Stomach cancer incidence in Brazil:
an ecologic study with selected risk factors
1Inc id ê nc ia d e c ânc e r d e e stô mag o no Brasil:
e stud o e c o ló g ic o c o m fato re s d e risc o
se le c io nad o s
11 Pap er p resen ted at th e An n u a l M eet in g of t h e In t ern a t ion a l Associa t ion of Ca n cer Regist ries, Rio d e Ja n eiro, Bra z il, N ov em b er 1995. 2 Dep artm en t of Ep id em iology a n d Qu a n t it a t iv e M et h od s, N a t ion a l Sch ool of Pu b lic Hea lt h , Osw a ld o Cru z Fou n d a t ion , M in ist ry of Hea lt h , Av. Leop old o Bu lh ões 1480, Rio d e Ja n eiro, RJ 21041- 210, Bra z il. Sergio Koifm a n 2
Rosa lin a Jorge Koifm a n 2
Abst ract Con t ra ry t o m a n y in d u st ria liz ed cou n t ries in w h ich a sh a rp d eclin e in st om a ch ca n -cer in cid en ce h a s b een ob serv ed , Bra z il st ill sh ow s in t erm ed ia t e t o h igh in cid en ce ra t es. An eco-logic a n a lysis w a s p erform ed t o ex p lore v a ria b les p ossib ly a ssocia t ed w it h t h e d ev elop m en t of st om ach can cer. Clu st er an alysis, p rin cip al com p on en t an alysis, an d fact or an alysis w ere carried ou t w it h p op u la t ion d a t a , in clu d in g t h e follow in g: st om a ch ca n cer in cid en ce ra t es in t h e ea rly 1990s ob t a in ed from p op u la t ion - b a sed ca n cer regist ries in Port o Alegre, Ca m p in a s, Fort a lez a , Belém , a n d Goiâ n ia ; a n d d a t a from a Bra z ilia n n a t ion a l su rv ey on fa m ily ex p en d it u res (sev era l d iet con su m p t ion it em s a n d a v a ila b ilit y of h om e refrigera t ors) ca rried ou t in 1974- 75. T h e re-su lt s re-su ggest ed t h a t p a st a v a i la b i li t y o f a h o m e ref ri gera t o r, i .e. f o o d p reserv a t i o n , m a y h a v e p la yed a n im p ort a n t role in cu rren t ly ob serv ed d ifferen ces in st om a ch ca n cer in cid en ce a m on g t h e v a riou s p op u la t ion s st u d ied in Bra z il. Differen ces in liv in g st a n d a rd s a m on g p op u la t ion s in t h ese cit ies also ap p ear t o h av e p layed an im p ort an t role in t h e observed in cid en ce d ifferen ces. Key words St om ach ; Can cer; Risk Fact ors; Clu st er; Fact or
Resumo De form a d ist in t a d a q u ela v erifica d a em m u it os p a íses in d u st ria liz a d os on d e se vem ob serv a n d o u m m a rca d o d eclín io d a s t a x a s d e in cid ên cia d e câ n cer d e est ôm a go, o Bra sil a in d a a p resen t a t a x a s con sid era d a s in t erm ed iá ria s ou eleva d a s d est a d oen ça . Visa n d o rea liz a r u m es-t u d o ex p lo ra es-t ó ri o d a s p o ssí v ei s ra z õ es p a ra eses-t a s d i f eren ça s, se rea li z o u u m eses-t u d o eco ló gi co at rav és d e an álise d e agru p am en t o (clu st er), an álise d e com p on en t es p rin cip ais e an álise fat ori-al. Foram in clu íd os n est as an álises as t ax as d e in cid ên cia d e cân cer d e est ôm ago n o in ício d a d é-ca d a d e 90 – d et erm in a d a s p elos regist ros d e câ n cer d e b a se p op u la cion a l n o p a ís (Port o Alegre, Ca m p in a s, Fort a lez a , Belém e Goiâ n ia ) –, b em com o a q u eles ob t id os a t ra v és d e in q u érit o n a cion al d e d esp esas fam iliares (EN DEF) realiz ad o em 197475. Est e lev an t ou d ad os p orm en oriz a -d o s -d o co n su m o -d e -d i v erso s a li m en t o s, b em co m o -d a -d i sp o n i b i li -d a -d e -d e gela -d ei ra s n a s -d i f e-ren t es regiões d o p a ís. Os resu lt a d os ob t id os su gerem q u e a h et ereogen eid a d e q u a n t o à d isp on ibilid ad e d e gelad eiras n a d écad a d e 70, e p ort an t o d a con servação d e alim en t os, p od e t er d esem -p en h ad o u m im -p ort an t e -p a-p el em relação às d iferen ças d e in cid ên cia d e cân cer d e est ôm ago h o-je ob serv a d a s en t re a q u ela s cid a d es. Diferen ça s q u a n t o à s con d ições d e v id a p od em t er t a m b ém d esem p en h a d o im p ort a n t e p a p el ex p lica t iv o d a s d iferen ça s h oje ob serv a d a s n a in cid ên cia d e cân cer d e est ôm ago en t re as p op u lações d as cid ad es an alisad as.
