R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 (1 ) : 1 3 - 2 0 , j a n - m a r , 1 9 9 2
T H E I N F L U E N C E O F T H E R E G IO N A L B A S IC D IE T F R O M N O R T H E A S T B R A Z IL O N H E A L T H A N D N U T R I T I O N A L C O N D IT IO N S O F M IC E I N F E C T E D W IT H S C H I S T O S O M A
M A N S O N I .
E rid a n M . C outinho, L u cila P .C .G . de Freitas and Frederico G .C . A bath
P r o te in n u tr itio n a ls ta tu s in d ic a to r s w e r e s tu d ie d in w e a n lin g a lb in o S w is s m ic e in fe c te d w ith S. m anso n i a n d f e d th e R e g io n a l B a s ic D ie t ( R B D ) fr o m N o r th e a s t B r a z il, a m u ltid e fic ie n t d ie t o f lo w -p r o te in c o n te n t. E a c h m o u s e w a s in fe c te d p e r c u ta n e o u s ly w ith 8 0 c e r c a r ia e . T h e e x p e r im e n t la s te d 6 3 d a y s . T h e g r o w th c u r v e , f o o d c o n s u m p tio n , p r o te in in ta k e , w e ig h t g a in , P r o te in E ffic ie n c y R a tio (P E R ) a n d N e t P r o te in R a tio (N P R ) w e r e th e p a r a m e te r s in v e s tig a te d . R B D - f e d m ic e s h o w e d a m a r k e d w e ig h t lo ss, a lo w e r f o o d a n d p r o te in in ta k e , a s lo w e r b o d y w e ig h t g a in a n d lo w e r r a te s o f f o o d p r o te in u tiliza tio n w h e n c o m p a r e d to c a s e in - fe d a n im a ls . D iffe r e n c e s b e tw e e n in fe c te d a n d n o n - in fe c te d m ic e w e r e n o t c o n s is te n t. T h e p r e s e n t r e s u lts s u g g e s t th a t th e e ffe c ts o fR B D - in d u c e d m a ln u tritio n o n h e a lth a n d n u tr itio n a l c o n d itio n s o f th e m ic e a r e m o r e s e v e r e th a n th o s e o f M a n s o n ’s s c h is to s o m ia s is , in th e in itia l p h a s e o f th e d is e a s e .
K e y - w o r d s : S chistosom a m ansoni. M ic e . M a ln u tr itio n . P ro te in .
M a ln u tritio n areas and m ajo r S c h is to s o m a
m a n s o n i endem ic foci o verlap consid erably in
N o rth e ast B razil9. M u ltip le deficiencies, m ainly o f th e calo rie-p ro tein ty pe, h av e been detected in th e p o p u la tio n liv in g in these areas5 8 9 10 12 14 23. B ased o n food habits o f this p op u latio n, a definition w as p ossible fo r th e R egional B asic D iet (RB D ), a foo d b len d o f low p ro te in content (kidney beans-
P h a s e o l u s v u l g a r i s , m a n io c f l o u r- M a n i h o t
e s c u le n ta , salted and d ried m eat-"charq ue"and
sw eet p otatoes-I p o n a e a b a t a t a s ) , w hich reproduces d ietary d eficie ncies p re v alen t in th e region 9 1132.
T o m anio c flo u r an d sw eet p otatoes h ave been ascrib ed the am ino acid im balance and furth er decrease in the p ro te in content o f this m ultideficient diet.
A ty p e o f m aln utritio n rath er sim ila r to the m arasm atic fo rm o f calo rie-p ro tein m aln utritio n seen in hum ans, w hich is quite com m on in N ortheast B razil, h as b een induced in w eanlin g m ice9 11 and
C e n tr o d e P e s q u is a s A g g e u M a g a lh ã e s (F u n d a ç ã o O s w a ld o C r u z ) R e c i f e , P E , B r a z il.
S u p p o r te d b y C N P q a n d F A C E P E .
A d d r e s s f o r c o r r e s p o n d e n c e ' . D r a . E rid a n M . C o u tin h o . C e n tr o d e P e s q u is a s A g g e u M a g a lh ã e s /F I O C R U Z , C P : 7 4 7 2 , 5 0 7 2 2 - 9 7 0 R e c i f e , P E , B r a z il.
