Pulmonary resection for metachronous metastatic gastric cancer diagnosed using multi-detector computed tomography: Report of five cases

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ContentslistsavailableatScienceDirect

International

Journal

of

Surgery

Case

Reports

jo u r n al ho me p a g e :w w w . c a s e r e p o r t s . c o m

Case

Series

Pulmonary

resection

for

metachronous

metastatic

gastric

cancer

diagnosed

using

multi-detector

computed

tomography:

Report

of

ﬁve

cases

Noriyuki

Nishiwaki

a,b

_,

_Hideaki

_Kojima

c

_,

_Mitsuhiro

_Isaka

c

_,

_Etsuro

_Bando

a

_,

Masanori

Terashima

a

_,

_Yasuhisa

_Ohde

c,∗

a_Division_of_Gastric_Surgery,_Shizuoka_Cancer_Center,₁₀₀₇_{Shimonagakubo,}_{Nagaizumi-cho,}_Sunto-gun,_Shizuoka,_411-8777,_Japan

b_Department_of_{Gastroenterological}_Surgery,_Okayama_University_Graduate_School_of_Medicine,_Dentistry_and_{Pharmaceutical}_Sciences,_2-5-1_Shikata-cho,

Kita-ku,Okayama,700-8558,Japan

c_Division_of_Thoracic_Surgery,_Shizuoka_Cancer_Center,₁₀₀₇_{Shimonagakubo,}_{Nagaizumi-cho,}_Sunto-gun,_Shizuoka,_411-8777,_Japan

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received14May2020

Receivedinrevisedform16July2020 Accepted17July2020

Availableonline24July2020

Keywords: Gastriccancer Pulmonarymetastasis Pulmonaryresection

a

b

s

t

r

a

c

t

INTRODUCTION:Aspulmonaryresectionformetastaticgastriccancerhasbeenrarelyreportedon,the

roleofmetastasectomyremainsunclearinsuchsettings.Wereviewedtheclinicopathological

character-isticsandsurgicaloutcomesofpatientswithmetachronouspulmonarymetastasisfromgastriccancer

(MPMGC)diagnosedusingmulti-detectorcomputedtomography(MDCT)whounderwentpulmonary

resection.

PRESENTATIONOFCASE:FromSeptember2002toMay2018,ﬁvepatientsunderwentpulmonaryresection

forMPMGCatShizuokaCancerCenter.Allpatientsreceivedcurativeresectionforinitialgastriccancer.

Threepatientsreceivedadjuvantchemotherapy.Themedianageatpulmonaryresectionwas70years.

Themediandisease-freeintervalbetweeninitialgastrectomyandMPMGCdiagnosiswas41months.

Theﬁrstsiteofrecurrencewasthelunginallpatients.Allpatientswerediagnosedashavingprimary

lungcancerusingMDCTbeforepulmonaryresectionandﬁtthesurgicalindicationforprimarylung

cancer.Lobectomywasperformedinthreepatients,whilewedgeresectionwasperformedintwo.The

medianoverallsurvivalfollowingpulmonaryresectionwas79(range,18–89)months.Twopatients

experiencedrecurrence.Whileoneshowedrecurrenceinthemediastinallymphnode,intheotherit

wasobservedintheremnantlung;thelatterunderwentrepeatedpulmonaryresectionfollowedby

systemicchemotherapy.Fourpatientssurvivedforlongerthan4yearsafterpulmonaryresection.

CONCLUSIONS:OftheﬁvepatientswithMPMGCdiagnosedusingMDCTwhounderwentpulmonary

resection,long-termsurvivalwasachievedafterpulmonaryresectioninfour.Thus,pulmonaryresection

maybeconsideredforthosediagnosedwithlungnodulesaftersurgeryforgastriccancer,andwhoﬁt

thesurgicalindicationforprimarylungcancer.

undertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Abbreviations:MPMGC,metachronouspulmonarymetastasisfromgastric can-cer;MDCT,multi-detectorcomputedtomography;PS,performancestatus;DFI, disease-freeinterval;TTF-1,thyroidtranscriptionfactor-1;CT,computed tomog-raphy.

∗ Correspondingauthor.

E-mailaddresses:nori.nishiwaki@gmail.com(N.Nishiwaki),

looklookword@yahoo.co.jp(H.Kojima),mi.isaka@scchr.jp(M.Isaka),

e.bando@scchr.jp(E.Bando),m.terashima@scchr.jp(M.Terashima),y.ode@scchr.jp

(Y.Ohde).

