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w w w . j c o l . o r g . b r

Journal

of

Coloproctology

Original

Article

Results

of

surgical

treatment

of

colorectal

cancer

in

nonagenarian

patients

Arthur

Manoel

Braga

de

Albuquerque

Gomes

,

Fábio

Lopes

de

Queiroz,

Rodrigo

de

Almeida

Paiva

HospitalFelícioRocho,BeloHorizonte,MG,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received9May2017 Accepted12July2017

Availableonline12August2017

Keywords:

Colorectalcancer Surgery

Nonagenarian Morbidity Mortality

a

b

s

t

r

a

c

t

Purpose:Theobjectiveofthepresentstudywastocomparetheresultsofsurgicaltreatment ofnonagenarianpatientshavingcolorectalcancerwithpatientsyoungerthan90years.

Methods:A total of622patientswho underwent curativesurgery wereincludedin the presentstudy.Thedatabaseofthesurgicalservice,intheperiodfrom2007to2013,was usedtoobtainthesample.Thisisadescriptive,retrospectivestudythatcomparedthe pro-filesof17nonagenarianpatients(GroupI)with605patientsyoungerthan90years(Group II).Thegroupswerecomparedregardingsurgicalcomplications,lengthofhospitalstay,type ofsurgeryperformedandASAclassification.

Results:Themeanagebetweenthegroupswas92.2yearsand61.2years.Themeanlength ofhospitalstayinGroupsIandIIwas17.3daysand8.75days,respectively.Thesurgery performedmostfrequentlywastherightcolectomy,inbothgroups.Themostcommon postoperativecomplicationwassepsis(11.8%)amongthenonagenarians,andparalyticileus (4.5%)amongthoseyoungerthan90years.Laparoscopicsurgerywasperformedon5out ofatotalof17patientsevaluatedinGroupI.Amongthethreemortalitiesregisteredinthis lattergroup,twowereclassifiedasASAIIIandonlyoneasASAI.

Conclusion: Theresultsindicatethatcolorectalsurgerymaybeperformedinthisgroup,with acceptablemorbidityandmortalityrates,inpatientswithlowpreoperativerisk(ASAI/II).

©2017SociedadeBrasileiradeColoproctologia.PublishedbyElsevierEditoraLtda.This isanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/ licenses/by-nc-nd/4.0/).

Resultados

do

tratamento

cirúrgico

do

câncer

colorretal

em

pacientes

nonagenários

Palavras-chave:

Câncercolorretal Cirurgia

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e

s

u

m

o

Finalidade:Oobjetivodopresenteestudofoicompararosresultadosdotratamentocirúrgico depacientesnonagenáriosportadoresdecâncercolorretalversuspacientescommenosde 90anos.

Correspondingauthor.

E-mail:arthurmanoel1@hotmail.com(A.M.Gomes). http://dx.doi.org/10.1016/j.jcol.2017.07.002

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Nonagenário Morbidade Mortalidade

Métodos: Oestudoenvolveu622pacientesqueforamsubmetidosàcirurgiacurativa.Para obtenc¸ãodaamostra,utilizamosobancodedadosdoservic¸odecirurgia,abrangendoo períodode2007-2013.Esteéumestudoretrospectivodescritivoquecomparouosperfisde 17pacientesnonagenários(GrupoI)versus605pacientescommenosde90anos(Grupo II).Osgruposforamcomparadosparacomplicac¸õescirúrgicas,durac¸ãodapermanênciano hospital,tipodecirurgiarealizadaeclassificac¸ãoASA.

Resultados: AmédiadeidadeparaosGruposIeIIfoi,respectivamente,92,2e61,2anos. Adurac¸ãomédiadepermanêncianohospitalnosGruposIeIIfoi,respectivamente,17,3 diase8,75dias.Acirurgiamaisfrequentementerealizadafoicolectomiadireita,nosdois grupos.Acomplicac¸ãopós-operatóriamaiscomumfoisepse(11,8%)entreosnonagenários, eíleoparalítico(4.5%)entreospacientescommenosde90anos.Cirurgialaparoscópicafoi realizadaem5pacientes,emumtotalde17pacientesavaliadosnoGrupoI.Considerando astrêsmortalidadesregistradasnesseúltimogrupo,duasforamclassificadascomoASAIII eapenasumacomoASAI.