Introduction
Desp ite th e sh a rp d eclin e in th e in cid en ce o f stom ach can cer ob served in variou s cou n tries (Howso n et a l., 1986; To m in a ga , 1987), th is is still on e of th e m ost relevan t tu m ors in Brazil, a s o b ser ved in a ll p o p u la tio n -b a sed ca n cer registries in th e cou n try. In d eed , it is ob served am on g th e th ree m ost frequ en t typ es of can cer in m en (a n d a m o n g th e five m o st freq u en t in wom en ) in all Brazilian p op u lation b ased can -cer registries (INCA, 1995). Co m p a red to th e wo rld ’s h igh est a ge-sta n d a rd ized in cid en ce ra tes fo r sto m a ch ca n cer, o ccu rrin g in Ja p a n (Parkin et al., 1992), ran gin g from 80 to 90 cas-es p er h u n d red th o u sa n d m en in th e 1980s, a n d th e lowest, in New So u th Wa les, Au stra lia (11.8 d u rin g 1983-87), th e Brazilian rates were 53.6 in São Pau lo (1978), 51.6 in Belém (1989), 31.6 in Fo rta leza (1985), 29.0 in Po rto Alegre (1991), 26.2 in Ca m p in a s (1992), a n d 22.4 in Goiân ia (1991).
Even con sid erin g som e evid en ce of a tem -p o ra l d eclin e in m o rta lity ra tes, th ere a re still rem arkab ly h igh in cid en ce rates for th is can cer in Bra zil. Th is fa ct h a s th u s b een a so u rce o f co n cern , a n d th e sea rch is u n d er wa y fo r im -p rovin g ou r u n d ersta n d in g of th e d isea se d is-trib u tion .
Certain risk factors are su sp ected to p lay an im p ortan t role in th e d evelop m en t of stom ach ca n cer, p erh a p s exp la in in g th e d istin ct ep i-d em iological p attern s ob servei-d am on g i-d iffer-en t p op u lation s. Th ese in clu d e variou s agiffer-en ts with d a m a gin g effects o n th e n o r m a l ga stric e p it h e liu m , a s m e n t io n e d in t h e lit e ra t u re.
Helicob a ct er p yloriin fectio n ( Ta ylo r & Bla ser,
1991; Form an et al., 1994; Nigh tin gale & Gru e-b er, 1994; Mu n õz, 1994), p erh a p s m a in ly d u r-in g ea rly p erio d s o f life (Go o d m a n & Co rrea , 1995), n itrosam in e p recu rsors in in d u strialized fo o d s (Mir vish , 1994), a n d fa cilita tin g fa cto rs a ssocia ted with eith er a sa lt-rich d iet, a lcoh ol in take, or d eficien t con su m p tion of fresh fru its a n d vegeta b les h a ve b een m en tion ed a s a sso-cia ted with sto m a ch ca n cer (An to n io li, 1994; Hwa n g et a l., 1994; Kod a m a et a l., 1984; Risch et al., 1985; Steh r et al., 1985).
A p ro p o sed exp la n a to r y m o d el in vo lvin g th ese a gen ts (Co rrea , 1992) is b a sed o n th e p rem ise th at ep ith eliu m -irritatin g factors like a salt-rich d iet cou ld facilitate b acterial activity, in clu d in g th at of H. p ylorian d oth ers (Megrau d
et al., 1989), lead in g to gastric ep ith elial lesion (ch ron ic gastritis), facilitatin g th e d irect action of carcin ogen s (i.e. n itrosam in es). On th e oth er h a n d , a vit a m in r ich d ie t co u ld im p e d e e n -d o ge n o u s n it ro sa m in e p ro -d u ct io n fro m n
i-trite – an d n itrate-rich food stu ffs (Weisb u rger, 1985; Bartsch et al., 1988). Th e exact step s an d ch ro n o lo gica l o rd er in wh ich a ll th ese fa cto rs in terven e rem ain s to b e ascertain ed .