1. Introduction

Followingcurativeresectionforgastriccancer,themost com-monly observed sites of recurrence are the peritoneum and lymphnodes,whilethemostfrequentlynotedsiteof hematoge-nousrecurrence is theliver, followed by the lungs, brain, and bones[1–4].Althoughthestandardtreatmentformetastatic gas-triccancerissystemicchemotherapy,surgicalresectionforliver metastasisis considereda treatmentoption for select patients according to Japanese gastric cancer treatment guidelines [5]. In our institute, surgical resection is performed for cases with livermetastasisfromgastriccancerasclinicalpractice,withan associated median overall survival time of 49 months and 5-https://doi.org/10.1016/j.ijscr.2020.07.062

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year survival rate of 32% [6]. In contrast, the role of surgical resectionfor pulmonarymetastasisfromgastriccancerremains unclear.

Theuseofpulmonarymetastasectomyhasbeenproposedfor solidtumors,suchassarcomas,adrenalcorticalcarcinomasand gastrointestinalcancers[7–9].Althoughpulmonaryresectionfor metastatic colorectal canceris commonly performedin clinical practice, this is only based on retrospective studies; no ran-domizedcontrolledtrials have focusedonthetopic[9,10]. The in-progressPulmonaryMetastasectomyinColorectalCancertrial [11]istheﬁrstrandomizedcontroltrialtobeconductedinsuch settings.

Pulmonarymetastasisfromgastriccancerisnormally associ-atedwithcarcinomatouslymphangitis,malignantpleuraleffusion, numerous lesions, or concomitant metastatic sites [12,13], whereassolitarypulmonarymetastasisfromgastriccanceroccurs extremelyrarely.Therefore, pulmonary resectionfor metastatic gastriccancerhasbeenrarelyreportedon.Moreover,thesurgical outcomes of this procedure are not satisfactory as per previ-ousreports[14–19],witharecentsystematicreviewshowinga medianoverallsurvivalafterlungresectionof45(range,1–123) months,andamediandisease-freesurvivaldurationof9(range, 3–65)months [14]. However,that reviewwasbasedon single-centerretrospectivereportsofrelativelysmallsamplesizes,and thediagnosticmodalitiesusedforpulmonarymetastasiswerenot describedindetail[14–17].Astheefﬁcacyofmulti-detector com-puted tomography (MDCT) for pulmonary tumor diagnosis has beendemonstrated[20],weuniﬁedthediagnosesofthepresent caseswithmoderndiagnostictechnology.

In this report, we present a review of the clinicopatho-logical characteristics and surgical outcomes of patients with metachronouspulmonarymetastasisfromgastriccancer(MPMGC) diagnosed usingMDCTwho underwent pulmonaryresectionat ShizuokaCancerCenter[21].Further,weevaluatedthesigniﬁcance ofsurgicalresectionforpatientswithpulmonarynodulesfollowing surgeryforgastriccancer.

2. Presentationofcase

From September 2002 to May 2018, five patients under-wentpulmonaryresectionforMPMGCatShizuokaCancerCenter. The collectionand analysis of datain this retrospectivecohort study were approved by theInstitutional Review Board of the Shizuoka Cancer Center (Approval No. 29-J31-30-1-3). Tumor stageand histologicalclassification were determinedaccording tothe3rdEnglisheditionof theJapaneseClassificationof Gas-tric Carcinoma [22] (Table 1). All patients underwent curative resectionfor initialgastric cancer. Theinitial tumor stagewas StageIIorIIIinfourpatients;however,it wasStageIAinone. Thehistologicaltypeofgastric cancerwaspredominantly well-differentiatedadenocarcinoma.Themediandisease-freeinterval (DFI)betweeninitialgastrectomyandpulmonarymetastasis diag-nosiswas41(range,25–56)months.Thefirstsite ofrecurrence wasthe lung in all patients. The medianinterval between ini-tialgastrectomyandpulmonaryresectionwas42(range,29–59) months.

TheclinicalcoursesareshowninFig.1.Threepatientsreceived adjuvant chemotherapy for initial gastric cancer. None of the patientsreceivedchemotherapyforthetreatmentofpulmonary metastasisbeforepulmonaryresection.

Thecharacteristicsofthepulmonarymetastasesareshownin Table2.Themedianageatpulmonaryresectionwas70(range, 59–78)years. The Eastern CooperativeOncology Group perfor-mancestatus(PS)was0inallpatients.Allpatientswerediagnosed usingMDCT;fourwerediagnosedashavingasinglenodule,and

oneashavingtwonodules(Fig.2).Preoperativebiopsyofthe pul-monarynoduleswasperformedintwopatientsbronchoscopically, leadingtothediagnosisofadenocarcinoma;intheotherpatients, biopsywasnotperformedbecauseofthenodulelocation.Asitwas difﬁculttodifferentiatetheMPMGCfromtheprimarylung can-cerhistologicallyandradiologically,allpatientswerediagnosedas havingprimarylungcancerbeforesurgery.

