January 1975
50
The Journal o f P E D I A T R I C S
Digestibility of starches in infants and children The digestibility of various starches has been studied in normal infants o f d~ff'erent ages. During balance periods of 3 days, while the infiTnts were receiving known dietary quantities of the starch to be tested, the fecal content o f lactic acid, glucose, dextrins, and starch was measured After the first year of liJe, children were able to absorb almost completely 170 gm/m 2 o f body surface of cooked wheat starch given in the.form of biscuit or macaroni. A lower absorption coefficient was found for potato starch given in the form of biscuit. Cooked wheat, tapioca, corn, rice, and potato starch in amounts of 45 and 85 gm/m21day, respectively, for 1-and 3-moold infants, were almost completely absorbed. In 1-mo-old infants larger amounts (110 gm/m2/day) of cooked rice starch were well tolerated; it should therefore be possible to provide a large part o f the carbohydrate requirements of infants from the first month o f life with cooked starches.
B. De Vizia, M.D., F. Ciccimarra, M.D., N. De Cicco, M.D., and S. A u r i c c h i o , M . D . , * N a p l e s , I t a l y
THE ABILITY of the intestine to digest and absorb starch depends upon the efficiency of intraluminal and mucosal digestion and the transport of glucose through the brush border m e m b r a n e of the enterocyte. 1 In adults and children starch is rapidly hydrolyzed in the intestinal lumen by salivary and pancreatic amylase to glucose, maltose, maltotriose, and b r a n c h e d dextrins. 2 These carbohydrates are further hydr01yzed to glucose by the so-called maltases of the brush border of the enterocyte. 3-7 In infants the intraluminal c~-amylolytic digestion of starch is slow, because of the low level of a-amylase activity in the intestine. = T h e most active m a l t a s e s (sucrase and isomaltase) are, however, fully developed at birth. 8 Starch is one of the carbohydrates added to some formulas fed to infants during the first months of life. In spite of the early introduction of starch into the infant's d i e t o n l y p r e l i m i n a r y d a t a are a v a i l a b l e o n t h e digestibility of starch in infancy. 9
From the Institute of Pediatrics, H Faculty o f Medicine, University of Naples. The present research was supported in part by a grant from the Italian Department of Health. *Reprint address: Clinica Pediatrica, 2 ~Facolt~ di ,~'ledicina e Chirurgia; Via Orsolone ai Cangiani 80131, Napoli, Italy.
Vol. 86, No. 1, pp. 50-55
In the p r e s e n t study the digestibility o f various starches has been studied in normal infants of different ages by measuring, in balance periods of 3 days, the fecal content of lactic acid, glucose, dextrins, and starch and by relating the quantities excreted to the starch content of the diet.
MATERIALS AND METHODS During the first month of life infants were given halfs k i m acidified p o w d e r e d milk c o n t a i n i n g sucrose, maltose, and dextrins as added carbohydrates, and during the second and third months an acidified powdered whole m i l k containing sucrose, maltose, dextrins, and starch as added carbohydrates. Starch represented 1.9 gm/dl of the diluted formula. Normal infants 30 to 50 days of age (1-mo-old infants) and 90 to 110 days of age (3-too-old infants) were studied while receiving a diet containing wheat, corn, and tapioca starches during three successive metabolic study periods, each lasting 3 days. Each starch was introduced in the diet 3 days before the beginning of stool collections. A second group of normal infants of the same age was investigated, with the same procedure, while being fed a diet c o n t a i n i n g p o t a t o and rice starches. The formula during the balance periods was composed of cow's milk, 100 ml/kg body weight; water, 60
Volume 86 Number 1
Starch digestibility in infants
51
Table I. Absorption of starch in children 1-2 yr of age (mean values + 1 SD and observed ranges in parentheses) I
Starch in diet No. of ubjects 20
Kind of starch
Quantity (gm/m2/day) Starch
Stool findings (gm/day)
Glucose
Lact& acM
Fat 2.4 '• 0.92 (1.2 -4.4)
Nitrogen
Absorption coefficient (%)
Starch
Fat