A d eclin e o f sto m a ch ca n cer in Ja p a n wa s a lso o b ser ved sim u lta n eo u sly to th e in crea se in th e availab ility of h ou seh old refrigerators in th a t co u n tr y (Howso n et a l., 1986; To m in a ga , 1987). Th is fact was in terp reted as evid en ce of th e im p a ct o f b etter fo o d p reser va tio n o n th e d evelop m en t of stom ach can cer.
Th is p ap er rep orts on ou r ecologic an alysis of association s b etween cu rren tly ob served in -cid en ce ra tes o f sto m a ch ca n cer in d ifferen t Brazilian p op u lation s an d exp osu re of th e lat-ter to a series of th e ab ove-m en tion ed risk fac-tors n early a d ecad e p reviou sly.
M ethodology
Age-stan d ard ized in cid en ce rates for stom ach ca n cer b y gen d er in 1989-91 were o b ta in ed from th e Brazilian cities of Porto Alegre, Belém , Fo rta leza , Ca m p in a s, a n d Go iâ n ia , in wh ich p op u lation -b ased can cer registries are cu rren t-ly b ein g kep t. Pop u lation sam p le d ata from ei-th er ei-th e cities ei-th em selves (Belém , Porto Alegre, an d Fortaleza) or n on -m etrop olitan u rb an ar-ea s in wh ich o th ers a re lo ca ted (Go ia n ia a n d Cam p in as) were gath ered in 1974-75 by ENDEF, a n a tion a l su rvey of Bra zilia n fa m ily exp en d i-tu res (FIBGE, 1978).
Th e n a tio n a l su r vey ga th ered in fo rm a tio n o n a ll fa m ily exp en d itu res fro m a sta tistica lly rep resen ta tive sa m p le of a ll Bra zilia n region s. Two to th ree tim es a d ay for an en tire week, an in terviewer weigh ed all food th at was eaten or resid u a l (co o ked b u t u n ea ten ) a t h o m e. Th is su r vey p rovid ed a la rge sto re o f d a ta o n d iet ch aracteristics in th e variou s region s, in clu din g estim a ted p er ca p ita co n su m p tio n o f sp ecific fo o d stu ffs like vegeta b les, fru its, citru s fru its, b ea n s, fresh fish , sa lted fish , fresh red m ea t, can n ed m eat, salt, tom ato sau ce, sau sage, an d alcoh olic b everages, am on g oth ers.
Th e sam e su rvey p rod u ced in form ation on th e d istrib u tio n o f fa m ily own ersh ip o f go o d s b a sed o n to ta l exp en d itu res, in clu d in g co n -su m p tio n a n d ta xes. Th erefo re, a va ila b ility o f h om e refrigerators am on g lower socioecon om -ic stra ta (i.e., th e p ercen ta ge o f refrigera to rown in g fa m ilies in th e 40th p ercen tile fo r in -co m e d istrib u tio n ) in th e m id -1970s in th e sam e region s was also ob tain ed .
a n a lysis with va rim a x ro ta tio n b a sed o n th e aforem en tion ed variab les. Hierarch ical clu ster an alysis was p erform ed with SPSS software an d p rin cip al com p on en ts an d factor an alysis were d evelop ed with BMDP software.
Results
Recen t a ge-sta n d a rd ized in cid en ce ra tes o f stom ach can cer an d b oth sp ecific d iet item in -take an d refrigerator availab ility in 1974-75 in selected Brazilian cities are p resen ted in Table 1. Th e h igh est in cid en ce ra tes a re o b ser ved in Belém a n d Fo rta leza fo r m en (with th e sa m e p lu s Go iâ n ia fo r wo m en ), wh ile th e lowest rates are seen in Cam p in as an d Porto Alegre.
Past con su m p tion of d iet item s also sh ows im p ortan t variab ility am on g th e d ifferen t p op -u la tio n s, m a in ly fo r vegeta b les, citr-u s fr-u its, sa u sa ges, fresh fish , a n d a lco h o lic b evera ges. In deed, Porto Alegre’s p op u lation h ad a sau sage an d liqu or m ean in take eigh t to ten tim es h igh -er th a n o b s-erved in Belém a n d Fo rta leza . On th e oth er h an d , citru s fru it an d vegetab le m ean con su m p tion in Porto Alegre was two to th ree tim es th a t o f Belém a n d Fo rta leza . Belém’s p op u lation sh owed a very h eavy con su m p tion of fresh fish as com p ared to all th e oth er cities stu d ied . Average salt con su m p tion was sim ilar in all th e cities. Vegetab le con su m p tion in Por-to Alegre an d Cam p in as was also sim ilar.