Data onthesurgicalproceduresusedand pathological diag-nosesareshowninTable3.Althoughfrozensectionexaminations wereconductedonspecimens obtainedfromfourpatients dur-ing surgery, only two patients received an MPMGC diagnosis. Lobectomywasperformedinthreepatients,whilewedge resec-tionwasperformedintwo;thosetwo patientsreceivedlimited resectionaccordingtothediagnosisofMPMGCbyfrozensection examination duringsurgery.The mediansurgery time was226 (range,67–305)minutes,andthemedianbleedingamountwas 14(range,0–68)g.Themedianpostoperativestaydurationwas 8 (range,7–20) days,and nopostoperative complications were observed.

The pulmonary nodules were histologically diagnosed as MPMGCwithmorphologicalsimilaritytotheprimarygastric can-cer.Inaddition,immunohistochemistrywasperformedbystaining thyroidtranscriptionfactor-1(TTF-1)fordiagnosisconﬁrmation; allpatientswerenegativeforTTF-1.Onepatienthadlymphnode metastasisatthehilum.Althoughtherewasadivergenceinthe diagnosisofthenumberofnodulesinonepatient,the radiologi-calandpathologicaldiagnoseswerealmostidenticalregardingthe numberofmetastasesandnodulediameters.

The median overall survival duration following pulmonary resectionwas79(range,18–89)months(Table4).Threepatients receivedchemotherapyafterpulmonaryresectionandtheother twodidnotduetopatientpreference.Twopatientsshowed recur-rence.Oneexperiencedrecurrenceinthemediastinallymphnode during systemic chemotherapy following pulmonary resection. Although thepatient continued chemotherapy after recurrence witha regimenchange,hediedduetodiseaseprogression.The otherpatientshowedrecurrenceintheremnantlung,underwent repeatedpulmonaryresectionfollowedbysystemic chemother-apy,and achievedlong-term survival. Oftheﬁve patients, four survivedforlongerthan4yearsfollowingpulmonaryresection.

3. Discussions

Inthisreport,wepresentthecasesofﬁvepatientswho under-wentpulmonaryresectionforMPMGC,demonstratingremarkably bettersurvivalvalues followingresectioncomparedtoprevious reports[14–18].AllpatientsshowedgoodPSandDFIvalues,and the preoperative diagnosis was primary lung cancer across all cases.Threepatientswerepathologicallydiagnosedashavinga singlelesionandachievedlongdisease-freesurvival, whiletwo withmultiplelesionsshowedrecurrenceaftersurgery;onepatient underwentrepeatedresectionandachievedlong-termsurvival.

PulmonaryresectionforMPMGCcouldbethetreatmentoption forselectpatients.Accordingtocurrenttreatmentguidelines,the standard treatment for MPMGC is systemic chemotherapy [5]; however,theassociatedsurvivaloutcomesarenotsatisfactory.The medianOSinpatientswithpulmonarymetastasisis4months,and eveninthosetreatedwithchemotherapy,the5-yearsurvivalrate isonly2–4% [12,23].Pulmonaryresectionfor MPMGChasbeen rarelyreportedonowingtoitslowfrequencyofuse;additionally, ithaspreviouslybeenconsideredfutile[19].Recently,however, severalreportshavedemonstrated long-termsurvivalfollowing pulmonary resectionfor MPMGC [15,24];therefore, pulmonary metastasectomyhasbeenreconsideredasatreatmentoptionin suchsettings.

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Table1

Clinicopathologicalfeaturesoftheﬁvepatients.

Patient Ageat gastrectomy (y) Sex Typeof gastrectomy Residual tumor Pathological stage Histological type DFIfollowing gastrectomy (months) Firstsiteof recurrence Intervalbetween gastrectomyand pulmonaryresection (months)

1 67 Male DG R0 IIA differentiated 41 Lung 42

2 54 Female TG R0 IIA undifferentiated 56 Lung 59

3 63 Male TG R0 IIIA differentiated 27 Lung 30

4 67 Male DG R0 IA differentiated 25 Lung 29

5 74 Male DG R0 IIA differentiated 47 Lung 49

DFI,disease-freeinterval;DG,distalgastrectomy,TG,totalgastrectomy.

Fig.1.Clinicalcoursesoftheﬁvepatients.