R e c e b id o p ara p u b lic a ç ã o e m 1 9 /0 8 /9 1 .
rats2132 fed R B D . In additio n to g ro w th d isturbances9 112132, RB D in tak e resu lts in a deficient g lycem ic re g u la tio n 33, a re d u c tio n in th e s c ia tic n e rv e conduction velo city28 and im paired p ro p ag atio n o f spreading depression in the cerebral cortex o f Sprague- D aw ley ra ts19.
F o r fu rth er in form atio n o n the effects o f R B D on th e in i t i a l p h a s e o f e x p e r im e n ta l m a n s o n ic schistosom iasis in alb in o m ice, p a rtic u la rly o n the p ro tein n utritio nal status o f th e h o st, bio lo gical
assays (Protein E fficiency ra tio -P E R and N et p ro tein R a tio -N P R ) w e re p e rfo rm e d to d e te rm in e th e u tiliz atio n o f d ietary p ro tein . In ad d itio n , som e o th er indicato rs o f p ro tein m etab olism 25, such as the w eig h t gain , g ro w th curve, foo d co nsu m ption and
p ro tein intake w ere investigated.
T h e p roposed experim ental m odel repro d uces
th e relationship b etw een u nd e rn o u rish e d h o st and parasite infectio n as it is found am o ng B razilian populatio n s liv in g in schisto som iasis en dem ic areas.
T h e experim ent w as desig ned: 1) to study th e effects on th e h o st, o f m aln u tritio n induced by R BD intake; 2) to detect, by u sin g som e in d icato rs o f p ro tein n utritio nal statu s, th e in flu en ce o f th is d ie t o n p ro tein utilization in th e body o f m ice in fected w ith S.
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a s ic d ie t f r o m n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith Schistosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 : 1 3 - 2 0 , j a n - m a r , 1 9 9 2 .
M A T E R IA L S A N D M E T H O D S
D i e t s
T h e R egion al B asic D iet (RB D ) is based on hum an staple foods usu ally ingested in N orth east B razil (k id n ey beans- P h a s e o lu s v u lg a r is , m anioc flo u r- M a n ih o t e s c u le n ta , salted and dried m eat and
sw eet p o ta to - I p o n a e a b a t a t a s ) . It has th e follo w in g co m p o sitio n (g /1 0 0 g): kid ney beans (protein s- 3 .9 6 , c arb o h y d rates-1 0 .6 6 , fats-0 .24 , m in erals- 0 .5 7 , fib e rs-1 .0 9 ); m anioc flo u r (pro tein s-0 .82 , c a rb o h y d ra te s-4 8 .5 9 , fa ts-0 .1 2 , m in erals-0 .4 3 ), f i b e r s - 5 . 6 4 ) ; “ c h a r q u e ” ( p r o t e i n s - 2 . 7 4 ,
c arb o h y d ra te s-0 .4 3 , fats-0 .2 1 , m in erals-0.0 6); fat fro m “ c h a rq u e ” (fat-0 .3 5 ); sw eet p otato (proteins-0 .3 (proteins-0 , carbohydrate s-9.99, fats-(proteins-0.(proteins-03, m inerals-(proteins-0.2(proteins-0, fib ers-0 .4 8 ). T h is food blen d contains, p er 100 g, 7 .8 2 % p ro te in s, 6 9 .6 7 % carbohydrates, 0.95 % fats and 1.26 % fib ers. B oth co ntrol diets contained casein an d h ad differen t total p ro tein levels: 7 .8 2 % (co n tro l d ie t I) and 2 2 .6 0 % (control d ie t II).
T h e contro l diet I had the follow ing com position (g% ): casein (p ro te in -7 .0 6 ), soybean o il (fat 8 .00 ), c o m starch (p ro te in -7 .7 6 , carbo h y drate-7 4.3 7 ),
cellu lo se (fib e rs-3 .5 0 ).
T h e co ntrol diet II had the follow ing com position (g% ): casein (p ro tein -2 2 .0 9 ), soybean oil (fat- 1 3 .0 0 ), c o m starch (p ro te in -0 .5 1 , carbohydrate- 5 0 .1 9 ), cellu lo se (fibers-4 .0 0).