Th e correlation m atrix of all th ese variab les ( Ta b le 2) sh ows h igh co rrela tio n co efficien ts b etween m a le in cid en ce ra tes a n d co n su m p -tio n o f sa lt (r = -0.97), vegeta b les (r = -0.90), fresh fish (r = 0.89), a n d fru its (r = -0.79). A m o d era te co rrela tio n wa s o b ser ved b etween refrigera to r a va ila b ility (r = 0.59) a n d co n -su m p tio n o f sa lted fish (r = 0.75) a n d to m a to sau ce (r = 0.67).
Hiera rch ica l clu ster a n a lysis o f a ll th e a b ove-m en tio n ed d iet item s (vegeta b les ex-clu d ed ), refrigerator availab ility, an d stom ach ca n cer in cid en ce ra tes resu lted in a sp ecficic clu sterin g p a ttern : Po rto Alegre a n d Go iâ n ia m erged first, fo rm in g a n in itia l clu ster ; Fo rt-a lezrt-a rt-a n d Belém th en estrt-a b lish ed rt-a seco n d clu ster; su b seq u en tly th ese two clu sters m erged ; a n d Ca m p in a s wa s th e la st city to m erge in th e d en d o gra m (Figu re 1). Wh en we d ro p p ed th e va ria b le “refrigera to r a va ila b ility in th e 1970s” fro m th e m o d el, th e clu sterin g p attern ch an ged : Cam p in as m erged with Goiâ-n ia, estab lish iGoiâ-n g th e first clu ster, iGoiâ-n wh ich Por-to Alegre was su b sequ en tly in clu d ed (Figu re 2).
Fu rth erm ore, p rin cip al com p on en ts an aly-sis a n d fa cto r a n a lyaly-sis were d evelo p ed with
th ese variables, an d th e p ercen tage of total vari-an ce exp lain ed by th e id en tified com m on fac-tors was th e followin g: factor 1 – 56.7%; factor 2 – 26.8%; factor 3 – 9.2 %; an d factor 4 – 7.2 %. Th u s, over 83% of th e total varian ce can b e ex-p lain ed by th e first two factors. Th e resex-p ective factor-rotated p lot (factors 1 an d 2) is disp layed in Figu re 3.
Discussion
Ecologic an alysis h as b een p erform ed in m an y situ ation s as a p relim in ary p roced u re aim ed at ge n e ra t in g h yp o t h e se s t o b e fu r t h e r in ve st i-gated in ob servation al stu d ies. Desp ite th e fre-q u e n t r isk o f in t ro d u cin g a n e co lo gic fa lla cy (Klein b au m et al., 1982) in wh ich false associ-ation s can b e raised , ecologic stu d ies can b e a u se fu l t o o l, so lo n g a s t h e y a re ca re fu lly e m -p loyed with regard to th eir valid ity restrain ts.
Tab le 1
Sto mac h c anc e r inc id e nc e b y g e nd e r (1990-91) and d ie t ite m intake (1974-75)
and re frig e rato r availab ility (1974-75) in se le c te d Brazilian c itie s *
Variable Porto Alegre Belém Fortaleza Goiânia Campinas
alc h 8.0 1.3 0.6 1.8 2.9
b e an 13.4 10.6 24.2 18.6 18.8
c itrus 10.6 4.6 5.3 10.9 18.3
ffish 2.0 16.2 6.0 2.3 3.3
fruit 34.2 28.7 34.8 35.1 36.1
me at 32.8 33.0 14.6 24.0 18.8
re frig 25.4 14.6 14.4 17.5 48.8
salt 4.5 2.9 3.6 4.5 4.9
saus 3.3 0.3 0.3 0.1 0.4
ve g e t 38.8 14.0 11.7 29.8 38.4
c me at 0.5 0.4 0.3 0.1 0.4
sfish 0.1 2.1 1.3 0.3 0.4
to ms 0.8 0.1 0.1 0.6 1.0
minc 29.0 42.5 44.6 25.3 22.2
finc 6.8 16.8 16.7 16.2 10.8
* Po rto Ale g re , Camp inas, G o iânia, Fo rtale za and Be lé m
alc h: p e r c ap ita annual alc o ho lic b e ve rag e intake (lite rs), 1974-75 b e an: p e r c ap ita annual b e an c o nsump tio n (kg ), 1974-75 c itrus: p e r c ap ita annual c itrus fruit c o nsump tio n (kg ), 1974-75 ffish: p e r c ap ita annual fre sh fish c o nsump tio n (kg ), 1974-75 fruit: p e r c ap ita annual fruit c o nsump tio n (kg ), 1974-75
me at: p e r c ap ita annual fre sh re d me at c o nsump tio n (kg ), 1974-75 re frig : re frig e rato r availab ility (% ) amo ng the 40% p o o re st familie s, 1974-75 salt: p e r c ap ita annual salt c o nsump tio n (kg ), 1974-75
