Tobacco smoking and intestinal metaplasia: Systematic review and meta-analysis identified

ContentslistsavailableatScienceDirect

Digestive

and

Liver

Disease

j o ur n a l ho me p a g e :w w w . e l s e v i e r . c o m / l o c a t e / d l d

Oncology

Tobacco

smoking

and

intestinal

metaplasia:

Systematic

review

and

meta-analysis

Samantha

Morais

_,

_Sandra

_Rodrigues

_,

_Liliana

_Amorim

_,

Bárbara

Peleteiro

_,

_Nuno

_Lunet

a_{EPIUnit–InstituteofPublicHealth,UniversityofPorto,Porto,Portugal}

b_{DepartmentofClinicalEpidemiology,PredictiveMedicineandPublicHealthoftheUniversityofPortoMedicalSchool,Porto,Portugal}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received27May2014

Accepted2August2014

Availableonline5September2014

Keywords: Meta-analysis Precancerousconditions Smoking Stomachneoplasms

a

b

s

t

r

a

c

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Background:Theevaluationofspecificriskfactorsforearlyendpointsinthegastriccarcinogenesis path-waymayfurthercontributetotheunderstandingofgastriccanceraetiology.

Aims:Toquantifytherelationbetweensmokingandintestinalmetaplasiathroughsystematicreview andmeta-analysis.

Methods:Articlesprovidingdataontheassociationbetweensmokingandintestinalmetaplasiawere identifiedinPubMed®_,Scopus®_{andWebofScience}TM_{,searcheduntilApril2014,andthroughbackward} citationtracking.Summaryoddsratioestimatesand95%confidenceintervalswerecomputedusingthe DerSimonianandLairdmethod.HeterogeneitywasquantitativelyassessedusingtheI2_statistic. Results: A total of 32 articles wereincluded in this systematic review and 19 provided data for meta-analysis.Smokingwas definedasevervs.never(crudeestimates,sixstudies,summaryodds ratio=1.54,95%confidenceinterval:1.12–2.12,I2_{=67.4%;adjustedestimates,sevenstudies,summary} oddsratio=1.26,95%confidenceinterval:0.98–1.61,I2_{=65.0%)andcurrentvs.non-smokers(crude} esti-mates,sevenstudies,summaryoddsratio=1.27,95%confidenceinterval:0.88–1.84,I2_{=73.4%;adjusted} estimates,twostudies,summaryoddsratio1.49,95%confidenceinterval:0.99–2.25,I2_=0.0%). Conclusion:Theweakandnon-statisticallysignificantassociationfoundthroughmeta-analysisofthe availableevidencedoesnotconfirmsmokingasanindependentriskfactorforintestinalmetaplasia.

©2014EditriceGastroenterologicaItalianaS.r.l.PublishedbyElsevierLtd.Allrightsreserved.

1. Introduction

Gastriccanceristhefifthmostcommonmalignancyintheworld and thethird leading cause of cancermortalityworldwide [1]. Incidenceandmortalityrateshavebeendiminishingfor several decades[2,3],mostlyduetothedecreaseinthefrequencyof can-cersofthe“intestinal”histologicaltype[4,5],whichaccountfor approximatelyuptothree-quartersofthetotal[4,6–9].However, recenttrendsshowthatinsomecountriesthedeclinesare becom-inglessmarked[3].

Itiswidelyacceptedthatintestinaltypegastriccarcinomasare precededbyatrophicgastritis,intestinalmetaplasia(IM),and dys-plasia,followingasetofsequentialsteps,knownasCorrea’scascade

∗ Correspondingauthorat:DepartamentodeEpidemiologiaClínica,Medicina

PreditivaeSaúdePública,FaculdadedeMedicinadaUniversidadedoPorto,Al.Prof.

HernâniMonteiro,4200-319Porto,Portugal.Tel.:+351225513652.

E-mailaddress:nlunet@med.up.pt(N.Lunet).

[10].AlthoughHelicobacterpyloriinfectionplaysanessentialrole inthisprocess,otherenvironmentalexposuresareneededforthe progressiontowardscancer[11].Theevaluationofspecificrisk fac-torsforearlyendpointsinthegastriccarcinogenesispathwaymay furthercontributetotheunderstandingofgastriccancer aetiol-ogy.

