Anemia and intestinal parasitic infections
in primary school students in Aracaju,
Sergipe, Brazil
Ane mia e p arasito se s inte stinais e m e sc o lare s
d e p rime iro g rau e m Arac aju, Se rg ip e , Brasil
1 Liverp ool Sch ool of Trop ica l M ed icin e. Pem b rok e Pla ce, Liv erp ool L3 5QA, U K.
2 Un iversid ad e Fed eral d e Sergip e, N ú cleo d e Pós- Gra d u a çã o em M ed icin a . Ru a Cla u d io Ba t ist a s/no, sa la 125, 2oa n d a r, Ba irro Sa n a t ório, Ara ca jú , Sergip e, 49060- 100, Bra z il. Reik o Tsu yu ok a 1 J. W en d y Ba iley 1
Alz ira M . d ’Av ila N ery Gu im a rã es 2 Rica rd o Q. Gu rgel 2
Lu is E. Cu ev a s 1
Abstract An em ia is est im at ed t o affect h alf t h e sch oolage ch ild ren an d ad olescen t s in d evelop -in g cou n t ries. Th e m a -in ca u ses a re p a ra sit ic -in fect ion s, m a la ria , a n d low iron -in t a k e. Th is st u d y a im ed t o d escrib e t h e p rev a len ce of a n em ia , p a ra sit ic in fect ion s, a n d n u t rit ion a l st a t u s of ch il-d ren a t t en il-d in g p u blic p rim a ry sch ools in Ara ca ju , N ort h ea st Bra z il. Of 360 st u il-d en t s, 26.7% w ere a n em ic, a n d p rev a len ce w a s h igh er in ch ild ren u n d er 8 a n d ov er 15 yea rs of a ge. Ov era ll p rev a -len ce of i n t est i n a l p a ra si t es w a s 42%, w i t h Asca r is lu m b r ico id e s (28.7%),Tr ich u r is t r ich iu ra
(15.6%), a n d h ook w orm (1.7%) m ost freq u en t ly fou n d . Th ere w a s a n a ssocia t ion b et w een p a ra -sit ic in fect ion s a n d p oor sa n it a ry con d it ion s, b u t t h ere w a s n o a ssocia t ion b et w een a n em ia a n d p resen ce of in t est in al p arasit es. Heigh t -for-age Z scores w ere low er t h an t h e N CHS st an d ard , an d p revalen ce of st u n t in g w as 5.4%. Alt h ou gh in t est in al p arasit es w ere n ot associat ed w it h an em ia, ch ild ren w it h p arasit es h ad low er n u t rit ion al in d ices (w eigh t - an d h eigh t -for-age Z scores) t h an t h ose w it h ou t p arasit es.
Key words An em ia; Parasit es; N u t rit ion al St at u s; An t h rop om et ry; Sch ool Healt h
Resumo Est im a - se q u e a a n em ia a fet a m et a d e d os escola res e a d olescen t es n os p a íses em d e-sen v olv im en t o. As p rin cip a is ca u sa s sã o en t erop a ra sit oses, m a lá ria e/ou b a ix a in gest a d e ferro. Est e est u d o objet ivou d escrever a p revalên cia d e an em ia e d e en t erop arasit oses, assim com o o es-t a d o n u es-t ricion a l d e escola res d e p rim eiro gra u d e escola s p ú b lica s m u n icip a is d e Ara ca ju , SE, Bra sil. Dos 360 est u d a n t es, 26,7% est a v a m a n êm icos, sen d o a p rev a lên cia m a ior n os m en ores d e oit o a n os e n os m a iores d e 15. A p rev a lên cia gera l d e en t erop a ra sit oses foi d e 42%.Asca ris lu m
-b rico id e s(28,7%),Trich u ris trich iu ra(15,6%) e a n cilost om íd eos (1,7%) est a v a m en t re os m a is freq ü en t em en t e en con t ra d os. Hou v e a ssocia çã o en t re en t erop a ra sit ose e m á con d içã o d e sa n ea -m en to, -m as n ão en tre an e-m ia e p resen ça d e en terop arasitos. Os escores d e d esvio p ad rão (Z-scores) d e a lt u ra p a ra id a d e fora m in feriores a os p a d rões d o N CHS, com p rev a lên cia d e 5,4% d e d esn u -t riçã o p regressa (stu n tin g). Ap esa r d e a s en t erop a ra sit oses n ã o t erem sid o a ssocia d a s com a n e-m ia, as crian ças qu e t in h ae-m p arasit as ao ex ae-m e ap resen t avae-m p ior est ad o n u t ricion al (p eso/al-t u ra) qu e aqu elas cu jos ex am es resu leso/al-t aram n egaeso/al-t ivos.