Conclusão: Osresultadosobtidosindicamque,nessegrupo,acirurgiacolorretaléopc¸ão válida,compercentuaisaceitáveisdemorbidadeemortalidade,empacientescombaixo riscopré-operatório(ASAI/II).

©2017SociedadeBrasileiradeColoproctologia.PublicadoporElsevierEditoraLtda.Este ´eumartigoOpenAccesssobumalicenc¸aCCBY-NC-ND(http://creativecommons.org/ licenses/by-nc-nd/4.0/).

Introduction

Colorectalcancer(CRC)ismoreprevalentinpeopleaged65 ormoreanditsincidenceincreaseswithage.Consideringthe increaseinlifeexpectancyofthepopulation,accordingtodata providedbytheWorldHealthOrganization,thediagnosisof CRCintheelderlyhasincreasedconcomitantly.Alower physi-ologicalreservetoaddresshomeostasisimbalances,whether incardiovascular,metabolicorrespiratoryareas,associated withamuchgreatercoexistenceofcomorbidities,makesthis agegroupmoresubjecttocomplications.Thus,thebenefitof surgeryandanesthesiamustbecarefullyevaluated,aswell as the prognosis and survivalrates. Cancerin this elderly populationisanethicaldilemma forsurgeonsand oncolo-gistsregardingthedecisionabouttheaggressivenessofthe treatment,balancingthebenefitofsurgeryandtheincrease ofassociatedrisks,inanagegroupwithshortexpectancyof survival.1

Therearefewavailablestudiesonthepostoperativeresults ofsurgicaltreatmentofcolorectalcancerinpatientsover90 yearsormore,bothofthelaparoscopicandtheconventional procedures.2

Ingeneral,therandomizedtrials,inthemedicalliterature, haveshownthatlaparoscopiccolorectalresectionforcancer hadsurvivalandrecurrenceratessimilartothoseshownin openresectionsurgery,butwithareductioninhospitalstay, postoperativepainandmorbidity.3

Theobjective of the present study wasto compare the resultsofsurgicaltreatmentinnonagenarianpatientswith colorectal cancer,with patients of less than 90 years. The little evidence available in the literature on the subject, associated with the fact that there is a predominance of articleswithsmall samples, confirmsthe relevanceofthis study.

Materials

and

methods

Thisisaretrospectiveanddescriptivestudy,with622patients with colorectal cancer, undergoing curative surgery in the periodfrom2007to2013.Theservicedatabasewasusedto obtainthesamplewhichcomparedtheprofileof17 nonage-narianpatients(GroupI)with605patientslessthan90years ofage(GroupII).Thegroupswereanalyzedastothe occur-renceofpostoperativecomplications,lengthofhospitalstay, thetypeofsurgeryperformedandtheASAclassification.The Clavien-Dindoclassificationwasalsousedtocategorize com-plicationsthatoccurred.

Thosewithoutindicationforemergencysurgery,withno history ofrecurrentcolorectal cancer,withnofixed, palpa-ble mass and without involvement of adjacent structures were consideredsuitable forthe laparoscopicapproach. All surgeonsinvolvedhadperformed20ormorecolorectal laparo-scopicsurgeriesandhadthenecessaryknowledgeregarding theprinciplesofcancersurgery.

StatisticalanalysiswasperformedusingStata(version9.1) and SPSS (version 20.0). Thelevel ofsignificancewas0.05. Thestatisticaltestsusedwere theasymptoticPearson Chi-square,tocomparegenderbetweenthegroups,andthetests ofproportionsforpostoperativecomplicationsandtypesof surgicaltechniques.TheMann–Whitneytestwasusedto com-parelengthofhospitalstay,andtheexactPearsonChi-square testwasusedtocompareASA.

Results

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Table1–Levelofsignificanceaccordingtosex distribution.