saus: p e r c ap ita annual sausag e c o nsump tio n (kg ), 1974-75 ve g e t: p e r c ap ita annual ve g e tab le c o nsump tio n (kg ), 1974-75 c me at: p e r c ap ita annual c anne d me at c o nsump tio n (kg ), 1974-75 sfish: p e r c ap ita annual salte d fish c o nsump tio n (kg ), 1974-75 to ms: p e r c ap ita annual to mato sauc e c o nsump tio n (kg ), 1974-75
minc : male inc id e nc e o f sto mac h c anc e r (ag e -stand ard ize d rate s p e r 100,000), 1990-91
finc : fe male inc id e nc e o f sto mac h c anc e r (ag e -stand ard ize d rate s p e r 100,000), 1990-91
In th is p a p er we u sed a n eco lo gic a n a lysis to im p rove o u r u n d ersta n d in g o f th e a sso ciation s b etween in cid en ce rates for stom ach can -cer in Brazil an d p ast exp osu re to -certain p os-sib le risk factors often m en tion ed in th e litera-tu re. Co n tra r y to o th er slitera-tu d ies o n th is to p ic, ou r an alysis in clu d es a large tim e lag b etween exp o su re m ea su rem en ts (197475) a n d o u t -co m e (sto m a ch ca n cer ra tes in ea rly 1990s). Th erefo re, we so u gh t to gu a ra n tee th e a p p ro p riate tim e in terval corresp on d in g to th e laten -cy p eriod for tu m or d evelop m en t, th u s a llow-in g for resu lts llow-in h yp oth etical agreem en t with cu rren t kn owled ge of carcin ogen esis.
A d eta iled exp la n a tio n o f th e sta tistica l fou n d ation s of d escrip tive p roced u res su ch as clu ster a n d fa cto r a n a lysis (Klein b a u m et a l., 1988; Neter et al., 1990) is b eyon d th e scop e of th is p ap er, an d th e followin g d iscu ssion focu ses on th e criteria ad op ted by th e au th ors for in -terp retin g resu lts. Briefly, clu ster a n a lysis is a
tech n iq u e in wh ich th e o b ser ved su b jects (Bra zilia n cities in o u r ca se) a re gro u p ed a c-co rd in g to th eir sim ila rities fo r th e va rio u s stu d y va ria b les (i.e., ca n cer in cid en ce, d iet item in ta ke, h o m e refrigera to r a va ila b ility, o r oth ers). In th is tech n iqu e, th e con cep ts of sim -ila rity a n d d ista n ce exp ress clo sen ess a m o n g th e su b jects u n d er stu d y. Th e su m o f th e sq u a red d ifferen ces a m o n g va ria b les is o b -ta in ed , p rovid in g a d is-ta n ce in d ex ca lled th e sq u a red Eu clid ea n d ist a n ce,wh ich is fu rth er stan d ard ized , an d th e greater th e sim ilarity b tween two su b jects, th e lesser th e d istan ce b e-tween th em . A m eth o d ca lled sin gle lin ka ge com p ares d istan ces am on g su b jects an d com -b in es th em sh owin g th e clo sest d ista n ces o r grea test sim ila rity. Clu sters a re o rga n ized b y co m p a rin g th e m a trix o f sq u a red Eu clid ea n d ista n ce co efficien ts a fter sta n d a rd iza tio n o f variab les. In on e varian t of th is tech n iq u e (ag-glom erative h ierarch ical clu sterin g), th e greater
Tab le 2
Co rre latio n matrix o f sto mac h c anc e r inc id e nc e rate s (1990-91) and d ie t ite m intake and re frig e rato r availab ility (1974-75)
in se le c te d Brazilian c itie s*
alch bean citrus ffish fruit meat refrig salt saus veget cmeat sfish toms minc finc
alc h 1.00
b e an -0.42 1.00
c itrus 0.03 0.13 1.00
ffish -0.46 -0.49 -0.64 1.00
fruit 0.19 0.72 0.67 -0.93 1.00
me at 0.53 -0.96 -0.23 0.36 -0.66 1.00
re frig 0.30 0.07 0.93 -0.42 0.52 -0.23 1.00
salt 0.49 0.28 0.90 -0.91 0.86 0.25 0.72 1.00