Introduction
An em ia is th e m ost com m on m an ifestation of d isease ob served in th e trop ics. Iron d eficien -cy an em ia affects ab ou t 1.3 b illion p eop le, with th e h igh est p revalen ce an d m orb id ity in you n g ch ild ren an d p regn an t wom en (Gillesp ie et al., 1991). It is estim ated th at u p to h alf of sch ool-a ge ch ild ren in d evelo p in g co u n tries ool-a re ool-a n em ic (De Ma e ye r e t a l., 1989). An e em ia in in -fan ts an d ch ild ren is associated with in creased m ortality (Stoltzfu s, 1997), growth retard ation (An geles et al., 1993), d elayed m otor d evelop -m en t, p oor cogn itive ab ilities ( Watkin s &a-mp; Pol-litt, 1998), red u ced sch ool p erform an ce (Lozoff et al., 1991), an d an im p aired im m u n e system (Dallm an , 1987).
Sch oolch ild ren are an easily id en tified tar-get grou p, an d sch ools cou ld b e u sed as a d is-trib u tio n system fo r p u b lic h ea lth . However, in terven tion s m u st b e b ased on ep id em iologi-ca l in fo rm a tio n co n cern in g th e m a in lo iologi-ca l ca u ses o f a n em ia . Mo st La tin Am erica co u n -tries lack su ch in form ation , an d th e Pan -Am er-ica n Hea lth Orga n iza tio n o f th e Wo rld Hea lth Organ ization (PAHO/ WHO) h as p rop osed col-lectin g th e n ecessary in form ation (Freire, 1997). Th is stu d y a im ed to esta b lish th e p reva len ce o f a n em ia , in testin a l p a ra sites, a n d n u -tritio n a l sta tu s o f ch ild ren a tten d in g p rim a r y sch ools in Aracaju , Brazil.
M aterials and methods
Th is was a crosssection al d escrip tive stu d y in -volvin g p u b lic p rim ary sch ool stu d en ts in Ara-ca ju , Sergip e, No rth ea st Bra zil. Ara Ara-ca ju h a s a tro p ica l clim a te with tem p era tu res ra n gin g from 20 to 30oC. Eigh ty p ercen t of Aracaju’s 200 p rim a r y sch o o ls a re p u b lic a n d 20% p riva te (Fap ese, 1996). On e p u b lic sch ool was ran d om -ly selected fo r ea ch o f th e 5 u rb a n h ea lth d is-tricts, a n d th e stu d en ts were selected b y a ge grou p (<8, 9 to 11, 12 to 14, an d >15 years). All stu d en ts a tten d in g d u rin g a n o rm a l wo rkin g d ay in th e selected sch ools were en rolled . Data were collected d u rin g Ap ril an d May 1998.
Th e estim ated sam p le size to estab lish th e p reva len ce of a n em ia a n d in testin a l p a ra sites wa s 81 stu d en ts p er a ge gro u p, a ssu m in g th a t th e p reva len ce of a n em ia a n d in testin a l p a ra -sites wa s 30% with a p recisio n o f ± 10%. Th is sam p le size was in creased to 90 p er age grou p to allow for a 10% d rop ou t.
In terviews were p erform ed by local n u rsin g an d m ed ical stu d en ts u n d er th e su p ervision of th e p rin cip a l in vestiga to r (R. T.) to o b ta in in
-form ation on san itary con d ition s at h om e, p ast an d p resen t illn esses, an d p aren ts’ ed u cation . Paren ts’ ed u cation was grou p ed in to com p lete or in com p lete p rim ary ed u cation . Weigh t was m ea su red u sin g a sta n d in g sca le a n d h eigh t wa s o b ta in ed u sin g a p a p er sta d io m eter a t-tach ed to a straigh t wall.
