Attendance at day care centers increases
the risk of childhood pneumonia among the
urban poor in Fortaleza, Brazil
1Prátic as re lac io nad as ao s c uid ad o s d a c rianç a
aume ntam o risc o d e p ne umo nia nas
c rianç as me no re s d e d o is ano s e m Fo rtale za,
Brasil
11 Th is stu d y w as su p p orted w it h gra n t s from t h e In t ern a t ion a l Dev elop m en t Resea rch Cen t re (IDRC, Ca n a d a ) a n d t h e Con selh o N a cion a l d e Desen v olv im en t o Cien t ífico e Tecn ológico (CN Pq, Bra z il). 2 Dep artam en to d e Saú d e Com u n it á ria , Un iv ersid a d e Fed era l d o Cea rá , Ru a Ba rb osa d e Freit a s 650/402, Fort a lez a , CE, 60170- 020, Bra z il. 3 M atern al an d Ch ild Ep id em iology Un it , Lon d on Sch ool of Hygien e a n d Trop ica l M ed icin e, Kep p el St reet , Lon d on W C1 7H T, U .K. 4 Program a d e Mestrado em Ep id em iologia, Un iv ersid a d e Fed era l d e Pelot a s, C. P. 464, Pelot a s, RS,
96100- 000, Bra z il. 5 Hosp ital Ped iatrico San to An t on io, Av. Cea rá 1549, Port o Alegre, RS, 90000- 000, Bra z il. W a lt er Fon seca 2 Bet t y R. Kirk w ood 3 Alu isio J. D. Ba rros 4 Ch iz u ru M isa go 3 Lu cia n o L. Correia 2 Jose A. M . Flores 5 Sa n d ra C. Fu ch s 4 Cesa r G. Vict ora 4
Abst ract W e ca rried ou t a ca se- con t rol st u d y t o in v est iga t e risk fa ct ors for ch ild h ood p n eu m o-n ia io-n t w o grou p s of 650 ch ild reo-n aged u o-n d er t w o years io-n t h e cit y of Fort alez a, Ceará, Braz il. Th e ca ses w ere ch i ld ren recru i t ed a t t h e m a i n p ed i a t ri c h o sp i t a l w i t h a ra d i o lo gi ca l d i a gn o si s o f p n eu m on ia, an d con t rols w ere ch ild ren of t h e sam e age grou p recru it ed from t h e n eigh bou rh ood of t h e ca ses. In t h is p a p er w e focu s on v a ria b les rela t ed t o ch ild ca re p ra ct ices. Work in g m ot h ers, p rop ort ion of t im e t h e m ot h er h a d w ork ed sin ce t h e ch ild w a s b orn , a n d u se of d a y ca re cen t ers em erged a s im p ort a n t risk fa ct ors w it h est im a t ed rela t ive risk s of 1.58, 1.76 a n d 5.22, resp ect ive-ly. Also im p ort an t w ere t h e n u m ber of ch ild ren liv in g in t h e h ou se an d p resen ce of gran d p aren t s. How ev er, t h e p resen ce of sib lin gs u n d er t w o yea rs a n d t h e b irt h ord er w ere n ot a ssocia t ed w it h p n eu m on ia . All a n a lysis in clu d ed a d ju st m en t for con fou n d in g b y in com e, p a ren t s’ ed u ca t ion , an d ot h er risk fact ors as ap p rop riat e. Th is is t h e first st u d y from a d ev elop in g cou n t ry t o id en t ify a t t en d a n ce a t d a y ca re cen t ers a s a risk fa ct or for in crea sed ch ild h ood m orb id it y, in t h is ca se p n eu m on ia . Th is fin d in g is of sign ifica n t p u b lic h ea lt h im p ort a n ce for cou n t ries su ch a s Bra z il w it h grow in g u rb a n p op u la t ion s a n d a n in crea sin g n eed b y m ot h ers t o fin d w ork ou t sid e t h e h om e.
Key wordsPn eu m on ia ; M orb id it y; Ch ild Hea lt h ; Ep id em iology
Resumo Est u d ou - se o risco d e p n eu m on ia n a s cria n ça s m en ores d e d ois a n os n a regiã o m et ro-p olit an a d e Fort alez a en t re ju n h o/89 e m aio/90. Foram in v est igad as as ro-p rát icas relacion ad as aos cu id a d os d a cria n ça com o p ossíveis fa t ores d e risco d e p n eu m on ia . Fa t ores m a t ern os, a m b ien -t a is e sócio- econ ôm icos fora m -t a m b ém es-t u d a d os d ev id o a su a p ossível rela çã o com a s p rá -t ica s n o cu id a d o d a cria n ça . Foi u t iliz a d a m et od ologia d e ca so- con t role, sen d o ca sos a s cria n ça s com d ia gn óst ico clín ico e ra d iológico d e p n eu m on ia , e con t roles a q u ela s cria n ça s com d iferen ça d e id a d e in ferior a d ois m eses q u e n ã o a p resen t a ssem sin t om a s d e in fecçã o resp ira t ória , e q u e re-sid issem n a v iz in h a n ça d o ca so selecion a d o. Ra z ã o d e “od d s” (RO) foi u t iliz a d a p a ra est im a r os riscos rela t iv os, a t ra v és d e regressã o logíst ica con d icion a l. Os p rin cip a is fa t ores d e risco en con -t ra d os fora m a freq ü ên cia a crech e (RO=5,2), -t ra b a lh o d a m ã e (RO=1,6) e p resen ça d os a v ós n o d om icílio (RO=1,4). A id a d e d a m ã e, o n ú m ero d e gest a ções e a a glom era çã o t a m b ém est ivera m a ssocia d os com p n eu m on ia .
Introduction
Ac u t e re sp ira t o r y in fe c t io n s (ARI) a re a m o n g th e lea d in g ca u ses o f ch ild h o o d m o rb id ity a n d m o rt a lit y in d e ve lo p in g co u n t r ie s, a cco u n t in g fo r a p p ro xim a t e ly o n e - t h ird o f t h e 15 m illio n d ea th s th a t occu r a n n u a lly a m on g ch ild ren u n -d e r t h e a ge o f five ye a r s (AH RTAG, 1991). Th e m a jo r it y (75%) o f t h e se ARI d e a t h s a re d u e t o p n e u m o n ia u n a sso cia te d with m e a sle s ( WH O, 1989).
