothe

preventionofhypocalcemia.

Infact,thistreatmentpreventeda



significantdecreaseofserumcalciumlevelsaswellasthesubsequentdevelopmentofmajorhypocalcemicsymptomsaftertotalthyroidectomy.Thesymptomsreportedbypatients

wereminimalandonlysevenrequiredintravenouscalciumadministrationafterhispersistentsignificant

hypocalcemiafailedtorespondtoimplementationoforalcalciumandvitaminD.However,

inthiscasehypocalcemicstatuswasprobablyduetothe



accidentalremovalofparathyroidtissueduringsurgery,asshownbyhystologicalanalysis.

Twostudieshaveevaluatedtheefficacyofroutinecalciumsupplements

forthepreventionofhypocalcemiaafterthyroidectomy[28,29].Moore[28]reportedthatonly

4of124patientswhoreceiveddailytreatmentofcalcium(5g)after

bilateralthyroidresectiondevelopedhypocalcemia,and1requiredadministrationof



intravenouscalcium.Basedonempiricalobservations,theprophylacticuseoforalcalciumtoreducetheriskofhypocalcemiccrisisandincreasethelikelihoodof

earlyhospitaldischargewasrecommended.Bellantoneetal

[29]reportedin

aprospectivecontrolstudythatonly3of26patients(11%)receivingoralcalciumsupplement(3g/d)hadsymptomsrelated

tohypocalcemiaaftertotalthyroidectomy,whereas11of27patients



(40%)notreceivingcalciumsupplementhadsymptoms.Thesestudiessuggestthatpostthyroidectomyhypocalcemiacanbeconsiderablypreventedbytheroutineadministrationofcalciumsupplements.The

riskforpostoperativehypocalcemiaforpatientsundergoingTTwashigherthanthatfor

patientswithadvancedage.

Recently,therehasbeenagreatdeal

ofinterestinidentifyingperioperativefactorsthatcanpredictthe



developmentofhypocalcemiaafterthyroidectomy[30,31].Thedrivetowardsashorterhospitalstayfollowingtotalthyroidectomyhasledtoanumberofstudiesevaluating

theuseofplasmabiochemicalmarkerstopredictthedevelopmentofhypocalcaemia.Thyroid

surgeryimpairsPTHsecretionbytheparathyroidglandsresultinginpostoperativeparathyroidinsufficiencyandsubsequent

developmentofhypocalcaemia[32].Themeasurementofserumcalciumconcentration



followingthyroidectomyhasbeenusedinanattempttopredictthedevelopmentofhypocalcaemia.However,themeasurementoftotalserumcalciumisinaccurate,at

leastinpart,owingtopostoperativehaemodilution[33,34].

Thevalueof

PTHinpredictingpost-thyroidectomyhypocalcemiahasbeenextensivelyinvestigatedand

reported

intheliterature[35,36]AlthoughtheuseofPTHpost-thyroidectomy



mayallowshorterhospitaladmission,rapidaccesstoresultsofpostop-erativePTHmeasurementisnotwidelyavailableinmosthospitals.Inaddition,thereis

noconsensusonthethresholdforPTHandtheoptimaltimingforits

measurementpost-thyroidectomy.ThePTHmeasurementonthefirstpostoperativedayhasbeenshown

tobeausefulmethodtopredictpost-thyroidectomyhypocalcemia[37].



SerumPTHconcentration,whenchecked1-6hafterthyroidectomy,hasahigheraccuracyinpredictinghypocalcaemia[38].WhilsttheuseofserumPTHlevels

topredictpost-thyroidectomyhypocalcaemiaiswellestablished,itappearstolackthedesirable

100%accuracyrate.Wewerenotabletoanalysethepostoperativepercentagedecline

inPTHowingtothelackofpreoperativePTHdata.



However,bothabsolutelevelsandpercentagedeclinehavebeenusedtopredicthypocalcaemiawithsimilaraccuracy,and,althoughsimilar,levelsvarybetweeninstitutions[36].

Also,wethinkthatpost-operativehypocalcemiacanbereducedwhena

preciseminimalsurgicaldissectionisperformed;infact,theuseofharmonicscalpel

canhelptoavoidenergyspread,bloodlossandedema,



thuslimitingparathyroidfunctionimpairment[17-20].