Gastric cancer is now considered a tobacco-related cancer [12,13];currentsmokerswereestimatedtohaveahigherriskof gastriccancerwhencomparedtoneversmokers(summary rela-tiveriskestimates:1.62inmenand1.20inwomen)[14,15].The associationsarelowerwhencomparingformerandneversmokers (summaryrelativeriskestimates:1.34inmenand1.16inwomen) suggestingsmokingcessationleadstoareductioninrisk[16].The relationbetweensmokingandprecancerouslesions,especiallyIM, hasbeenextensivelystudied[17];however,toourknowledge,no meta-analysesofstudiesquantifyingthisassociationareavailable. Weaimedtoquantifytherelationbetweentobaccosmokingand IMthroughsystematicreviewandmeta-analysisofthepublished epidemiologicalevidence.

http://dx.doi.org/10.1016/j.dld.2014.08.034

2. Materialsandmethods

Astudyprotocolwaspredefinedbytheauthorsandfollowed throughoutthereview.

2.1. Searchstrategy

PubMed®_,Scopus®_{andWebofScience}TM_{weresearched,from}

inceptiontoApril2014,toidentifypublishedarticlesevaluatingthe relationshipbetweentobaccosmokingandIM,withnolanguage restrictions;thesearchexpressionsare providedinthePRISMA systematicreviewflowchart(Fig.1).Thelistofbibliographic refer-encesoftheoriginalreportsconsideredeligibleforthesystematic reviewandreviewarticlesonthesetopicswerealsoscreened.

2.2. Selectionofthestudies

The listof referenceswas independently screened by three reviewers(SM,SRandLA),inthreeconsecutivesteps,applying pre-definedcriteria.Inthefirststep,studieswereexcludedconsidering onlyinformationpresentedinthetitleandabstract.Inthesecond step,fulltextsofarticlesnotpreviouslyexcludedwereassessed todeterminetheireligibilityforthesystematicreview.Inthelast step,fulltextswerere-evaluatedtodetermineeligibilityfor meta-analysis.

Publishedarticleswereincludedwhenallofthefollowing crite-riaweremet:(1)originalreportsofcase–controlorcross-sectional studies,includingbaselineevaluationsofrandomizedclinicaltrials orcohortstudies;(2)articlesaddressingtheassociationbetween tobaccosmokingandtheoccurrenceofIMinhumanadults;(3) exposure defined as smoking cigarettes, pipes, bidis or cigars; and(4)outcomedefinedasintestinalmetaplasiaofthestomach, excludingthecardia,asthisisamoreheterogeneousconditionthat mayfollowtheaetiologyofoesophagealmorecloselythanthatof gastriccancer[18–20].Amongreportswithoverlappingsamples, weselectedthoseprovidingdataregardingthelargestnumberof casesorpresentingmoredetailedinformationregardingtobacco exposure.

Thedecisionstakenindependentlybythereviewersineachstep werecomparedanddiscrepancieswereresolvedbyconsensus,or involvingafourthresearcher(BPorNL).

2.3. Dataextractionandmeta-analysis

Weextracted dataonthefollowing items:publication year; countrywherethesamplewasassembled;selectionofthe par-ticipantsandsamplesize;numberofbiopsyfragmentsandcriteria usedforthediagnosisofIM;oddsratio(OR)estimatesand cor-responding95% confidence intervals (95%CI), orthe necessary informationtocomputethem,fortheassociationbetweensmoking andIM;controlforpotentialconfoundingfactors.

WhenastudyprovidedORestimatesadjustedforadifferent numberofpotentialconfounders,theoneadjustedforthelargest numberofvariableswasselected.Forstudiesprovidingadjusted estimatesonlyfortherelationbetweenexposuresotherthan smok-ingandIM,crudeestimatesfortheassociationbetweensmoking andIMwerecomputedifsufficientdatawasavailable.Lastly,if onlycrudeestimatesorthenecessaryinformationtocomputethem wereavailable,thesewereextracted.

WhendataregardingIMindifferentstomachlocationswere presented separately, the measures referring to antrum were selectedfor meta-analyses,asthis betterreflectsthemore fre-quentlocationofadenocarcinomas,speciallyoftheintestinaltype [20–23].

