Cancer patterns and trends in Central and South America

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Cancer

patterns

and

trends

in

Central

and

South

America

$

Mónica

S.

Sierra

a,

*

,

Isabelle

Soerjomataram

a

,

Sébastien

Antoni

a

,

Mathieu

Laversanne

a

,

Marion

Piñeros

a

,

Esther

de

Vries

b

,

David

Forman

a

a

InternationalAgencyforResearchonCancer,SectionofCancerSurveillance,France b

DepartmentofClinicalEpidemiologyandBiostatistics,PontificiaUniversidadJaveriana,Bogota,Colombia

ARTICLE INFO

Articlehistory: Received22March2016

Receivedinrevisedform15July2016 Accepted21July2016

ABSTRACT

Rationaleandobjective:CancerburdenisincreasinginCentralandSouthAmerica(CSA).Wedescribethe

currentburdenofcancerinCSA.

Methods:We obtainedregionaland national-levelcancerincidence datafrom48population-based

registries(13 countries) and nation-widecancermortality data fromtheWHO (18countries). We

estimatedworldpopulationage-standardizedincidenceandmortalityratesper100,000person-years.

Results:Theleadingcancersdiagnosedwereprostate,lung,breast,cervix,colorectal,andstomach,which

werealsotheprimarycausesofcancermortality.Countriesofhigh/veryhighhumandevelopmentindex

(HDI)intheregionexperiencedahighburdenofprostateandbreastcancerwhilemediumHDIcountries

hadahighburdenofstomachandcervicalcancers.Betweencountries,incidenceandmortalityfromall

cancerscombinedvariedby2–3-fold.FrenchGuyana,Brazil,Uruguay,andArgentinahadthehighest

incidenceofallcancerswhileUruguay,Cuba,Argentina,andChilehadthehighestmortality.Incidenceof

colorectum,prostateandthyroidcancersincreasedinArgentina,Brazil,ChileandCostaRicafrom1997to

2008,whilelung,stomachandcervicalcancersdecreased.

Conclusion:CSAcarriesadouble-burdenofcancer,withelevatedratesofinfection-andlifestyle-related

cancers.Encounteredvariationincancerratesbetweencountriesmayreflectdifferencesinregistration

practices,healthcareaccess,andpublicawareness.Resource-dependentinterventionstoprevent,early

diagnose,andtreatcancerremainanurgentpriority.Thereisanoverwhelmingneedtoimprovethe

qualityandcoverageofcancerregistrationtoguideandevaluatefuturecancercontrolpoliciesand

programs.

ã2015InternationalAgencyforResearchonCancer;LicenseeElsevierLtd.Thisisanopenaccessarticle

undertheCCBY-NC-NDIGO3.0license(https://creativecommons.org/licenses/by-nc-nd/3.0/igo/).

1.Introduction

CountriesinCentralandSouthAmerica(CSA)haveundergone

significant economic and social changes during the last few

decades[1,2].Declinesinreproductivepatterns,urbanizationand

increasesinlifeexpectancyareleadingtomajorchangesin the

populationstructure and associated increases in theburden of

non-communicable diseases, including cancer [1]. GLOBOCAN

estimatesof 2012indicatedthat annually1 millionnewcancer

casesand500,000cancerdeathsoccurredinCSA;thesefiguresare

expectedtonearlydoublebytheyear2030(1.7millionnewcases

and 1 millioncancerdeaths)becauseof ageingandpopulation

growth.Thecancerprofileischangingandcancerssuchasprostate

andbreastcancerareincreasinglycommoninCSA[3,4]probably

reflectingchangesinreproductiveandlifestylefactorsrelatedto

economicdevelopment(i.e.increasingageatfirstchildbirth,lower

parity, tobacco smoking, alcohol use, diets low in fruits and

vegetables,obesity,andphysicalinactivity)[4–10].Asaresult,the

region is facing a double cancer burden with high rates of

infection-related cancers(i.e.cervix, stomachandliver) and an

increasein(Western)lifestylerelatedcancers(i.e.prostate,breast,

andcolorectum)[2–4,11].

Epidemiologic data on the cancerburden fromCSA derives

mainlyfrommortalitydata;informationregardingtheincidence

ofcancer,thoughimproving,remains variablein itsavailability.

$ ThisisanOpenAccessarticlepublishedundertheCCBYNCND3.0IGOlicense which permits users to downloadand share the article for non-commercial purposes,solongasthearticleisreproducedinthewholewithoutchanges,and providedtheoriginalsourceisproperlycited.Thisarticleshallnotbeusedor reproducedinassociationwiththepromotionofcommercialproducts,servicesor any entity. There should be no suggestion that IARC endorses any specific organisation,productsorservices.TheuseoftheIARClogoisnotpermitted.This noticeshouldbepreservedalongwiththearticle’soriginalURL.

* Correspondingauthor.

E-mailaddresses:monica.sierra@alumni.uth.edu,SierraM@fellows.iarc.fr

(M.S. Sierra).

http://dx.doi.org/10.1016/j.canep.2016.07.013

1877-7821/ã2015InternationalAgencyforResearchonCancer;LicenseeElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-NDIGO3.0license(https://

creativecommons.org/licenses/by-nc-nd/3.0/igo/).

ContentslistsavailableatScienceDirect

Cancer

Epidemiology

The

International

Journal

of

Cancer

Epidemiology,

Detection,

and

Prevention

(2)

Whilethenumberofpopulation-basedcancerregistries(PBCR)in

CSAhasincreasedinrecentyears,onlyasmallnumberhavemet

thedataqualitystandards tobeincludedin thelast editionof

Cancer Incidence in Five Continents (CI5), covering 8% of the

population [12]. Statistics on population cancer incidence and

mortalityareessentialtoidentifydisparitiesincancerburden,to

developandevaluatecancercontrolprograms,andtoguidefuture

research[8]. In this paper, we provide an overview of cancer

patternsinCSA,includingpreviouslyunpublishedincidencedata.

2.Methods

The data sourcesand methods aredescribed in detail in an

earlier paper in this supplement issue. In brief, we obtained

regionaland national-level incidencedata from48

population-basedcancerregistriesin13countries;andnationalmortalitydata

fromtheWorldHealthOrganization(WHO)mortalitydatabasefor

18countries[13].Toallowdatacomparisonsacrosscountries,we

usedstandard methodstochecktheincidencedataconsistency

andquality[14].Allincidencedatawereconvertedtothelatest

version of ICD-O (ICD-O-3) [15]; the data were subsequently

translatedtothe10theditionoftheInternationalClassificationof

Diseases (ICD-10) [16]. Nationwide mortality data from WHO

systematicallyundergodataverification,andthedataarecodedin

ICD-10toavoidmisclassificationofcancermortalityovertime[13].

Incidence and mortality data were available from most CSA

countriesexceptinHondurasandGuyanawhereneitherincidence

nor mortality data were available; French Guyana and Bolivia

whereonlyincidencedatawereavailable;andBelize,Guatemala,

Nicaragua, Panama, Paraguay, Suriname, and Venezuela where

onlymortalitydatawereavailable.Weestimatedage-standardized

incidence(ASR)andmortality(ASMR)ratesper100,000

person-years for 30 cancersites (Annex 1 Table A1) using the direct

methodandtheworldstandardpopulation[17,18].Weestimated

nationalASR byaggregatingthedata fromtheavailable cancer

registries using a weighted average of local rates. Our trend

analysiswaslimitedtofourcountrieswith10ormoreyearsofdata

available(Table1).Wechosetopresentincidenceandmortality

trendsonlyforthecountriesthathadbothincidenceandmortality

data available in order todistinguish possible determinants of

observablechangeovertimee.g.earlydetection,riskfactororpoor

treatment,despitethattheWHOmortalitydatabasemakesdata

availableforseveralcountriesintheregion.Todescribeincidence

dataandmortalitytimetrends,wecalculatedtheestimatedannual

percent change (EAPC) for the 4 countries that provided

permission touse individual yearof diagnosis for at least

10-years(Table1)usingthemethodproposedbyEsteveetal.[19].All

EAPCsweretestedforequalitytozerobyusingthecorresponding

standarderrors,andconsideredtobestatisticallysignificantifthe

p-value0.05.Weusedreallocationmethodstoseparatecervix

andcorpus uterifrom impreciselycoded uterinecancerdeaths

[20].WeconductedallanalysesinStataversion12.1(StataCorp)

[21].

We also present cancer rates for the United States (US) for

2003–2007forcomparison.WhileincidencedatasetsintheCSA

regionwereobtained directlyfromtheregistries, weextracted

incidence data from CI5 Volume X [22], using data from the

9 oldest cancer registries included in the US National Cancer

Institute’s Surveillance, Epidemiology, and End Results (SEER)

Program,whichcoversapproximately10% oftheUSpopulation

[23].Similartothecountriesinthisreport,wetookmortalityrates

fortheUSfromtheWHOmortalitydatabase[13].

