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INTRODUCTION
Thefirstliverresectionwasperformedin1716byBerta
whoremovedpartiallytheliverofatraumapatient(9).Afterthat,
ittookmorethanahundredyearstovonBruns,in1870,to performtheprocedureagaininasoldieroftheFranco-Prussian
war(1).However,thefirstsuccessfulelectiveliverresection,a
leftlobectomyinapatientpresentingwithahepaticmass,was
performed only in 1888 by Langenbuch(9). In 1908, a great
technicaladvancewasimplementedbyPringle,whoestablished the vascular control of the liver by compressing the portal
triad,amaneuversubsequentlynamedafterhim(27).However,
therealbreakthroughinliversurgerywassetbyCOUINAUD in1957,whenheextensivelydescribedtheportalsegmental hepatic anatomy which nowadays provides the rationale for
segment-orientedresections(5).
The aim of the present study is to evaluate our 10-year experiencewithliverresections,mainlytheindications,perioperative featuresandpathologicalfindingsinordertodeterminerisk factors,morbidityandmortalityofhepatectomy.
PATIENTSANDMETHODS
Medicalrecordsofpatientswhounderwentliverresection at the Digestive Surgery Division, “Hospital de Clínicas”, Federal University of Parana, Curitiba, PR, Brazil, between January1994andMarch2003werereviewed.Aprotocolwas createdinordertoobtainthefollowingdata:age,sex,relevant
pastmedicalhistory,includingcirrhosis,chronichepatitisand previousneoplasm,indicationofhepatectomy,intraoperative datasuchastumorlocation,extensionofresection,employment of vascular exclusion, blood transfusion requirements and procedure duration, information related to the pathologist report(tumorsizeandhistologicaltype),anddataregarding postoperative outcome, mainly postoperative complications, mortalityindexandhospitalstay.
OperativeProcedure
Abilateralsubcostalincisionwasemployedinallprocedures, with an upward midline extension whenever necessary. Cholecystectomy, when the gallbladder was present, was performedforrighthepatectomy.Whenevervascularexclusion wasnecessary,itwasperformedasacontinuousocclusionof theportaltriadwithavascularclampforupto60minutesin non-cirrhoticpatientsandupto30minutesincirrhoticpatients. No pre-conditioning occlusion was employed. Parechymal transectionwasperformedbybluntdissectionwithaKellyclamp andligationofvesselsandbileductbranches.Eletrocoagulation wasalsowidelyemployed.Operativebloodtransfusionwas definedasthenumberofpackedredcellsinfusedduringthe operationandintheimmediatepostoperativeperiod.
NomenclatureandSurgeryExtension
The type of resection was classified according to the
anatomicalnomenclatureofCOUINAUD(5).Resectionswere
considered extended when involving five or more segments
LIVERRESECTION:
10-yearexperiencefromasingleinstitution
JulioCezarUili
COELHO
1,2,ChristianoMarloPaggi
CLAUS
2,TiagoNoguchi
MACHUCA
1,
WagnerHerbert
SOBOTTKA
1andCarolinaGomes
GONÇALVES
2ABSTRACT-Background–Liverresectionconstitutesthemaintreatmentofmostliverprimaryneoplasmsandselectedcasesofmetastatic tumors.However,thisprocedureisassociatedwithsignificantmorbidityandmortalityrates.Aim–Toanalyzeourexperiencewithliver resectionsoveraperiodof10yearstodeterminethemorbidity,mortalityandriskfactorsofhepatectomy.Patientsandmethods–Retrospective reviewofmedicalrecordsofpatientswhounderwentliverresectionfromJanuary1994toMarch2003.Results–Eighty-three(41women and42men)patientsunderwentliverresectionduringthestudyperiod,withameanageof52.7years(range13-82years).Metastatic colorectalcarcinomaandhepatocellularcarcinomawerethemainindicationsforhepaticresection,with36and19patients,respectively. Extendedandmajorresectionswereperformedin20.4%and40.9%ofthepatients,respectively.Bloodtransfusionwasneededin38.5% oftheoperations.Overallmorbiditywas44.5%.Life-threateningcomplicationsoccurredin22.8%ofcasesandthemostcommonwere pneumonia,hepaticfailure,intraabdominalcollectionandintraabdominalbleeding.Amongminorcomplications(30%),themostcommon werebiliaryleakageandpleuraleffusion.Sizeofthetumorandbloodtransfusionwereassociatedwithmajorcomplications(P=0.0185 andP=0.0141,respectively).Operativemortalitywas8.4%andriskfactorsrelatedtomortalitywereincreasedageanduseofvascular exclusion(P=0.0395andP=0.0404,respectively).Medianhospitalstaywas6.7days.Conclusion–Liverresectionscanbeperformed withlowmortalityandacceptablemorbidityrates.Bloodtransfusionmaybereducedbyemployingmeticuloustechniqueand,whenever indicated,vascularexclusion.