saus 0.96 -0.39 0.09 -0.35 0.08 0.54 0.10 0.29 1.00
ve g e t 0.73 -0.16 0.86 -0.71 0.56 0.17 0.73 0.90 0.53 1.00
c me at -0.24 0.99 -0.11 0.35 0.99 0.89 0.99 -0.51 0.89 0.23 1.00
sfish 0.94 -0.21 0.90 0.76 -0.18 0.20 -0.10 0.89 0.29 0.84 -0.18 1.00
to ms 0.89 -0.22 0.76 0.86 -0.18 0.16 -0.10 0.91 0.27 0.92 -0.14 0.95 1.00
minc -0.48 -0.19 -0.83 0.89 -0.79 0.13 -0.59 -0.97 -0.28 -0.90 -0.46 0.75 0.67 1.00
finc -0.86 0.74 -0.21 0.01 0.23 -0.73 -0.32 -0.16 -0.83 -0.54 0.14 0.14 0.14 0.14 1.00
* Po rto Ale g re , Camp inas, G o iânia, Fo rtale za, and Be lé m alc h: p e r c ap ita annual alc o ho lic b e ve rag e intake (lite rs), 1974 b e an: p e r c ap ita annual b e an c o nsump tio n (kg ), 1974-75 c itrus: p e r c ap ita annual c itrus fruit c o nsump tio n (kg ),1974-75 ffish: p e r c ap ita annual fre sh fish c o nsump tio n (kg ), 1974-75 fruit: p e r c ap ita annual fruit c o nsump tio n (kg ),1974-75
me at: p e r c ap ita annual fre sh re d me at c o nsump tio n (kg ), 1974-75 re frig : re frig e rato r availab ility (% ) amo ng p o o re st familie s,1974-75 salt: p e r c ap ita annual salt c o nsump tio n (kg ), 1974-75
saus: p e r c ap ita annual sausag e c o nsump tio n (kg ), 1974-75 ve g e t: p e r c ap ita annual ve g e tab le c o nsump tio n (kg ),1974-75 c me at: p e r c ap ita annual c anne d me at c o nsump tio n (kg ), 1974-75 sfish: p e r c ap ita annual salte d fish c o nsump tio n (kg ), 1974-75 to ms: p e r c ap ita annual to mato sauc e c o nsump tio n (kg ), 1974-75
th e sim ilarity b etween two com p ared su b jects (cities in o u r stu d y), th e fa ster th eir m ergin g, th u s yield in g a clu ster. Su b sequ en tly, eith er th e two n ext closest su b jects m erge to form a sec-on d clu ster or an in d ivid u al su b ject m ay m erge with th e p revio u s o n e (a s sh own in Figu re 2 with Porto Alegre). On ce a clu ster is form ed , it is n ot d ism issed , an d th ese step s p roceed u n til all su b jects h ave m erged in to on e of th e p reex-istin g clu sters, th u s yield in g a d en d ogram (Fig-u res 1 a n d 2). Den d o gra m s eith er d isp la y th e step s in wh ich th e su b jects a gglo m era te (th e clu sterin g ord er sh own by cities m ergin g in ou r stu d y) or th e sp eed by wh ich th ese step s were carried ou t.
In o u r stu d y, clu ster a n a lysis with a ll va ri-ab les – vegetri-ab le con su m p tion was fu rth er ex-clu d ed takin g in to accou n t th e sim ilar average p rop ortion s ob served in b oth Porto Alegre an d Cam p in as (Tab le 1) – p rod u ced an u n exp ected resu lt: Ca m p in a s wa s th e la st city to m erge with th e p reviou sly existin g clu sters (Figu re1). In o th er wo rd s, th is m ea n t th a t Belém , Fo rta -leza, an d Goiân ia were in d eed closer (or m ore sim ila r) to Po rto Alegre th a n Ca m p in a s, a c-cord in g to all variab les selected by th e au th ors. Th e su rp rise resu lted from ou r a ssu m p tion of m o re sim ila rities b etween Po rto Alegre a n d Ca m p in a s th a n , fo r in sta n ce, b etween Belém a n d th e fo rm er. Besid es d isp la yin g low sto m -ach can cer in cid en ce rates, Cam p in as an d Por-to Alegre a re lo ca ted in Bra zil’s in d u stria lized So u th a n d h a ve h isto rica lly h a d h igh er livin g sta n d a rd s th a n th e o th er geo gra p h ic p o p u la tion s an alyzed in ou r stu d y. Th erefore, con sid -erin g th a t th is resu lt co u ld b e a n a r tifa ct, we p roceed ed to in vestigate variab le(s) th at m igh t exp lain th is su rp risin g resu lt.