Dataonhumandevelopmentindex(HDI)fortheyear2010were

obtainedfromtheUnitedNationsDevelopmentProgrammeand

theInstitutnationaldelastatistiqueetdesétudeséconomiques

[24,25,27].

The CSA region was sub-classified according to geographic

location(CentralAmerica,includingCuba,andSouthAmerica)and

the Global Burden of Disease study [26] (Andean, Central,

Southern,Tropical,andCaribbean)(Annex1TableA2).

3.Results

Thisstudyincorporatesdatafromnearly546,000newcancer

cases(47%malesand53%females)andmorethan2millioncancer

deaths(52%malesand48%females)fromCSAbetween2003and

2007.Figs.1–4showtherankingsacrossallcancersitesbetween

CSAcountriesbyhumandevelopment(HDI)formalesandfemales

in2003–2007,unlessotherwisespecified.Prostate,femalebreast,

cervix,lung,colorectum,andstomachcancersaccountedfor63%of

alltheincidentcasesand49%ofallcancerdeathsinCSAinboth

sexescombined.

TheleadingmalecancersdiagnosedinCSAwereprostate,lung,

colorectal,stomach,andnon-Hodgkinlymphoma(NHL);andthe

leadingfemale cancerswerebreast, cervix,colorectal,stomach,

thyroid,andlung(Figs.1and3).Themostfrequentcancerdeaths

were fromstomach, prostate, lung, colorectal,and livercancer

among males and breast, cervix,stomach, lung, colorectal,and

livercanceramongfemales(Figs.2and4).

3.1.Overallcancerburden

The incidence of all cancers combined (excluding

non-melanoma skin cancer) varied by about 2-fold between CSA

countries.Maleshadupto60%higherincidenceofallcancersthan

females, except in Ecuador, Peru and Mexico (male-to-female

ratios,M:F=1:1)aswellasBolivia(M:F=0.5:1)andElSalvador(M:

F=0.4:1). French Guyana, Brazil, and Uruguay had the highest

incidence of all cancers among males (ASR: 297.2–307.1) and

Brazil,Uruguayand Argentinahadthehighest incidenceamong

females (210.8–236.1) whereas for most CSA countries, male

incidence rates were below 229 and female rates below 200.

Mortalityratesvariedby2–3-foldbetweencountries,andtherates

in males were about 2-fold higher than in females, except in

Guatemala,Ecuador,Peru,ElSalvador,andNicaragua(M:F=1:1).

Uruguay, Cuba, and Argentina had the highest mortalityof all

cancersamongmales(ASMR:137.3–181.7)andUruguay,Cubaand

Chile had the highest mortality among females (91.8–98.2),

whereas for most CSA countries, mortality rates were below

125 among males and below 90 among females (Fig. 5). The

incidence of all cancers combined remained stable in the

4 countries evaluated(Argentina, Brazil, Chile, and Costa Rica)

from1997to2008.Mortalitydeclinedbyabout1.5%peryearin

both sexesinChile andby 2%peryearin Costa Ricanfemales.

Table1

Countriesandcancerregistriesincludedintheanalysisoftimetrends.

Country Nameofregistriesincluded Period %ofthenationalpopulationcovered

Argentina BahiaBlanca 1993–2007 0.8

Brazil Aracaju,Fortaleza,Goiania,SaoPaulo 1997–2006 8.0

Chile Valdivia 1993–2008 2.2

(3)

Fig.1.Cancersranked*byage-standardizedincidenceratesamongmalesinCentralandSouthAmerica.

Fig.2.Cancersranked*

(4)

Fig.3.Cancersranked*

byage-standardizedincidenceratesamongfemalesinCentralandSouthAmerica.

Fig.4.Cancersranked*

(5)

StablemortalityrateswereseeninbothsexesinArgentinaand

BrazilandinCostaRicanmales(Tables2and3).

Inmales,time trendanalysisforArgentina,Brazil,Chile,and

CostaRicashoweddeclinesintheincidenceoflung,oesophageal,

stomach cancer, and leukaemias (except in Chile) while the

incidence of prostate, colorectal, and testicular (except in

Argentina)cancersincreased,atdifferentratesforeachcountry.

Infemales,declinesincervical,stomach,andgallbladdercancers

wereobservedwhereastheincidenceofbreastandthyroidcancers

increased, again, at different rates for different countries

(Tables2and3).

Belowwebrieflydescribeincidenceandmortalitypatternsfor

severalcommoncancersites,includingthosesiteswithhighburden

and striking regional variations; nearly all cancer sites showed

importantbetween-countryvariationsandsex-disparitiesincancer

incidenceandmortality(Annex1Fig.A1).Theaccompanying14

cancersite-specificpapersinthissupplement issuedescribeindetail

thegeographicandtemporalpatternsformajorcancers.

Table2

Estimatedannualpercentagechangeinage-standardizedincidenceandmortalityrates(per100,000),males.

Argentina(1998–2007) Brazil(1997–2006) Chile(1997–2008) CostaRica(1997–2007) Incidencea Mortality Incidencea Mortality Incidencea Mortality Incidencea Mortality

Lip,oralcavity,andpharynx(C00–14) –4.7 –1.9 –0.8 1.1 –3.1 –1.9 –0.4 1.4

Esophagus(C15) –2.3 –2.1 –2.1 0.4 –3.0 –3.8 –1.5 –0.9 Stomach(C16) –0.7 –2.0 –3.9b –1.4 –4.2b –3.3b –4.4b –4.4b Colorectum(C18–20)c 2.5 0.5 2 2.5 4.1b 1.8 3.1 2.3 Liver(C22) –0.4 –1.2 1.9 2 –1.8 –0.8 0.6 –1.7 Gallbladder(C23–24) –1.1 –0.9 –1.3 0 –2.2 –2.5 –1.5 –1.1 Pancreas(C25) –9.9b 0.2 –2.9 1.4 1.5 0.1 0.3 –0.1 Larynx(C32) –6.0 –2.7 –2.8 –0.3 –4.1 –3.8 –1.9 –2.4 Lung(C33–34) –5.2b –2.1 –3.8b –0.3 –2.0 –1.4 –1.7 –3.6 Melanomaofskin(C43) –0.7 0.5 0.7 0.5 10.2b –2.1 1.5 3.7 Prostate(C61) 4.8b –0.8 2.8b 1.6 3.2b –0.8 3.8b –0.5 Testis(C62) –5.0 0.9 3.8 2.8 4.5b –2.9 4.4 4.6 Kidney(C64) 2.7 1.3 1.4 2.7 7.3b –0.8 1.1 –0.3 Bladder(C67) 2.1 –1.1 –3.3 0.7 –1.4 0.4 –1.4 4.1 Brain,CNS(C70–72) 5.3 0.9 –2.3 1.6 5.1 2 –1.4 –0.6 Thyroid(C73) –2.0 0.9 5.5 –0.04 –1.4 –0.9 4.7 8.9 HL(C81) 1.7 –5.0 –0.5 –2.6 0.4 –7.6 –1.5 –6.1 NHL(C82–85,96) 2.4 –1.0 –0.6 0.4 –2.9 –0.3 1.5 2.8 Leukemia(C91–95) –9.3b –1.4 –3.8 1.2 2.9 –0.9 –3.5 –0.8

Otherandunspecified 4.8 –0.9 2.5 –– –3.2 –1.6 –0.1 0.2

AllsitesbutC44 –0.7 –1.0 –0.1 0.7 0.4 –1.5b

0.3 –1.3

HL,Hodgkinlymphoma;NHL,non-Hodgkinlymphoma.

aIncidencerateswereestimatedusingaggregateddatafromregionalcancerregistries. b Theestimatedannualpercentagechangeisstatisticallydifferentfromzero(P0.05). c

Mortalitydataforcolorectalcanceralsoincludestheanus(C21).

Table3

Estimatedannualpercentagechangeinage-standardizedincidenceandmortalityrates(per100,000),females.