Data extraction was performed independently by two researchers (SM and SR) and disagreements were resolved by consensus,orinvolvingathirdresearcher(BPorNL).

Weconductedmeta-analysesfortheassociationbetween smok-ing (ever vs. never and current vs. non-smokers) and IM. The DerSimonianandLairdmethodwasusedtocomputesummary ORestimates,and respective95% CI.Heterogeneitywas quanti-fiedusingtheI2_{statistic[24].Visualinspectionofthefunnelplots}

andtheEgger’sregressionasymmetrytestwereusedfor assess-mentofpublicationbias[25].Sensitivityanalyseswerecarriedout takingdifferentinclusioncriteriaintoaccount,asdescribedinthe footnotesoftheforestplotsusedtosummarizetheresults.

ThestatisticalanalysiswasperformedwithSTATA®_,version11

(STATACorp.,CollegeStation,TX,USA). 3. Results

3.1. Systematicreview

Thirty-twoarticleswereincludedinthesystematicreview (Sup-plementaryTablesS1andS2).Fifteenstudieswereconductedin Asia[26–40](fivefromJapan,fourfromChina,threefromKorea, two from Iran and one fromTaiwan), eight in Europe[41–48] (amulticentre studyandone eachfromEngland, Finland,Italy, Netherlands,Poland,PortugalandSpain),fourinNorthAmerica [49–52](participantswereAsian/Hawaiianintwoofthem),three inSouthAmerica[53–55](Venezuela,PeruandElSalvador)and oneeachinOceania[56](NewZealand)andinAfrica[57] (Mozam-bique).

Seventeen studies [27,28,30–33,40,41,43,44,46–52,56,57] recruitedonlypatientsreferredduetogastrointestinalcomplaints. Twelve study populations [26,29,35–37,39,45,53–55] included volunteersfromcommunityscreeningprogrammes.Twostudies [38,42] included participants referred due to gastrointestinal complaintsas wellas volunteers,and one study [34] recruited first-degreerelativesofgastriccancerpatients.

The number of biopsies performed for histological diagno-sisranged betweentwo and 14 (Supplementary Tables S1 and S2);however,three articles[36,49,51]didnotprovide informa-tion on the number of biopsies. Only 15 studies specified the classification systemused toassess IM; from these,13 studies [11,27,30–32,34,35,37,38,43,44,47,48] usedthe Updated Sydney System.

3.2. Meta-analyses

Atotalof19articles[28–30,32–38,42,48,50–56]provided quan-titative information on the relation between tobacco smoking and IM, mostof themfollowing a cross-sectional evaluation of theparticipants(17cross-sectional,fromwhichsixwerea base-lineevaluation of a cohort and one a baseline evaluation of a randomizedcontrolledtrial)and fivewerecase–controlstudies (SupplementaryTableS1).

3.2.1. Evervs.neversmokers

A total of 13 studies [28,29,32,33,35–37,42,48,50,51,53,55], evaluating3410IMpatientsand8630controls, classified smok-ingexposureasevervs.never(Fig.2).ThecombinedORestimate fortheassociationbetweeneversmokingandIMwas1.54(95% CI:1.12–2.12, I2_{=67.4%) for crude estimates,and 1.26(95%CI:}

0.98–1.61,I2_{=65.0%)whenconsideringonlythesevenstudies}

pro-viding adjusted OR estimates. The results remainedessentially unchangedwhensensitivityanalyseswereconducted(Fig.2).

Visualinspectionofthefunnelplotfor evervs. never smok-ing(Fig.4)suggestedanunderrepresentationofsmallstudieswith

Records identified throughdatabase searching(PubMed®a_,SCOPUS®b

andWebof KnowledgeTMc) (n =2656)

Scre

e

ni

ng

In

cl

ud

ed

Eli

gibi

lity

Id

ent

ifi

ca

tion

Additionalrecordsidentified through other sources

(backwardcitationtracking) (n =1181)

Recordsafterduplicatesremoved (n = 1466)

Recordsscreened (n =1466)

Records excluded (n = 1255)

Full-text articles assessedforeligibility

(n = 211)