Sea rch in g fo r sim ila rities a n d d ifferen ces a m o n g th e stu d y va ria b les in b o th cities, we ob served th at Cam p in as (in d eed , th e n on -m et-ro p o lita n u rb a n p o p u la tio n fet-ro m th e Sta te o f Sã o Pa u lo a s a wh o le, wh ere Ca m p in a s is th e largest city) h ad exp erien ced a h igh er p rop or-tio n o f refrigera to r a va ila b ility a m o n g th e p o o rest stra ta a s co m p a red to o th er cities in -clu d ed in th is stu d y. In fact, refrigerator avail-ab ility was h igh est in Cam p in as (48%) in 1974-75, twice th a t o b ser ved in Po rto Alegre a n d th ree tim es th at of Fortaleza, Belém , an d Goiâ-n ia ( Ta b le 1). To test th is h yp oth esis – th a t re-frigerator availability cou ld m odify a p reviou sly exp ected clu sterin g p attern (im m ed iate m erg-in g o f Ca m p erg-in a s a n d Po rto Alegre) – we a t-tem p ted to exclu d e th e a fo rem en tio n ed va ri-a b le fro m th e ri-a n ri-a lysis. Wh en we exclu d ed th e va ria b le “refrigera to r a va ila b ility” fro m th e m od el, Cam p in as p rom p tly m erged with
Goiâ-n ia , a Goiâ-n d Po rto Alegre fu rth er jo iGoiâ-n ed th is clu ster (Figu re 2). Th ese d ifferen t m od el b eh aviors b ased on th e p resen ce or ab sen ce of p rior availab ility of refrigera to rs su ggest th a t th is covariate, i.e., food p reserva tion , m a y h a ve p la yed a n im p o rta n t ro le in th e cu rren t m agn itu d e of stom ach can cer in cid en ce o b ser vecid in th e stu cid y p o p u la tio n s. Mo re -over, given th is ob servation – even con sid erin g th e p a u city o f cities stu d ied in wh ich in cid en ce d a ta on stom ach can cer were availab le – we cou ld p re-d ict a m a jo r fu tu re re-d eclin e in th e in cire-d en ce o f sto m a ch ca n cer in Bra zil fo llowin g th e in crea sed availab ility of refrigerators in th e cou n try.
Fu rth erm o re, p rin cip a l co m p o n en ts a n d fa ctor an alyses were d evelop ed . Both statistical tech -n iq u es were u sed to id e-n tify h id d e-n relatio-n sh ip s am on g th e stu d y variab les. Th is was p erform ed by d eterm in in g th e p rop ortion of varian ce exp lain ed by com m on factors, or “com m u n alities”, an d th en sp littin g th e variab les accord in g to th eir relation sh ip s with th ese factors. In reality, a factor is a con -stru ct p ro d u ced b y a resea rch er, a n d th e b est re-su lts a re o b ta in ed in a p r in cip a l co m p o n en ts
Fig ure 1
De nd o g ram o f re frig e rato r availab ility (1974-75), d ie t ite ms intake (ve g e tab le s
e xc lud e d ), and c urre nt inc id e nc e rate s o f sto mac h c anc e r, Brazilian se le c te d c itie s.
Fig ure 2
De nd o g ram o f d ie t ite ms intake (1974-75) and c urre nt inc id e nc e rate s o f sto mac h
a n a lysis wh en a h igh er p ro p o rtio n o f th e ex-p lain ed varian ce yield ed by th e stu d y variab les is a ch ie ve d wit h t h e le a st n u m b e r o f fa ct o rs. Ne ve rth e le ss, visu a liza tio n o f th e se re la tio n -sh ip s in sp a ce is o ft e n n o t a sim p le m a t t e r. Fa cto r a n a lysis u ses tech n iq u es in wh ich th e co o rd in a t e s o f e a ch va ria b le a re m a in t a in e d a fter d ifferen t kin d s o f sp a tia l ro ta tio n . Ro ta -tio n is u sefu l fo r im p rovin g id en tifica -tio n o f d ifferen t grou p s of variab les sp atially situ ated in a sp ectru m of varyin g d istan ces to th e d iffer-en t id iffer-en tified factors. Th is is ob tain ed th rou gh id e n tifica tio n o f fa cto r lo a d in gs co rre sp o n d -in g t o e a ch o f t h e st u d y va ria b le s. Th is st u d y a d o p ted a va rim a x-ro ta ted so lu tio n , b eca u se it lim its th e n u m b er o f va ria b les with h igh lo a d in gs in o n e fa cto r, th u s en h a n cin g fa cto r in t e rp re t a t io n . A fin e re so lu t io n is a ch ie ve d wh en th e stu d y va ria b les o n ly sh ow h igh fa c-tor load in gs for on e facc-tor. Th u s, facc-tor an aly-sis m a y a llow o n e t o e xp lo re h id d e n co n n e c-t io n s b e c-t we e n c-t h e a n a lyze d va ria b le s wh ich
o t h e r wise wo u ld b e n o t e a sily id e n t ifie d o r even su sp ected .