Argentina(1998–2007) Brazil(1997–2006) Chile(1997–2008) CostaRica(1997–2007) Incidencea

Mortality Incidencea

Mortality Incidencea

Mortality Incidencea

Mortality

Lip,oralcavity,&pharynx(C00–14) –7.5 0.1 –0.7 1.3 4.3 0.4 1.4 –1.1

Esophagus(C15) –10.6 –1.0 –0.4 0.2 –5.8 –3.8 –5.7 –8.8 Stomach(C16) –2.8 –2.3 –2.2 –1.3 –3.4 –3.4 –3.5 –4.5 Colorectum(C18–20)b 3.6 0.02 0.9 1.8 1.4 0.5 1.9 1 Liver(C22) 0.2 –2.4 0.04 0.9 –0.9 –0.3 –2.2 –3.5 Gallbladder(C23–24) –2.8 –1.5 –2.6 –1.3 –2.1 –3.2 –3.8 –4.2 Pancreas(C25) 1.6 0.6 –2.3 1.9 –0.8 1.6 –1.8 –1.2 Larynx(C32) –4.3 –1.4 0.2 –0.4 0.9 –3.2 –3.5 –4.0 Lung(C33–34) –4.6 1.9 0.1 2.4 –1.4 1.4 0.6 –3.4 Melanomaofskin(C43) –6.8 2.6 –1.1 1 1.6 –2.1 1.6 –3.3 Breast(C50) –1.8 –0.9 –0.7 0.4 2.5 –1.0 1.7 0.2 Cervixuteri(C53) –6.7c –0.4 –4.2c –0.2 –6.2c –4.4 –5.1c –8.3c Corpusuteri(C54) –2.3 –3.9 0.3 1.4 –0.8 0.1 –0.1 –1.0 Ovary(C56) 4.8 0.8 –4.2 0.9 –4.3 –1.1 0.2 –0.9 Kidney(C64) –1.2 0.9 1.2 1 3.8 –0.1 2.4 0.7 Bladder(C67) 2.1 –0.9 0.4 0.8 –2.6 1.8 0.7 –1.5 Brain,CNS(C70–72) 5.8 1.4 –3.0 2.1 –0.3 3.3 –3.0 –2.6 Thyroid(C73) 17.9c –2.9 6.2c –0.6 6.2 –1.0 8.5c –1.8 HL(C81) 1.6 –1.9 –0.5 –1.2 10.7 –2.0 –0.2 –1.3 NHL(C82–85,96) –0.4 –1.3 –0.1 0.6 –0.5 –0.6 2.7 6 Leukemia(C91–95) 0.2 –0.9 –3.6 0.8 2.8 –0.02 –1.4 –0.3

Otherandunspecified 13.6c –1.6

3.3 –– –5.0c –2.0 –0.1 –1.8

AllsitesbutC44 –0.6 –0.6 –0.4 0.6 –0.8 –1.4c –0.1 –2.0c

HL,Hodgkinlymphoma;NHL,non-Hodgkinlymphoma. a

Incidencerateswereestimatedusingaggregateddatafromregionalcancerregistries. b

Mortalitydataforcolorectalcanceralsoincludestheanus(C21). c

(6)

3.2.Variationsbasedonsub-regions,HDIlevel,andcountry

Withinsub-regionsofCSA,differentcancerpatternswerenoted;

forinstance,theincidenceandmortalityratesfrombreastcancerin

SouthAmerica were2–5-timeshigherthaninCentralAmerica while

theincidenceandmortalityratesofcervicalcancerwereupto

3-timeshigherinCentralthaninSouthAmerica.Theincidenceof

colorectalcancerwasthehighestinsomesouthernandtropicalCSA

countries,withratesrangingbetween25.2–34.2formalesandfrom

16.9–24.7 for females, as compared to other partsof CSA (ASR

<16.9andASMRaround11orbelow).Lungcancerincidenceand

mortalitywerethehighestamongmalesinsouthernCSAandCuba

(ASR:30.5–50.2andASMR:18–44.5)incomparisonwithmalesin

otherCSAregions(ASR<27andASMR<16). Theincidenceand

mortalityfromstomachcancerwashigheramongmalesinChileand

somecountrieslocatedincentralCSA(ASR:25.3–29.1andASMR:

17.4–24.6)and amongfemales in theAndean region and some

centralCSAcountries(ASR: 12.7–15.1and ASMR:9.3–11.2)than

amongmales andfemalesinother CSAregions(ASR<22.0andASMR

<16.0formales;andASR10.3andASMR<9.0forfemales)(Fig.5).

Countries withhigh/very highHDI suchasArgentina, Brazil,

FrenchGuyanaandUruguay,hadahighburdenofprostateand

breastcancerandarelativelylowburdenofstomachandcervical

cancer,whereas incountriesofmedium HDIsuchas Bolivia,El

Salvador, Guatemala, Nicaragua, and Suriname, the burden of

stomachandcervicalcancerswasrelativelyhigh(Figs. 1–4).Alsoin

high/veryhighHDIcountries,theincidenceofbreastcancerwas

high(ASR:67.7–71.2)whiletheincidenceofcervicalcancerwas

low(ASR:17.1–18.2);and,incontrast,theoppositewastruefor

mediumHDIcountrieslikeElSalvadorandBolivia(ASR<13for

breastvs.22–28.9forcervix).However,inChile(veryhighHDI)the

incidenceofbothbreastand cervicalcancerswasrelativelylow

(35.4and13.9,respectively),andinPeru(highHDI)theincidence

ofbreastcancerwaslow(35.1)buttheincidenceofcervicalcancer

washigh(22.1)(Fig.5).

Interestingcontrastsincancerpatternswereseenalsobetween

countries; for example, unlike other countries in CSA, Chilean

malesandfemaleshadupto12-timeshigherincidenceandupto

30-timeshighermortalityratesofgallbladdercancer.Malesand

femalesinArgentina,Brazil,Chile,andUruguayandmalesinCuba

had5–10-timeshighermortalityratesofoesophagealcancerthan

malesandfemalesinanyotherCSAcountry(Fig.5).Cubanmales

andfemaleshad5–13-timeshighermortalityoflung,larynxand

oropharyngealcancersthanmalesandfemalesinanyotherCSA

country,exceptforlungcanceramongUruguayanmales,ASMR:

44.5(Fig.5andAnnex1Fig.A1).

3.3.Variationsbysex

Apartfrombreastcancer,onlytwocancertypeshadahigher

incidencein females compared with males: thyroid

(0.16:1-to-0.24:1),andgallbladder(M:F=0.25:1-to-0.83:1)exceptinFrench

Guyana(M:F=2:1) wheregallbladderistwicemorecommonin

malesthan infemales.For othercancersites,maleshadhigher

ratesthanfemales;for example,M:Frate ratiosforlung cancer

rangedfrom2:1-to-6:1forbothincidenceandmortality.M:Fratios

forstomachcancerwere3:1forincidenceandmortality(Fig.5and

Annex1Fig.A1).ThemostdrasticM:Fratiowasnotedforlarynx,

with incidence M:F ratio ranging from 5:1-to-14:1, except in

Bolivia(M:F=2:1),andmortalityM:Fratiorangingfrom

4:1-to-21:1(Annex1Fig.A1).

4.Discussion

This paper provides a comprehensiveoverviewof themost

recentincidenceandmortalitypatternsand trendsofcancerin

CSA. In the last 5-years available, the most common cancer

diagnoses in the region were cancers of the prostate, lung,

colorectal, stomach,and NHL among males and cancers of the

breast, cervix, colorectal, stomach, thyroid, and lung among

females. With the exclusion of NHL and the inclusion of liver

cancer,thesesiteswerealsothemostimportantcausesofcancer

deaths.Someimprovementswereobservedsuchasthedeclining

ratesofmalelungcancerinBrazilandArgentinaaswellasthe

decline in cervical and stomach cancer rates, particularly in

countrieswheretheburdenwashigh.Ontheotherhand,increased

incidence rates wereobserved for prostate and female thyroid

cancers.Observedpatternsandtrendsseemtoreflectvariationin

HDI, exposure to common risk factors (Table 4), detection

practices, and disparities in healthcare access [2,3,9,11,28–33].

We also observed high incidence and mortality of gallbladder

cancerintheregion,particularlyinChilewithsomeofthehighest

incidenceandmortalityratesintheworld[13,22];althoughthe

reasonsforthehighburdenofgallbladdercancerisstillunknown,

thehighfrequencyofgallstones(majordeterminantfor

gallblad-der cancer)along withpooraccess togallbladder surgery may

contributetotheobservedpatterns[34].

Overall, incidence and mortality rates from all cancers

combinedwerecomparativelylowerinCSAthanintheUS,except

formalemortalityinUruguay,Cuba,andArgentina(6–40%higher)

whichcouldreflectthehighmortalityratesfromspecificcancer

sites,includingthosesiteswhichusuallyhavepoorsurvival(i.e.

lungandstomach).Althoughcolorectal,lung,breast,cervix,and

leukaemia have good prognosis in higher income countries, in

Uruguay,Cuba,andArgentina andotherCSAcountries, survival

remains lower which, again, indicatesinadequate and delayed

access to healthcare (diagnosis and optimum treatment) [35].

DespitethehighHDIlevelofFrenchGuyana,disparitiesincancer

care,particularlyamongthoselivinginremoteareas,havebeen

shown in women with advanced breast cancer and invasive

cervical cancer where mortality from these diseases could be

similartothatofneighbouringcountries[36,37].