HEADINGS–Liver,neoplasms,surgery.Neoplasmmetastasis.Carcinoma,hepatocellular.Hepatectomy.Riskfactors.
1DigestiveSurgeryDivision,“HospitaldeClínicas”,FederalUniversityofParanaand2HospitalNossaSenhoradasGraças,Curitiba,PR,Brazil.
(extendedrightlobectomyandextendedlefthepatectomy),majorwhen threeorfoursegmentswereinvolved(rightandlefthepatectomies), and minor when one or two segments were resected or whenever a non-anatomicalresectionwasperformed.
PostoperativeComplicationsandMortality
Complicationsleadingtolife-threateningconditionswereclassified asmajor.Theseincludedmajorpostoperativebleeding,anyorganic failure, intra-abdominal abscess, sepsis and portal vein thrombosis. Complications with no fatal potential were considered minor and includedpleuraleffusion,woundinfection,urinarytractinfectionand atelectasis.Biliaryleakagewasalsoconsideredaminorcomplication sinceitwasself-limitedinthemajorityofcases.
Operativemortalitywasdefinedasanydeathoccurringduringthe
surgicalprocedureorwithinthe30thpostoperativeday.Whendeath
occurredinthesameadmissionofthesurgicalprocedure,itwasdefined ashospitalmortality.
StatisticalAnalysis
Valueswereexpressedasmean±standarddeviation.Inunivariate analysis,quantitativevariableswerecomparedusingtheMann-Whitney testandqualitativevariablesusingFisher’sexacttest.Variablesfound
tobestatisticallysignificantatalevelofP<0.05wereevaluatedfor
amultivariateanalysisusingthestepwiselogisticregressionmodel.
SignificancewasalsodefinedasP<0.05forthisstatisticalmodel.
RESULTS
A total of 83 liver resections were performed during the study period.Forty-onepatientswerewomenand42men.Themeanagewas 52.7years,rangingfrom13to82.In37patients(44.6%)anunderlying chronicdiseasewasdetectedinthepreoperativeevaluation,usually systemic hypertension or diabetes mellitus. Chronic liver disease wasdiagnosedin13patients(15.7%).Theoperationsperformedare summarizedinTable1.
TheindicationsforliverresectionarelistedinTable2.Themostcommon indicationwassecondaryhepaticmalignancy,whichoccurredin41patients (49.3%).Colorectalcarcinomawastheprimarytumorin36ofthesecases. Stomach,gallbladder,kidney,breastandampullaofVaterweretheprimary siteofthetumorinonecaseeach.Primaryhepaticmalignancywasthe indicationforresectionin24patients(28.9%):hepatocellularcarcinoma
in19(22.9%),cholangiocarcinomain4(4.8%),andangiosarcomain1 (1.2%).Ofthepatientswithhepatocellularcarcinoma,sevenhadliver cirrhosisandonechronichepaticdisease.Hepaticresectionwasperformed forbenignconditionsin18patients,3withfocalnodularhyperplasia,3with hematoma,3withfibroticnodule,2withadenoma,2withhemangioma,2 withcyst,1withbiliaryfistula,1withlefthepaticductstenosisassociated withcholangitis,and1withcirrhoticnodule.