Full-text articles excluded, with reasons (n = 179:18non-eligible publication types(review, commentorbook chapter);

1 not conductedin human adults; 157did notprovide

informationon the association between smokingand IMand 3 evaluated thesame

sample) Studies includedin qualitative synthesis (n = 32) Studies includedin quantitative synthesis (meta-analysis) (n =19)

Fig.1.PRISMAsystematicreviewflowchart.a_PubMed®_{SearchExpression:(“precancerousconditions”OR“precancerouslesions”OR“atrophicgastritis”ORatrophyOR}

“intestinalmetaplasia”ORdysplasia)AND(stomachORgastricORcardia)AND((smokingORsmokeORsmokerORtobaccoORcigarORcigaretteORpipeORbidiORbiddis

ORbeedie)OR(lifestyle)OR((alcoholORalcoholic)AND(consumptionORbeverageORdrinking))OR(dietORdietarypatternORsaltyfoodORcuredfood)).b_SCOPUS®

SearchExpression:(“precancerousconditions”OR“precancerouslesions”OR“atrophicgastritis”OR“atrophy”OR“intestinalmetaplasia”OR“dysplasia”)AND(“stomach”

OR“gastric”OR“cardia”)AND(“smoking”OR“smoke”OR“smoker”OR“tobacco”OR“cigar”OR“cigarette”OR“pipe”)OR(“bidi”OR“biddis”OR“beedie”OR“smoker”OR

“lifestyle”OR“alcohol”OR“alcoholic”OR“consumption”OR“beverage”OR“drinking”OR“diet”OR“dietarypattern”OR“saltyfood”OR“curedfood”)inINDEXTERMSOR

TITLE-ABS-KEY.c_{WebofKnowledge}TM_{SearchExpression:Topic=((“precancerousconditions”OR“precancerouslesions”OR“atrophicgastritis”ORatrophyOR“intestinal}

metaplasia”ORdysplasia))ANDTopic=((stomachORgastricORcardia))ANDTopic=(((smokingORsmokeORsmokerORtobaccoORcigarORcigaretteORpipeORbidiOR

biddisORbeedie)OR(lifestyle)OR((alcoholORalcoholic)AND(consumptionORbeverageORdrinking))OR(dietORdietarypatternORsaltyfoodORcuredfood))((smoking

ORsmokeORsmokerORtobaccoORcigarORcigaretteORpipeORbidiORbiddisORbeedie)OR(lifestyle)OR((alcoholORalcoholic)AND(consumptionORbeverageOR

drinking))OR(dietORdietarypatternORsaltyfoodORcuredfood))).

negativeassociations,althoughtheEgger’sregressionasymmetry test(p=0.133)showednostatisticallysignificantbias.

3.2.2. Currentvs.non-smokers

Ninestudies[30,34,38,42,51,52,54–56]includedinthis meta-analysis,evaluating1050IMpatientsand4280controls,compared current and non-smokers (Fig.3).All studies, except one [51], showedapositiveassociationbetweenexposureandoutcome.

ThecombinedORestimatefortheassociationbetweencurrent smokingandIMwas1.27(95%CI:0.88–1.84,I2_{=73.4%)forcrude}

estimatesand1.49(95%CI:0.99–2.25,I2_=0.0%)when

consider-ingonlythetwostudies(conductedinsubjectsreferreddueto gastrointestinalcomplaints) which provided adjusted estimates (Fig.3).

Visualinspectionofthefunnelplotforcurrentvs.non-smokers (Fig.4)suggested anunderrepresentation ofsmallstudies with stronger positive associations, in accordance with the Egger’s regressionasymmetrytest(p=0.046).

3.3. Studiesnotconsideredformeta-analysis

Atotalof13articles[26,27,31,39–41,43–47,49,57]includedin thesystematicreviewwerenotincludedinthemeta-analysisas theydidnotprovideenoughinformationtocomputequantitative estimatesregardingtheexposuretotobacco,comparedexposureor outcomecategoriesnotdirectlycomparablewiththosepresented inmostoftheotherreports,orevaluatedonlyH.pylori-infected subjects(SupplementaryTableS2).