B oth c o n tro l diets w e re supplem ented w ith m in eral salts (2 .5 0 g % ) and v itam in m ix tu res (1 g % w a te r-so lu b le and 1 g% fat-so lu ble vitam in s), a cco rd in g to T a g le & D o n oso 31. A ll th ese diets w e re giv en in p ellet form .
T h e n o n -p ro tein d iet, used in th e N et P ro tein R atio bio lo gical assay (N P R ), w as com posed as follow s (g% ): soybean o il (fat-8.0Q ), m ineral salts
(4 .0 0 ), fat-so lu ble vitam in m ix tu re (1 .0 0 ), w ater- soluble v itam in m ix tu re (1 .0 0 ), c o m starch (protein-0 .8 2 , carb o h y d rate s-7 2 .(protein-0 3 , fa t- (protein-0 .16, m ineral salts-0 .1 2 ), cellu lo se (fib ers-4 .salts-0 salts-0 ). It w as giv en d urin g
10 days to a g ro u p o f 10 anim als used as co ntro ls fo r th at assay.
E x p e r im e n ta l a n i m a ls
A tota l o f 70 alb in o Sw iss m ice w e re used. T w en ty m ale an d fem ale anim als w e re fe d each d iet and d ivid ed in to infected and non-infected subgroups
o f 10 m ice each. A n additio nal g ro u p o f 10 n o n infected m ice w as giv en a n o n -p ro te in d ie t and w as used as control fo r th e N e t P ro tein R atio biolo gical assay.
I n fe c tio n
A S . m a n s o n i strain isolated fro m São L ourenço
d a M ata (P ernam buco State, B razil) an d m ain tain ed re g u larly in o u r lab o rato ry w as used. E ach anim al w as in fected percu tan eo usly w ith 80 cercariae shed fro m B i o m p h a l a r ia g l a b r a t a rea re d an d in fected in th e laboratory (in fections up to 100 to 150 cercariae p e r m ouse are w ell tolerate d24 34).
E x p e r im e n ta l p r o t o c o l
T w enty -o ne-day old w eanlin g m ice w eig h in g 9 to 12 g w ere k e p t in in d ivid ual w ire b o tto m cages. W ate r and diets w ere p ro v id ed “a d lib itu m ” . T he body w eight w as determ ined w eek ly an d th e food in take w as record ed daily. T h e ex perim en t lasted 63 days.
Subgroups o f 5 m ice p e r co ntro l d iet w ere subm itte d to a p air-feed in g trial alo n g th e first 28 days o f th e experim ent. So, th e daily foo d in tak e o f control m ice (diets I and II) w as restricted to th e “ad lib itu m ” intake o f R B D -fed anim als.
T h e post-w ean lin g ra p id g ro w th p e rio d o f th e m ouse w as observed d u rin g th e first 28 days o f th e in vestig atio n (P hase I). H en cefo rth , th e S . m a n s o n i
ovip o sitio n and m atu ration o f h epatic an d in testin al lesio ns w ere in vestig ated (P h ase II).
I n d ic a to r s o f th e p r o t e i n n u t r i t i o n a l s t a t u s
T h e w eig h t cu rv e, to tal foo d c o nsu m ption , p ro te in intake, w eig h t g ain , P ro tein E fficiency R atio (P E R ) an d N e t P ro te in R atio (N P R ) v a lu e s w ere th e p aram ete rs studied. P E R is a b io lo gical assay devised to d eterm ine th e g ram s g ain p e r g ram p ro te in co nsum ed, w h ile N P R m easures the w eig h t loss o f a n eg ativ e c o n tro l g ro u p fed a n o n -p ro tein d iet, ad ded to th e w eig h t g ain o f th e experim ental gro u p (R B D -fed m ice) an d d iv id ed b y th e p ro tein consum ed by th e latter22.
S t a t i s t i c a l a n a ly s is
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a s ic d ie tf r o m n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith Sc histosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 :1 3 - 2 0 , j a n - m a r , 1 9 9 2 .
w ere u sed , p ro p o rtio n s b ein g com pared by norm al ap pro x im atio n. T h e p ro b ab ility level consid ered sig n ifican t w as p < 0 .0 5 .