Severa l fa cto rs h a ve b een p o stu la ted fo r in crea sed risk o f ARI a m o n g ch ild ren in d evelo p -in g co u n t r ie s. Th e se -in clu d e low b ir t h we igh t , failu re to b reastfeed an d / or in ap p rop riate wean in g p ra c t ic e s, m a ln u t r it io n , in d o o r a ir p o llu -t io n , a n d o -t h e r so c ia l fa c -t o r s su c h a s fa m ily size, sh o rt b irt h in t e r va ls, low in co m e a n d low le ve l o f e d u ca t io n o f t h e p a re n t s, h o u sin g a n d in a p p ro p r ia t e ch ild - ca re p ra ct ice s ( Vict o ra e t a l., 1989). Howe ve r, e vid e n ce re ga rd in g th e a s-so c ia t io n b e t we e n a n y o f t h e se fa c t o r s a n d p n e u m o n ia in c h ild re n in d e ve lo p in g c o u n -tries is sca rce, a n d ca se m a n a gem en t is still th e m a in cu rren t stra tegy fo r ARI co n tro l.
Th ere is an in creasin g in terest in th e im p orta n ce of ca re for ch ild su r viva l, growth , a n d d e -ve lo p m e n t . Se -ve ra l st u d ie s fro m d e -ve lo p in g co u n tries su ggest a n a sso cia tio n b etween p o o r ch ild care an d m aln u trition (En gle, 1990) wh ich is kn own to red u ce resistan ce to d iseases an d to in crease th eir severity (Ch an d ra, 1991). Howev-e r, t h Howev-e rHowev-e la t io n sh ip b Howev-e t wHowev-e Howev-e n fa ct o rs rHowev-e la t Howev-e d t o ch ild ca re a n d a cu t e lowe r re sp ira t o r y in fe c-t io n s (ALRI) a m o n g ch ild re n in d e ve lo p in g cou n tries h as received very little atten tion (Pelto & Ken d all, 1990). In p articu lar, on ly two stu d -ie s co u ld b e id e n tif-ie d e xa m in in g th e lin k with ch ild h o o d p n eu m o n ia .
In t h is p a p e r we p re se n t re su lt s fr o m a c a se - c o n t r o l st u d y e xa m in in g t h e e ffe c t o f m o t h e r’s wo rk a n d u se o f d a y- c a re fa c ilit ie s a n d t h e r isk o f p n e u m o n ia a m o n g c h ild re n . Oth er fa cto rs su ch a s b irth o rd er, to ta l n u m b er o f c h ild re n , a n d p re se n c e o f gra n d p a re n t s a t h o m e a re a lso d iscu sse d , sin ce it wa s p o ssib le to rela te th em to ch ild ca re p ra ctices.
M ethodology
A ca se co n t ro l st u d y wa s co n d u ct e d in Fo r t a -le za , a cit y o f t wo m illio n p e o p -le in No r t h e a st Bra zil, lo ca ted a t 3oSo u th in a tro p ica l zo n e. At t h e t im e o f t h e st u d y t h e in fa n t m o r t a lit y ra t e wa s a p p ro xim a t e ly 90 p e r t h o u sa n d (U NICEF, 1989). Acco rd in g to o fficia l estim a tes, over h a lf o f th e p o p u la tio n live in p reca rio u s co n d itio n s
in fa v ela s[o r sh a n t yt own s]. Re sp ira t o r y t ra c t in fe c t io n s a re t h e se c o n d h igh e st in fe c t io u s c a u se o f in fa n t d e a t h , a c c o u n t in g fo r 11% o f su ch d ea th s (UNICEF, 1989).
Justification for choice of study design
Ca se - c o n t r o l st u d ie s we re in it ia lly u se d fo r stu d yin g th e cau sality of n on -in fectiou s (“rare”) d ise a se s. It h a s b e e n sh o wn t h a t t h e ra re d is-ea se a ssu m p tio n is n o t a lwa ys n ecessa ry. In re-cen t years th eir u se h as b een exp an d ed to p rac-tically every typ e of d isease, in clu d in g com m on co m m u n ica b le d ise a se s (Kirkwo o d , 1988; Ro -d rigu es & Kirkwoo-d , 1990).
Th e ch o ice o f a ca se - co n t ro l d e sign ra t h e r t h a n a lo n git u d in a l d e sign t o id e n t ify r isk fa c-t o rs fo r p n e u m o n ia wa s b a se d o n b o c-t h e c-t h ica l a n d lo gist ic gr o u n d s. Fir st , a lo n git u d in a l d e sign wo u ld re q u ire a co n sid e ra b ly la rge r sa m -p le size, sin ce th e o ccu rre n ce o f -p n e u m o n ia is re la t ive ly ra re. Fo r e xa m p le , a re c e n t st u d y fro m th e Ga m b ia fo u n d a n in cid en ce ra te o f 17 e p iso d e s p e r 100 ch ild ye a rs (Ca m p b e ll, 1989). Th u s, 100 ch ild re n wo u ld h a ve t o b e fo llowe d fo r a fu ll yea r to d etect 17 ca ses o f p n eu m o n ia . Th e n u m b e r o f ch ild re n th a t wo u ld n e e d to b e fo llowe d fo r a ye a r (a ssu m in g a sim ila r in c i-d e n c e ra t e ) in o ri-d e r t o a c c u m u la t e su ffic ie n t ca ses wou ld m a ke th e stu d y b oth costly a n d lo -gistica lly com p lex.
Se co n d , e th ica l co n sid e ra tio n s d icta te th a t ch ild re n u n d e r su r ve illa n ce sh o u ld b e t re a t e d a t t h e fir st sign t h a t a n e p iso d e o f ARI is p r o -gre ssin g t o a se ve re st a ge . Th is t re a t m e n t wo u ld t h e re fo re in t e r fe re wit h t h e o ccu rre n ce o f se ve re p n e u m o n ia , m a kin g it d iffic u lt t o stu d y se ve re p n e u m o n ia a s th e o u tco m e o f in -terest.
Th u s , lo n git u d in a l s t u d ie s w it h e a r ly d i-a gn o s is i-a n d t r e i-a t m e n t o f ARI e p is o d e s t e n d t o in clu d e a la r ge r p r o p o r t io n o f le ss se ve re ep iso d es o f p n eu m o n ia . Th erefo re, th ey wo u ld n o t b e a p p ro p ria te fo r th e stu d y o f risk fa cto rs fo r severe p n eu m o n ia , wh ich is th e m o st co m -m on ca u se of d ea th d u e to ARI.