Onestudy [26] showedthemean metaplasia scorefor non-smokers and smokers (3.4 and 2.6, respectively, p-value=0.10) andanother[41]didnotprovidedetailedinformationconcerning tobaccoexposureasitcomparedthenumberofcigarettessmoked andfoundthatsmoking10ormorecigarettesadaywasassociated withadefiniteincreaseinIM(p<0.002).

Otherarticles[27,31,39,40,43,44,49,57] included participants whichallhadIMwithdifferentextentsandseverities.Forexample, Jedrychowskietal.[44]comparedparticipantswithmoderateor severeIMvs.thosewithnilormildIMandfoundasignificant asso-ciationforevervs.neversmokers(OR=1.42,95%CI:1.10–1.84).

Fig.2.Meta-analysisofthestudiesassessingtherelationbetweensmoking(evervs.neversmokers)andintestinalmetaplasia.OR(95%CI)–oddsratio(95%confidence

interval).a_{ThisORestimatewascomputedbytheauthorsofthepresentreview,withdataprovidedintheoriginalreports.}b_{ThisORestimateforthecomparisonbetween}

everandneversmokerswascomputed,usingtheDerSimonianandLairdmethod,withdataprovidedintheoriginalreportontheassociationbetweentobaccosmokingand

IMseparatelyforex-andcurrentvs.neversmokersorothersimilarclassifications;asensitivityanalysisreplacingthesevalueswithcurrentvs.neveror,forthosewithother

classifications,replacedwiththegroupwhichhadthelargestnumberofparticipants,yieldedasummaryORof1.27(95%CI:0.96–1.68,I2_=60.9%).c_{ThisORestimateisfrom}

studiesconductedinvolunteersfromcommunityscreeningprogrammesandasensitivityanalysisincludingonlytheseyieldedasummaryORof1.26(95%CI:1.09–1.45,

I2_=0.0%).

Fig.3. Meta-analysisofthestudiesassessingtherelationbetweensmoking(currentvs.non-smokers)andintestinalmetaplasia.OR(95%CI)–oddsratio(95%confidence

Fig.4. Funnelplotsofthestudiesassessingtherelationbetweensmoking(evervs.

neverandcurrentvs.non-smokers)andintestinalmetaplasia.

Abadiretal.[49]andChooietal.[27]comparedpatientsaccording totheprogressionofthepathologyandalsofoundaclearpositive associationbetweentobaccosmokingandIMprogression.

Threestudies[45–47]includedonlysubjectsinfectedwithH. pylori.Koivistoetal.[47]showedvirtuallynodifferencesbetween currentandnon-smokers(OR=1.04,95%CI:0.58–1.88),whereas theremainingshowedapositiveassociationthatincreasedwith theamountsmoked(Russoetal.[45],OR=1.79,95%CI:0.95–3.31 forex-vs.neversmokers,OR=1.88,95%CI:0.91–3.89for smok-ers of≤20 cigarettes/day vs. never smokers and OR=4.75, 95% CI:1.33–16.99forsmokersof>20cigarettes/dayvs.never smok-ers;Peleteiroet al.[46],OR=1.78, 95%CI:0.84–3.76forex-vs. neversmokersandOR=3.19,95%CI:1.51–6.73forcurrentvs.never smokers).

4. Discussion

Toourknowledge,this is thefirstsystematic review onthe relationshipbetweentobaccosmokingandIM.Themeta-analysis showsaweakandnon-statisticallysignificantpositiveassociation, withoddsbeing25–50%higheramongsmokers.

Weconductedacomprehensivesystematicreviewusingmore thanonedatabaseand backwardcitationtracking.Althoughno evidenceofpublicationbiaswasobservedfortheevervs.never analysis,therewasanunderrepresentationofsmallstudieswith strongerpositiveassociationsinthecurrentvs.non-smokers anal-ysis.Thisreflectsthefactthattheassociationbetweensmoking andIMisweak,andORestimatesarelikelytobeevenclosertothe nullwhenex-smokersareincludedinthereferencecategory,since

theriskofIMinthisgroupisclosertocurrentthannon-smokers, andtheseindividualsmayhavequitsmokingbecauseofassociated gastricpathologies[6,58].Furthermore,astheseresultsarebased ona largenumberofstudies,itisunlikelythat theinclusionof additionalunpublisheddatawouldchangeourconclusions.