Blo o d sa m p les were co llected b y fin ger p rick. Hem o glo b in co n cen tra tio n wa s d eter-m in ed by th e Heeter-m oCu e b lood Hb systeeter-m (He-m o Cu e Ltd , Sch effield , UK) a n d He(He-m a to crit was m easu red u sin g h ep arin ized m icro-h em a-tocrit tu b es an d a m icro-h em aa-tocrit cen trifu ge (Am es Ltd , Bed ford sh ire, UK). Th in b lood film s were fixed an d stain ed with Leish m an’s stain for th e p resen ce o f m icro cytic a n d h yp o ch ro m ic an em ia an d to exclu d e sicklcell an em ia. An e-m ia wa s d efin ed a s a h ee-m o glo b in o f less th a n 110 g/ l for ch ild ren u n d er 6 years old , less th an 120g/ l for m ale an d fem ale ch ild ren b etween 6-14 years of age an d fem ales over 15 year of age, a n d less th a n 130 g/ l in b oys over 15 yea rs o f age accord in g to th e WHO d efin ition of an em ia (DeMaeyer, 1985). Mean corp u scu lar h em oglo-bin con cen tration (MCHC) was calcu lated from th e h em oglob in an d h em atocrit. Defin ite iron d eficien cy an em ia was d efin ed as a MCHC b e-low 30% in th e p resen ce o f m icro cyto sis a n d h yp och rom ia . An MCHC b etween 30 a n d 32% in th e p resen ce of low h em oglob in was con sid -ered a p ossib le case of iron d eficien cy.
Sto o l co n ta in ers were d istrib u ted th e d a y b efo re th e su r vey to o b ta in a feca l sa m p le. Sam p les were fixed th e sam e d ay with 10% for-m ol - salin e an d th e volu for-m etric con cen tration tech n iqu e was u sed th e followin g d ay. All p ara-site ova a n d cysts seen o n x10 a n d x40 m i-croscopy were record ed . Th e n u m b er of h ook-wo rm ova were co u n ted a n d exp ressed a s n u m b er of eggs p er gram s (ep g) of feces as d escrib ed by Ash ford et al. (1992). A ran d om sam -p le of 10% of b lood film s an d stools were reex-am in ed in Liverp ool for qu ality con trol.
Data were an alyzed u sin g Ep i-In fo Version 6 (De a n e t a l., 1995) t o ca lcu la t e t h e p re va -le n ce o f a n e m ia a n d p a ra sit e s. Ch i-sq u a re d a n d ch i-sq u a re d fo r t re n d we re u se d t o t e st d iffe re n ce s o f d iscre t e va ria b le s a n d t re n d s. Co m p a riso n o f n u t rit io n a l st a t u s o f t h e ch il-d re n t o t h e NCH S re fe re n ce p o p u la t io n wa s p e rfo rm e d u sin g t h e Ep in u t p ro gra m wit h in Ep iIn fo. Wastin g, stu n tin g, an d m ixed m aln u -trition were defin ed as a score below -2 Z-scores o f we igh t / h e igh t ( WH Z), h e igh t / a ge (H AZ), an d weigh t/ age (WAZ), resp ectively.
in fectio n s. Sch o o l sta ff were in fo rm ed o f a n y ca se o f m o d era te o r severe a n em ia a n d sch is-to so m ia sis. In fo rm ed co n sen t wa s o b ta in ed fro m p a ren ts o f p a rticip a tin g ch ild ren . Th is stu d y was ap p roved by th e Liverp ool Sch ool of Trop ical Med icin e Research Eth ics Com m ittee an d th e Federal Un iversity of Sergip e p ost-grad-u ate research com m ittee.
Results
Th ree h u n d red a n d sixty stu d en ts were en rolled. Th ree h u n dred an d fiftyfou r blood sam -p les (98.3%) were collected from th e stu d en ts. Th e a ge d istrib u tio n wa s 4 to 24 yea rs. On e h u n d red an d eigh t stu d en ts were u n d er 8 years old , 124 were 9 to 11 years old , 85 were 12 to 14 yea rs o ld , a n d 43 over 15 yea rs o ld . On e h u n -d re-d a n -d seven ty-o n e (47.5%) were m a le a n -d 189 (52.5%) fem ale.
Th e m ea n (SD) h em o glo b in wa s 129 g/ l (1.26) with a ran ge b etween 88 g/ l an d 171 g/ l. Nin ety-o n e ch ild ren (26.7%) h a d a n em ia a c-cord in g to th e WHO d efin ition , with 19 (20.8%) h a vin g a h em o glo b in <110 g/ l. MCH C wa s availab le for 320 of th e stu d en ts. Th e MCHC of 11 (12.1%) o u t o f th e 91 a n em ic stu d en ts wa s b elow 30%, a n d 20 (22%) were m icrocytic a n d h yp och rom ic. Seven (7.7%) of th e an em ic stu -d en ts h a -d iro n -d eficien cy a n em ia b y MCH C an d m icrocytic fin din gs. Th e MCHC of a fu rth er 27 of th e 91 an em ic stu d en ts was b etween 30% a n d 32%, a n d th ey were su sp ected o f h a vin g iron deficien cy an em ia. No m acrocytosis or ob-viou s h yp er-segm en ted n eu trop h ils were seen , an d n on e of th e sam p les sh owed h yp och rom ia o r n u m ero u s ta rget cells. All h yp o ch ro m ic o r
m icro cytic sa m p les were a n em ic. Th ere were n o ca ses o f sickle-cell a n em ia . Th e h igh est p revalen ce of an em ia (35.7%) was ob served in teen a gers over 15 yea rs a n d ch ild ren u n d er 8 (35.4%) a s sh own in Figu re 1. Th ere wa s a sta tistica lly sign ifica n t d ifferen ce in th e p reva -len ce of an em ia by age (p < 0.05) b u t n ot by sex or p aren ts’ ed u cation (d ata n ot sh own ).