Th e d is a d va n t a ge s o f t h e c a s e - c o n t r o l m eth o d lie in th e ca refu l co n sid era tio n n eed ed in th e d e sign in o rd e r to m in im ize th e typ e s o f b ia s t h a t m a y o c c u r, a n d in t h e re la t ive ly so -p h ist ic a t e d a n a lysis re q u ire d (Sc h le sse lm a n , 1982). Co n sid er first selectio n b ia s. Hea lth ca re c ove ra ge fo r t h e p o p u la t io n in t h is h o sp it a l’s c a t c h m e n t a re a is h igh , a n d lo c a l e xp e r ie n c e a n d d iscu ssio n with h o sp ita l sta ff su gge st th a t a h igh p e rc e n t a ge o f t h e c h ild re n wit h p n e u -m on ia livin g in th e ca tch -m en t a rea a re likely to b e se e n a t t h e o u t p a t ie n t d e p a r t m e n t . Th u s, ca se s re cr u it e d fro m t h e h e a lt h fa cilit y will b e fa ir ly re p re se n t a t ive o f a ll c a se s t h a t o c c u r in t h e n e igh b o u r h o o d a n d will n o t re p re se n t a m a jo r so u rce o f selectio n b ia s.
Selection of cases
Ca se s we re c h ild re n u n d e r t wo ye a r s o f a ge seen a t th e ou tp a tien t clin ic of th e Alb er t Sa b in Pe d ia tric Ho sp ita l with a h isto r y o f re sp ira to r y in fe ctio n . Afte r m e d ica l e xa m in a tio n , ch ild re n wit h su sp e ct e d p n e u m o n ia we re su b m it t e d t o a ch e st X-ra y, a n d o n ly th o se p re se n tin g a p u l-m o n a r y in filt ra t e we re in c lu d e d . All X- ra ys we re e xa m in e d b y t h e sa m e p e d ia t r ic ra d io lo -gist . Ch ild re n we re n o t e ligib le fo r t h e st u d y if t h e y p re se n t e d wit h wh e ezin g o r h a d a re ce n t h istory of a sp ira tion of liq u id or a foreign b od y. Also e xc lu d e d we re c h ild re n wit h m e a sle s, sym p t o m a t ic c o n ge n it a l h e a r t d ise a se , c o n -ge n it a l m a lfo r m a t io n , ce re b ra l p a lsy, cyst ic fi-b ro sis, o r AIDS. Fo u r p ercen t o f p o ten tia l ca ses were exclu d ed b y th ese criteria .
Moth ers (or gu a rd ia n s) of th e p oten tia l ca s-e s ws-e rs-e first co n t a ct s-e d a t t h s-e clin ic b s-e fo rs-e t h s-e c h ild wa s su b m it t e d t o a n X- r a y. At t h is t im e th e y we re a ske d to p a rticip a te in th e stu d y. Af-ter th e exclu sion criAf-teria were a p p lied , d eta iled in fo rm a tio n o n p la ce o f re sid e n ce wa s co lle ct-e d . Mo rct-e t h a n 99% o f t h ct-e h o u sct-e s wct-e rct-e lo ca t ct-e d a n d o n ly o n e m o th er refu sed to a llow h er ch ild to p a rticip a te in th e stu d y.
Selection of controls
Co n t r o ls we re c h ild re n re c r u it e d fro m t h e n e igh b o u r h o o d o f t h e c a se s a n d m a t c h e d b y a ge grou p (0 to 5, 6 to 11, a n d 12 to 23 m on th s). Wid e a ge b ra c ke t s we re c h o se n t o fa c ilit a t e m a t c h in g wh ile a llo win g fo r a b r o a d a ge b a l-a n ce, l-a n d d id n o t p re clu d e t h e l-a n l-a lysis o f r isk a sso cia ted with sm a ller a ge in ter va ls. Ch ild ren were n ot eligib le a s con trols if th ey h a d a resp i-ra to r y i-ra te a b ove 50 b rea th s/ m in fo r in fa n ts o r
a b ove 40 b re a t h s/ m in fo r o ld e r ch ild re n , o r if t h e y h a d p re se n t e d sym p t o m s o f m e a sle s o r p e r t u ssis in t h e p re ce d in g t e n d a ys. Ot h e r e x-clu sio n crit e r ia a p p lie d t o ca se se le ct io n we re u sed in th e selection of con trols. In ord er to re-d u ce th e p o ssib ility o f selectio n b ia s, o n ly ch il-d ren wh o wo u lil-d a tten il-d govern m e n t se r vices if t h e y we re se r io u sly ill we re in c lu d e d a s c o n -trols.
Sample size
A t o t a l o f 650 ca se s a n d 650 m a t ch e d co n t r o ls we re re cr u it e d fr o m Ju n e 1989 t o M a y 1990. Th is wa s su fficie n t fo r d e t e ct in g a re la t ive r isk o f 2 wit h 90% p o we r a s sign ific a n t a t t h e 5% level, if th e p reva len ce of exp osu re a m on g con -tro l su b jects ra n ged fro m 4% to 85%.
Data collection
A q u estion n a ire wa s a d m in istered to th e m oth -e r o f -e a c h c a s-e a n d c o n t r o l, o r t o t h -e c h ild ’s n o rm a l gu a rd ia n , a n d in clu d ed in fo rm a tio n o n a n u m b e r o f p o t e n t ia l r isk a n d c o n fo u n d in g fa cto rs, su ch a s b rea st-feed in g, en viro n m e n ta l fa cto rs, in d o o r a ir p o llu tio n , p a ren ta l sm o kin g, so cio eco n o m ic fa cto rs, a n th ro p o m etric sta tu s, d em o gra p h ic fa cto rs, a n d ch ild -ca re p ra ctices. In fo rm ed co n sen t wa s o b ta in ed fro m a ll m o th -e r s b y t h -e fi-e ld wo r k-e r s b -e fo r-e r-e c r u it m -e n t , a n d t h e c o n fid e n t ia lit y o f t h e d a t a c o lle c t e d wa s e n su re d b y u se o f co d e d id e n t ifica t io n fo r t h e su b je c t s. St a n d a rd ize d , p re - c o d e d q u e s-t io n s we re u se d fo r m o ss-t va r ia b le s. Qu a lis-t y o f t h e in fo r m a t io n co lle ct e d b y in t e r vie we rs wa s a sse sse d b y ra n d o m ly re p e a t in g 10% o f t h e q u e st io n n a ire s. Disa gre e m e n t s we re re so lve d by th e p rin cip a l in vestiga tor. Th e d a ta were en -tered in to a n IBM-com p a tib le m icro-com p u ter u sin g Db a seIII+. Ra n ge a n d con sisten cy ch ecks we re ca rr ie d o u t fo r a ll va r ia b le s a n d t h e d a t a we re cle a n e d a n d e d it e d u sin g D b a se III+ a n d SPSS/ PC+.