Gender <90years

n(%)

>90years

n(%)

p-valuea

Female 314(51.8) 10(58.8) 0.568

Male 291(48.2) 7(41.2)

Total 605 17

a AsymptoticPearsonChi-squaredtest.

Table2–Age(years).

<90years >90years

Mean±SD 62.1±13.2 92.2±1.9

Median(Q1;Q3) 62.0(53.0;72.5) 92.0(91.0;93.5)

Table3–Lengthofhospitalstay(days).

<90years >90years p-valuea

Mean±SD 8.8±10.6 16.7±14.7 0.001

Median(Q1;Q3) 6.0(5.0;9.0) 9.0(7.0;27.0)

a Mann–Whitneytest.

theyoungestpatientwas20yearsoldandtheoldestwas89 (Table2).

ThemeanlengthsofhospitalstayinGroupIandinGroup II, considering only patients who received discharge, were 17.3daysand 8.75days, respectively.OnepatientinGroup I was admitted for 56 days due to several complications, suchasAMI,woundinfection,andbronchospasmcrises.The patient with the shortest hospital stay in this group was

6days (Table3). Comparing the same variable only inthe

nonagenariangroup,amongthoseundergoing laparoscopic orconventional procedures,demonstrated ashorter hospi-talstayinthosewithminimallyinvasiveaccess(5patients, 13days)inrelationtothosewithopensurgery(19.5days,12 patients),butwithp>0.05(Table4).

Table4–Lengthofhospitalstaybetweenopensurgery andlaparoscopyinGroupI.

GroupI Conventional

method

Laparascopic method

p-valuea

Time(days)/ patients

19.5d/12p 13d/5p 0.599

Median(Q1;Q3) 9.5(7.0;28.3) 7.5(6.0;22.5) Mean±SD 16.50±16.55 12.00±10.10

a Mann–Whitneytest.

GroupIhadcomplicationsin36.2%ofthecases,withthree mortalities,whileGroupIIhadcomplicationsin36.3%ofthe sample.SepsiswasthemostprevalentcomplicationinGroup I(2cases);onewasofpulmonaryetiologyandtheotherdue toananastomoticfistula.Inthelatter,therewasnoevidence ofeventssuchasparalyticileus,SRISandneurogenic blad-der.InGroupII,paralyticileuswasmoreprevalent(27cases). Evaluatingstatisticalsignificance,theonlyvariablethat pre-sentedp<0.05wastheurinarytractinfection(5.9%and0.4%,

p=0.001)(Table5).

Nostatisticaldifferencewasfoundwhenthemostsevere complicationssuchassepsis,anastomotic fistulaand peri-tonitiswereanalyzedseparately.However,whenthesewere puttogetherforbetween-groupscomparison(Clavien-Dindo IIIandIV),adifferenceofp<0.05wasfound,denoting pre-dominanceoftheseadversitiesinGroupI(Table6).

Regarding theASAclassification,therewas asignificant differenceatthe0.05level.Thegroupover90hasmoreASAIII andIVthanthegroupyoungerthan90.Amongthe17patients inGroupI,fourwereASAI,sevenASAII,fiveASAIIIandone ASAIV.Examiningtherateofcomplications,onlythose iden-tifiedasASAIIIappearedmorefrequentlyinGroupIthanin GroupII,withp<0.05(Tables7and8).

Regardingtypeofsurgery,therightcolectomywasthemost frequently performed procedure in both groups (p=0.069), followed by left colectomy (p=0.833) and total mesorectal

Table5–Postoperativecomplications.

Complications <90years

n(%)

>90years

n(%)

p-valuea Clavien-Dindob

Paralyticileus 27(4.5) 0(0.0) –

Sepsis 25(4.1) 2(11.8)*** 0.128 IVA

Wallabscess 17(2.8) 1(5.9) 0.456 IIIA

Anastomoticfistula 14(2.3) 1(5.9) 0.346 IVA

SRIS 10(1.7) 0(0.0) –

Peritonitis 8(1.3) 1(5.9) 0.120 IVA

Neurogenicbladder 7(1.1) 0(0.0) –

Pneumonia 6(1.0) 1(5.9) 0.061 IVA

AMI 0(0.0) 1(5.9) – IVB

Ileostomyobstruction 0(0.0) 1(5.9) – IIIA

Hypertensivecrisis 1(0.2) 1(5.9) –

UTI 2(0.4) 1(5.9) 0.001

Others 61(10.1) 0(0.0) –

Presentedcomplications 220(36.3) 7(35.2) 0.926

SIRS,systemicinflammatoryresponsesyndrome;AMI,acutemyocardialinfarction;UTI,urinarytractinfection. a Z-testforcomparisonofproportions.