Ahighvariabilityamongstudieswasobservedconcerningthe adjustmentfor possibleconfounders,populationsevaluatedand assessment of IM, which needstobetaken into accountwhen interpretingthehomogeneityoftheresultsacrossstudies,andthe validityofthesummaryestimates.

For mostof thestudies,quantifyingtheassociationbetween smokingandIMwasnotthemainobjective,henceadjustedORs werepresentedfor exposuresotherthansmokingand onlythe necessary information tocompute crude ORs for smoking was available. Olderpeople are known tohave a higher risk of IM [23,59],and aremore likely tohave been exposed tosmoking throughoutlife.Althoughanagerestrictiontoincludeparticipants olderthan40yearsoldwasusedinafewofthestudies,crude esti-matesarelikelytobeconfounded.Ontheotherhand,eventhough thestudiesprovidingadjustedmeasuresofassociationtookinto accountdifferentsetsofpotentialconfounders,allaccountedfor theeffectofage.

In addition to a higher prevalence of daily smoking being observed in men compared to women, theaverage number of cigarettes smoked per dayby menis higher than for women, probablyleadingtoahighercumulativetobaccoexposureinmen [60–62].Consideringthatallstudiesreliedonabroaddefinition ofexposuretosmoking,reflectingdifferentlevelsofconsumption amongthesmokers,wewouldexpecthigherORestimatesinmen compared towomen,as observedfor gastriccancer[16]; how-ever,wewereunabletoconductananalysisstratifiedbygender, whichmayhavecontributedtothemoderatelyhighheterogeneity observed.Moststudies,includingthoseinthissystematicreview, acknowledgetheimportanceoftakingintoaccounttheamountand durationoftobaccoexposure,andhighlighttheneedformodelsto quantifytheeffectoftobaccoexposureovertime onthegastric mucosa.

Anotherfeature,whichmayhavecontributedtoheterogeneity, isthatthesourcepopulationwasmainlycomprisedofparticipants withgastriccomplaints.Themajorityofthestudiesusedas con-trolsgroupswithsomechangeofthegastricmucosa,whichmay beassociatedwithtobaccosmoking[63,64].

Thediversityinthenumberofbiopsiesandthemethodused toassessIMmayhavealsocontributedtovariabilityinthe preva-lenceofIM.ClassificationmethodsotherthantheUpdatedSydney Systemwereusedandalthoughsomeappeartobesimilar,itis possiblethatspecificchangestotheoriginalsystemmay compro-misethecomparisonbetweenstudies.Ofparticularinterest,isthe articlebyNametal.[39],whichusedtheOperativeLinkonGastric IntestinalMetaplasiaAssessment(OLGIM),arecentclassification system,andprovidedestimatesforhigh-riskstagesofIM.

It has been widely accepted that smoking is an important behaviouralriskfactorforgastriccancer,despitetheweak associ-ationobserved[16,65,66].Althoughonlyafewstudiesspecifically evaluatedthisassociationaccordingtohistologicaltype,the avail-ableevidencedoesnotsupportsignificantdifferencesaccording tothemainsubtypes[6,67–69].Regardingtherelationbetween smokingandprecancerouslesions,moststudiesaddressingchronic atrophic gastritis failed to clearly demonstrate an association [35,36,52,53,70], and the current meta-analysis is inconclusive regardingacausalroleofsmokingintheoccurrenceofIM. Nev-ertheless,takentogethertheseresultsareinaccordancewiththe hypothesisofsmokingactingmostlyinlategastriccarcinogenesis. Inconclusion,thepresentsystematicreviewandmeta-analysis doesnotconfirmsmokingasanindependentrisk factorforIM. Additionalmethodologicallyrobuststudiesareneededtoreduce

heterogeneityandclarifytheroleofuncontrolledconfoundingin theweakandnon-statisticallysignificantassociationobserved. Conflictofinterest

Nonedeclared. Acknowledgement

Thisworkwassupportedby“Fundac¸ãoparaaCiênciaea Tec-nologia”(PTDC/SAUEPI/122460/2010andSFRH/BPD/75918/2011). AppendixA. Supplementarydata

Supplementarymaterialrelatedtothisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.dld.2014.08.034. References

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