R E SU L T S
W e ig h t c u r v e s
In g en eral, th e w eig h t c u rv e v alu es fo r in fected and n on -in fected anim als fed casein diets w ere
h ig h e r th an th o se fed R B D (F ig u re 1). A s expected, th e h ig h e st v alu es w ere achieved b y m ice fed the 22.6 0 % casein diet. T h e w eig h t o f th e infected R BD anim als decreased in Phase II o f the experim ent, b u t this red u ctio n w as less ap paren t in casein-fed in fected anim als. A lso, th e m ean body w eig h t o f j R BD n on -in fected m ice w as lo w er than that o f | an im als fed casein diets,
f
1 F o o d in ta k e
T h e S. m a n s o n i infection resulted in a significant ‘ redu ctio n in R B D intake. R egardin g th e casein-fed g ro u p s, h ow ever, data w ere n on-signific ant f (T able 1).
1 P r o t e in in ta k e
R egard in g p ro tein in take, both in fected and n on -in fected m ice fed R B D show ed a significant
d ifference (p < 0 .0 0 1 ) w hen co m pared to th e o th e r g ro u p s, th e lo w est v alues for th e in fected ones. A co m parison am ong th e g ro u p s show ed that: a) p ro tein intake w as alw ays h ig h e r fo r th e an im als fed th e 2 2.6 0 % casein d iet; b) d urin g th e overall experim ental p erio d sign ifican t d ifferen ces w ere detected betw een the lo w -p ro tein fed in fected and non-in fected an im als and th o se fed th e 2 2.6 0 % casein d iet (F ig u re 2).
W e i g h t g a in
The m ean body w eig h t gain w as significan tly and co nsistently h ig h e r fo r th e n on -in fected R B D - fed g ro u p , w hen com pared to in fected m ice u nd er the sam e diet. T he infectio n, h o w ev er, d id n o t seem to affect in th e sam e w ay th e w eig h t gain o f the casein-fed g ro u p s. A c o m p a ra sio n am o ng th e different groups show ed th at the h ig e st v alu es for body w eig ht gains w ere found in casein-fed m ice, particularly in th e 22.60% casein g roup, irrespective o f th e presence o f schistosom e in fection.
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a sic d ie t f r o m n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith Sc histosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 : 1 3 - 2 0 , j a n - m a r , 1 9 9 2 .
T a b le 1 - M e a n f o o d in ta k e ( g ) o f in f e c te d a n d n o n - in fe c te d m ic e f e d R B D a n d C a s e in d ie ts .
D iets an d A nim al su b g ro u p s
P h ase I
(X ± SEM )
P h ase 11
(X ± SE M )
O v erall ex p erim en tal p eriod (X + SE M )
R B D (infected) R B D (n on-infe cted)
89 .15 + 9.31 1 1 4 .6 0 + 4 .2 9 S ignificant (p < 0 .0 5 )
8 8 .9 4 + 7 .9 7 141.00 + 8.1 6 Significant ( p < 0 .0 0 0 1 )
1 9 1 .9 9 ± 2 1 .54 25 7.0 1 + 10.68 S ignificant ( p < 0 .0 2 )
7 .8 2 % casein (infected) 7 .8 2 % casein (non-infected)
1 0 7 .0 5 + 6 .8 7 9 4 .7 2 + 7 .2 6
N on-significant
135.35 + 11.53 172.91 + 11.62 Significant ( p < 0 .0 5 )
2 4 2 .4 0 + 11.95
2 7 0.2 3 + 14.57 N on- sig nificant
2 2 .6 0 % casein (infected) 2 2 .6 0 % casein (n on-infected)
1 2 1 .6 8 + 7 .7 3 108.46 + 7 .3 6 N on-significant
1 2 5 .5 5 ± 7 .2 9
1 3 8 .2 0 + 3 .7 5 N on-signifio ant
24 3 .8 3 ± 1 3 .6 1 2 4 0 .8 4 + 1 2 .7 7 N o n -significant
X = arithm etic m ean
SE M = sta nd ard e rro r o f th e m ean RB D = R e gio n al B asic D iet
P h ase I = T h e first 28 days a fter w eanlin g.
P h ase II = F rom the 29th day to th e end o f th e trial
T a b le 2 - P r o t e i n s e f fic ie n c y r a t i o o f in f e c te d a n d n o n d i e t s (c o n tr o ls )* .