Theincidenceandmortalityratesofallcancerscombinedwas

twiceashighinmalesthaninfemales, exceptinBoliviaandEl

Salvador;thedisparityinthesetwocountriesprobablyreflectsthe

highrates of cervicalcancer among women[11].Although the

reasonsforsexdisparityincancerriskarenotfullyunderstood,

sex-specifichormonesandgenetic susceptibilitymayplaysome

rolealongsidedifferentialexposuretoriskfactors[38–40].

Declinesintheincidenceandmortalityofallcancerscombined

observedinChileandCostaRicafrom1997to2008maypartially

reflectdeclinesinstomachandcervicalcancers.Regional

differ-encesinincidenceandmortalitypatternsofallcancerscombined

reflectthevariabilityof specific cancersites (i.e.breast, cervix,

prostate, lung, stomach, colorectum, liver, etc.) and perhaps

differences across HDI levels as well as differences in the

distributionofmajordeterminantsofcancer(i.e.H.pyloriinfection,

smoking),detectionpractices,advancedstageatcancerdiagnosis,

anddisparitiesinhealthcareaccess[2,3,11,28,30].Interpretationof

datapatternsfromallcancerscombinedischallenginggiventhe

wide variation in the distribution of risk factors between and

withincountriesthatcouldcontributetodifferencesincancerrisk;

moreover, under-registration of cancer patients may lead to

underestimationofincidenceand/ormortalityrates.Forinstance,

mediumHDIcountriessuchasNicaragua,ElSalvador,Suriname,

Panama, andParaguay,and a coupleof highHDI countrieslike

Peru, and Ecuador had some of the lowest mortality from all

cancerscombinedintheworld[13],ifthesestatisticsarenotdueto

substantial under registration, they may result from the high

competingmortalityburdenduetoothercausessuchasviolence,

ischemicheartdisease,roadinjuries,lowerrespiratoryinfections,

(7)

ASR

ASR ASR

ASR

Fig.5. Age-standardizedincidence(light)andmortality(dark)ratesper100,000 forselectedcancersinCentralandSouthAmericafortheperiod2003–2007,unless otherwisespecifiedy.

yPeriodofnationalmortalitydatamatchedascloseaspossibletotheincidenceperiod. 1

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ASR

ASR

ASR

ASR

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4.1.Changesinriskfactorsandoverallcancerburden

Tobaccosmokingandalcoholconsumptionremainimportant

publichealthproblemsinCSA[42,43],giventheirhighprevalencein

somecountriesandstrongcausalassociationwithseveralcommon

cancers(Table4).TheWHOhasestablishedaframeworkfortobacco

controlandhasdevelopeda globalstrategytoreduce theharmfuluse

ofalcohol;whileallCSAcountrieshave(partially)implementedthe

frameworkfortobaccocontrol,onlyafewcountrieshavestartedto

developand/orimplementtheWHOalcoholpolicies[44,45].Brazil,

Panama,andUruguayhaveimplementedsomeofthemoststringent

tobacco smoking policies in the region and the prevalence of

smokinghasdeclinedthereinrecentdecades[46–48].Thesepolicies

arealikelycauseofthedeclininglungcancertrendsinmalesfor

someofthehigherHDIcountries.

Obesity trends across CSA countries revealed a remarkable

changefromunderweighttooverweightoverthelastfewdecades

[49,50].Highintakeofenergy-richfoods,combinedwithlowlevels

ofphysicalactivityaresuggestedtocausethismarkedincreasein

bodyweight[49].Obesityhasbeenassociatedwithtwelvecancer

sites(Table4)andrecentestimatesindicatethataround15%ofthe

incidentcancersthatoccurredinCSAandtheCaribbean2012could

beattributedtoobesity,assumingacausalrelationship[51].As

obesityincreasesin CSAit ispossible thattheburden of these

cancerswillincreaseinthefuture,underliningtheimportanceof

controllingthisproblem.

Wealsoobserved contrastingpatterns in breastand cervical

cancerbyHDIlevelswhichmayreflectchangesinriskfactors(Table

4) [3,9,29,31–33] as well as disparities in healthcare access

(including screening services, early detection, and treatment of

precancerouslesions)betweenandwithincountries[2,10,33,52,53].

Changes in reproductive patterns such as a reduced numberof

pregnanciesandlaterageatfirstpregnancyhavebeenassociated

withanincreasedriskofbreastcancer[10,33].InhighHDIcountries

inCSAsuchasArgentina,BrazilandUruguaytheburdenofbreast

cancerishighandfertilityrateswithanaverageof2childrenper

woman (similarto thatin theUS); incontrast, in mediumHDI

countries like Guatemala and Nicaragua and some high HDI

countrieslikePeru, andEcuador, theburden ofbreastcancer is

lowandfertilityratesrangebetween3to4childrenperwomen[54].

In addition to the growing burden of cancers related to

economic development, the burden of cancers associated with

chronicinfectionsandpovertyremainshigh.Themaininfectious

agentsassociatedwithanincreasedriskofcancerareshownin

Table4.Estimatesfor2008revealedthat17%ofalltheincident

cancercasesoccurringinSouthAmericaandMexicoweredueto

infections(150,000/910,000cases),includingH.pylori,HPV,HBV,

HCV, and EBV, among others [55]. However, these estimates

underscoretheimportanceofHPVandH.pyloriinfectionswhich

arehighlyprevalentinCSA(12.3–20.4%[56],and50–95%[57–59],

respectively)ascomparedtotherelativelylowprevalenceofHCV

(1.4–2.5%[60])andHBV(<2%inCentralandtropicalCSA,and2–4%

intheCaribbean,AndeanandSouthernCSA[61]).

Nearly90%of allthecervical, vulva,vagina,anal,penile,and

oropharyngealcancercasescombined(75,000/84,000)inCSAcould

beattributedtoHPVinfections,withthevastmajorityofthesecases

being cervical cancers (68,000, 91%) [62]. As of 2006, HPV

vaccinationwasintroducedinthenationalimmunizationschedule

amongwomen9–20yearsoldinsixCSAcountries[2]andby

mid-2014, 18 countries in the region offered thevaccine via public

immunizationprograms[63].Anongoingclinicaltrialconductedin

CostaRicasuggeststhatHPVvaccinationinwomeniseffectivein

preventingoral-HPVinfectionwhichcouldpotentiallyreducethe

riskofHPV-associatedoropharyngealcancer[64].

ASR

ASR

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AlthoughthereisnovaccineagainstH.pylori,evidencesuggests

thateradicationoftheinfectionmayreducetheprogressionofearly

gastriclesions[65].DeclinesintheprevalenceofH.pyloriinfection,

along with improvements in sanitation, and preservation and

storageoffoodsarethoughttoberesponsiblefortheworldwide

declineinstomachcancerratesoverthepastfewdecades[48,66–

68].Despite thereporteddeclines,mortalityfrom stomach cancerin

CSAremainsamongthehighestintheworld[13]perhapsduetothe

highprevalenceofH.pyloriandunhealthydietaryhabitssuchasa

highconsumptionofprocessedmeatandsalt[69,70].

HBVcanbepreventedviavaccinationbut,currently,thereare

novaccinesavailableforHCV[65].TheintroductionoftheHBV

vaccineinCSAbetweenthe1980sand2000seemstocoincidewith

declinesinlivercancer;however,theextenttowhichHBVandHCV

contributedtotheobservedratesisstillunknown[2,71].

Estimatesfor2002indicatethat5–28%oftheglobalnumberof

livercancer (25,200–155,000/550,000–600,000 cases) couldbe

attributed to aflatoxin exposure; however, only 2% of these

occurredin CSA (589–2980cases).Interestingly, in Mexico,the

estimatednumberofaflatoxin-relatedlivercancer(hepatocellular

carcinoma)was11-timeshigherthanthenumberofHBV-related

livercancers(152–924casesper100,000inHBV-negativepeople

vs.14–83casesper100,000 inHBV-positive people)[72],thus,

suggestingthataflatoxinexposuremaybeanimportant

contribu-torintheburden ofliver cancerinthis countryandshouldbe

furtherevaluated.

4.2.Screeningprogramsandearlydetection

Differencesinprostate,breast,cervical,colorectal,andthyroid

cancerratesbetweenCSAcountriesmaypartiallyresultfromcancer

screening programs (increased medical surveillance), unequal

healthcareaccessand treatment services,and public awareness

[2,75–92].Forexample,incidencepatternsofprostatecancerlikely

reflectdifferencesintheuseofprostatespecificantigen(PSA)testing

between countries [66,78,81,83,93,94]. Moreover,

community-specific projects on particular cancers could have also led to

increasedsurveillanceandmayexplainsomeofthestrong

differ-ences between cancer sites. For example, the Barretos Cancer

Hospital (Sao Pablo, Brazil) has established an early detection

programwhichoffersscreeningforskin,breast,cervix,andprostate

usingmobile units in231 municipalitiesin 6 statessince 2004

[76,95].