VitaminDhasacriticalroleincalciumhomeostasis.VitaminDdeficiencyhasbeenfrequentlydocumented

inmedicallyillandfree-livingpopulations[39,40]Advancedageisreportedtobe

amajorriskfactorforvitaminDdeficiency.Agingisassociatedwithalterations

invitaminDmetabolism.Studieshaveobserved

(1)



anage-relateddecreaseinrenal1-hydroxylaseactivityandintestinalcalciumabsorption,and(2)anage-relateddeclineinthecutaneousaccumulationof7-dehydrocholesterol,which

isconvertedintoprevitamin-D3bysolarultravioletradiation.Insufficientcalciumabsorptiondue

tolowvitaminDconcentrationsleadstoanincreaseinPTHsecretion.Increased

PTHstimulatesthesynthesisofcalcitriolandtherebyimprovescalcium



absorptionefficiency[39,40].Inpreviousstudies,regimensoforalcalciumaloneandofacalciumandvitaminDcombinationwereeffective.Thestudyfrom

BellantoneetAl[29]alsorevealedthattheadditionofvitaminDto

oralcalciumsupplementswasassociatedwithsignificantlyhigherserumcalciumconcentrationsonpost-operative

days2and3andwithalowerincidenceof



hypocalcemia.AlthoughithasbeenreportedthatvitaminDadministrationinhibitsiPTHsecretionbynormallyfunctioningparathyroidglands,priorstudiesandourownresults

showedthatiPTHsecretionwasnotaffectedbyvitaminDadministrationinpostthyroidectomy

patients.Therefore,theearlyuseofvitaminDinadditiontocalciumsupplements

canberecommendedforpatientsundergoing




totalthyroidectomy.Thedosagesanddurationsofcalcium

andvitaminDadministrationarealsoofconcern.InastudyfromRoh

andPark[32],routineoralcalciumandvitaminDsupplementswereeffectivein

reducingtheincidence(6%)andseverityofhypocalcemiaaftertotal



thyroidectomy.Onlyaminorityofpatientsreceivingthesupplementspresentedwithminimalsymptomsrelatedtohypocalcemia,andhigherlevelsofserumcalciumduringthe

firstfewdaysaftertotalthyroidectomyweremeasuredinpatientsreceivingthesupplement.

Inapreviousstudy,wealsodocumentedthatregimensoforalcalciumaloneandofacalciumand

vitaminDcombinationwereeffectiveinmostcasesofthyroidectomy



performedforbenignthyrodealpathology[41-44].

Conclusions

Thepreventionofsignificantsymptomatichypocalcemiawillallowearlydischargeofpostthyroidectomypatients

fromthehospital.Inturn,earlydischargeeliminatesthenecessityofmultipleblood

samplingsforclosemonitoringofserumcalciumoriPTHlevels.However,therisk

ofpostoperativehypocalcemiaforpatientsundergoingTTwashigherthan



thatforpatientswithadvancedage.Inthesepatients,anaccurateclinicalandlaboratoristicfollowupduringthepost-operativeperiodisnecessary.

Inconclusion,ourdatasuggestthatpostoperativeoralcalciumandvitaminDsupplements

cantakearolethepreventionofpostoperativehypocalcemiaandforincreasingthe

likelihoodofasafeandearlydischargefromthehospital.



Listofabbreviations

TT:TotalThyroidectomy;PTH:ParathyroidHormone;iPTH:intactParathyroidHormone

Competinginterests

The

authorsdeclarethattheyhavenocompetinginterests.

Authors contributions

ST,RR,PLhavemadesubstantialcontributionstoconceptionanddesign;RP,

GRhavemadesubstantialcontributionstoacquisitionofdata;GC,



AB,VA,ADAhavemadesubstantialcontributionstoanalysisandinterpretationofdata;ST,RR,IVhavebeeninvolvedindraftingthemanuscript;RR,

PL,GDG,LB,DPhavebeeninvolvedinrevisingitcriticallyforimportant

intellectualcontent;ST,RRandLDhavegivenfinalapprovaloftheversion

tobepublished.

Authors information

ST:



ResearchGrantFellowatSecondUniversityofNaples;RR:AssistantProfessorofSurgeryatSecondUniversityofNaples;GDG:AssistantProfessorofSurgeryatSecondUniversity

ofNaples;LB:SeniorDoctoratSecondUniversityofNaples;DP:AssistantProfessorof

SurgeryatSecondUniversityofNaples;VA:SurgicalFellowResidentatSecondUniversityofNaples;GC:

SurgicalFellowResidentatSecondUniversityofNaples;IV:SeniorDoctoratSecond



UniversityofNaples;AB:SurgicalFellowResidentatSecondUniversityofNaples;ADA:SurgicalFellowResidentatSecondUniversityofNaples;RP:SurgicalFellowResidentatSecondUniversity

ofNaples;GR:SeniorDoctoratSecondUniversityofNaples;PL:AssistantProfessorof

Surgeryat

SecondUniversityofNaples;LD:FullProfessorofSurgeryatSecond

UniversityofNaples.

Declarations

Fundingof



thisarticlehascomefrompersonalfunds.ThisarticlehasbeenpublishedaspartofBMCSurgeryVolume13Supplement2,2013:Proceedingsfrom

the26thNationalCongressoftheItalianSocietyofGeriatricSurgery.Thefull

contentsofthesupplementareavailableonlineathttp://www.biomedcentral.com/bmcsurg/supplements/13/S2

Published:8

October2013

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