■ infected m ic e f e d th e R e g io n a l B a s i c D i e t a n d C a s e in
D iets an d A nim al su bg ro u p s
PE R (X ± SEM )
S tu d e n t's "t" test
RB D (infected)
X
7 .8 2 % casein (infected)
0 .5 9 + 0 .0 8
1 .6 4 + 0 .0 8
Significant (p < 0 .0 0 1 )
R B D (infected)
X
7 .8 2 % ca se in (n on-infected)
0 .5 9 + 0 .0 8
1 .9 3 + 0 .0 8
S ignificant ( p < 0 .001 )
RBD (non-infe cted)
X
7 .8 2 % casein (n on-infected)
1 .0 4 + 0 .0 8
1 .9 3 + 0 .2 3
S ig nificant ( p < 0 .005)
X = arithm etic m ean RBD = R egional Basic D iet
SE M = sta nd ard e r r o r o f th e m ean P E R = p ro tein efficiency ratio b io log ical assay
(*) T h is assay w as n o t p e rfo rm e d fo r th e su bg ro u p fed 2 2 .60 % casein diet b ecau se a p ro tein c o n te nt lo w e r th an 10% is req u ired .
show ed th at th e in fecte d R B D -fed m ice had th e I n d ic a to r s o f f o o d p r o t e i n u til iz a tio n
lo w est v alues fo r th e b od y w eig h t gain. P air-fed
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a s ic d ie t f r o m n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith Schistosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 : 1 3 - 2 0 , ja n - r n a r , 1 9 9 2 .
T a b le 3 - N e t P r o t e i n R a t i o o f i n f e c t e d a n d n o n - in fe c te d m i c e f e d th e R e g io n a l B a s i c D i e t a n d C a s e in diets*-.
D iets and A nim al
su bgroups
N PR
(X ± SE M )
S tu d e n t's "t" test
RB D (infected) 1.68 + 0.23
R B D (n on-infected) 2 .0 8 + 0.1 7 N o n -sig n ificant ( p > 0 .0 5 )
7 .8 2 % casein (infected) 3 .9 9 ± 0 .5 2
7 .8 2 % casein (non-infe cted) 4 .9 0 + 0.5 0 N o n -sig n ificant ( p > 0 .0 5 )
X = arith m etic m ean
S E M = sta nd ard e rro r o f th e m ean
RBD = R egion al B asic D iet
N PR = net pro tein ratio b io lo gical assay
(*) T h is assa y w as n o t p e rfo rm e d fo r th e su bg ro u p fed 22 .60 % casein d iet b ecau se a p ro tein c o n te nt lo w e r than 10% is req u ired .
level b elo w 10% as requ ired for this biolo gical assay. O nly RB D gro u p s show ed a significant difference regarding P E R values (p < 0.002) betw een infected an d n on -in fected m ice. W hen th e groups
w ere com pared to each o th er, ag ain th e low est v a lu e s w e re d e te c te d in th e R B D -fe d m ice, p a rtic u la rly w h e n S . m a n s o n i in fe c tio n w as associated (T able 2). N P R v alu es w ere apparently
hig h er for the n on-in fected m ice. H o w ev er, resu lts w ere n o t statistically sign ifican t (T able 3).
D ISC U S SIO N
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a s ic d ie t f r o m n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith Schistosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 : 1 3 - 2 0 , ja n - m a r , 1 9 9 2 .
A decreased p ro tein and lip id u tilizatio n w as repo rted in in fected m ice and w as ascribed to the altered hepatic function o r to th e acu te intestinal in fla m m atio n seen in th is ex perim en ta l h o s t16.
P E R and N P R assays h ave been extensively used in evalu ating th e n u tritiv e v alu e o f food p ro te in s22. In th e p re se n t in v e stig a tio n , th ese in dicators w ere consistently lo w e r in R B D -fed m ice; infected anim als presen ted th e lo w est valu es.
C linical, ep id em iolo g ic al an d ex perim en tal studies have suggested th at deficiency states induced by m aln utritio n depress h o st d efense m echanism s, aggravating the course o f infectious and p arasitic diseases, including schisto som iasis27. H ow ever, this has n ot been supported by som e investig atio n s in hum ans9 30. Som e experim ents su ggest th a t the a p p e a r a n c e o f th e c l i n i c a l s y m p to m s o f schisto som iasis depends o n th e h o s t’s n u tritio n al statu s1 2 3 4 20. A ccordin g to p rev io u s findings, how ever, schisto som e in fectio n only c o ntrib u tes to aggravate m aln utritio n 9 10 11.