99.6 • 0.25 94.6 • 2.7 (99.1 - 99.9) (90.3 - 97.3)
Wheat (biscuits and macaroni)
170 • 21 0.37 _+ 0.2 0.03 • 0.04 (125 - 200) (0.02 - 0.66) (0 - 0.13)
5
Potato (biscuits)
180 • 23 5.5 • 3.5 (140 - 200) (1.80 - 9.6)
3
3 • 0.82 0.62 • 0.26 99.7 + 0.15 93.2 • 2.3 Potato 162 • 16 0.12 • 0.1 0.01 • 0.01 0.04 • 0.04 (0-0.02) (0-0.08) (2.3-.3.9) (0.46-0.92) (99.6-99.9) (90.6-94.6) (biscuits cooked (148 - 180) (0 - 0.19) in water)
0.23 • 0.48 0.11 + 0.0.7 1.9 • 0.65 0.63 • 0.18 92.6 • 4.4 94.9 • 1.7 ( 0 - 1.1) (0.05- 0.20) (0.97- 2.6) (0.38 - 0.82) (87 4 - 96.7) (92.9 - 97.5)
and 40 ml/kg for 1- and 3-mo-old infants, respectively; the concentration of carbohydrate in the diluted cow's milk was 6 and 7% for 1- and 3-too-old infants, respectively. The added carbohydrates were represented by sucrose and approximately 10 or 23 gm (45 or 85 gin/ m2/day) of each kind of starch for 1- and 3-mo-old infants. Starch was given as flour from wheat, corn, tapioca, potato, and rice cooked for 10 rain in the water necessarY for the dilution of cow's milk. The starch concentration in 100 ml of the diluted cow's milk was 1.76 gm --- 0.32 and 3,28 gm + 0.71 (mean ---+ 1 SD) for 1and 3-too-old infants, respectively. Four normal 1-mo-old infants were tested for their capacity tO digest larger quantities of rice starch. In the diet of these children carbohydrates were added to the diluted cow's milk in the concentration of 6%. The added carbohydrates were represented by sucrose and approximately 25 gm of rice starch (110 gm/m2/day). The starch concentration in 100 ml of the diluted cow's milk was 4.46 gm -+ 0.28 (mean --+ 1 SD). A group of 1- to 2-yr-old children was also studied. The diet of these subjects contained the following carbohydrates: lactose (cow's milk 500 ml/day), sucrose (25 gin/day), a n d starch (170 g m / m 2 / d a y ) ; wheat starch was given to some of the Children as biscuits and m a c a r o n i (the former a c c o u n t i n g for 35% of total starch); in the diet of other children potato starch was provided in biscuits. During balance periods of 3 days stools were collected from the children receiving a standard diet and immediately frozen. The food was marked with carmine red at the beginning of the first and the fourth days of each balance period. Starch was assayed in food and stool according to the method previously described. 9 The starch content in food was calculated by multiplying by 0.9 the d,uantity
of glucose determined after enzymatic hydrolysis of starch by glucamylase from Rhizopus delemar. The factor of 0.9 is derived on the basis that during hydrolysis water is added to the starch molecule With a consequent increase in weight of approximately 10%. There was no free glucose in the food. Glucose was determined in stools both before (free glucose) and after enzymatic hydrolysis of starch (dextrins and malto-oligosaccharides) by the glucamylase method. The "starch" content in stool was calculated in the following way: quantity of glucose after enzymatic hydrolysis minus quantity of free glucose in stool, multiplied by 0.9. The absorption coefficient of starch was calculated from the glucose of the diet and from the total glucose of stools after enzymatic hydrolysis. The content of fat, 1~ lactic acid, 1~ and nitrogen in stools was also determined. RESULTS After the first year of life children were able to absorb almost completely 170 g m / m 2of body surface of cooked wheat starch as biscuits and macaroni. The same results were obtained when children were given the total quantity of wheat starch either as biscuit or as macaroni ~tlone. A lower absorption coefficient was observed for potato starch given as biscuits; w h e n biscuits were cooked in water for 10 rain, potato starch was almost completely absorbed (Table I). W h e a t , tapioca, corn, rice, and potato starch in amounts of 45 and 85 gm/m2/day were almost completely absorbed in 1- and 3-too-old infants when fed as cooked flours. This was well demonstrated for each starch by the very low fecal excretion of lactic acid, glucose, dextrins, and starch. The absorption coefficient of starch was higher than 98% in all infants studied. W h e n the amounts of starch indicated above were used
52
De Vizia et al.