BreastcancermortalityratesinCSAhaveincreasedoverthelast

fewdecadeswhileinhighincomecountriesmortalityhasdeclined

mainlyduetoscreeningand effectivetreatment[2,31,96,97].In

CSA,mostwomenarediagnosedatadvancedstagesandonly5–

10%arediagnosedinearlydiseasestages(stageI);thisproportion

variesbetweenandwithincountrieslikelyreflectinginequalities

inhealthcareaccessandinadequatemedicalinfrastructure[2,75].

Inresponsetothehighburdenofbreastcancer,asof2009,most

CSAcountrieshavedevelopedalegislativeframeworkfortheearly

detection, diagnosis, treatment and follow-up of breast cancer

[98,99]andasof2013,mostcountrieshavenational

recommen-dationsforbreastcancerscreening,exceptforEcuador,wherethe

guidelinesarecurrentlyunderdevelopment[100].

Although cytology-based cervical cancer screening has been

introduced in allCSA countriesin thelast fewdecades,it hashad little

impactontheburdenofcervicalcancerduetosuboptimalcoverage

andfollow-upcoupledwithdisparitiesinscreeningcomplianceand

pooraccesstohealthcare[33,53,56,101–106].However,Chile,Costa

Rica, Mexico, Brazil, Colombia and Uruguay have made some

improvementsintheseareasinrecentyearsleadingtobettercontrol

ofcervicalcancer[2,53].Cervicalcancerstudiestogather

informa-tiononfeasibilityand effectivenessofscreening, andpre-cancer

treatmentinlimited-resourcesettingsarealsoongoingin 5CSA

countries [107]. It is possible that improved cervical screening

activitiesandtreatmentofpre-invasivelesionsaswellas

improve-mentsin socioeconomic conditions could reduce theburden of

cervical cancer in the future, as has already occurred in North

AmericaandsomeEuropeancountries[62,66].

4.3.Healthcareaccess,diseasemanagementandtreatment

SeveralCSAcountrieshaveincludedcancertreatmentaspartof

theirnationalhealthinsurancecoverage,focusingparticularlyfor

those living in poverty, resulting in increased access to health

services[1,108]andprobablystableorimprovedsurvivalforsome

Table4

PotentialfactorsassociatedwithanincreasedriskofcancerinCentralandSouthAmerica[69,73,74].

RiskFactors Cancersite

Lifestyle

Tobacco Bonemarrow(myeloidleukemia),cervix,colorectum;kidney,larynx,liver,lung;nasalcavityandparanasalsinus;esophagus,oral cavity;ovary;pancreas;pharynx,stomach,uterus,urinarybladder

Alcohol Breast(female),colorectum,larynx;liver(hepatocellularcarcinoma),esophagus,oralcavity,pharynx

Obesity Corpusuteri,ovary,postmenopausalbreast,gallbladder(females),esophagealadenocarcinoma,colorectum,pancreas,kidney Adultattainedheight Breast,colorectum

Dieta

Redmeat,processedmeat Colorectum beta-carotenesupplements(high

doses)

Lung(amongsmokers)

Infections

Helicobacterpylori Stomach

Humanpapillomavirus(HPV) Cervix,vulva,vagina,anus,penis,headandneck(oralcavity,andoropharynxandtonsil) HepatitisCvirus(HCV) Liver(hepatocellularcarcinoma),NHL

HepatitisBvirus(HBV) Liver(hepatocellularcarcinoma)

Epstein–Barrvirus(EBV) Burkitt’slymphoma,HL,NHL,lymphoma,nasopharynx Humanherpesvirustype8(HHV–8) Kaposi’ssarcoma

Humanimmunodeficiencyvirus type1(HIV–1)

Anus;cervix;eye(conjunctiva);HL,Kaposisarcoma,NHL

Aflatoxins Liver,bileduct

Schistosomahaematobium Bladder Opisthorchisviverrini(Liverflukes) Bileduct a

Severaldietaryandnutritionalfactorshavebeenevaluatedbutconvincingevidenceforthecarcinogenicorprotectiveeffectsagainstcancerarelimited[74]:i.e.foods containingbeta-caroteneprobablyprotectagainstesophagealcancerwhileredmeatprobablyincreasestheriskofpancreaticandprostatecancer[69,74].

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cancersitesamenabletotreatmentsuchascervical,breast,colon,

ovarian, and prostate in a few CSA countries where this was

introduced[35].

In spite of the improvements in healthcare systems in CSA,

includingtheavailabilityofcancertreatments(radiotherapyand

chemotherapy)inthepublicsector[100],inequitiesremaininaccess

to optimal cancer services due to a series of factors including

availabilityofandaccessibilitytoadequatemedicalinfrastructure,

suboptimalhealthcarecoverage,andlackoffundingandunequal

distributionofresourcesforparticularpopulations[2,75].Health

systemsinmostcountriesarefragmentedorsegment-structured

andprovideminimumcare(focusingonemergencycare);hence,

therearedelaysincancerdiagnosisandtreatment.Suchdelaysare

usually associated with an advanced-diseasestage at diagnosis when

treatmentsarelesseffective[1,2,75,100,108].Thesefactors,along

withlowscreeningrates,couldprobablyexplainthe

disproportion-atecancermortalityinCSAascomparedto severalhighincome

countries[2].

Cervical,breast andcolorectal cancerarepotentiallycurable

withearlydetectionandtreatment(includingsurgery,

radiother-apy and chemotherapy), while testicular cancer, lymphoma,

sarcomaandacutelymphoblasticleukaemiaarealsopotentially

curablewithadequatetreatment.Unfortunatelyscreeningand/or

treatmentsarenotreadilyaccessiblefornumerouspeopleinlow

and middle income countries [108]. Hence, differences in the

adoptionofmoderntherapiesanddisparitiesindisease

manage-ment probably contributed to some of the observed cancer

patternsinCSAaswell[67,78,109–111].

4.4.Strengthsandweaknessesofstudy

Thisstudyhasseveralstrengthsandlimitations.Thisoverview

aimedtopresentthecurrentpatternsandtrendsofcancerinCSA

and included the most readily available incidence data from

13countries(48cancerregistries),includingdatanotpublishedin

thelatestvolumeofCI5(8countries,22cancerregistries)[22]and

nationalmortality datafrom18 countries. The final population

coverageforincidencedatawas10%.Althoughthisfigureisstill

low,itdoesrepresentthelargestcompilationofcancerincidence

datain the regionand the mostreadily accessible data source

availabletodate.Intheabsenceofnationalincidencedata(except

for Costa Rica and Uruguay), nationwide incidence rates are

representedbyaggregateddatafromregionalregistrieswhichdo

notcovertheentirecountryandmaynotberepresentativeofthe

cancerburdenatthenationallevel.PBCRmaydifferin

complete-nessanddataqualitywhich,amongotherfactors,dependonthe

maturityofthecancerregistry;thiscouldexplainwhysomeofthe

rates observed in Mexico, Bolivia and El Salvador were low.

Approximately5%ofthetotalnumberofcancersdiagnosedinCSA

wereclassifiedasotherandunspecified.Ahighproportionofcases

classified as “other and unspecified” indicates poor diagnostic

precisionorinabilitytospecifythesiteoftheprimarycancer(for

casesdiagnosedusingtissuefromametastasis)[12].

Ratescouldbeinfluencedbydifferencesincaseascertainment

and reportingofcertain cancersacrosscountriesand registries

withintheregion;forexample,theinterpretationoflivercancer

patternsdependsontheaccuracyoftheICD-10coding[112].The

qualityofnationalmortalitydatarelyoncompleteness,coverageof

the registration, and the proportion of deaths classified as “ill

defined”causes; in someCSA countriesmortality datamay be

consideredofmediumorlowquality[85,113–115].Becauseliver

cancerisacommonmetastasislocation,theunderlyingcauseof

deathcaneasilybemisclassifiedastheprimarysiteinsteadofthe

metastatic site which can also bias the rate estimations [116].

Therefore,differencesincancerburdenbetweencountriesinthis

paper must be interpreted with caution, considering the large

variationinthequalityofthecancerregistriesincludedandthe

qualityofmortalitydata.

Aside from the data quality evaluations performed for data

previouslysubmittedtoCI5,evaluationsofdataqualityformost

PBCRintheregionarescarce[117–119].Forinstance,inColombia,a

recentevaluationindicatedthatdespitegoodlevelsof

complete-nessanddataqualityfromthePBCRofCaliandPasto,thereis

under-coverage for some specific cancer sites (i.e. liver, pancreas,

gallbladder,kidney,andleukaemia)probablybecausesomesources

ofinformationwereomitted[117,118];thereisalsounder-coverage

by cancerregistrationinthePBCR ofBucaramangaandManizales,as

death registries were not systematically used as a source of

information[118].Whiletherewasnoselectionbasedonquality

criteria,alldatasetsreceivedforthisprojectwerepassedthrough

thesamestandardconsistencycontrolandcheckingproceduresas

usedinCI5[22],andtheresultsproducedforthisstudyprovidea

generalpictureofthecancerburdenintheregion.However,thelack

of adequate epidemiological data in CSA limit the countries'

capacitytocreateandevaluateoptimumcancercontrolactivities,

includingpreventionandscreeningprograms[2].