In th is stu d y, a p rin cip al com p on en t an aly-sis id en tified com m on factors am on g th e stu d y va ria b les d isp la yin g so m e h id d en rela tio n -sh ip s. In d eed , th e first two fa cto rs exp la in ed 83% of th e total varian ce, a qu ite reason ab le re-su lt. After rotation , factor 1 d isp lays h igh p osi-tive correlation with th e variab les refrigerator availab ility, fem ale in cid en ce of stom ach can -cer, a n d co n su m p tio n o f ca n n ed m ea t, fru its, b ean s, fresh red m eat, an d sau sage. On th e oth -er h a n d , fa ctor 2 sh ows close a ssocia tion s b e-tween th e variab les m ale in cid en ce of stom ach can cer an d con su m p tion of salted fish , tom ato sa u ce, a lco h o lic b evera ges, sa lt, citru s fru its, vegetab les, an d fresh fish .
As p reviou sly m en tion ed , in terp retation of resu lts yield ed by factor an alysis u su ally is n ot straigh tforward , b u t som e ob servation s can b e m a d e. Th e first is th a t m a le a n d fem a le in ci-d en ce o f sto m a ch ca n cer a re a sso cia teci-d with b oth factors at d ifferen t levels. Secon d ly, it was n ot p ossib le to clearly aggregate kn own risk or p ro tective va ria b les. Desp ite th e fa ct th a t a sim p le stru ctu re ap p ears to h ave been ach ieved b y ro ta tio n – a ll va ria b les fa il to d isp la y la rge load in gs in b oth factors – it is d ifficu lt to id en-tify th e h id d en com m on relation sh ip s b etween th e stu d y variab les in th is p articu lar case. If we on ly con sid er va ria b les with h igh loa d in gs for o n e fa cto r, fa cto r 1 a p p ea rs to b e a sso cia ted with ch ea p er d iet co m p o n en ts in Bra zil (i.e., b ea n s, ca n n ed m ea t, a n d sa u sa ge), q u ite d ifferen tly th an ob served with factor 2. In th is sen se, factor 1 ap p ears to in volve “h om elin ess” (h om em a d e m ea ls, ch ea p er d iet item s, refrig-erator availab ility), wh ile factor 2 m ay in d icate “a fflu en ce” (e.g., co n su m p tio n o f a lco h o lic b everages an d salted an d u n salted fish , wh ich u sed to b e, an d gen erally still are m ore exp en -sive th an red m eat in Brazil).
As a wh o le, b o th a p p ro a ch es (clu ster a n d fa ctor a n a lysis) a p p ea r to im p rove ou r u n d er-stan d in g an d in terp retation of th e p ossib le fac-to rs in vo lved in th e p ersisten tly h igh ra tes o f sto m a ch ca n cer in cid en ce o b ser ved in Bra zil. On th e on e h an d , refrigerator availab ility in th e cou n try – still low in th e 1970s, ran gin g from 15 to 25% am on g th e p oorest fam ilies in th e stu d y cities, excep t fo r th o se lo ca ted in th e Sta te o f Sã o Pa u lo –, a p p ea rs to h a ve p la yed a m a jo r role in th e fu rth er d ifferen tiation b etween in ci-d en ce ra tes fo r sto m a ch ca n cer in th e ea rly 1990s. On th e oth er h an d , d ifferen ces in livin g stan dards an d oth er con dition s associated with d iet p attern s m ay also h elp exp lain th e p revail-in g revail-in cid en ce of stom ach can cer revail-in Brazil.
Fig ure 3
Ro tate d fac to r lo ad ing s.
Variab le s are d e no te d b y 1,...,9, a,...,Z o ve rlap s are d e no te d b y an aste risk. Symb o l variab le .
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