The Journal of Pediatrics January 1975
T a b l e II. A b s o r p t i o n o f v a r i o u s s t a r c h e s in 1 - m o - o l d i n f a n t s ( m e a n v a l u e s - 1 S D a n d o b s e r v e d r a n g e s in
Starch in diet
No. of subjects
K&d of starch Wheat Corn Tapioca
Rice Potato
4
Stool findings (gm/day)
Quantity (gm/m2/day)
Quantity (gm/day) 10.6 • (7.5 11.8• (11.3 10.5 • (9.2 -
1.8 12.3) 0.47 12.4) 0.74 11.0)
46.8 (32.0 51.8 (46.2 45.4 (38.4
• + _ -
10.5 (7.7 10.1 (8.7
1.9 11.7) 0.97 10.7)
48.5 (35.2 46.7 (39.7
• 8.9 -- 54.0) -4- 5.0 -- 50.6)
Rice
• • -
Concentration in diluted cow's milk (gm/dl)
25
1.7 ___0.43 (1.2 - 2 . 3 ) 1.9 • 0.36 (1.6 - 2 . 5 ) 1.7 • 0.34 (1.3 - 2 . 2 )
9.2 55.1) 5.4 60.0) 7.0 54.7)
1.7 (1.3 1.6 (1.5
111.8 _+ 6.8 (102.0--117.9)
• -• --
0.28 1.9) 0.14 1.7)
4.5 • 0.28 (4.2--4.9)
Glucose
Starch 0.05 (0.02 0.02 (0.009 0.04 (0.01
_ 0.04 - 0.12) +_ 0.02 - 0.067) • 0.03 - 0.08)
0
(0.01 (0 0.02 (0.01
• 0.00) - 0.01) • 0.01 -- 0.03)
(0 -- 0.01) 0
0.33 • 0.34 (0.03--0.66)
0.01 • 0.01 (0--0.02)
0 (0 - 0.01) 0 _ 0.01 (0 - 0.02) 0
T a b l e III. A b s o r p t i o n o f v a r i o u s s t a r c h e s in 3 - m o - o l d i n f a n t s ( m e a n v a l u e s +_ 1 S D a n d o b s e r v e d r a n g e s in
Starch in diet
No. of subjects 5
Kind of starch Wheat Corn Tapioca
Rice Potato
Quantity (gm/day)
Stool findings (gm/day) Concentration in the diluted cow's milk (gm/dl)
Quantity (gm/m2/day)
21.9 ( 13.4 24.4 ( 15.9 22.3 (18.0
_ • -• -
4.8 24.3) 4.9 28.2) 2.5 24.3)
83.2 (47.8 92.2 (57.1 84.1 (65.9
• -_ -• --
21.7 103.4) 20.9 105.0) 13.2 96.3)
24.0 (23.5 21.9 (19.6
• 0.44 - 24.3) ___ 1.4 - 23.0)
89.1 (80.7 81.5 (76.7
• -_ --
6.5 97.2) 4.4 87.8)
3.2 ( 1.7 3.5 (2.1 3.2 (2.3 3.4 (2.8 3.1 (0.02
• • • -
Starch
1.1 4.2) 1.0 4.6) 0.69 3.9)
0.18 (0.01 0.13 (0.01 0.04 (0
• 0.15 - 0.34) • 0.16 -- 0.41) ___0.03 - 0.08)
___0.44 - 4.0) • 0.29 - 0.1)
0.02 (0.01 0.05 (0.02
• 0.02 -- 0.05) + 0.03 -- 0.1)
Glucose 0.03 (0.01 0.03 (0 0.01 (0
• 0.01 -- 0.04) • 0.03 -- 0.08) • 0.01 -- 0.02)
0.01 _+ 0.01 (0 -- 0.02) 0
in t h e fecal e x c r e t i o n o f fat a n d n i t r o g e n ( T a b l e s II a n d
c o w ' s m i l k in a c o n c e n t r a t i o n o f 6 g m / d l ; t h e q u a n t i t y o f s t a r c h f e d to t h e s e i n f a n t s w a s a p p r o x i m a t e l y 40 g m / day (178 g m / m 2 / d a y ) . T w o i n f a n t s d e v e l o p e d a f e r m e n -
III). D u r i n g t h e s e c o n d m o n t h o f life, larger a m o u n t s o f
glucose, dextrins, and starch (Table IV; Subjects 4 and
c o o k e d rice s t a r c h w e r e well t o l e r a t e d : 110 g m / m 2 / d a y
5).