In conclusio n, the data p resen ted in this p ap er in dicate that, at least in th e in itial stage o f the disease and u n d er o u r experim ental c o nd ition s, the harm ful effects o f R B D -in duced m aln u tritio n are
m ore severe than those o f M anson ’ s schistosom iasis.
R E S U M O
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a s ic d ie tf r o m n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith S chistosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 : 1 3 - 2 0 , ja n - m a r , 1 9 9 2 .
n u tr ic io n a l d o h o s p e d e ir o , d o q u e a q u e le s r e s u lta n te s d a A C K N O W L E D G E M E N T S in fe c ç ã o p e l o S. m a n s o n i, n a f a s e in ic ia l d a d o e n ç a .
W e are indebted to M iss L íg ia P ed ro sa fo r h er
P a l a v r a s - c h a v e s : S c h i s t o s o m a m a n s o n i . critical review and M iss Ivan ild a V . N ascim ento C a m u n d o n g o s . M á - n u tr iç ã o . P r o te ín a s. fo r ty p in g th e m anuscript.
R E FE R E N C E S
1. A kpom C A . S u p ression o f g ran u lo m e form ation
aro u n d S c h is to s o m a m a n s o n i eg gs in se v e re pro tein m aln utrition: th e ro le o f th e eg g . T ran sactio n s o f the R oyal S ociety o f T ro p ic a l M ed icin e and H y g ien e 7 5 :4 4 4 -4 4 6 , 1981.
2. A k p o m C A . S c h i s t o s o m i a s i s : n u t r i t i o n a l im plications. R eview s o f Infectious D iseases 4 :7 7 6-; 7 8 2 , 1982.
j 3. A k p o m C A , W a rre n K S. C a lo rie an d p ro te in I m a ln u tritio n in c h ro n ic m u rin e sch istosom ia sis ' m ansoni: effect on th e p a ra site and th e host. T he
> Jo u rn a l o f Infectious D iseases 132:6-1 4, 1975. * 4. A kpom C A , W arre n K S. T h e inhibition o f granulom e
form atio n aro u n d S c h is to s o m a m a n s o n i eggs. V I. P ro tein , c a lo rie an d vitam in d eficiency. A m erican Jo u rn a l o f P ath o log y 7 9 :4 3 5 -4 5 2 , 1975.
5. B atista Filho M , C haves N , V arela R M , M artin M H S , S alzano A C , B azan te M O , T e ix e ira SM G , L im a E JC , Reis F M , M artin s G C , L in h ares E R . Inq u érito n utricio n al em á re a urbana da Z ona da M a ta d o N o r d e s te b r a s i l e i r o (Á g u a P r e ta ,
P e rn am b u co ). O H ospital 7 9 :7 0 7 -7 2 3, 1971. 6. C h en M G , M ott K E . P rog re ss in assessm en t o f
m o rbid ity d u e to S c h is to s o m a m a n s o n i infection (A review o frecen tliteratu re). T ro pical D iseases Bulletin 8 5 :1 -5 6 , 1988.
7. C outin ho A , L o u reiro P. A sp ectos bio quím ico s da
insuficiên cia hepática na esquistossom ose m ansônica h ep ato-esplen ica. A nais d a F a cu ld ad e d e M edicina da U n iv e rsid a d e d e R ecife 2 0 :2 7 -4 9 , 1960. 8. C ou tin h o E M . O b serv açõ es p relim inares so b re o
p a d r ã o d i e t é t i c o e m á r e a s e n d ê m i c a s d e esq u isto sso m o se m ansô n ica. Jo rn a l B rasileiro d e M ed icin a 8 :3 3 9 -3 4 4 , 1964.
9. C outin ho E M . R elações hosp ed eiro -p arasito na esq u isto sso m o se m an sô n ica, em função da D ieta B á s ic a R e g io n a l ( E s tu d o e p id e m io ló g ic o e a n a t o m o p a t o l ó g ic o ) . T e s e d e D o u to r a d o , U n iv ersid ad e F e d e ra l d e P e rn am b u co , R ecife, PE , 1976.
10. C outinho E M . E stado n u tricio n ale esquistossom ose.
R evista da S ociedade B rasileira d e M ed icin a T ropical 1 3 :9 1-96, 1980.