On e h u n d red an d fifty-two (42%) of th e 360 stool sam p les h ad at least on e p arasite; 30.3% o f t h e sa m p le s h a d o n ly o n e p a ra sit e, 9.2% h ad 2 p arasites, 2.5% h ad 3, an d on ly 0.3% h ad 4 or m ore. Th e p revalen ce of p arasite ova by age is sh own in Ta b le 1. Old er stu d en ts seem ed to h ave a h igh er p revalen ce, b u t th is was n ot sta-tistically sign ifican t (χ2for tren d p > 0.05), an d
Giard ia lam bliawas m ore p revalen t in ch ild ren
u n d er 8 a n d over 15 yea rs o f a ge th a n in ch
il-Fig ure 1
Pre vale nc e o f anae mia b y ag e .
0
p
re
v
a
le
n
c
e
(
%
)
10 20 30 40 50 60
< 08 9-11 12-14 > 15 ag e (ye ars)
e rro r b ar = 95% C.I.
Tab le 1
Pre vale nc e o f p arasite s b y ag e g ro up .
Parasites Age group
< 8 9-11 12-14 15 < To tal
n = 108 (% ) n = 124 (% ) n = 85 (% ) n = 43 (% ) n = 360 (% )
Ho o kwo rm 5 (4.6) 8 (6.5) 6 (7.1) 4 (9.3) 23 (6.4)
Sc histo so ma manso ni 3 (2.8) 1 (0.8) 1 (1.2) 1 (2.3) 6 (1.7)
Tric huris tric hiura 18 (16.7) 20 (16.1) 13 (15.3) 5 (11.6) 56 (15.6)
Asc aris lumb ric o ide s 28 (25.9) 32 (25.8) 26 (30.6) 17 (39.5) 103 (28.7)
Hyme no le p sis nana 3 (2.8) 4 (3.2) 3 (3.5) 1 (2.3) 11 (3.0)
Ente ro b ius ve rmic ularis 1 (0.9) 1 (0.8) 3 (3.5) 0 (0) 5 (1.4)
Entamo e b a histo lytic a 26 (24.1) 14 (11.3) 16 (18.8) 6 (14.0) 62 (17.2)
G iardia lamb lia 20 (18.5) 9 (7.3) 4 (4.7) 5 (11.6) 38 (10.6)
d ren 9-11 a n d 12-14 yea rs o ld (p < 0.01). Dis-trict 1 h a d th e h igh est p reva len ce o f Asca ris lu m b ricoid es(39.4%), fo llowed b y d istricts 5 a n d 4 (p = 0.04). Sim ila rly, Trich u ris t rich iu ra
wa s fo u n d m o st co m m o n ly in d istrict 1 (30.9%), followed by d istricts 2 an d 4 (p < 0.01). Th ere wa s n o sign ifica n t d ifferen ce b etween d istricts fo r th e o th er p a ra sites. Th ere wa s n o rela tio n sh ip b etween p reva len ce o f p a ra site ova an d p aren ts’ ed u cation (p > 0.05). Stu d en ts wh o h a d n o to ilet o r h a d a p it la trin e h a d a h igh er p reva len ce o f p a ra site ova th a n th o se wh o h ad a toilet, as sh own in Figu re 2 (p < 0.01). Preva len ce o f T. t rich iu raa n d A. lu m b ricoid es
wa s h igh er in stu d en ts wh o h a d n o to ilet o r a p it la trin e (p < 0.01). However, p reva len ce o f oth er ova an d cysts was n ot related to th e avail-ab ility of a toilet. Th ere was n o sign ifican t d if-feren ce b etween th e m a in so u rce o f d rin kin g water an d p arasites.