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Table6–Criticalcomplications,accordingto Clavien-Dindoclassification.

Clavien-Dindo GroupI GroupII p-valuea

III 2/17(11.76) 17/605(2.81) 0.0344

IV 6/17(35.29) 53/605(8.76) 0.0002

a Z-testforcomparisonofproportions.

Table7–ASAclassification.

<90years

n(%)

≥90years

n(%)

p-valuea

I 290(47.9)* 4(23.5)* 0.013

II 259(42.8) 7(41.2)

III 51(8.4)* 5(29.4)*

IV 5(0.8)* 1(5.9)*

a ExactPearsonChi-squaredtest.

Table8–Comparisonoftheindexofcomplications accordingtoASAclassification.

Indexofcomplications <90years >90years p-valuea

ASAI 74/605(12.23) 1/17(5.88) 0.428

ASAII 73/605(12.07) 2/17(11.76) 0.969 ASAIII 14/605(2.31) 3/17(17.65) 0.0001

ASAIV 3/605(0.50) 0(0.00) –

a Z-testforcomparisonofproportions.

Table9–Typeofsurgicaltechniqueperformed.

<90years

n(%)

>90years

n(%)

p-valuea

Rightcolectomy 165(27.1) 8(47.1) 0.069 Leftcolectomy 83(13.5) 2(11.8) 0.833

Totalcolectomy 34(5.4) 0(0.0) –

Partialcolectomy 2(0.3) 0(0.0) –

Totalexcisionofthe mesorectum

106(17.3) 1(5.9) 0.215

Upperanterior resection

84(13.7) 1(5.9) 0.352

Loweranterior resection

14(2.1) 0(0.0) –

Anteriorresection withstapler

43(7.1) 1(5.9) 0.847

Abdominoperineal amputation

32(5.3) 0(0.0) –

Coloanal anastomosis

11(1.8) 0(0.0) –

Ileostomy 3(0.5) 0(0.0) –

Endoanallowering 3(0.5) 0(0.0) –

Others 25(4.1) 4(23.5)b 0.0002

a Z-testforcomparisonofproportions.

b ThreeHartmannsurgeriesandarectosigmoidectomy.

excision (p=0.215). In Group I, 5 of the 17 nonagenarians underwent laparoscopy. There was statistical significance forbothHartmannandrectosigmoidectomysurgeries(23.5% and4.1%,p=0.0002),analyzingGroupsIandII,respectively (Table9).

Discussion

Elderly patientsclearlyhavea higherprevalenceof comor-bidities.Theriskinherentinsurgeryisdirectlyrelatedtothe numberofconcurrentdiseasesandtothepatient’s physiolog-icalreserve.2Thefactthatcolorectalcanceristhethirdmost

diagnosedintheworld,associatedwiththeagingtrendofthe population,leadstotheincreasinglyfrequentdiagnosisofthis disease.4

In a randomized, prospective study, the applicability of laparoscopic colorectalsurgery wasevaluated in16 elderly patients, with 9being 90 years or older and 7between 80 and89years.Inthistrial,therewerenostatistically signifi-cantdifferencesastotheanesthetic-surgicalrisk(ASAscore), postoperative morbidity,surgical time,blood lossand time requiredtoresumeoralintake.Therewasnoneedfor conver-siontoopensurgeryandnopatientdiedaftertheintervention. Allpostoperativecomplicationsweretreatedbyconservative methods,includingananastomoticfistulaintheoctogenarian group.2

In our study, 5 ofthe 17 nonagenarian patients under-wentthelaparoscopicapproachwithnoneedforconversion. Moreover,astherewerenostatisticallysignificantdifferences regarding most complications when evaluated separately, postoperative morbidity might notbe aparameter to con-traindicatesurgeryintheover-90population.However,itis worthrememberingthatintheanalysisofthewhole,ofthe mostseverecomplicationswithrespecttotheClavien-Dindo classification,GroupIprevailedwithp<0.05.