Analysis
Od d s ra tio s a n d th eir 95% co n fid en ce in ter va ls we re ca lcu la t e d . An a lysis we re ca rr ie d o u t u s-in g Ep i In fo 5.1 a n d Egre t , t a ks-in g s-in t o a cco u n t t h e m a t c h in g o f c a se s a n d c o n t r o ls b y n e igh -b o u rh o o d a n d a ge.
p a irs, th a t is, th e n u m b er of p a irs for wh ich th e ca se wa s exp osed a n d its m a tch ed con tr ols u n -e xp o s-e d , d ivid -e d b y t h -e n u m b -e r o f p a ir s fo r wh ich t h e ca se wa s u n e xp o se d a n d it s co n t ro l e xp o se d (Kirkwo o d , 1988). Two - t a ile d sign ifi-ca n ce tests were u sed .
Fo r risk fa cto rs with se ve ra l e xp o su re ca te -go ries, co n d itio n a l lo gistic regressio n wa s u sed to exa m in e wh eth er th ere wa s a lin ea r tren d o f in cre a sin g r isk o f p n e u m o n ia wit h in cre a sin g le ve l o f e xp o su re, a n d if so, wh e t h e r t h e re wa s a n y evid en ce of d ep a rtu re from lin ea rity in th is t re n d . Co n d it io n a l lo gist ic re gre ssio n wa s a lso u sed to in vestiga te th e effect o f risk fa cto rs, a f-te r co n tro llin g fo r p o f-te n tia l co n fo u n d in g va ri-a b le s (Ro t h m ri-a n , 1986). A st e p wise p ro c e d u re wa s n o t u se d . Ra th e r, se le ctio n o f va ria b le s fo r in clu sio n in t h e m o d e l wa s b a se d o n a n a p r i-o r i c i-o n sid e ra t ii-o n i-o f a like ly lin k b e t we e n d if-fe re n t va r ia b le s a n d o n t h e re su lt s o f t h e u n i-va ria te a n a lyses. Ca se-co n tro l p a irs with m iss-in g iss-in fo rm a tio n fo r th e va ria b le were exclu d e d fro m th e a n a lysis. Fu ll d eta ils o f th e m eth o d o l-o gy e m p ll-oye d h a ve b e e n p r l-ovid e d e lse wh e re ( Victora et a l., 1994; Fon seca et a l., 1996).
Results
Ta b le 1 sh ows t h e r isks a sso cia t e d wit h m o t h -e rs wo rkin g a n d with u s-e o f d a y-ca r-e fa ciliti-e s. Aft e r a d ju st m e n t fo r in co m e a n d le ve l o f e d u -c a t io n o f t h e fa t h e r a n d m o t h e r, t h e re wa s a sign ific a n t lin e a r t re n d (p =0.001) fo r wo r k b y t h e m o t h e r. Ch ild re n o f m o t h e rs wo rkin g o u t -sid e th e h o m e were a t 1.58 tim es h igh er r isk o f h a vin g p n e u m o n ia (CI=1.21, 2.07) t h a n c h il-d re n o f n o n - wo rkin g m o t h e r s, wh ile c h ilil-d re n w h o s e m o t h e r s w o r ke d a t h o m e w e r e a t a n in t e r m e d ia t e risk o f 1.22 (CI= 0.77, 1.91). Th e p ro p o r t io n o f m o t h e r s’ wo r kin g t im e wa s e x-p ressed a s th e to ta l n u m b er o f m o n th s wo rked sin ce t h e ch ild wa s b o r n d ivid e d b y t h e ch ild ’s age. Th ere was a sign ifican t lin ear tren d (p =0.02) with an od d s ratio of 1.76 (CI=1.13, 2.73) for th e h igh est ca tegor y, in wh ich m oth ers h a d worked m o re t h a n 75% o f t h e ch ild ’s life, co m p a re d t o th e b a selin e ca tego ry o f m o th ers wh o were n o t workin g.
Atten d a n ce a t d a y-ca re cen ters wa s a lso a s-so cia t e d wit h in cre a se d r isk. Aft e r a d ju st m e n t fo r se ve ra l so c io e c o n o m ic va r ia b le s, u se o f d a y c a re fa cilit ie s in cre a se d t h e r isk o f p n e u -m o n ia b y 5.22 t i-m e s (CI=2.13, 12.79) a n d t h is wa s st a t ist ica lly h igh ly sign ifica n t (p <0.001). Th e va st m a jo r it y (80%) o f ch ild re n a t t e n d in g d a y-ca re cen ters h a d m o th ers wo rkin g o u tsid e th e h om e.
Tab le 1
Wo rk b y mo the r and use o f d ay-c are fac ilitie s as risk fac to rs fo r c hild ho o d p ne umo nia.
Risk factor O dds ratio (95% CI)
Case s Co ntro ls Unad juste d ** Ad juste d ***
n % n %
Work by mother No 395 60.8 445 68.7 1.00 1.00
Ye s, at ho me 45 6.9 40 6.2 1.27 0.81-1.97 1.22 0.77-1.91 Ye s, o utsid e ho me 210 32.3 163 25.1 1.52 1.17-1.97 1.58 1.21-2.07
LRT* (2d f) 10.24 p = 0.006 11.32 p = 0.003
(tre nd , 1d f) 10.22 p = 0.001 11.30 p < 0.001
Proportion of mother’s No ne 395 61.0 445 68.7 1.00 1.00
working time – % < 25% 72 11.1 69 10.6 1.21 0.84-1.75 1.28 0.88-1.86 25-74% 120 18.5 92 14.2 1.50 1.10-2.05 1.55 1.12-2.14
≥75 61 9.4 42 6.5 1.74 1.12-2.68 1.76 1.13-2.73
LRT* (3d f) 10.89 p = 0.01 11.59 p = 0.009
(tre nd , 1d f) 4.63 p = 0.03 5.60 p = 0.02
Use of day-care facilities No 619 95.2 642 98.8 1.00 1.00
Ye s 31 4.8 8 1.2 4.83 2.01-11.64 5.22 2.13-12.79
LRT* (1d f) 16.45 p < 0.001 17.24 p < 0.001
* Like liho o d ratio te st.