11. C outin ho E M . P ato biologia da d esnutrição nas
doenças parasitá ria s. M em órias do Instituto O sw aldo
C ru z 7 5 :6 3 -7 6 , 1980.
12. Co utin ho E M , A m aral JA , B a rb o sa J M . A lteraçõ es bioquím icas n a esqu isto sso m o sem an sô n ica hum ana, com esp ecial refe rên cia ao m etabo lism o lip ídico. Jo rn a l B rasileiro d e M ed icin a 1 1 :1 5 7 -1 6 8, 1966. 13. C outinho E M , B a rb osa F S , B a rb o sa J M , P e sso a D ,
Pinto R F , O liv eira P A , R o d rig u es BA . In quérito c lín ic o -n u tric io n a le a n tro p o m é tric o p re lim in a r, em
área s end êm icas d e esq u isto sso m o se m a nsô n ica, no N o rd este do B rasil. R evista d a S o cied ad e B rasileira
d e M edicina T ro p ica l 6 :2 1 1 -2 3 6 , 1972.
14. Coutinho E M , C osta L P , S alzano A C , C am pos FS,
M elo M E B , L ap a A . N íveis e tip os d e p ro te ín a
alim en tar e suas re p e rc u ssõ e s so b re a b iologia do h o sp ed eiro , na e sq u isto sso m o se ex p erim en tal (S. m a n so n i) do cam undong o albin o . In: A nais da 3 a Jo m a d a C ientífica da F u n d ação O sw ald o C ruz, Rio d e Jan eiro p. 454-45 5 , 1985.
15. Coutinho E M , E spírito Sa nto M , B a rb osa JM ,
M ello SA . Padrão a lim e n ta re m áre a s en d êm icas d e esquisto sso m o se m ansô n ica, no N o rd e ste do B rasil. R e vista B ra sile ira d e M a la rio lo g ia e D o e n ç a s
T ro picais 16:5 53-5 89, 1964.
16. D e W itt W B . E ffects o f S c h is to s o m a m a n s o n i infections on th e ability o f m ice to d ig e st and ab so rb
dieta ry fats and pro tein s. T h e Jo u rn a lo fP a ra s ito lo g y 4 3 :3 2 , 1957.
17. D e W itt W B , O liv er-G o n zález J , M ed in a E . E ffects o f im provin g the n utritio n o f m aln o u rish ed p eo p le infected w ith S c h is to s o m a m a n s o n i. T h e A m erican Jo u rn a l o f T ro p ica l M ed icin e an d H y g ien e 13:25- 3 5 , 1964.
18. G ale M M , C raw fo rd M A . T h e effect o f A frican
staple foodstuffs on g u in ea-pig g ro w th c u rv e s. T ra n sa c tio n s o f the R o y al S o ciety o f T ro p ic a l M edicine an d H y g ien e 6 3 :8 2 1 -8 2 5 , 1969.
19. G uedes R C A , A n d ra d e A F D , C a b ral Filho JE . P ropagation o f co rtical sp read ing d e p ressio n in m alnourished rats: facilitatory effect o fd ie tary protein
d e fic ie n c y . B ra z ilia n J o u r n a l o f M e d ic a l an d Biological R esearch 2 0 :6 3 9 -6 4 2 , 1987.
C o u tin h o E M , F r e ita s L P C G , A b a th F G C . T h e in flu e n c e o f th e r e g io n a l b a sic d ie t f r o n t n o r th e a s t B r a z il o n h e a lth a n d n u tr itio n a l c o n d itio n s o f m ic e in fe c te d w ith Schistosom a m ansoni. R e v is ta d a S o c ie d a d e B r a s ile ir a d e M e d ic in a T r o p ic a l 2 5 : 1 3 - 2 0 , j a n - m a r , 1 9 92 .
in acute m urine schistosom iasis m ansoni. T h e Journal o f In fectio us D ise ase s 1 2 0:560-575 , 1969. 2 1 . L ago E S , P e sso a D C N P , T eo dósio N R , C a bral
Filho JE . L o ng ev ity an d grow th c u rv e o f chro nically m aln ourished rats fed the Regional Basic D iet (R BD ).
In : A b strac t o f th e 2 n<^ In ternatio nal Sy m posiu m o f N u tritio n , P ro c eed in g s, R ecife p .4 0 -41, 1988.