Inaretrospectivestudy,289patientsbetween80and 95 years were evaluated. 150 patients underwent the laparo-scopic approach and 139 underwent open surgery, with colorectalcancerasthemostcommonindication.Thegroup thatunderwentopensurgeryshowedthegreaternumberof mortalities,longerhospitalstays,higherincidenceofparalytic ileusandincreasedmorbidity,withallthosevariables show-ingp<0.05.Thesedatasuggestthatlaparoscopiccolectomy maybeapreferableoptionfortheelderly,includingpatients over90.5,6

SimilarresultswerepublishedbyChaudharyetal., high-lighting thefactthatthelaparoscopicapproachshouldnot becontraindicatedforcolorectalcancerpatientsbasedonly onage,and thatelectivesurgeryintheelderlyissafewith acceptableratesofmorbidityandmortality.3,7,8

Another retrospective series, examined short-and long-term results in44 nonagenarianpatients havingcolorectal cancer whounderwent electiveor emergencysurgery.This series, in agreement with the present study, shows that femalesprevailedwith10/17cases.Thisresult,however,was withoutstatisticalsignificance(p=0.568).Thepredominance (48/74)wasattributedtothegreaterlifeexpectancyamong women.

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rateforelectivesurgeries(12%vs17.6%)werelowerthanin thepresentstudy.1Inthelatter,onepatientfromGroupIwas

admittedfor56daysduetovariouspostoperative complica-tions.

Consequently,tothedetrimentofstatisticallysignificant evidenceastothegreaterlengthofhospitalstayinthe nona-genariangroup,suchhospitalstaywasnotaccompaniedbya higherrateofcomplications.Thissuggests,therefore,thatthis variablecannotbeadoptedasaparameterthat contraindi-catesthesurgicalapproachinthispopulation,asreportedby Roscioetal.9,10

Also in this context, due to the trend toward shorter hospitalstaysamongthoseundergoinglaparoscopy,the nona-genariangroupisrelatedtolowerhospitalcostscomparedto thosewithinthesame age rangeundergoingopensurgery, accordingtothereportofBottinoetal.11

Moreover,ofthethreemortalitiesreportedinGroupI,two wereclassifiedasASAIIIandonlyonewasclassifiedasASAI. Itisworthnotingthat,comparingtheprevalenceof complica-tionsaccordingtoASAclassification,therewaspredominance onlyamongASAIIIpatientsinGroupI.Therefore, consider-ingthefactthatthegreaternumberofASAIIIandIVpatients inGroupIwasstatisticallysignificant,thismakesASAa rea-sonabledeviceforpredictingtheresultsandevaluatingthe applicabilityornotofsurgicalinterventioninthesepatients. ThisissimilartotheresultsdescribedbyJeongetal.12Inthis

latterstudy,aninterestingaccountwasgivenofthe laparo-scopicpostoperativesuccessofa102-year-oldpatient with colorectalcancer.

Another descriptive, retrospective study, that compared the profile of 52 octogenarian patients (Group I) with 386 patientsyoungerthan80years(GroupII),from2007to2011, foundanaveragelengthofhospitalstayequalto9.3daysand arateofpostoperativecomplicationsof28.84%inthegroupof octogenarians.4Thus,accordingtothesedata,itwasobserved

that nonagenarianshave a hospital stay (17.3 days)and a postoperativecomplicationrate(36.2%)higherthan octoge-narians. Theright colectomy was also the most prevalent surgeryandsepsisthemostcommonpostoperative complica-tioninthegroupdescribed,aswiththenonagenariansample evaluatedhere.