Tab le 2
Numb e r o f c hild re n at ho me as risk fac to rs fo r c hild ho o d p ne umo nia.
Risk factor O dds ratio (95% CI)
Case s Co ntro ls Unad juste d ** Ad juste d ***
n % n %
Total number of 1-2 290 44.6 333 51.2 1.00 1.00
children living at home 3-4 229 35.2 218 33.5 1.22 0.95-1.58 1.17 0.90-1.53
5-6 88 13.5 74 11.4 1.40 0.97-2.02 1.39 0.93-2.10
7+ 43 6.6 25 3.9 2.17 1.23-3.81 2.36 1.26-4.43
LRT* (3d f) 10.30 p = 0.02 8.53 p = 0.04
(tre nd , 1d f) 9.79 p = 0.002 7.52 p = 0.006
N umber of children 1 218 33.5 275 42.3 1.00 1.00
under 6 years of age 2-3 380 58.5 343 52.8 1.43 1.13-1.82 1.35 1.05-1.75
living at home 4+ 52 8.0 32 4.9 2.29 1.36-3.85 2.05 1.17-3.60
LRT* (2d f) 11.55 p = 0.003 8.73 p = 0.01
(tre nd , 1d f) 10.80 p = 0.001 8.60 p = 0.003
N umber of children No ne 316 48.6 373 57.4 1.00 1.00
aged 6 years or more 1-3 279 43.0 237 36.5 1.53 1.17-2.00 1.47 1.14-1.90
living at home 4+ 55 8.5 40 6.2 2.11 1.21-3.68 2.11 1.26-3.55
LRT* (2d f) 5.64 p < 0.001 12.95 p = 0.002
(tre nd , 1d f) 10.98 p < 0.001 12.94 p < 0.001
* Like liho o d ratio te st.
** Base d o n the analysis o f matc he d c ase -c o ntro l se ts.
*** Ad juste d fo r inc o me , e d uc atio n fo r fathe r and mo the r, mo the r’s ag e , and c ro wd ing .
Cru d e a n d a d ju sted a n a lyses of th e a ssocia -t io n b e -t we e n -t h e n u m b e r o f c h ild re n in -t h e h om e an d p n eu m on ia are sh own in Tab le 2. Ad -ju st m e n t fo r c o n fo u n d in g in c lu d e d in c o m e , e d u ca t io n fo r t h e fa t h e r a n d m o t h e r, m o t h e r’s a ge a n d crowd in g, d e fin e d a s t h e m e a n n u m -b er of p eop le p er room .
Th e re wa s a sign ific a n t lin e a r t re n d (p < 0.006) fo r th e to ta l n u m b er o f ch ild ren livin g a t h om e. Ch ild ren from fa m ilies with a tota l n u m -b e r o f 7 o r m o re c h ild re n we re a t 2.36 t im e s h igh e r r isk o f h a vin g p n e u m o n ia (CI=1.26, 4.43) co m p a red with th e b a selin e ca tego ry o f 1 a n d 2 c h ild re n . Ch ild re n wh o se fa m ilie s h a d b etween 5 a n d 6 ch ild ren a n d th o se with 3 a n d 4 ch ild ren h a d a n in term ed ia te risk o f 1.39 a n d 1.17, resp ectively.
Sign ific a n t t re n d s a lso e xist e d wh e n t h e n u m b e r o f c h ild re n we re d ivid e d in t o t h o se a ge d u n d e r six ye a rs livin g a t h o m e a n d t h o se a ge d six ye a r s o r m o re. Ch ild re n wit h t wo t o th ree sib lin gs u n d er six yea rs a n d ch ild ren with 4 o r m o re sib lin gs we re a t 1.35 a n d 2.05 t im e s h igh e r risk o f h a vin g p n e u m o n ia , re sp e ctive ly, t h a n t h o se h a vin g o n ly o n e sib lin g u n d e r six yea rs a t h o m e. Th is tren d wa s sign ifica n t a t th e p =0.003 le ve l. Sim ila rly, th e re wa s a h igh ly sig-n ifica sig-n t lisig-n e a r t re sig-n d (p <0.001) fo r t h e sig-n u m b e r of sib lin gs aged six years or m ore livin g at h om e. Ch ild re n wit h 4 o r m o re sib lin gs a n d ch ild re n with 1 to 3 sib lin gs we re a t 2.11 a n d 1.47 tim e s h igh e r r isk, re sp e c t ive ly, c o m p a re d t o t h o se
with n o sib lin gs aged six years or m ore at h om e. Th e c r u d e a n d a d ju st e d a n a lysis o f t h e p resen ce o f sib lin gs u n d er two yea rs o f a ge liv-in g a t h o m e d id n o t sh ow a sta tistica lly sign ifi-c a n t in ifi-c re a se d r isk o f p n e u m o n ia ( Ta b le 3, p =0.13). Th e to ta l n u m b er o f ch ild ren wa s a lso m o re im p o rt a n t t h a n b irt h o rd e r ( Ta b le 3). Al-t h o u gh Al-t h e re wa s a Al-t re n d o f in cre a sin g r isk o f p n e u m o n ia wit h h igh e r b ir t h o rd e r, ch ild re n h a vin g six o r m o r e yo u n ge r sib lin gs b e in g a t 1.32 t im e s t h e r isk o f fir st - b o r n , t h is wa s n o t st a t ist ica lly sign ifica n t a ft e r a d ju st m e n t fo r co n fo u n d in g va ria b les (p =0.37).
Ta b le 4 sh ows th a t a h igh p rop ortion of ca s-e s (29.8%) a n d c o n t r o ls (24.0%) h a d a t ls-e a st o n e gra n d p a re n t livin g a t h o m e, a n d t h a t t h is wa s sign ific a n t ly a sso c ia t e d wit h p n e u m o n ia (OR=1.40, CI=1.03, 1.89) a ft e r a d ju st m e n t fo r severa l co n fo u n d in g va ria b les, in clu d in g fa m i-ly in co m e, ed u ca tio n o f th e fa th er a n d m o th er, m o t h e r’s a ge, wo rk b y t h e m o t h e r, u se o f d a y-ca re fa cilities, a n d crowd in g.