Ta b le 2 d escrib es th e p reva len ce o f p a ra -sites b y th e p resen ce o r a b sen ce o f a n em ia . Th ere wa s n o a sso cia tio n b etween th e p res-en ce of p arasites an d an em ia.
Prevalen ce of stu n tin g, wastin g, an d m ixed m aln u trition (HAZ, WHZ, WAZ) was 5.4%, 2.5%, an d 4.4% resp ectively. Th ere were n o sign ifican t d ifferen ces in HAZ, HWZ, WAZ b etween th ose with a n d with o u t a n em ia . On th e o th er h a n d , H AZ (SD) fo r th o se with a n d with o u t h o o k-worm was -0.935 (1.032) an d -0.212 (1.117), re-sp ectively (p < 0.05), a n d fo r th o se with a n d with ou t Hym en olep sis n an awas -1.106 (1.215)
a n d -0.230 (1.112), resp ectively, a s sh own in Ta b le 3 (p < 0.05). WAZ (SD) fo r stu d en ts with an d with ou t h ookworm was -0.937 (1.102) an d -0.223 (1.124), re sp e ct ive ly (p < 0.05). Sim
i-la rly, t h e d iffe re n ce b e t we e n t h o se wit h a n d wit h o u t T. t rich iu rawa s st a t ist ica lly sign
ifi-ca n t (-0.610 (0.853) an d -0.202 (1.170) resp ec-tively) (p < 0.05).
Discussion
It is estim a ted th a t p reva len ce o f a n em ia a m o n g ch ild ren a ged 6-12 yea rs in tro p ica l So u th Am erica is 24% (DeMa eyer, 1985). Ou r fin d in g, a 26.7% p revalen ce rate for an em ia in Aracaju’s p u b lic p rim ary sch ool stu d en ts, is in a greem en t with th is figu re. Iro n d eficien cy a n em ia wa s p resen t in 41.7% o f th e ch ild ren with an em ia, alth ou gh th is is d ifficu lt to assess wh en an em ia is m ild . Mean cell volu m e, seru m ferritin , seru m iron , an d total iron b in d in g ca-p a city wo u ld h elca-p to co n firm iro n d eficien cy a n em ia , b u t th is wa s n o t p o ssib le given th e sm all b lood volu m e taken .
Preva len ce o f a n em ia is h igh er in th e yo u n gest a n d o ld est ch ild ren (<8 a n d >15). Presch o o l ch ild ren a n d a d o lescen ts d u rin g growth sp u rts h a ve th e grea test p h ysio lo gica l d em an d s for iron an d are at th e h igh est risk of iron d eficien cy an em ia (Viteri, 1997). Men stru -a tin g girls -a lso h -a ve h igh er d em -a n d s fo r iro n ; h owever, ou r teen agers h ad sim ilar Hb levels in b oth sexes.
Preva len ce o f a n em ia in 1996 wa s 47.1% a m o n g 1,909 stu d en ts u n d er 8 yea rs o f a ge in th e city’s sch ools (Fap ese, 1996). Prevalen ce of an em ia in ou r ch ild ren from th is age grou p was 35.4% (p = 0.02). Th is m ay b e d u e to th e season o f th e stu d y a n d th e ch a ra cteristics o f th e sch o o ls selected , sin ce th e Fa p ese stu d y in clu ded 4 sch ools from th e ru ral area. Both stu d -ies sh owed th at th ere were n o statistically sig-n ifica sig-n t d ifferesig-n ces isig-n th e p reva lesig-n ce o f a sig-n e-m ia by sex or d istrict.
Th e overa ll p reva len ce o f p a ra site ova wa s 42%, with A. lu m b ricoid es, T. t rich iu ra, a n d h o o kwo rm th e b ein g m o st freq u en tly reco rd -ed . Wo rld wid e, A. lu m b ricoid es, T. t rich iu ra,
a n d h o o kwo rm a re th e m o st p reva len t p a ra -sites, with h o o kwo rm b ein g m o re co m m o n th a n T. t rich iu ra ( Wa rren et a l., 1993). In th e Fap ese stu d y, 88.3% of th e stu d en ts were p osi-tive for at least on e p arasite (Fap ese, 1996). Th e h igh est p reva len ce wa s fo r A. lu m b ricoid es
(66.7%) fo llowed b y T. t rich iu ra(17.7%) a n d h ookworm (9.5%).