in t h e diet, n o d i f f e r e n c e w a s a p p a r e n t in d i g e s t i b i l i t y among various starches. No differences were observed
o f this s t a r c h w e r e a b s o r b e d a l m o s t c o m p l e t e l y ( T a b l e II). T h e t o l e r a n c e for still larger q u a n t i t i e s o f c o o k e d rice s t a r c h w a s s t u d i e d in five i n f a n t s d u r i n g t h e s e c o n d m o n t h o f life ( T a b l e I V ) . I n t h e diet o f t h e s e i n f a n t s , s t a r c h w a s t h e o n l y c a r b o h y d r a t e a d d e d to t h e d i l u t e d
tative diarrhea
with high excretion
of lactic acid,
DISCUSSION M a l a b s o r p t i o n o f s t a r c h is a s s o c i a t e d w i t h t h e fecal e x c r e t i o n o f t h e p o l y s a c c h a r i d e a n d its i n t e r m e d i a r y p r o d u c t s o f i n t e s t i n a l h y d r o l y s i s ; t h e latter, e x p e c i a l l y
Volume 86 Number 1
Starch digestibility in infants
53
parentheses)
Absorption coefficient (%)
Lactic acid 0.02 0 0.02 (0.01 0.02
Fat
Nitrogen
Starch
___0.02 - 0.04 • 0.02 - 0.07) • 0.02 - 0.04)
0.99 (0.65 0.84 (0.46 0.98 (0.44
• • • -
0.32 1.4) 0.32 1.2) 0.58 1.9)
0.22 (0.14 0.19 (0.11 0.16 (0.10
• • • -
0.01 • 0.01 ( 0 - 0.02) 0.01 • 0.01 (0 - 0.03)
0.93 (0.51 1.1 (0.73
• • -
0.34 1.2) 0.35 1.6)
0.18 (0.12 0.15 (0.07
_• 0.06 - 0.26) _ 0.08 - 0.27)
0.19 • 0.04 (0.14 - 0.23)
(0
0.06 • 0.04 (0.03 - 0.12)
1.2 • 0.50 (0.63 - 1.7)
0.10 0.39) 0.05 0.25) 0.06 0.25)
99.4 (98.4 99.8 (99.4 99.6 (99.2
• • • -
Fat
0.6 99.7) 0.2 99.9) 0.2 99.8)
92.6 (90.1 93.5 (90.0 92.9 (88.0
• • • -
2.4 95.4) 2.8 96.9) 3.6 97.0)
99.8 _ 0.1 (99.7 - 99.9)
93.0 (90.8 91.6 ( 88.0
• • -
2.5 96.0) 2.6 94.0)
98.7 • 1.4 (97.3 - 99.9)
90.1 • 3.9 (86.0 - 94.7)
99.9
parentheses)
Absorption coefficient (%)
Fat
Lact& acid 0.06 (0.01 0.09 (0.01 0.02
+ + •
Nitrogen
Starch
Fat
0.04 0.1) 0.11 0.3) 0.01 0.03)
0.91 (0.56 1.3 (0.83 0.97 (0.20
+ 0.45 - 1.7) +__0.64 - 2.3) _ 0.79 - 2.0)
0.18 (0.10 0.23 (0.14 0.13 (0.05
+ • • -
0.08 0.28) 0.07 0.32) 0.05 0.20)
99.1 (98.4 99.4 (98.3 99.8 (99.6
+ • • -
0.67 99.9) 0.66 99.9) 0.17 100)
95.7 (92.6 94.5 (91.8 95.6 (90.6
+ • • -
1.8 97.3) 2.3 96.6) 3.5 98.6)
0.01 + 0.01 ( 0 - 0.03) 0.01 + 0.02 (0 - 0.04)
1.50 (0.46 1.4 (0.36
_ + -
0.26 (0.15 0.17 (0.07
• _ -
0.09 0.37) 0.06 0.20)
99.9 (99.8 99.8 (99.5
+ + -
0.05 99.9) 0.17 99.9)
91.5 (82.0 91.9 (85.6
+ + -
6.1 96.9) 4.1 97.0)
(0 -
1.1 3.1) 0.78 2.5)
those of lower molecular weights, are transformed i n t e s t i n a l b a c t e r i a i n t o lactic acid. 12 W h e n
by
feeding of
a n d 23 g m / d a y ( 4 5 a n d 85 g m / m 2 / d a y )
s t a r c h is n o t f o l l o w e d b y e x c e s s i v e f e c a l e x c r e t i o n o f
corresponds
lactic a c i d as well as o f g l u c o s e , d ~ x t r i n s , a n d p o l y s a c -
fed milk formulas
char•
•
it c a n b e c o n c l u d e d c o n f i d e n t l y t h a t s t a r c h is
in 1- a n d 3 - m o -
o l d i n f a n t s , r e s p e c t i v e l y ; t h e q u a n t i t y o f 10 g m o f s t a r c h to t h e q u a n t i t y g i v e n to 1 - m o - o l d i n f a n t s containing
not only sucrose
but also small amounts
and
of the polysac-
w e l l d i g e s t e d a n d a b s o r b e d . It is p o s s i b l e , h o w e v e r , t h a t
char•
the intestinal microflora might utilize starch without
a p p r o x i m a t e l y to t h a t g i v e n to 3 - m o - o l d i n f a n t s r e c e i v -
T h e q u a n t i t y o f 23 g m o f s t a r c h c o r r e s p o n d s