2 2. M cL au g h lan J M , C am p bell JA . M etho dolo g y o f p ro te in ev alu atio n . In: M unro H N (ed) M am m alian p ro te in m etabo lism , A cad em ic P ress, N ew Y ork , vol. 3 p .3 9 1 -4 2 2 , 1969.
23. M ello A V , B aez M C , B azan te M D , C oelho H A L , M artin s M H S , Paes A G , D antas L Y S. Inquérito de co n sum o alim e n ta r no m unicípio d e C aten d e, Z ona da M a ta Sul d e P e rn a m b u c o . Boletim do Instituto de N u triçã o d a U n iv e rsid a d e F e d e ra l d e P ernam b uco
1:7 -4 9 , 1973.
2 4. M o o re D V , Y olles T K , M ele ney H E . A co m parison o f c o m m o n lab orato ry an im als as experim ental hosts fo r S c h is to s o m a m a n s o n i. T h e Jo urna l o f P arasito log y 3 5 :1 5 6 -1 7 0 , 1949.
2 5. O liv eira JE D , S antos A C , W ilson E D . N utrição B ásica, E d ito ra S a rv ie r, São P aulo, 1982. 2 6. R a m o s - A li a g a R . A s p e c to s b io q u ím ic o s y
n u tricio n ale s en ra tas en d esarro llo q u e reciben p ro te in as d e d o s p atro ne s d ie ta rio s de los A ndes del P e ru . A rc h iv o s L atin o am erican o s d e N utrición 2 8 :3 7 8 -4 0 0 , 1978.
2 7 . S crim sh aw N S , T a y lo r C E , G ord on JE . N u trición y In feccio n es: su acc ió n re c ip ro ca. O rg anización M un d ial d e la S alu d (O M S: S e rie m onografias n 0, 57) G en eb ra, 1970.
2 8. Silva A T , C osta F B R , C osta JA , T eo dósio N R ,
C a b ra l F ilh o J E , G u ed es R C A . S c iatic n e rv e conduction velocity o f m aln o u rish ed rats fed the hum an “B asic R egion al D ie t” o f th e n o rth ea st o f B razil. B razilian Jo u rn a l o f M edic al and B iological R esearch 2 0 :3 8 3 -3 9 2 , 1987.
29. S ou za N , E lias L G , B ressan i R. E stu d io s, en ra tas, del efecto d e u na dieta b á sic a del m edio ru ra l de
G uatem ala, su plem en tada c o n le c h e d e v a c a y una m ezcla de p ro te in as. A rch iv o s L atin o am erican o s de N u trición 2 0 :2 9 3 -3 0 7 , 1970.
30. Stephenson L S . Schistosom iasis and hum an n utritio n . C orn ell Internatio nal N utrition M o n o g ra p h Series n °- 16, N ew Y o rk p. 1-21, 1986.
31. T a g le M A , D o n o so G. N et p ro te in utilizatio n d eterm ined in sh o rt and lon g term ex p erim en ts w ith rats. Jo u rn a l o f N u trition 8 7 :1 7 3 -1 7 8 , 1965. 32. T eo dósio N R , L ago E S , M ed eiro s M C , F e rre ira
L M P , Santos E T V . C a rb o h y d ra te m etabo lism in m alnutrition in duced b y th e R egion al B asic D iet. 1.
F astin g gly cem ia and liv er g ly co g en in rats w ith R B D -induced m a ln utrition. In: A b stra c t o f th e 1st Internatio nal Sym posium o fN u tritio n , P ro c eed in g s, R ecife p .4 0 -41, 1986.
3 3. T eo dósio N R , R o m ani S A M , L ago E S . D ieta ry deficiencies and m a lnutrition. 1. A n ex p erim en tal dietetic m odel. In: A b strac t o f th e 1st In tern atio nal Sym posium o fN u tritio n P ro c e e d in g s, R e cife p .38- 39, 1986.
3 4 . W a rre n KS. T h e influ en ce o f tre a tm e n t on the d evelopm ent and c o u rse o f m u rin e h ep ato-splenic sch istosom iasis m ansoni. T ran sactio n s o f th e R oyal Society o f T ro p ica l M ed icin e and H y g ie n e 5 6 :5 1 0 -