Themeanoperativetimewas290minutes,rangingfrom120to630 minutes.Thelongestmeanoperativetime(340minutes)wasobserved inpatientswhounderwentextendedresections.Pringle’smaneuverwas employedin28patients(33.7%).Thirty-twopatients(38.5%)required bloodtransfusion,withameanofthreeunitsofpackedredcells.
Complicationswereobservedin37patients(44.5%)andtheyare showninTable3.Majorcomplicationsoccurredin19patients(22.8%). Pneumoniawasthecommonestmajorcomplication,occurringinseven patients(8.4%).Hepaticinsufficiencydevelopedinsixcases(7.2%)and itwasassociatedwiththehighestmortalityrateofthestudy(50%).In thisgroup,fourpatientsunderwentanextendedresectionandtwoamajor resection.Intrabdominalfluidcollectionwasobservedinsixpatients.In fourofthem,abscessformationwasdiagnosedandsuccessfullytreated witheitheropenorpercutaneousdrainage.Intheremainingtwo,the collectionresolvedspontaneouslywithconservativeapproach.Intrabdominal bleedingoccurredinfivecases(6%).Itwassuccessfullymanagedwith fluidinfusionandbloodtransfusioninthreecases.Intheothertwocases, thepatientsdiedoffailureofmultipleorgansandsystems.
Majorcomplicationratevariedwithindicationandextensionof liverresection.Thesecomplicationsoccurredin2of4patients(50%) whounderwenthepatectomyforcholangiocarcinoma,8of19patients (42.1%) for hepatocellular carcinoma, 7 of 41 patients (17%) for metastaticdisease,and2of18patients(11.1%)forbenignconditions. Majorcomplicationswereobservedin6of17patients(35.2%)whowere subjectedtoextendedresections,9of34(26.4%)tomajorresections, and4of32(12.5%)tominorresections.
Thesizeofthetumorcorrelatedwithmorbidity.Themeansizeof thetumorwas9.42cminpatientswithmajorcomplicationsand6.22 cminpatientswithminorcomplications.
TABLE1-Operativeprocedures
Procedure n
ExtendedResections
Rightlobectomy Leftextendedhepatectomy
Majorresections
Righthepatectomy Lefthepatectomy
Minorresections
Bisegmentectomy Segmentectomy Non-anatomicalresection
17
14
3
34 22 12
32
7 14 11
TABLE2-Indicationsforliverresection
Diagnosis n
Malignanttumors
Metastasis
Hepatocellularcarcinoma Cholangiocarcinoma Angiosarcoma
Benignlesions
Focalnodularhyperplasia Hematoma
Fibroticnodule Adenoma Hemangioma Cyst Biliaryfistula Ductstenosis Cirrhoticnodule
65
41 19 4 1
18
Bloodtransfusionwasneededin13of19patients(68%)withmajor complicationsandonlyin21of83patients(32.8%)withoutmajor complications.Tumorsizecorrelatedwiththerequirementofblood transfusion.Inthegroupofpatientswhoreceivedbloodtransfusion, themeantumorsizewas9.14cm,whereasinthegroupofpatients withouttransfusion,themeansizewasonly5.39cm.
Major complications occurred in 2 of 13 patients (15.3%) with chronichepaticillness,andin16of70patients(22.8%)withnormal liverfunction.
In the univariate analysis, only the size of the tumor and the requirementofbloodtransfusionwereassociatedwithmajorcomplications
(P=0.0185andP=0.0141,respectively).Inmultivariateanalysis,no
statisticalsignificancewasobservedforanyvariable(Table4).