p r o d u c i n g a n i n c r e a s e in fecal e x c r e t i o n o f lactic a c i d o r
i n g , in a d d i t i o n to s u c h m i l k , c o m m e r c i a l l y
Of h y d r o l y t i c p r o d u c t s o f t h e p o l y s a c c h a r i d e .
cereals.
W i t h t h i s l i m i t a t i o n in m i n d , w e s t u d i e d t h e d i g e s t ibility o f v a r i o u s s t a r c h e s in a m o u n t s a p p r o x i m a t i n g
10
The results clearly demonstrate
prepared
that young infants
are capable of digesting the quantities of the starches
54
De Vizia et al.
The Journal of Pediatrics January 1975
Table IV. Absorption of rice starch in 1-mo-old infants Starch in diet Subject No. 1 2 3 4 5
Quantity Quantity (gm/day) (gmlm2/day) 39.6 31.7 48.6 39.7 40.0
137.7 156.9 186.9 182.1 180.2
Stool findings (gm/day)
Absorption coefficient (%) r 84
Starch 0.07 0.04 0.04 1.1 1.14
G l u c o s e Lactic acid 0 0.27 0 0.46 0.37
which were studied. This may be explained by the fact that the c~-amylase of the intestinal secretions, although low, may still be sufficient to digest dietary starch, or that digestion of starch and of the intermediary products of a-amylolysis might be provided, at least in part, by the glucamylase activity of the maltase, which splits starch and dextrins directly into glucose. 4,6,7In this way mucosal maltases not only complete but also provide alternative pathways for intestinal digestion of starch .7 These results cannot be extended to other kinds of starches or to the same starches which are Processed in a different way. Native granular starches are hydrolyzed b y enzymes t-o different degrees, depending on their botanical origin. Starches whose granular structure has been destroyed by cooking are much more readily hydrolyzed, and differences between varieties are almost eliminated. 13 In this report it is interesting that the absorption of potato starch given as biscuits to 1-yr-old children was improved when biscuits were cooked in water for 10 min (Table I). Larger quantities of rice starch (110 gm/m2/day) are well absorbed by 1-mo-old infants (Table II); it should therefore be possible to provide a large part of carbohydrate requirements of infants from the first months of life with cooked starchesl Further research is necessary before formulas containing starch (and high-molecularweight dextrins) can be utilized instead of formulas containing disaccharides for the feeding of infants. Since the intraluminal hydrSlysis is slow, starch feeding in young infants results in lpwer and more prolonged increases of blood glucose, as compared to feeding with sucrose or other disaccharides. 13-t5Whether or not this is an advantage for the intermediary metabolism remains to be established. Also, long-term experiments are required to study whether starch feeding is compatible with a normal growth in young infants. It should be finally pointed out that the tolerance of y o u n g i n f a n t s to very large quantities of starch is limited, probably as a consequence of low levels of ~-
0.04 0.16 0.01 0.41 0.53
Fat 0.49 0.61 2.2 1.6 1.02
Nitrogen 0.08 0.18 0.39 0.25 0.31
Starch
Fat
99.9 99.0 99.9 96.1 96.3
96.4 94.3 87.0 87.6 92.1
amylase activity in the intestinal juice16: in our experience 178 gm/ma/day of rice starch may cause malabsorption of starch and fermentative diarrhea in 1-moold infants. We thank Dr. N. Pisani of Industria Buitoni, Perugia, Italy, for the generous gift of the flours. REFERENCES