Discussion
Th is p a p e r e xa m in e s th e re la tio n sh ip b e twe e n several variab les related to ch ild care an d an in creased risk of p n eu m on ia. We fou n d th at m oth er’s p aid em p loym en t ou tsid e th e h ou se was in -d ep en -d en tly a sso cia te-d with th e o ccu rren ce o f p n eu m on ia a fter con trollin g for severa l socioe-c o n o m isocioe-c va r ia b le s. Th is is in a gre e m e n t wit h two re ce n t stu d ie s ca rrie d o u t in So u th Am e ri-c a wh iri-c h a lso fo u n d t h a t ri-c h ild re n o f m o t h e r s workin g ou tsid e th e h om e were at h igh er risk of acu te lower resp iratory in fection . However, n ei-t h e r o f ei-t h e se sei-t u d ie s in clu d e d a d ju sei-t m e n ei-t fo r co n fo u n d in g va r ia b le s (Ce rq u e iro e t a l., 1990; Ho rta l et a l., 1990). We a lso fo u n d th a t ch ild ren wh ose m oth ers h a d worked 75% or m ore of th e t im e sin c e t h e c h ild wa s b o r n we re a t 1.76 (CI=1.13, 2.73) tim es h igh er r isk o f p n eu m o n ia th a n th o se wh o se m o th ers d id n o t wo rk.
It h a s b een su ggested by o th ers th a t th e n e-gle c t o f a yo u n g c h ild d u r in g t h e m o t h e r’s wo rkin g h o u rs m a y b e a fa cto r p red isp o sin g to m a ln u t r it io n (En gle , 1991; En gle & Pe d e r se n , 1989) a n d resp ira to ry in fectio n (Reich en h ein & Ha rp h a m , 1989). It is a lso kn own th a t th e stress an d an xiety for b oth m oth er an d ch ild affect th e ch ild’s im m u n e fu n ction (Gra h a m , 1990). Th u s, b o th stre ss a n d in a p p ro p ria te ch ild -ca re p ra c-tices m a y h a ve a n im p o rta n t ro le in in crea sin g th e risk o f p n eu m o n ia in yo u n g ch ild ren .
At t e n d a n ce a t a d a y ca re ce n t e r wa s fo u n d to b e stron gly a ssocia ted with p n eu m on ia , with a n in crea sed risk o f m o re th a n 5, a fter co n tro l-lin g for in com e a n d p a ren ta l level of ed u ca tion . A re c e n t c a se - c o n t r o l st u d y in ve st iga t e d r isk fa ct o rs fo r ra d io lo gica lly co n fir m e d p n e u m o -n ia i-n t h e gre a t e r m e t r o p o lit a -n a re a o f Po r t o Ale gre, in So u t h e rn Bra sil. Da yca re ce n t e r a t -t e n d a n c e d isp la ye d -t h e h igh e s-t r isk, wi-t h a n
Tab le 3
Numb e r o f sib ling s und e r two ye ars o f ag e living at ho me and b irth o rd e r as risk fac to rs fo r c hild ho o d p ne umo nia.
Risk factor O dds ratio (95% CI)
Case s Co ntro ls Unad juste d ** Ad juste d
n % n %
N umber of siblings No ne 533 82.0 552 85.0 1.00 1.00a
under 2 years of age 1+ 117 18.0 98 15.0 1.31 0.94-1.82 1.30 0.93-1.82
living at home LRT* (1d f) 2.53 p = 0.11 2.31 p = 0.13
Birth order First b o rn 173 26.8 204 32.0 1.00 1.00b
2-3 380 58.5 343 52.8 1.43 1.13-1.82 1.35 1.05-1.75 4-5 108 16.7 106 16.6 1.23 0.87-1.75 1.10 0.73-1.67
6+ 89 13.8 70 11.0 1.53 1.03-2.26 1.32 0.79-2.22
LRT* (3d f) 5.10 p = 0.17 1.95 p = 0.58
(tre nd , 1d f) 4.23 p = 0.04 0.96 p = 0.37
* Like liho o d ratio te st.
** Base d o n the analysis o f matc he d c ase -c o ntro l se ts.
[a] Ad juste d fo r inc o me , e d uc atio n fo r fathe r and mo the r, mo the r’s ag e , and c ro wd ing . [b ] Ad juste d fo r inc o me , e d uc atio n fo r fathe r and mo the r, mo the r’s ag e , numb e r o f c hild re n
living in the ho me , wo rk b y mo the r, use o f d ay-c are fac ilitie s, and c ro wd ing .
Tab le 4
Pre se nc e o f g rand p are nts in the ho use as risk fac to rs fo r c hild ho o d p ne umo nia.
Risk factor O dds ratio (95% CI)
Case s Co ntro ls Unad juste d ** Ad juste d ***
n % n %
Grandparents No 456 70.2 494 76.0 1.00 1.00
living in the home Ye s 194 29.8 156 24.0 1.39 1.07-1.80 1.40 1.03-1.89
LRT* (1d f) 6.20 p = 0.01 4.68 p = 0.03
* Like liho o d ratio te st.
** Base d o n the analysis o f matc he d c ase -c o ntro l se ts.
a d ju st e d o d d s r a t io o f 11.75 ( Vic t o ra e t a l., 1994). Th ese a re th e first two stu d ies from a d eve lo p in g c o u n t r y t o in eve st iga t e t h is a sso c ia -t io n . Mo s-t o f -t h e p re vio u s s-t u d ie s o n d a y-ca re c e n t e r a t t e n d a n c e we re c a r r ie d o u t in d e ve lo p e d clo u n t r ie s a n d flo cu se d lo n u p p e r re sp ira -tory in fection s (Ha skin s & Kotch , 1986). A ca se-co n t ro l st u d y ca r r ie d o u t in t h e U SA re p o r t e d t h a t r isk o f h o sp it a liza t io n fo r ALRI t r ip le d fo r ch ild re n a tte n d in g d a y-ca re ce n te rs co m p a re d to th o se wh o d id n o t, a fter co n tro llin g fo r co n -fou n d in g (An d erson et a l., 1988).
In t h e o r y, a we ll- m a n a ge d se t t in g sh o u ld n ot in crea se th e risk of severe resp ira tory in fec-tio n in a h ea lth y ch ild (Ha skin s & Ko tch , 1986). However, p o o r q u a lity o f ca re wh ich d ep rives a c h ild o f st im u la t io n a n d a ffe c t io n in a sso c ia -t io n wi-t h in c re a se d e xp o su re -t o re sp ira -t o r y p a th o gen s a n d in a p p ro p ria te feed in g p ra ctices m igh t le a d t o a n in c re a se d r isk o f se ve re d is-ea ses su ch a s p n eu m on ia .