Table2

Characteristicsofpulmonarymetastases. Patient Ageat pulmonary resection(y) PS Tumor location Preoperative numberof lesions Preoperative tumorsize (cm) Preoperative clinical diagnosis Biopsy Histological diagnosis

1 70 0 Apicalsegmentofrightupperlobe 1 2.8 Primary>Meta + adenocarcinoma

2 59 0 Apicalsegmentofleftupperlobe 1 1.4 Primary>Meta – –

3 65 0 Apicalsegmentofrightupperlobe 1 1.0 Primary>Meta – –

4 70 0 Apicalsegmentofrightupperlobe

lateralsegmentofrightlowerlobe

2 1.0,0.8 PrimaryorMeta – –

5 78 0 Apicalsegmentofrightupperlobe 1 1.8 PrimaryorMeta + adenocarcinoma

PS,performancestatus.

Fig.2. Multi-detectorcomputedtomographyshowedpulmonarynodules.(a)Inpatient2,thenodulewasfoundattheapicalsegmentoftheleftupperlobeandwas consideredtobeprimarylungcancerratherthanmetachronouspulmonarymetastasisfromgastriccancer(MPMGC).(b)Ontheotherhand,inpatient3,thenodulewas foundattheapicalsegmentoftherightupperlobe,makingitdifﬁculttodifferentiatebetweenMPMGCandprimarylungcancer.

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Table3

Surgicalproceduresandpathologicaldiagnosesoftheﬁvepatients. Patient Surgical proce-dure Frozen section examination Histological diagnosis Pathological maximumtumor size(cm) LNmetastasis

1 Lobectomy+systematicnodaldissection – – 3 4.0 Hilar

2 Lobectomy+systematicnodaldissection + adenocarcinoma 1 1.2 None

3 Lobectomy+systematicnodaldissection + adenocarcinoma 1 2.0 None

4 Wedgeresection + metastaticgastriccancer 2 1.0 None

5 Wedgeresection + metastaticgastriccancer 1 1.7 None

LN,lymphnode.

Table4

Outcomesoftheﬁvepatients.

Patient Patternsof recurrence DFSfollowing pulmonary resection (months) OSfollowing pulmonary resection (months) OSfollowing gastrectomy (months) Status 1 MediastinalLN 6 18 61 Dead 2 Disease-free 79 79 138 Alive 3 Disease-free 89 89 120 Alive 4 Lung 21 79 108 Alive 5 Disease-free 49 49 96 Alive

DFS,disease-freesurvival;OS,overallsurvival;LNlymphnode.

Although previoussystematic reviews were conducted with

theaimofselectingpatientsinwhomlong-termsurvivalcanbe

achievedby pulmonarymetastasectomy,theyfailed to

demon-strate any statistically signiﬁcant prognostic factors [14,15].

However,thosestudiesconsistentlyreportedatrendforbetter sur-vivalincaseswithasinglemetastasisandlongDFI[7,14,15,17]. Thesestudiesmayhavefailedtoshowsigniﬁcantprognostic fac-tors in partdue tothe wide range of study periodsthat were included,andthediagnosticmodalitiesusedforpulmonary metas-tasis.MDCThasgreatersensitivity thanconventionalcomputed tomography (CT) in the detection of small lesions [20]. In the presentreport,alltumorswerediagnosedusingmodern diagnos-tictechnologies,andthediagnoseswerealmostidenticaltothose achievedthroughpathologicalstudy.Ourpatientsachieved bet-tersurvivalvaluesthanthoseinpreviousstudiesaswediagnosed tumorsatanearlystageanddidnotmissthepresenceofsmall duplicatelesionsusingsensitiveMDCT.Althoughnostudyhas pre-viouslydemonstratedadiagnosticmodalityformetastaticgastric cancerorcomparedradiologicalandpathologicaldiagnoses,there isa chancethat smallmultiplemetastases werepresented and missed.Inourstudy,thepatientwithasinglepulmonary metasta-sisdiagnosedusingmoderndiagnostictechnologywhoshoweda longDFIaftersurgeryforgastriccancermaybeconsideredagood candidateformetastasectomy.