Efforts to collect cancer incidence data in CSA have been

remarkabledespitethelimitedresourcesallocatedtomostofthese

registries. However, improvements in coverage and quality of

cancer registrations in CSA are urgently needed to minimize

missingorincompletedata.Giventheanticipatedincreaseinthe

cancerburdenintheCSA,thereisstillanoverwhelmingneedfor

highqualitydataandincreasedcoveragetoprovidevitalguidance

forfuturecancercontrolactivities.TheGlobalInitiativeonCancer

RegistryDevelopment(GICR),convenedbyInternationalAgency

for Research on Cancer (IARC) in 2011,aims to increase global

capacitytocollecthighqualitypopulation-basedcancerregistry

datainlowandmiddleincome-countries(http://gicr.iarc.fr/).To

address the lack of high-quality cancer data in CSA, the Latin

American Regional Hub was established in 2013 to provide

increasedtechnicalandadvocacyassistance.

5.Conclusion

Overthestudyperiod,theleadingcancersdiagnosedin CSA

wereprostate,lung,femalebreast,cervix,colorectal,andstomach.

Thesecancers,werealsotheprimarycausesofcancermortalityin

theregion.ThemarkeddifferenceintheburdenofcancerinCSA

differedaccordingtoHDIlevel,betweencountriesandwithinthe

region,andalsobysex.Theseresultsconfirmthedoublecancer

burdenofcancerinseveralCSAcountrieswithelevatedratesof

bothinfection-relatedcancersandcancersassociatedwithmore

affluentlifestyles.

ThecancerpatternsandtrendsacrossCSAcountriesalsoreveal

differencesindiseaseascertainmentanddiagnosis,deathcerti

fi-cation, and healthcare access. The disproportionately high

mortalityfromcancerinsomecountriesorregionsinCSAmay

reflectdeficiencies inprevention,early detectionand/ordisease

management. There are important opportunities to reduce the

cancerburden in thefuture through resource-dependent

inter-ventions such as the implementation and/or strengthening of

tobaccoandalcoholcontrolpoliciesandvaccinationagainstHPV.

Increasing public awareness of breast, cervix, colorectum, and

prostatecancercouldleadtoearlydetectionandtreatment and

probablybetteroutcomes.Finally,this studydemonstrates that

there is an overwhelming need to improve the quality and

coverage of population-based cancer registries to guide future

cancercontrolpoliciesandprograms.

ConflictofInterest

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Funding

ThisworkwasundertakenduringthetenureofaPostdoctoral

FellowshiptoDrMónicaS.SierrafromTheInternationalAgency

for Research on Cancer, partially supported by the European

CommissionFP7MarieCurieActions –People– Co-fundingof

regional,nationaland internationalprogrammes(COFUND).

Contributionoftheauthors

Studyconceptionanddesign:DF,MS.

Acquisitionofdata:MS,SA,ML.

Analysisofdata:MS.

Interpretationofdata:MS,IS,SA,ML,MP,EdV,DF.

Writingthearticle:MS,IS.

Criticalrevisionofthearticle:MS,IS,SA,ML,MP,EdV,DF.

Finalapprovalofthearticle:MS,IS,SA,ML,MP,EdV,DF.

Acknowledgements

The authors would like tothank sincerely all of the cancer

registry directorsand theirstaff (listed in theAppendix tothe

IntroductionofthisSupplement)fortheirconsiderableeffortsin

collectingthedatapresentedinthispaper,togetherwithmembers

of the IARC Section of Cancer Surveillance, especially Murielle

Colombet, Melina Arnold, Morten Ervik, Jacques Ferlay, Eric

MasuyerandKatiuskaVeselinovic,fortheirvaluablecollaboration.

TheauthorswouldalsoliketothankG.Nogueras,E.RenteriaandD.

McKayfortheirimportantcontributions.

Annex1.

TableA1

Definitionofcancersites.

Site Codesa

Description

Oropharynx C00-C14 Lip,oralcavityandpharynx

Oesophagus C15 Oesophagus

Stomach C16 Stomach

Colorectumb

C18-C20 Colonandrectum

Liver C22 Liver

Gallbladder C23-C24 Gallbladderandextrahepaticbiliarytract

Pancreas C25 Pancreas

Nose,sinuses C30-C31 Nasalcavityandaccessorysinuses

Larynx C32 Larynx

Lung C33-C34 Lung,tracheaandbronchus CutaneousMelanoma C43 Melanomaofskin Mesothelioma C45 Mesothelioma Kaposisarcoma C46 Kaposisarcoma

Breast C50 Breast

Cervix C53 Cervixuteri

Corpus C54 Corpusuteri

Ovary C56 Ovary Penis C60 Penis Prostate C61 Prostate Testis C62 Testis Kidney C64 Kidney Bladder C67 Bladder

Brain,CNS C70-C72 Brainandcentralnervoussystem(CNS)

Thyroid C73 Thyroid

Hodgkinlymphoma C81 Hodgkinlymphoma Non-Hodgkin

lymphoma

C82-85,C96 Non-Hodgkinlymphoma

Multiplemyeloma C88+C90 Multiplemyeloma

Leukaemia C91-95 Acutelymphatic,chroniclymphatic,otherandunspecifiedlymphatic,acutemyeloid,chronicmyeloid,otherandunspecified myeloid,andleukaemia,cellunspecified

Allcancerscombined C00-C96,but C44

Allsitesbutnon-melanomaskincancer

Otherandunspecified cancers

a

InternationalClassificationofDiseases,10threvision(ICD-10). b

Mortalitydataalsoincludesanus(C21).

TableA2

Subregionalclassification. Geographiclocation

CentralAmerica Belize,CostaRica,Cuba,ElSalvador,Guatemala,Honduras,Mexico,Nicaragua,Panama

SouthAmerica Argentina,Brazil,Bolivia,Chile,Colombia,Ecuador,FrenchGuyana,Guyana,Paraguay,Peru,Suriname,Uruguay,Venezuela GlobalBurdenofDiseaseRegions[23]

AndeanCSA Bolivia,Ecuador,Peru

CentralCSA Colombia,CostaRica,ElSalvador,Guatemala,Honduras,Mexico,Nicaragua,Panama,Venezuela SouthernCSA Argentina,Chile,Uruguay

TropicalCSA Brazil,Paraguay

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Pancreas (C25) ASR 0.4 1.0 1.6 1.60.3 0.3 1.8 2.1 2.1 2.2 2.5 2.4 2.7 4.8 2.4 2.6 3.1 3.7 3.2 3.1 3.3 3.1 3.3 3.2 3.3 3.1 3.6 1.5 2.4 2.4 4.0 3.8 4.5 3.93.7 4.5 4.7 3.8 4.5 4.0 4.7 2.5 4.7 4.4 1.2 1.4 3.7 3.0 5.2 4.2 4.9 4.74.2 5.3 7.7 5.65.5 7.2 7.4 5.4 8.4 6.3 8.6 6.1 9.2 6.5 Females Males 10 8 6 4 2 0 2 4 6 8 10 Bolivia1 (2011) El Salvador1 (1999-03) Guatemala Nicaragua Paraguay Belize Ecuador1 Venezuela Colombia1 Panama Suriname Peru1 (2001-05) Costa Rica Cuba1 (2004-07) French Guyana1 (2003-08) Mexico1 (2006-10) Brazil1 Chile1 Argentina1 US Uruguay (2005-07)

Lip, oral cavity, and pharynx (C00-14)