1. Auricchio S, Ciccimarra F, Della Pietra D, and Vegnente A: Intestinal hydrolysis of starch. Symposium on intestinal absorption and malabsorption, Mod Probl Pediatr 11:22, 1968. 2. Auricchio S, Della Pietra D, and Vegnente A: Studies on intestinal digestion of starch in man. II. Intestinal hydrolysis of amylopectin in infants and children, Pediatrics 39:853, 1967. 3. Auricchio S, Semenza G, and Rubino A: Multiplicity of human intestinal disaccharidases. II. Characterization of the individual maltases, Biochim Biophys Acta 96:498, 1965. 4. Thompson DL: Separation and characterization of human intestinal mucosal amylases, Gastroenterology 48:432, 1967. 5. Messer M, and Kerry KR: Intestinal digestion of maltotriose in man, Biochim Biophys Acta 132:432, 1967. 6. Eggermont E: The hydrolysis of the naturally occurring a-glucosides by the human intestinal mucosa, Europ J Biochem 9:483, 1969. 7. Auricchio S, and Ciccimarra F: Glucamylolytic digestion of starch in human intestinal mucosa, Proc 7th Int Congr Clin Chem, Geneva/Evian, 1969; in Digestion and intestinal absorption, Basel, 1970, S. Karger AG, vol 4, pp 45-50. 8. Auricchio S, Rubino A, and M~rset G: Intestinal glycosidase activities in the human embryo, foetus and newborn, Pediatrics 35:944, 1965. 9. Auricchio S, Ciccimarra F, Rubino A, and Prader A: Studies on intestinal digestion of starch in man. III.,The absorption coefficient of starch in infants and children, Enzymol Biol Clin 9:321, 1968. 10. Kamer JH van de, Bokkel Huinink H ten, and Weijers HA: Rapid method for the determination of fat in feces, J Biol Chem 177:347, 1969. 11. Weijers HA, Kamer JH van de, Dicke WK, and Ijsseling
Volume 86 Number 1
J: Diarrhea caused by deficiency of sugar splitting enzymes, I. Acta Paediatr 50:55, 1961. 12. Auricchio S, Ciccimarra F, and De Vizia B: Starch malabsorption, Proc XIII Int Congr Pediatr, Wien, 1971; in Nutrition and gastroenterology Wien, 1971, Wiener Medizinische Akademie, vol 2, pp 139-150, 13. Filer LJ: Modified food starches for use in infant foods, Nutr Rev 29:55, 1971. 14. Husband J, Husband P, and Mallinson CN: Gastric
Starch digestibility in infants
55
emptying of starch meals in the newborn, Lancet 2:290, 1970. 15. Anderson ThA, Fomon S, and Filer LJ: Carbohydrate tolerance studies with 3-day-old infants, J Lab Clin Med 79:31, 1972. 16. Lilibridge CB, and Townes PL: Physiologic deficiency of pancreatic amylase in infancy: A factor in iatrogenic diarrhea, J PEDIATR82:279, 1973.
50
The Journal o f P E D I A T R I C S
Digestibility of starches in infants and children The digestibility of various starches has been studied in normal infants o f d~ff'erent ages. During balance periods of 3 days, while the infiTnts were receiving known dietary quantities of the starch to be tested, the fecal content o f lactic acid, glucose, dextrins, and starch was measured After the first year of liJe, children were able to absorb almost completely 170 gm/m 2 o f body surface of cooked wheat starch given in the.form of biscuit or macaroni. A lower absorption coefficient was found for potato starch given in the form of biscuit. Cooked wheat, tapioca, corn, rice, and potato starch in amounts of 45 and 85 gm/m21day, respectively, for 1-and 3-moold infants, were almost completely absorbed. In 1-mo-old infants larger amounts (110 gm/m2/day) of cooked rice starch were well tolerated; it should therefore be possible to provide a large part o f the carbohydrate requirements of infants from the first month o f life with cooked starches.