We u sed co n cen tra tio n m eth o d s a n d ra n -d om qu ality con trol ch ecks to con firm th at th e p revalen ce of p arasites in ou r ch ild ren was re-liab le. Fu rth erm ore, water an d san itation ser-vices h a ve im p roved in th e la st few yea rs, a l-Fig ure 2
Typ e o f to ile t and p arasitic o va.
0
%
w
it
h
p
a
ra
s
it
e
s
20 40 60 80 100
no ne p it latrine witho ut flush with flush typ e o f to ile t
Tab le 2
Ratio o f ane mia amo ng tho se with and witho ut p arasite s.
Anemic students*(n = 91) N on-anemic students (n = 250)
p o sitive (% ) ne g ative p o sitive (% ) ne g ative
Ho o kwo rm 6 (6.6) 85 17 (6.8) 233
S. manso ni 3 (3.2) 88 3 (1.2) 247
T. tric hiura 17 (18.7) 74 37 (14.8) 213
E. histo lytic a 14 (15.4) 77 43 (17.2) 207
Ho o kwo rm + T. tric hiura 4 (4.4) 87 8 (3.2) 242
Ho o kwo rm + E. histo lytic a 1 (1.1) 90 2 (0.8) 248
T. tric hiura + E. histo lytic a 2 (2.2) 89 3 (1.2) 247
p > 0.05
* Ac c o rd ing to WHO d e finitio n, se e me tho d s.
Tab le 3
Z sc o re s o f he ig ht-fo r-ag e , we ig ht-fo r-he ig ht, and we ig ht-fo r-ag e b y ane mia and p arasite s.
Height for Age Weight for Height Weight for Age
Me an (SD) Z sc o re n< -2Z sc o re s/ n (%)• Me an (SD) Z sc o re n< -2Z sc o re s/ n (%)• Me an (SD) Z sc o re n< -2Z sc o re s/ n (%)•
Anaemia -0.331 (1.150)* 5 / 89 (5.6) -0.290 (1.067) 1 / 52 (1.9) -0.333 (1.028)* 4 / 89 (4.5)
N o anaemia -0.232 (1.117)* 14 / 262 (5.3) -0.042 (1.390) 8 / 129 (6.2) -0.245 (1.169)* 12 / 262 (4.6)
Hookworm
p o sitive -0.935 (1.032)* 4 / 22 (18.2) -0.559 (1.418) 1 / 10 (10.0) -0.937 (1.102)* 6 / 22 (27.3) ne g ative -0.212 (1.117)*† 15 / 329 (4.6) -0.087 (1.300) 8 / 171 (4.7) -0.223 (1.124)* 10 / 329 (3.0)
S. mansoni
p o sitive 0.153 (0.793) 0 / 6 (0) -1.287 (0.662) 0 / 3 (0) -0.682 (0.713) 0 / 6 (0)
ne g ative -0.265 (1.129)* 19 / 345 (5.5) -0.093 (1.307) 9 / 178 (5.1) -0.260 (1.139)* 16 / 345 (4.6)
T. trichiuria
p o sitive -0.400 (1.013)* 4 / 56 (7.1) -0.403 (0.997) 2 / 28 (7.1) -0.610 (0.853)* 5 / 56 (8.9) ne g ative -0.230 (1.144)* 15 / 295 (5.1) -0.060 (1.352) 7 / 153 (4.6) -0.202 (1.170)* 11 / 295 (3.7)
A. lumbricoides
p o sitive -0.260 (1.100)* 7 / 100 (7.0) -0.292 (1.259) 3 / 46 (6.5) -0.401 (1.049)* 6 / 100 (6.0) ne g ative -0.256 (1.136)* 12 / 251 (4.8) -0.052 (1.322) 6 / 135 (4.4) -0.214 (1.164)* 10 / 251 (4.0)
H. nana
p o sitive -1.106 (1.215)* 3 / 11 (27.3) 0.185 (1.849) 1 / 6 (16.7) -0.675 (1.465) 2 / 11 (18.2) ne g ative -0.230 (1.112)*† 16 / 340 (4.7) -0.123 (1.291) 8 / 175 (4.6) -0.254 (1.122)* 14 / 340 (4.1)
E. vermicularis
p o sitive -0.810 (0.210)* 0 / 5 (0) 0.635 (0.813) 0 / 2 (0) -0.322 (0.617) 0 / 5 (0)
ne g ative -0.249 (1.130)* 19 / 346 (5.5) -0.121 (1.311) 9 / 179 (5.0) -0.267 (1.140)* 16 / 346 (4.6)
E. histolytica
p o sitive -0.242 (1.128) 1 / 61 (1.6) -0.376 (1.134) 3 / 34 (8.8) -0.374 (1.004)* 3 / 61 (4.9) ne g ative -0.261 (1.125)* 18 / 290 (6.2) -0.052 (1.340) 6 / 147 (4.1) -0.245 (1.160)* 13 / 290 (4.5)
G. lamblia
p o sitive -0.514 (1.139)* 2 / 38 (5.3) 0.090 (1.591) 1 / 25 (4.0) -0.243 (1.365) 2 / 38 (5.3) ne g ative -0.226 (1.120)* 17 / 313 (5.4) -0.146 (1.259) 8 / 156 (5.1) -0.270 (1.105)* 14 / 313 (4.5)
* p < 0.05 whe n c o mp are d to the NCHS stand ard .