ASR 1.4 0.4 1.4 0.6 1.4 0.8 1.6 1.4 1.0 0.6 1.8 1.9 1.8 0.5 2.1 1.2 2.2 1.0 2.3 1.0 2.5 0.3 1.8 0.7 2.6 1.3 2.8 0.7 0.7 0.6 3.0 2.8 1.7 0.5 3.4 1.6 2.4 0.8 5.0 2.1 2.0 1.0 5.2 3.0 3.0 0.7 6.4 2.2 5.8 1.7 10.0 3.6 5.7 0.9 10.1 2.5 2.6 0.9 11.2 4.3 16.9 4.2 5.9 1.2 19.7 5.0 Females Males 20 15 10 5 0 5 10 15 20 Nicaragua El Salvador1 (1999-03) Bolivia1 (2011) Ecuador1 Suriname Guatemala Panama Venezuela Belize Mexico1 (2006-10) Paraguay Peru1 (2001-05) Chile1 Costa Rica Colombia1 Argentina1 Cuba1 (2004-07) Uruguay (2005-07) US French Guyana1 (2003-08) Brazil1 Larynx (C32) ASR 0.3 0.2 0.8 0.2 0.9 0.2 1.0 0.2 0.9 0.2 1.1 0.2 0.7 0.1 1.2 0.3 1.4 0.1 1.6 0.1 0.6 0.2 1.7 0.3 1.8 0.1 2.1 0.3 2.3 0.3 1.4 0.2 2.6 0.7 1.6 0.2 3.0 0.3 3.0 0.5 2.2 0.5 3.8 0.5 1.4 0.3 4.1 0.9 4.4 3.9 0.3 5.9 0.6 5.4 0.3 7.2 0.5 3.6 0.4 9.7 1.3 7.8 1.2 13.0 1.4 Females Males 15 10 5 0 5 10 15 Bolivia1 (2011) Guatemala Nicaragua Suriname El Salvador1 (1999-03) Ecuador1 Paraguay Panama Peru1 (2001-05) Belize Mexico1 (2006-10) Chile1 Costa Rica Venezuela Colombia1 US French Guyana1 (2003-08) Argentina1 Uruguay (2005-07) Brazil1 Cuba1 (2004-07) Nose, sinuses (C30-31) ASR 0.2 0.6 0.2 0.1 0.2 0.1 0.4 0.3 0.5 0.3 0.5 0.2 0.5 0.4 0.6 0.0 0.6 0.4 0.7 0.6 0.7 0.3 0.7 0.4 0.7 0.5 0.9 0.7 Females Males 1 0.5 0 0.5 1 Belize Guatemala Nicaragua Panama Paraguay Suriname Venezuela Bolivia1 (2011) Mexico1 (2006-10) El Salvador1 (1999-03) Costa Rica Uruguay (2005-07) Argentina1 Ecuador1 French Guyana1 (2003-08) US Colombia1 Chile1 Brazil1 Peru1 (2001-05) Cuba1 (2004-07)

Fig.A1. Age-standardizedincidence(light)andmortality(dark)ratesper100,000forselectedcancersinCentralandSouthAmericafortheperiod2003–2007,unless otherwisespecifiedy.

yPeriodofnationalmortalitydatamatchedascloseaspossibletotheincidenceperiod. 1

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Mesothelioma (C45) ASR 0.04 0.01 0.02 0.010.01 0.01 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.030.1 0.1 0.2 0.04 0.2 0.2 0.2 0.3 0.04 0.04 0.2 0.2 0.3 0.1 0.3 0.10.1 0.3 0.1 0.1 0.5 0.3 0.7 0.3 0.8 0.2 0.8 0.2 1.0 0.3 1.5 0 .5 1.0 1.5 0.5 1.5 1.0 Bolivia1 (2011) Nicaragua Paraguay Suriname Guatemala El Salvador1 (1999-03) Venezuela Panama Cuba1 (2004-07) Brazil1 Costa Rica Mexico1 (2006-10) Chile1 Ecuador1 Colombia1 Uruguay (2005-07) Peru1 (2001-05) Argentina1 Belize US French Guyana1 (2003-08) Females Males Cutaneous Melanoma (C43) ASR 0.2 0.2 0.3 0.1 0.4 0.3 0.03 0.030.3 0.4 0.5 0.3 0.5 0.4 0.5 0.3 0.7 0.3 0.7 0.7 0.4 0.3 1.6 1.8 0.7 0.5 2.1 2.0 0.5 0.3 2.2 2.1 0.9 0.5 2.5 2.2 1.0 0.7 2.6 2.1 1.2 0.7 3.1 2.8 0.6 0.5 3.1 2.9 0.4 0.3 3.2 3.4 3.9 2.3 1.2 0.6 4.6 3.6 0.8 0.5 4.9 3.8 2.5 1.1 17.3 13.2 Females Males 20 15 10 5 0 5 10 15 20 Nicaragua Suriname Belize El Salvador1 (1999-03) Guatemala Venezuela Panama Paraguay Bolivia1 (2011) Cuba1 (2004-07) Mexico1 (2006-10) Peru1 (2001-05) Costa Rica Chile1 Argentina1 Colombia1 Ecuador1 French Guyana1 (2003-08) Uruguay (2005-07) Brazil1 US Corpus uteri (C54) ASR 0.3 0.3 1.0 1.2 1.5 1.5 1.41.6 2.3 3.6 1.2 3.8 0.8 4.3 1.4 4.3 1.0 4.5 0.9 5.6 4.5 7.1 1.7 7.2 1.6 7.4 1.1 7.4 1.1 8.8 11.0 1.2 18.0 0 5 10 15 20 Guatemala Nicaragua Suriname Paraguay Venezuela Panama El Salvador1 (1999-03) Bolivia1 (2011) Belize Chile1 Mexico1 (2006-10) Ecuador1 Peru1 (2001-05) Colombia1 Cuba1 (2004-07) Costa Rica Argentina1 Brazil1 Uruguay (2005-07) French Guyana1 (2003-08) US Kaposi sarcoma (C46) ASR 0.01 0.01 0.1 0.02 0.1 0.1 0.4 0.05 0.5 0.1 0.5 0.1 0.5 0.1 0.7 0.1 0.7 0.1 1.0 0.1 1.1 0.3 1.3 0.2 1.6 0.2 Females Males 2.0 1.5 1.0 0.5 0 0.5 1.0 1.5 2.0 Belize Bolivia1 (2011) Guatemala Nicaragua Panama Paraguay Suriname Venezuela El Salvador1 (1999-03) Cuba1 (2004-07) Chile1 Mexico1 (2006-10) Uruguay (2005-07) Costa Rica Argentina1 Brazil1 Ecuador1 US Peru1 (2001-05) Colombia1 French Guyana1 (2003-08)

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Penis (C62) ASR 0.4 0.5 0.5 0.7 1.0 1.0 1.2 1.3 1.4 1.5 1.5 1.6 1.7 2.0 0 0.5 1.0 1.5 2.0 Belize Guatemala Nicaragua Panama Paraguay Suriname Venezuela US Ecuador1 El Salvador1 (1999-03) Bolivia1 (2011) Mexico1 (2006-10) Peru1 (2001-05) Costa Rica Chile1 Colombia1 Argentina1 Uruguay (2005-07) Cuba1 (2004-07) Brazil1 French Guyana1 (2003-08) Ovary (C56) ASR 0.8 1.0 1.3 1.0 1.8 2.0 2.6 2.6 3.2 3.6 3.7 5.2 2.9 5.4 3.0 5.5 3.5 5.7 2.0 7.2 3.3 7.6 2.0 7.7 2.7 8.1 8.2 4.4 8.4 4.1 9.1 5.5 9.3 0 2 4 6 8 10 Guatemala Belize El Salvador1 (1999-03) Nicaragua Paraguay Bolivia1 (2011) Panama Venezuela Suriname Mexico1 (2006-10) Cuba1 (2004-07) Costa Rica Chile1 Ecuador1 Colombia1 Peru1 (2001-05) Brazil1 French Guyana1 (2003-08) Uruguay (2005-07) Argentina1 US Kidney (C64) ASR 0.6 0.5 0.6 0.30.2 0.3 0.9 1.7 1.0 0.4 1.1 0.4 1.1 0.4 1.1 0.6 1.7 0.9 1.9 1.1 3.1 3.1 2.8 1.5 3.4 1.8 1.2 0.8 3.5 2.3 1.9 0.9 3.6 3.2 1.1 0.7 3.8 2.7 1.6 0.9 4.1 2.4 1.2 0.7 5.0 2.5 1.5 0.8 5.8 3.0 4.7 1.6 10.4 4.5 4.0 1.7 10.4 5.6 3.5 1.6 12.3 6.6 6.3 2.0 13.4 5.7 Females Males 15 10 5 0 5 10 15 Guatemala El Salvador1 (1999-03) Belize Suriname Nicaragua Bolivia1 (2011) Paraguay Panama Venezuela French Guyana1 (2003-08) Mexico1 (2006-10) Colombia1 Cuba1 (2004-07) Ecuador1 Costa Rica Peru1 (2001-05) Brazil1 Argentina1 Chile1 US Uruguay (2005-07) Testis (C62) ASR 0.2 0.3 0.4 0.4 0.10.4 0.4 0.4 0.30.6 0.6 1.0 0.3 2.2 0.4 2.8 0.7 2.9 0.4 3.2 0.4 3.4 0.3 4.4 0.2 5.3 0.7 5.3 0.8 5.4 1.1 8.3 0 2 4 6 8 10 Belize Nicaragua Venezuela Paraguay Guatemala El Salvador1 (1999-03) Panama Suriname Cuba1 (2004-07) Bolivia1 (2011) French Guyana1 (2003-08) Brazil1 Colombia1 Mexico1 (2006-10) Peru1 (2001-05) Costa Rica Ecuador1 US Uruguay (2005-07) Argentina1 Chile1