B. De Vizia, M.D., F. Ciccimarra, M.D., N. De Cicco, M.D., and S. A u r i c c h i o , M . D . , * N a p l e s , I t a l y
THE ABILITY of the intestine to digest and absorb starch depends upon the efficiency of intraluminal and mucosal digestion and the transport of glucose through the brush border m e m b r a n e of the enterocyte. 1 In adults and children starch is rapidly hydrolyzed in the intestinal lumen by salivary and pancreatic amylase to glucose, maltose, maltotriose, and b r a n c h e d dextrins. 2 These carbohydrates are further hydr01yzed to glucose by the so-called maltases of the brush border of the enterocyte. 3-7 In infants the intraluminal c~-amylolytic digestion of starch is slow, because of the low level of a-amylase activity in the intestine. = T h e most active m a l t a s e s (sucrase and isomaltase) are, however, fully developed at birth. 8 Starch is one of the carbohydrates added to some formulas fed to infants during the first months of life. In spite of the early introduction of starch into the infant's d i e t o n l y p r e l i m i n a r y d a t a are a v a i l a b l e o n t h e digestibility of starch in infancy. 9
From the Institute of Pediatrics, H Faculty o f Medicine, University of Naples. The present research was supported in part by a grant from the Italian Department of Health. *Reprint address: Clinica Pediatrica, 2 ~Facolt~ di ,~'ledicina e Chirurgia; Via Orsolone ai Cangiani 80131, Napoli, Italy.
Vol. 86, No. 1, pp. 50-55
In the p r e s e n t study the digestibility o f various starches has been studied in normal infants of different ages by measuring, in balance periods of 3 days, the fecal content of lactic acid, glucose, dextrins, and starch and by relating the quantities excreted to the starch content of the diet.
MATERIALS AND METHODS During the first month of life infants were given halfs k i m acidified p o w d e r e d milk c o n t a i n i n g sucrose, maltose, and dextrins as added carbohydrates, and during the second and third months an acidified powdered whole m i l k containing sucrose, maltose, dextrins, and starch as added carbohydrates. Starch represented 1.9 gm/dl of the diluted formula. Normal infants 30 to 50 days of age (1-mo-old infants) and 90 to 110 days of age (3-too-old infants) were studied while receiving a diet containing wheat, corn, and tapioca starches during three successive metabolic study periods, each lasting 3 days. Each starch was introduced in the diet 3 days before the beginning of stool collections. A second group of normal infants of the same age was investigated, with the same procedure, while being fed a diet c o n t a i n i n g p o t a t o and rice starches. The formula during the balance periods was composed of cow's milk, 100 ml/kg body weight; water, 60
Volume 86 Number 1
Starch digestibility in infants
51
Table I. Absorption of starch in children 1-2 yr of age (mean values + 1 SD and observed ranges in parentheses) I
Starch in diet No. of ubjects 20
Kind of starch
Quantity (gm/m2/day) Starch
Stool findings (gm/day)
Glucose
Lact& acM
Fat 2.4 '• 0.92 (1.2 -4.4)
Nitrogen
Absorption coefficient (%)
Starch
Fat
99.6 • 0.25 94.6 • 2.7 (99.1 - 99.9) (90.3 - 97.3)
Wheat (biscuits and macaroni)
170 • 21 0.37 _+ 0.2 0.03 • 0.04 (125 - 200) (0.02 - 0.66) (0 - 0.13)
5
Potato (biscuits)
180 • 23 5.5 • 3.5 (140 - 200) (1.80 - 9.6)
3
3 • 0.82 0.62 • 0.26 99.7 + 0.15 93.2 • 2.3 Potato 162 • 16 0.12 • 0.1 0.01 • 0.01 0.04 • 0.04 (0-0.02) (0-0.08) (2.3-.3.9) (0.46-0.92) (99.6-99.9) (90.6-94.6) (biscuits cooked (148 - 180) (0 - 0.19) in water)
0.23 • 0.48 0.11 + 0.0.7 1.9 • 0.65 0.63 • 0.18 92.6 • 4.4 94.9 • 1.7 ( 0 - 1.1) (0.05- 0.20) (0.97- 2.6) (0.38 - 0.82) (87 4 - 96.7) (92.9 - 97.5)