It may be reasonable to consider pulmonary resection for patientswithpulmonarynodulesaftersurgeryforgastriccancer who ﬁt thesurgicalindication forprimary lung cancer. Allthe patientsinthisstudywereclinicallydiagnosedwithprimarylung cancerbeforepulmonaryresection;thisisconsistentwithprevious reportsthatstatedthatlungcancerisamongfrequentlypresenting secondarymalignanciesfollowinggastriccancersurgery[25],and thatthelungsarelesscommonlytheinitialsitesofpostoperative gastriccancerrecurrence[26].Nakamuraetal.reporteddifﬁculties intheperformanceofdifferentialhistologicaldiagnosisbetween primarylungcancerandmetastasis;thus,surgicalresectionisthe onlyaccurateevaluationmethod[27].Withregardstothe surgi-calproceduresusedformetastaticgastriccancer,previousstudies failedtoshowtheadvantagesoflobectomyoverlimitedresection [14,15]. Inourstudy,twopatientsunderwentwedgeresection; onesurvivedwithoutrecurrencewhiletheothershowed recur-renceintheremnantlung.Althoughaverysmallnumberofcases

wereincludedinthispresentreport,evenlimitedresectionmay aidintheachievementoflongdisease-freedurationsincaseswith asinglelesion.Theseﬁndingssuggestthatwhenalungtumoris observedaftersurgeryforgastriccancer,itisreasonabletoindicate pulmonaryresectionaccordingtotheprimarylungcancer. Further-more,evenifthetumorisdiagnosedasMPMGCpre-operativelyor duringsurgery,limitedresectionmaybesufﬁcient.

Iidaetal.proposedthatmetastasestothelungandupstream organs,orliver,canberegardedas“semilocal”disease, explain-ingthefavorableoutcomesaftermetastasectomy[28].Therefore, pulmonarymetastasectomystillhasthepotentialtoyieldbetter survivalvaluesaslongasthelung’sdefensesystemis function-ingandiscapableofpreventingtumorcellsfromspreadingtothe downstreamorgans.Aspreviousstudieshavereported,themost commonlyobservedsiteofrecurrenceafterpulmonary metasta-sectomyisthelung,andpatientswithmultiplelesionshaveahigh riskofrecurrence.However,somepatientsachievelong-term sur-vivalafterrepeatmetastasectomy[14,29].Thus,carefulfollow-up usingperiodicCTforearlydetectionisstronglyrecommendedafter pulmonarymetastasectomy,especiallyforpatientswith patholog-icallyprovenmultiplelesions.

Thepresentstudyhasafewlimitations.Itwasaretrospective studyperformedinasingleinstitution;thus,thestudypopulation wasrelativelysmall.Althoughthisstudywasunderpowered,we onlyincludedpatientswhowerediagnosedusingmodern diagnos-tictechnology.Inthefuture,large-scalemulticenterstudiesshould beperformedtoinvestigatepulmonaryresectionforMPMGC diag-nosedusingMDCT.

4. Conclusions

Inthisreport,wepresentedourexperienceswithﬁvepatients in whomMPMGC wasdiagnosed using MDCT andwho under-went pulmonaryresection,and weobserved survival outcomes thatwereremarkablybetterthanthoseinpreviousreports. Pul-monaryresectionmaybeconsideredforpatientsdiagnosedwith pulmonarynodules aftersurgery forgastric cancer,who ﬁt the surgicalindicationsforprimarylungcancer;moreover,inselect patients,suchasthosewithgoodPSandDFIvalues,long-term sur-vivalmaybeachievedevenifthenoduleisdiagnosedasMPMGC post-operatively.

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DeclarationofCompetingInterest

Theauthorshavenoﬁnancialorpersonalcircumstanceswith pharmacistsororganizationsthatcouldinﬂuencetheoriginalityof thismanuscript.

Funding

Thereisnoﬁnancialfundingthatcontributestocollecting, inter-pretingdata,writing,andpublishingthemanuscript.

Ethicalapproval

Thecollectionandanalysisofdatainthisretrospectivecohort studywere approved by the Institutional Review Board of the ShizuokaCancerCenter(ApprovalNo.29-J31-30-1-3).

Consent

Allpatientsprovidedconsentforthepublicationofimages. Authorcontribution

NNand HK wereinvolved in gatheringthepatients’ clinical data.NN,HK,MT,andYOwrotethemanuscript.MIandEB par-ticipatedinthestudydesign.Allauthorsreadandapprovedthe ﬁnalmanuscript.

Registrationofresearchstudies

ResearchregistryUIN:TCTR20200708004. Guarantor

Dr.YasuhisaOhde. Provenanceandpeerreview

Notcommissioned,externallypeer-reviewed. Acknowledgements

Theauthorsacknowledgethefollowingparticipating investiga-torsinthisstudy:HayatoKonno,TetsuyaMizuno,SatoshiKamiya, MakotoHikage,YutakaTanizawa,andHirofumiYasui.Wewould liketothankEditage(www.editage.com)forEnglishlanguage edit-ing.

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