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Brain, CNS (C70-72) ASR 0.3 0.6 1.4 1.2 1.9 1.7 2.0 1.6 2.4 1.90.5 0.6 2.5 2.2 2.6 2.2 2.7 3.4 2.0 1.4 2.7 2.5 2.5 1.7 2.7 2.5 3.0 2.8 3.0 2.0 3.7 2.6 2.2 1.9 4.2 3.4 2.2 1.8 4.5 3.5 4.8 2.1 4.1 3.0 5.1 3.6 2.9 1.9 5.3 4.5 3.1 2.3 5.5 3.9 3.2 1.9 6.2 4.0 3.7 2.5 6.2 4.6 4.0 3.2 6.4 4.8 Females Males 10 5 0 5 10 Bolivia1 (2011) Paraguay Nicaragua Venezuela El Salvador1 (1999-03) Guatemala Belize Suriname Chile1 Mexico1 (2006-10) Panama Costa Rica Ecuador1 Peru1 (2001-05) French Guyana1 (2003-08) Cuba1 (2004-07) Argentina1 Colombia1 Uruguay (2005-07) US Brazil1 Bladder (C67) ASR 0.3 1.2 0.4 0.2 0.5 0.2 0.3 0.4 0.7 0.5 0.8 0.6 1.0 0.2 1.1 0.6 1.6 0.7 1.7 0.3 0.8 0.4 4.6 1.8 1.8 0.9 4.6 1.6 0.7 0.3 4.9 2.0 2.1 0.6 5.4 1.5 1.6 0.7 5.5 1.8 8.4 3.2 3.9 1.3 8.4 2.5 2.6 1.1 10.8 6.1 2.3 0.8 12.1 3.5 4.3 0.8 12.8 3.0 5.9 0.8 15.8 3.3 3.7 1.1 21.0 5.4

Females Males

25 20 15 10 5 0 5 10 15 20 25 Belize Guatemala Nicaragua El Salvador1 (1999-03) Bolivia1 (2011) Paraguay Panama Venezuela Suriname Peru1 (2001-05) Mexico1 (2006-10) Ecuador1 Costa Rica Colombia1 French Guyana1 (2003-08) Cuba1 (2004-07) Chile1 Brazil1 Argentina1 Uruguay (2005-07) US

Hodgkin lymphoma (C81)

ASR 0.3 0.2 0.3 0.1 0.3 0.3 0.4 0.2 0.4 0.2 0.5 0.40.3 0.4 0.6 0.5 0.6 0.1 0.6 0.4 0.3 0.2 0.9 0.7 0.3 0.2 1.1 1.1 0.4 0.2 1.3 0.5 0.7 0.4 1.4 1.0 0.5 0.4 1.7 1.1 0.5 0.2 1.8 1.6 1.8 0.6 0.7 0.6 1.9 1.4 0.3 0.2 2.0 1.5 1.0 0.7 2.1 1.4 0.4 0.3 2.1 1.5 0.4 0.2 2.9 2.4 3 2 1 0 1 2 3 Panama Paraguay Belize Guatemala Nicaragua El Salvador1 (1999-03) Suriname Bolivia1 (2011) Venezuela Peru1 (2001-05) Chile1 Ecuador1 Mexico1 (2006-10) Colombia1 Uruguay (2005-07) French Guyana1 (2003-08) Costa Rica Brazil1 Cuba1 (2004-07) Argentina1 US

Females Males

Thyroid (C73) ASR 0.2 0.4 0.2 0.4 0.2 0.6 0.2 0.3 0.3 1.9 0.3 0.6 0.3 0.6 0.4 0.4 0.6 2.7 0.5 0.9 1.2 4.9 0.3 0.4 1.4 5.5 0.4 0.6 1.4 8.2 1.4 6.6 0.3 0.4 1.5 7.7 0.4 0.4 1.6 6.8 0.3 0.7 1.7 7.5 0.4 0.5 2.1 12.6 0.4 0.8 2.5 10.7 0.2 0.4 3.4 14.4 0.5 0.9 3.5 16.0 0.3 0.3 4.2 13.2 Females Males 20 15 10 5 0 5 10 15 20 Belize Suriname Guatemala Nicaragua El Salvador1 (1999-03) Paraguay Venezuela Panama Bolivia1 (2011) Mexico1 (2006-10) Argentina1 Chile1 French Guyana1 (2003-08) Cuba1 (2004-07) Uruguay (2005-07) Peru1 (2001-05) Costa Rica Colombia1 Brazil1 Ecuador1 US

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Multiple myeloma (C88+C90) ASR 0.2 0.2 0.3 0.2 0.3 0.2 0.4 0.3 0.6 0.5 0.8 0.6 1.2 0.90.6 0.9 1.2 1.0 1.6 0.5 1.7 1.51.0 1.3 1.8 1.3 1.3 1.0 2.0 1.8 2.1 1.4 1.7 1.4 1.2 0.9 2.1 1.9 0.9 0.5 2.6 1.6 2.4 1.5 2.6 1.9 0.6 0.5 2.7 1.7 1.2 1.0 3.2 2.5 2.4 1.7 3.3 2.0 2.6 1.7 4.5 3.0 4.7 4.1 Females Males 1 2 3 4 5 0 1 2 3 4 5 Guatemala Bolivia1 (2011) El Salvador1 (1999-03) Nicaragua Paraguay Belize Mexico1 (2006-10) Venezuela Suriname Costa Rica Panama Argentina1 Cuba1 (2004-07) Colombia1 Peru1 (2001-05) Uruguay (2005-07) Ecuador1 Brazil1 Chile1 US French Guyana1 (2003-08) Non-Hodgkin lymphoma (C82-85, C96) ASR 0.8 0.5 0.5 0.5 1.4 1.3 1.6 1.0 1.7 1.2 1.9 1.2 2.0 1.4 2.8 2.0 2.9 2.0 3.4 1.3 3.4 2.4 4.3 4.3 3.0 2.1 5.2 4.4 3.8 2.7 6.8 5.4 3.4 2.2 7.8 5.1 3.5 2.2 8.1 5.9 2.3 1.6 9.1 6.5 9.5 7.0 2.8 1.9 10.2 6.9 2.7 2.0 10.2 8.8 2.4 1.8 10.6 9.2 4.8 3.0 10.9 6.4 4.9 3.1 16.3 11.4 Females Males 20 15 10 5 0 5 10 15 20 Guatemala El Salvador1 (1999-03) Nicaragua Belize Paraguay Suriname Venezuela Panama Bolivia1 (2011) Chile1 Mexico1 (2006-10) Costa Rica Cuba1 (2004-07) Argentina1 Brazil1 French Guyana1 (2003-08) Colombia1 Peru1 (2001-05) Ecuador1 Uruguay (2005-07) US

Other and unspecified cancers

ASR 1.3 1.3 2.1 2.4 5.0 4.6 5.5 6.3 5.7 6.5 5.9 5.4 10.1 10.7 7.1 7.0 11.1 9.1 10.2 9.0 11.7 11.1 9.8 8.3 11.8 9.8 7.5 7.1 11.8 10.1 4.0 4.5 17.2 15.2 13.2 10.2 17.4 10.9 17.5 14.0 Females Males 20 15 10 5 0 5 10 15 20 Bolivia1 (2011) El Salvador1 (1999-03) French Guyana1 (2003-08) Ecuador1 Peru1 (2001-05) US Cuba1 (2004-07) Costa Rica Colombia1 Chile1 Mexico1 (2006-10) Argentina1 Uruguay (2005-07) Brazil1 Leukaemia (C91-95) ASR 0.7 1.0 2.5 2.5 2.7 1.9 3.2 2.61.9 1.7 3.2 2.9 3.4 3.0 3.5 3.1 3.7 3.1 3.8 3.4 4.4 3.43.0 3.8 4.2 3.3 5.0 3.4 4.6 3.8 5.5 4.6 3.8 2.9 5.6 4.6 6.0 4.6 2.9 2.6 6.3 5.5 4.7 2.9 6.7 5.1 3.4 2.6 6.7 5.0 3.8 3.1 6.7 6.7 4.4 3.0 7.3 5.4 4.3 3.4 7.6 6.1 5.5 3.2 11.4 7.3 Females Males 10 15 5 0 5 10 15 Bolivia1 (2011) Belize Suriname El Salvador1 (1999-03) Nicaragua Paraguay Guatemala Venezuela Panama Mexico1 (2006-10) Cuba1 (2004-07) Costa Rica Chile1 French Guyana1 (2003-08) Peru1 (2001-05) Uruguay (2005-07) Brazil1 Ecuador1 Argentina1 Colombia1 US

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