Regardingcolorectalcancer,theincreasedagewas associ-atedwithdecreasedspecificsurvivalandthisdifferencewas relatedtoadecreaseintheuseofradicalsurgery.However, studies haveshown that the5-year survivalrate hasbeen equalamongbothelderlyandyoungpatientswhenthe appro-priatesurgicaltreatmentisperformed.So,wheneverpossible, surgeryshouldbeofferedasthefirsttreatmentofchoiceto elderlypatientswithcolorectalcancer.13

The non-randomized and retrospective nature of the presentstudywereconsideredlimitingfactorsofthiswork, openingthepossibility forbiasintheselectionofpatients between the two groups. The data analyzed showed that nonagenarian patients present no greater rate of compli-cation,whencompared withyoungerpatients. Thisshows that advanced age, in and of itself, should not be a rea-son to contraindicate surgery for the elderly, unless their

clinicalconditionandphysiologicalparametersdonotpermit largeresections.However,theyspendmoretimehospitalized, resultinginhigherhospitalcosts.Allresultsindicatethat colo-rectalsurgerycanbeperformedinthisgroupwithacceptable rates ofmorbidity and mortalityin patients withlow pre-operativerisk(ASAI/II).Theclinicallysignificantadvantages of laparoscopic surgery, according to the evidence already largely consolidated in the literature, havesocial and eco-nomicimplicationsinanagingsociety,justifyingthereturn ofthesepatientstoaproductivelifeinatimelymanner.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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1.ArenalJ,TinocoC,LabargaF,MartínezR,GonzaloM. Colorectalcancerinnonagenarians.ColorectalDis. 2012;14:44–7.

2.SomaT,SuganoM,KawasakiC,TsujiM,FukuiI.Colorectal resectioninnonagenarians:effectivenessoflaparoscopic surgery.AsianJEndoscSurg.2014;7:222–6.

3.ChaudharyB,ShabbirJ,GriffithJ,ParvaizA,GreensladeG, DixonA.Short-termoutcomefollowingelectivelaparoscopic colorectalresectioninoctogenariansenonagenarians. ColorectalDis.2012;14:727–30.

4.OliveiraFH,LacerdaFilhoA,QueirozFL,LaumonierPCC, CastilhoBA,RabeloFEF,etal.Feasibilityofsurgicaltreatment ofoctogenarianspatientswithcolorectalcancer.J

Coloproctol.2013;33:131–4.

5.ArveuxI,BoutronMC,ElMriniT,ArveuxP,LiabeufA, PfitzenmeyerP,etal.Coloncancerintheelderly:evidencefor majorimprovementsinhealthcareandsurvival.BrJCancer. 1997;76:963–7.

6.KurianA,SuryadevaraS,VaughnD,ZebleyD,HofmannM, KimS,etal.Laparoscopiccolectomyinoctogenariansand nonagenarians:apreferableoptiontoopensurgery?JSurg Educ.2010;67:161–6.

7.MutchM.Laparoscopiccolectomyintheelderly:whenistoo old?ClinColonRectalSurg.2006;19:33–9.

8.HoblerK.Colonsurgeryforcancerintheveryelderly.Cost and3-yearsurvival.AnnSurg.1986;203:129–31.

9.XieM,QinH,LuoQ,HeX,LanP,LianL.Laparoscopic colorectalresectioninoctogenarianpatients:isitsafe?A systematicreviewandmeta-analysis.Medicine(Baltimore). 2015;94:e1765.

10.RoscioF,BertoglioC,DeLucaA,FrigerioA,GalliF,Scandroglio I.Outcomesoflaparoscopicsurgeryforcolorectalcancerin elderlypatients.JSLS.2011;15:315–21.

11.BottinoV,EspositoMG,MottolaA,MarteG,DiMaioV,Sciascia V,etal.Earlyoutcomesofcolonlaparoscopicresectioninthe elderlypatientscomparedwiththeyounger.BMCSurg. 2012;12Suppl.1:s8.

12.JeongD,HurH,MinB,BaikS,KimN.Safetyandfeasibilityof alaparoscopiccolorectalcancerresectioninelderlypatients. AnnColoproctol.2013;29:22–7.

Imagem

Table 5 – Postoperative complications.
Table 9 – Type of surgical technique performed.

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