†p < 0.05 whe n c hild re n with and witho ut the p arasite s are c o mp are d .
th o u gh th is is u n likely to exp la in th e lower p revalen ce in ou r stu d y. Th e h igh er p revalen ce in 1996 was likely d u e to th e h igh est p revalen ce o f A. lu m b ricoid esin th e 4 sch o o ls fro m ru ra l areas an d th e age d istrib u tion of th e stu d en ts, sin ce p revalen ce of p arasites is often agerelated . Bo th stu d ies sh owagerelated a h o o kwo rm p reva -len ce b elow 10% a n d lower th a n th a t o f T. trich iu ra. A stu d y in 1991 an d 1992 sh owed th at
p revalen ce rates for A. lu m bricoid es, T. trich iu -ra, En t a m oeb a h ist olyt ica, a n d G. la m b liain ch ild ren o f low so cio eco n o m ic cla ss (30%, 36.7%, 40%, a n d 63.3%, resp ectively) were h igh er th a n th o se o f wea lth y ch ild ren (3.3%, 13.3%, 3.3%, an d 50%, resp ectively) (Pereira d e Agu iar et al., 1997).
Th ere were o n ly 6 ca ses o f Sch ist osom a m a n son i (1.7%). Th is is in a greem en t with
Pereira d e Agu ia r et a l. (1997), wh o sh owed a p revalen ce of 1.8% in th e region . It is n ot com -m o n fo r sch o o lch ild ren in Ara ca ju to p la y in th e river or p on d s, an d u rb an d wellers h ave lit-tle exp osu re to in fection .
Ch ild ren u su a lly b eco m e in fected with h o o kwo rm , T. t rich iu ra, a n d A. lu m b ricoid es
from 6-12 m on th s to 3 years of age (Kigh tlin ger et a l., 1995), a n d h o o kwo rm a n d A. lu m b ri-coid esin fection s in crease with age, reach in g a p lateau in late ad olescen ce an d 4 to 10 years of age, resp ectively (An d erson , 1986; Stoltzfu s et al., 1997a). Th e p revalen ce of a p arasitic in fec-tion in ou r stu d en ts in creased with age.
Th e m a jo rity o f stu d en ts rep o rted h a vin g a flu sh to ilet (69.4%) a n d a ccess to ta p wa ter (88.1%) a t h o m e. Th e a va ila b ility o f to ilets va ries a m o n g th e city’s n eigh b o rh o o d s. Stu -d en ts wh o h a -d n o to ilet o r o n ly a p it la trin e were m ore likely to b e in fected with p arasites. Ch ild ren from d istrict 1 h ad b oth less access to toilets an d th e h igh est p arasite p revalen ce.
We co u ld n o t d em o n stra te a n a sso cia tio n b etween p rotozoan cysts an d th e typ e of d rin k-in g wa ter, sim ila r to Pereira d e Agu ia r et a l. (1997), wh o rep orted th at th ere was n o associ-ation b etween G. lam bliaan d d rin kin g water.
Th e illitera cy ra te (7.2% o f th e fa th ers a n d 7.8% of th e m oth ers) was lower th an th e rep ort-ed illitera cy ra te in th e No rth ea st a s a wh o le (30.5%) (IBGE, 1997). However, th e m ajority of th e p aren ts h ad n ot com p leted p rim ary sch ool. It was exp ected th at th ere wou ld b e a relation -sh ip b etween th e p aren ts’ ed u cation an d an e-m ia or p arasitic in fection , b u t we were u n ab le to con firm th is.