Minorcomplicationswereobservedin25patients(30%).Biliary leakage and pleural effusion were the most common, occurring in 11patientseach(13.2%).Biliaryleakagewasminimalandresolved spontaneouslyinninepatients(10.8%).Intheremainingtwo(2.4%), surgicalreinterventionwasnecessary.Operativetimeandtheextension
ofresectioncorrelatedwithbiliaryleakage(P=0.0343andP=0.193,
respectively).Pleuraleffusionoccurredin17%oftherighthepatectomies andin9%oflefthepatectomies.
The operative mortality occurred in seven patients (8.4%). Hypovolemic shock was the main cause of death, which occurred in one patient during the surgical procedure and in two, during the postoperativeperiod.Twopatientsdiedduetohepaticinsufficiency, oneduetoacutemyocardialinfarctionandoneduetointra-abdominal sepsis.Statisticalanalysisrevealedthatincreasedage(64.71±9.66)
anduseofPringle’smaneuvercorrelatedwithoperativemortality(P
=0.0395andP=0.0404,respectively).Onepatientdiedofhepatic
insufficiencyinthe34thpostoperativeday,accountingforahospital
mortalityof9.6%.Themedianhospitalstaywas6.7days.
DISCUSSION
Despiteimprovementsinchemoembolization,cryosurgeryandother modalitiesoftreatment,liverresectionremainstheprocedureofchoice
inthemanagementofmostprimarylivertumors(25).Livertransplantation
isthebestapproachinselectedcases,mainlyinpatientswithliver
cirrhosisandsmalltumors(12).Hepatectomyisthemainstaytreatment
ofselectedpatientswithmetastaticlivertumors,especiallythosein
whichtheprimarysiteisthelargebowel(3).However,thisprocedure
hasbeenassociatedwithsignificantmorbidityandmortality. Themostcommonindicationofliverresectioninourserieswas metastaticlivertumors,accountingfor49.3%ofcases,followedby primaryhepaticmalignancy,with24%.Theseresultsaresimilarto thoseofarecentlypublishedmulticentricstudyreportingtheoutcomes of2,097patientssubjectedtohepatectomy.Inthisseries,52%ofthe patientsunderwentresectionformetastaticdiseaseand16%forprimary livermalignancy(6).
Liver resection has been associated with high morbidity and
mortality.Thereportedmorbidityhasrangedfrom16.2%to81%(4,
23,30).Thisenormousrangeispartiallyduetotheheterogeneityofthe
published series, with major differences in indication, extension of hepaticresection,percentageofpatientswithcirrhosisanddefinition ofpostoperativecomplication.Ourrateof44.5%isconsideredhigh whencomparedtoothers.However,westressthatameticulousdata reviewwasemployedsothatcomplicationssuchaspleuraleffusion wereconsideredevenwhenthoracocentesisandchesttubedrainage werenotrequired.Fatalcomplicationsoccurredin22.8%ofpatients and,analyzingspecificcomplications,ourratesaresimilartothoseof majorinternationalcenters.Forinstance,intra-abdominalsepsisoccurred in4.8%ofourresections,ascomparedto6.9%and3%inthereports
ofMIYAGAWAetal.(21)andLAIetal.(17),respectively.