In o u r st u d y p o p u la t io n , m o st o f t h e c h il-d re n ca m e fro m ve r y p o o r fa m ilie s, a n il-d a h igh p ro p o rtio n o f th o se a tten d in g d a y-ca re cen ters (80%) h a d m o t h e rs wo rkin g o u t sid e t h e h o u se to su p p lem en t th e fa m ily in co m e. Th e n u m b er o f ch ild re n a t t e n d in g d a y-ca re fa cilit ie s in t h e St a t e o f Ce a rá is in cre a sin g, a n d t h e lo ca l gov-e rn m gov-e n t h a s d gov-e cid gov-e d to d o u b lgov-e th gov-e n u m b gov-e r o f p u b licly fu n d ed cen ters in th e n ext th ree yea rs. Th u s, in fo r m a t io n o n p o ssib le wa ys in wh ic h d a yca re ce n t e rs m igh t b e d e sign e d a n d m a n a ge d t o m in im ize t h e r isk o f p n e u m o n ia is u r -gen tly n eed ed .
Ha vin g m a n y sib lin gs in cre a se d t h e risk o f p n eu m on ia , a fter con trollin g for socioecon om -ic va r ia b le s, m o t h e r’s a ge, a n d crowd in g. Ha v-in g seven o r m o re sib lv-in gs livv-in g a t h o m e m o re th a n d o u b le d th e risk o f p n e u m o n ia . Th is is in a greem en t with fin d in gs fro m p revio u s stu d ies from b oth d evelop ed a n d d evelop in g cou n tries (Cerqu eiro et al., 1990; Gardn er et al., 1984; Leed-e r Leed-e t a l., 1976). It h a s b Leed-e Leed-e n su ggLeed-e st Leed-e d t h a t t h Leed-e p re se n c e o f o t h e r yo u n g c h ild re n m a y c a u se ea rlier a n d m ore in ten se exp osu re to resp ira to-r y p a t h o ge n s ( Vict o to-ra e t a l., 1989). Th is m igh t le a d to a n in cre a se d risk o f a se ve re e p iso d e o f re sp ira t o r y in fe c t io n in c h ild re n , e sp e c ia lly a m on g th ose with m a ln u tr ition (Riley, 1984).
Th e st u d y re su lt s a re c o n sist e n t wit h t h e h yp o t h e sis t h a t fa c t o r s re la t e d t o c h ild c a re m a y h a ve a n im p o r t a n t ro le in t h e o ccu rre n ce of p n eu m on ia in ch ild ren . Th ere is a sm a ll p ro-p o r t io n o f c h ild re n (le ss t h a n 5%) a t t e n d in g d a yca re fa cilit ie s wh e n co m p a re d t o t h e p ro -p o rtio n o f m o th ers in -p a id em -p lo ym en t (m o re t h a n 30%). It is co m m o n p ra ct ice in Fo r t a le za (Fo n se ca e t a l., 1994) a s we ll a s in o t h e r d e ve
l-op in g cou n tries b esid es Bra zil (Cerq u eiro et a l., 1990) t o h a ve gra n d p a re n t s a n d / o r o ld e r sib -lin gs ta kin g ca re o f yo u n ge r ch ild re n wh e n th e m o t h e r is a wa y fr o m h o m e . Bo t h p re se n c e o f gran d p aren ts an d th at of ch ild ren over six yea rs o f a ge we re fo u n d t o b e in d e p e n d e n t r isk fa c-t o rs fo r p n e u m o n ia . Th is is in a gre e m e n c-t wic-t h fin d in gs fr o m p re vio u s st u d ie s o n ALRI fr o m d evelop in g cou n tries (Cerq u eiro et a l., 1990). It is im p orta n t to n ote th a t p resen ce of gra n d p a ren ts wa s fo u n d to b e a sso cia ted with p n eu m o -n ia , a ft e r co -n t ro lli-n g fo r se ve ra l co -n fo u -n d i-n g va r ia b le s, in clu d in g crowd in g. Th is co u ld re p -re se n t so m e b e h a vio ra l c h a ra c t e r ist ic o f e x-t e n d e d fa m ilie s a sso c ia x-t e d wix-t h la x-t e h e a lx-t h (ca re-seekin g).
Aft e r c o n t r o llin g fo r se ve ra l c o n fo u n d in g va r ia b le s, h a vin g a yo u n ge r sib lin g o r b e in g la te in b irth o rd er were n o t a sso cia ted with th e occu rren ce of p n eu m on ia .
References
AH RTAG (Ap p ro p r ia t e He a lt h Re so u rc e s a n d Te c h -n o lo gy Actio -n Gro u p ), 1991. Ch ild h o o d p -n eu m o-n ia ; stra tegies to m eet th e ch a lleo-n ge. Io-n : Proceed -in gs of t h e In t ern a t ion a l Con su lt a t ion on Acu t e Respiratory In fection s, Decem ber 1113, 1991, Wash in gt o n , D C. Lo n d o n : Ap p ro p r ia t e He a lt h Re -sou rces a n d Tech n ology Action Grou p.
AN D ERSON , L. J.; PARKER, R. A.; RAYM ON D, A. S.; FARRAT, J. A.; GAN GAROSA, E. J.; KEYSERLIN G, H . L. & SIKES, R. K., 1988. Da yca re ce n te r a tte n -d a n ce a n -d h o sp it a liza t io n fo r lo we r re sp ir a t o r y tra ct illn ess. Ped iatrics, 82:300-308.
CAMPBELL, H .; BYASS, P.; LAMONT, A. C.; FORGIE, I. M .; O’N EIL, K. P.; LLOYD - EVAN S, N . & GREENWOOD, B. M., 1989. Asse ssm e n t o f clin ica l crit e -r ia fo -r id e n t ifica t io n o f se ve -re a cu t e lowe -r -re sp i-ra tory in fection , Lan cet, 1:297-299.
CERQUEIRO, M. C.; MURTAGH, P.; HALAC, A.; AVILA, M. & WEISSENBACH ER, M., 1990. Ep id em io lo gic risk fa cto rs fo r ch ild ren with a cu te lower resp ira -t o r y -t ra c-t in fe c-t io n in Bu e n o s Aire s, Arge n -t in a : a m a tch ed ca se-co n tro l stu d y. Review s of In fectiou s Diseases, 12(su p p l):1021-1027.