Ho o kwo rm is a n im p o rta n t ca u se o f a n e-m ia wo rld wid e. Ro ch e &ae-mp; La yrisse (1966) a n d Pritch a rd et a l. (1991) rep o rted a sign ifica n t n ega tive co rrela tio n b etween p la sm a ferritin
levels a n d h o o kwo rm lo a d . Wh eth er o r n o t a p erson with h ookworm in fection develop s an e-m ia d ep en d s o n th e wo re-m sp ecies a n d lo a d , d u ration of in fection , b od y iron stores, d ietary in take an d ab sorp tion , an d p h ysiological iron requ irem en ts. A low h ookworm load can cau se a n em ia in p eo p le wh o se in ta ke o f iro n is low a n d wh o se iro n sto res a re a lrea d y d ep leted (Pa wlowski e t a l., 1991). On t h e o t h e r h a n d , Mich a e lse n (1985) re p o rt e d t h a t h o o kwo rm d id n o t ca u se se ve re a n e m ia in in fe cte d ch il-d re n in Bo tswa n a , e ve n in ch ilil-d re n with h igh wo rm lo a d s, b u t m o st in fe ct io n s we re ligh t an d a h igh iron in take was availab le. Th ere was n o a sso cia t io n b e t we e n a n e m ia a n d h o o k-worm , S. m an son i, or T. trich iu rain fection s in ou r stu d y, an d all p ositive cases of h ookworm h a d le ss t h a n 1,300 h o o kwo rm e p g o f fe ce s, wh ich m a y n o t ca u se su fficie n t b lo o d lo ss t o cau se an em ia.
Rob ertson et a l. (1992), rep orted th a t ch il-d ren with co n co m ita n t T. t rich iu raa n d h o o
k-worm in fection s h ave lower b lood h em oglob in levels th an ch ild ren with n eith er or on ly on e of th ese p a ra sites. E. h ist olyt icah a s b een kn own
to aggravate trichuriasis sym p tom s an d to cau se d ysen teric syn d rom e (Gilm an et al., 1976). We were u n ab le to d em on strate an y ad d itive effect of con com itan t in fection s b etween h ookworm ,
T. trich iu ra, or E. h istolytica.
Th e m ea n H AZ a n d WAZ sco re fo r Ara ca ju stu d en ts was lower th an th ose of th e NCHS ref-eren ce. In 1996, 11% a n d 5.9% o f th e ch ild ren h a d a H AZ a n d WAZ < -2SD, resp ectively (Fap ese, 1996).
An em ia ca n b e a ca u se o f growth reta rd a -tion (An geles et al., 1993; Stoltzfu s et al., 1997b). However, th ere wa s n o a sso cia tio n b etween ch ild ren with p oor n u trition al statu s an d an e-m ia . Mo st stu d y p o p u la tio n s h a ve h a d lower h em o glo b in levels th a n o u rs. Fo r exa m p le, Sto ltzfu s et a l. (1997b ) sh owed th a t 62.3% o f th e ch ild ren in Pem b a Isla n d , Ta n za n ia , h a d less th an 110 g/ l an d in Jakarta, In d on esia, on ly ch ild ren with Hb levels b etween 80 an d 110 g/ l were selected (An geles, 1993).
A sta tistica lly sign ifica n t d ifferen ce wa s sh own in H AZ a n d WAZ b etween th o se with an d with ou t h ookworm in fection , an d in WAZ b etween th o se with a n d with o u t T. t rich iu ra.
Ho o kwo rm , T. t rich iu ra, a n d A. lu m b ricoid es
an tagon ize th e ch ild’s n u trition al state th rou gh m alab sorp tion , n u trien t loss, altered m etab o-lism , a n d d im in ish ed a p p etite (Co o p er et a l., 1992; Step h en son , 1994). Callen d er et al. (1994) rep orted th at T. trich iu racau sed m ore stu n tin g th an wastin g. H. n an ash owed a statistically
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Acknowledgments
We th a n k th e o ffice o f th e Min istr y o f Ed u ca tio n in Sergip e fo r its su p p o rt a n d th e sch o o lch ild ren a n d teach ers for th eir coop eration . Ou r sp ecial gratitu d e t o Ms. C. Olive ira Ro d rigu e s d e Me n d o n ça , Ms. J. Correa d a Silva, Ms. F. Freire Feitosa, Ms. E Plech , an d Ms. A. D. d a Co sta Pereira , stu d en ts o f th e Fed era l Un iversity o f Sergip e, fo r th eir en th u sia stic a ssis-tan ce, esp ecially in gath erin g d ata in th e sch ools.
Th is stu d y was su b m itted by R.T. as a th esis to ob -tain a Master of Trop ical Med icin e d egree at th e erp ool Sch ool of Trop ical Med icin e, Un iversity of Liv-erp ool.
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