Riskfactorsforcomplicationsfollowinghepaticresectionhavebeen
addressedbyothers.NOGUCHIetal.(24)detectedalbumin,glutamic
oxaloacetatetransaminase,serumtotalbilirubin,plasmadisappearance rateofindocyaningreenand75goralglucosetolerancetestasfactors
associatedwithincreasedmorbidity.YAMANAKAetal.(32)reportedage
asariskfactor.MIYAGAWAetal.(21)demonstrated,inamultivariate
analysis,thatoperationduration,extensionofresectionandpreoperative cardiovascular disease correlated with postoperative complication period.Surprisingly,thisauthorobserved,inaunivariatemodel,that a histologically normal liver (except for the tumor) was associated withhighermorbidityrates.Thisfindingwaspossiblyduetothemore extensive liver resections performed in patients without underlying
TABLE3-Postoperativecomplications*
Complications n(%)
Majorcomplications 19(22.8%)
Pneumonia 7(8.4%)
Hepaticinsufficiency 6(7.2%)
Intraabdominalfluidcollection 6(7.2%)
Intraabdominalbleeding 5(6.0%)
Myocardialinfarction 1(1.2%)
Portalveinthrombosis 1(1.2%)
Minorcomplications 25(30%)
Biliaryleakage 11(13.2%)
Pleuraleffusion 11(13.2%)
Atelectasis 2(2.4%)
Urinarytractinfection 2(2.4%)
Woundinfection 2(2.4%)
*Somepatientshadmorethanonecomplication
TABLE 4 -Statistical analysis of variables for postoperative major complications
Variable Pvalueunivariate Pvaluemultivariate
Age 0.1898 NE
Underlyingchronic
disease 1 NE
Chronichepaticdisease 0.7229 NE
Previoussurgery 0.5982 NE
Indication 0.7495 NE
Extentofresection 0.0582 NE
Pringle’smaneuver 0.0952 NE
Operativetime 0.0843 NE
Bloodtransfusion 0.0141 0.4343
Tumorsize 0.0185 0.1860
liverdisease.Inadditiontothisfinding,wealsoobservedthatthesize oftumorandbloodtransfusionwerepredictorsofmajorpostoperative complications.Bloodtransfusionhaslongbeenassociatedwithtumor recurrence(20,23)andalsowithmorbidityandmortality(7,11,14,28).KOOBY
etal.(15)revealedthatperioperativebloodtransfusionisariskfactor
forpooroutcomeafterliverresection.Thegreatesteffectwasinthe perioperativecourse,wherethetransfusionwasanindependentpredictor ofoperativemortality,minorandmajorcomplicationsanddurationof hospitalstay.Thiseffectwasdose-related.Thepreoperativedetection ofpatientsatriskforbleedingisimportantinordertoschedulean
autologoustransfusiontoimproveoutcome(20).Althoughextensionof
liverresectionwasnotapredictorfactorofcomplicationinourstudy,
MIYAGAWAetal.(21)foundthatextensionofresectioncorrelatedwith
postoperativecomplicationinamultivariatemodel.Thisdifferencemay beduetoasmallernumberofpatientsinourstudy.
Liverresectioninpatientswithcirrhosispresentedamortalityrate
of58%by1970.(10)Intheeighties,AsianandWesterncountriesreported
rates of 20%(13, 16). Due to advances in perioperative management,
refinementofsurgicaltechnique,reducedhospitalstayandreduced requirementforintensivecareunitmonitoring,themortalityratesin
theninetiesreachedaplateaunear10%.(22).Our8.4%-rateissimilarto
thoseofothercenters,althoughzero-mortalityratehasbeenreported byafewhighlyspecializedcenters(8,31).
Inourstudy,Pringle’smaneuverandincreasedagewereassociated withmortality.Inanevaluationofextendedliverresections,WEIetal.(34)
demonstratedthatthepresenceofassociateddiseasesandperioperative bloodtransfusionwereriskfactorsformortality.Inthatstudy,Pringle’s
maneuverwasalsoapredictorofmorbidity.However,inaprospective randomized trial, Pringle’s maneuver was associated with less blood lossandbetterpostoperativeliverfunctionwithoutincreasingneither
complicationnormorbidityrates(19,30).Thesedifferentfindingsmaybedue
tolimitedcohort.AgewasalsodescribedasariskfactorbyDIMICKet
al.(6),whofound,inarecentmulticentricstudy,thatlow-volumehospitals
forhepatectomies,patientsolderthan65yearsofage,majorliverresection, primaryhepaticmalignancyasindicationforresectionandseverityof hepaticdysfunctionwereallindependentpredictorsofmortality.