CH AN D RA, R. K., 1991. Mc Co llu m Awa rd Le c t u re. Nu t r it io n a n d im m u n it y: le sso n s fro m t h e p a st a n d n e w in sigh t s in t o t h e fu t u re. Am erican Jou r-n al of Clir-n ical Nu tritior-n, 53:1087-1101.
EN GLE, P. L., 1990. Ca re a n d N u t rit ion : ICN Th em e Pap er. UNICEF. New York, U.S.A. (m im eo.) EN GLE, P. L., 1991. Ma t e r n a l wo rk a n d c h ild - c a re
st ra t e gie s in p e ri- u r b a n Gu a t e m a la : n u t r it io n a l effects. Ch ild Develop m en t, 62:954-965.
EN GLE, P. L. & PED ERSEN , M . E., 1989. Ma t e r n a l wo rk fo r ea rn in g a n d ch ild ren’s n u tritio n a l sta tu s in u rb a n Gu a t e m a la . Ecology of Food a n d N u t ri-tion, 22:211-223.
FON SECA, W.; KIRKWOOD, B.; VICTORA, C. G.; FU CH S, S. R.; FLORES, J. A. & MISAGO, C., 1996. Risk fa cto rs fo r ch ild h o o d p n eu m o n ia a m o n g th e u r b a n p o o r in Fo r t a le za , Bra zil: a c a se - c o n t ro l stu d y.Bu lletin of th e World Health Organ iz ation. (in p ress)
FON SECA, W.; M ISAGO, C. & N ATION S, M ., 1994. Mo t h e rs’ p e rce p t io n o f p n e u m o n ia in Fo r t a le za , Bra zil. (u n p u b lish ed )
GARDNER, G.; FRANK, A. L. & TABER, L. H ., 1984. Effe cts o f so cia l a n d fa m ily fa cto rs o n vira l re sp ira -to r y in fe ctio n s a n d illn e ss in th e first ye a r o f life. Jou rn al of Ep id em iology an d Com m u n ity Health, 38:42-48.
GRAH AM, N. M. H ., 1990. Th e ep id em io lo gy o f a cu te re sp ira t o r y in fe c t io n s in c h ild re n a n d a d u lt s: a glo b a l p e r sp e c t ive. Ep id em iologic Rev iew s, 12: 149-178.
H ASKINS, R. & KOTCH , J., 1986. Da y ca re a n d illn ess: e vid e n c e, c o st , a n d p u b lic p o lic y. Ped ia t rics, 77(su p p l):951-982.
HORTAL, M.; BENITEZ, A.; CONTERA, M.; ETORENA, P.; MON TAN O, A. & MEN Y, D. A., 1990. Co m m u -n ity-b a se d stu d y o f a cu te re sp ira to r y tra ct i-n fe c-tion s in ch ild ren in Uru gu a y. Review s of In fectiou s Diseases, 12(su p p l):966-973.
KIRKWOOD, B. R., 1988. Essen tials of Med ical Statis-tics. Oxford : Bla ckwell Scien tific Pu b lica tion . LEEDER, S.; CORKH ILL, R.; IRWING, L. M., 1976. In
-flu en ce of fa m ily fa ctors in th e in cid en ce of lower re sp ira t o r y illn e ss d u r in g t h e fir st ye a r o f life. British Jou rn al of Preven tive an d Social M ed icin e, 30:203-212.
PELTO, G. H .; CAPACCH IONE, C. M.; LINDSAY, H . A.; BACKSTRAN D, J. R.; CH AVEZ, A. & M EN ESES, L., 1996. Ma t e r n a l h o u se h o ld m a n a ge m e n t a n d ch ild ren’s size in ru ra l Mexico. Social Scien ce an d Med icin e. (in p ress)
PELTO, H . G.; KENDALL, C., 1990.Be h a vio ra l a sp e cts o f a cu te re sp ira to r y in fe ctio n in ch ild re n . In : AL-RI a n d Ch ild Su rv iv a l in Dev elop in g Cou n t ries, p p .145-151. Ba lt im o re : Ed . An n e Ga d o m ski. Th e Joh n s Hop kin s Un iversity.
REICH EN H EIM , M . & H ARPH AM , T., 1989. Ch ild h ealth in a Brazilian sq u atter settlem en t: acu te in -fe c t io n s a n d a sso c ia t e d risk fa c t o r s. Jou rn a l of Trop ical Ped iatrics, 35:315-320.
RILEY, I., 1984. Th e a e tio lo gy o f a cu te re sp ira to r y in -fectio n s in ch ild ren in d evelo p in g co u n tries. Pro-ceed in gs of an In tern ation al Work sh op,p p. 33-41. Syd n ey: Ed . Dou gla s RM a n d Kerby-Ea ton E. RODRIGU ES, L.; KIRKWOOD, B. R., 1990. Ca se co n
-t ro l d e sign s in -t h e s-t u d y o f c o m m o n d ise a se s: Up d a t e s o n t h e d e m ise o f t h e ra re d ise a se a s-su m p tio n a n d th e ch o ice o f sa m p lin g sch em e fo r co n t ro ls. In t ern a t ion a l Jou rn a l of Ep id em iology, 19:205-213.
ROTHMAN, K. J., 1986. Mod ern Ep id em iology. Boston : Little, Brown .
SCH LESSELM AN , J. J., 1982. Ca se- Con t rol St u d ies: Design , Con d u ct, An alysis. New Yo rk: Oxfo rd Un i-versity Press.
U N ICEF, 1989. A sa ú d e d a s c ria n ç a s c e a re n c e s: u m estu d o d e 8.000 fa m ília s. Fo rta leza : UNICEF. (u n -p u b lish ed ).
VICTORA, C. G.; FUCHS, S. C.; FLORES, J. A. C.; FON-SECA, W. & KIRKWOOD, B., 1994. Risk fa cto rs fo r p n eu m o n ia a m o n g ch ild ren in a Bra zilia n Metro -p olita n Area . Ped iatrics, 93:977-985.
VICTORA, C. G.; SMITH, P. G.; BARROS, F. C.; VAUGH-AN , J. P. & FU CH S, S. C., 1989. Risk fa c t o r s fo r d eath s d u e to resp iratory in fection s am on g Brazil-ia n In fa n ts. In tern ation al Jou rn al of Ep id em iolo-gy,18:918-925.