Biliarycomplicationsrepresentanothermajortopicinliversurgery.
Inarecentreport,TANAKAetal.(29)publishedaleakagerateof7.2%,
withasignificantnumberofthepatientswiththiscomplicationrequiring
reintervention.Inaseriesof5.5%ofbiliaryleakage,LAMetal.(18),in
agreementwithBISMUTHetal.(2),concludedthatintraoperativedye
testssignificantlyreducedfistularates.Inourseriestheleakagerate was13.2%.However,leakagewasminimalinmostcases,resolving
spontaneouslyinafewdays.Thus,weagreewithothers(22),thatthe
routineuseofdyetestsisnotjustified,sinceonlyasmallpercentageof patientsneedreintervention.Inaddition,evenwithroutineassessment
ofleakagewiththistest,casesofbiliaryfistulaarestillobserved(18).
Inconclusion,ourfindingsdemonstratethatliverresectioncanbe performedwithlowmortalityandacceptablemorbidityrates.Theimpact ofbloodtransfusiononperioperativeoutcomehighlightstheneedfor advancesincontrolofoperativebloodloss.Bloodtransfusionmaybe reducedbyemployingmeticuloussurgicaltechniqueand,whenever indicated,vascularexclusion.
CoelhoJCU,ClausCMP,MachucaTN,SobottkaWH,GonçalvesCG.Ressecçãohepática:experiênciade10anosdeumaúnicainstituição.ArqGastroenterol 2204;41(4):229-33.
RESUMO-Racional–Aressecçãohepáticaconstituioprincipaltratamentodamaioriadasneoplasiasprimáriasdofígadoedecasosselecionadosdetumores metastáticos.Entretanto,esteprocedimentoestáassociadoataxasexpressivasdemorbidadeemortalidade.Objetivo–Analisaraexperiênciacomhepatectomia emumperíodode10anosparadeterminarosfatoresderisco,amorbidadeeamortalidadedasressecçõeshepáticas.PacienteseMétodos–Revisão retrospectivadosprontuáriosmédicosdospacientesqueforamsubmetidosahepatectomianoperíododejaneirode1994amarçode2003.Resultados–Foi realizadahepatectomiaem83pacientes(41mulherese42homens)duranteoperíododoestudo.Aidademédiadospacientesfoide52,7anos,comvariação de13a82anos.Asprincipaisindicaçõesderessecçãohepáticaforamcarcinomadointestinogrossometastático(36pacientes)ecarcinomahepatocelular (19pacientes).Hepatectomiasampliadasemaioresforamrealizadasem20,4%e40,9%dospacientes,respectivamente.Transfusãosangüíneafoinecessária em38,5%dasoperações.Amorbidadetotalfoi44,5%.Complicaçõescomriscodevidaocorreramem22,8%doscasoseasmaiscomunsforampneumonia, insuficiênciahepática,coleçãointra-abdominalesangramentointra-abdominal.Entreascomplicaçõesmenores(30%),asmaiscomunsforamextravasamento biliarederramepleural.Otamanhodotumoretransfusãosangüíneaforamassociadascomcomplicaçõesmaiores(P=0,0185eP=0,0141,respectivamente). Amortalidadeoperatóriafoide8,4%eosfatoresderiscorelacionadoscomamortalidadeforamidadeavançadaerealizaçãodeexclusãovascular(P=0,0395 eP=0,0404,respectivamente).Operíododeinternaçãomédiofoide6,7dias.Conclusão–Ashepatectomiaspodemserrealizadascombaixamortalidade eaceitávelmorbidade.Transfusãosangüíneapodeserreduzidacomoempregodetécnicameticulosaequandoindicada,aexclusãovascular.
DESCRITORES–Neoplasiashepáticas,cirurgia.Metástaseneoplásica.Carcinomahepatocelular.Hepatectomia.Fatoresderisco.
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