and 40 ml/kg for 1- and 3-mo-old infants, respectively; the concentration of carbohydrate in the diluted cow's milk was 6 and 7% for 1- and 3-too-old infants, respectively. The added carbohydrates were represented by sucrose and approximately 10 or 23 gm (45 or 85 gin/ m2/day) of each kind of starch for 1- and 3-mo-old infants. Starch was given as flour from wheat, corn, tapioca, potato, and rice cooked for 10 rain in the water necessarY for the dilution of cow's milk. The starch concentration in 100 ml of the diluted cow's milk was 1.76 gm --- 0.32 and 3,28 gm + 0.71 (mean ---+ 1 SD) for 1and 3-too-old infants, respectively. Four normal 1-mo-old infants were tested for their capacity tO digest larger quantities of rice starch. In the diet of these children carbohydrates were added to the diluted cow's milk in the concentration of 6%. The added carbohydrates were represented by sucrose and approximately 25 gm of rice starch (110 gm/m2/day). The starch concentration in 100 ml of the diluted cow's milk was 4.46 gm -+ 0.28 (mean --+ 1 SD). A group of 1- to 2-yr-old children was also studied. The diet of these subjects contained the following carbohydrates: lactose (cow's milk 500 ml/day), sucrose (25 gin/day), a n d starch (170 g m / m 2 / d a y ) ; wheat starch was given to some of the Children as biscuits and m a c a r o n i (the former a c c o u n t i n g for 35% of total starch); in the diet of other children potato starch was provided in biscuits. During balance periods of 3 days stools were collected from the children receiving a standard diet and immediately frozen. The food was marked with carmine red at the beginning of the first and the fourth days of each balance period. Starch was assayed in food and stool according to the method previously described. 9 The starch content in food was calculated by multiplying by 0.9 the d,uantity
of glucose determined after enzymatic hydrolysis of starch by glucamylase from Rhizopus delemar. The factor of 0.9 is derived on the basis that during hydrolysis water is added to the starch molecule With a consequent increase in weight of approximately 10%. There was no free glucose in the food. Glucose was determined in stools both before (free glucose) and after enzymatic hydrolysis of starch (dextrins and malto-oligosaccharides) by the glucamylase method. The "starch" content in stool was calculated in the following way: quantity of glucose after enzymatic hydrolysis minus quantity of free glucose in stool, multiplied by 0.9. The absorption coefficient of starch was calculated from the glucose of the diet and from the total glucose of stools after enzymatic hydrolysis. The content of fat, 1~ lactic acid, 1~ and nitrogen in stools was also determined. RESULTS After the first year of life children were able to absorb almost completely 170 g m / m 2of body surface of cooked wheat starch as biscuits and macaroni. The same results were obtained when children were given the total quantity of wheat starch either as biscuit or as macaroni ~tlone. A lower absorption coefficient was observed for potato starch given as biscuits; w h e n biscuits were cooked in water for 10 rain, potato starch was almost completely absorbed (Table I). W h e a t , tapioca, corn, rice, and potato starch in amounts of 45 and 85 gm/m2/day were almost completely absorbed in 1- and 3-too-old infants when fed as cooked flours. This was well demonstrated for each starch by the very low fecal excretion of lactic acid, glucose, dextrins, and starch. The absorption coefficient of starch was higher than 98% in all infants studied. W h e n the amounts of starch indicated above were used
52
De Vizia et al.
The Journal of Pediatrics January 1975
T a b l e II. A b s o r p t i o n o f v a r i o u s s t a r c h e s in 1 - m o - o l d i n f a n t s ( m e a n v a l u e s - 1 S D a n d o b s e r v e d r a n g e s in
Starch in diet
No. of subjects
K&d of starch Wheat Corn Tapioca
Rice Potato
4
Stool findings (gm/day)
Quantity (gm/m2/day)
Quantity (gm/day) 10.6 • (7.5 11.8• (11.3 10.5 • (9.2 -
1.8 12.3) 0.47 12.4) 0.74 11.0)
46.8 (32.0 51.8 (46.2 45.4 (38.4
• + _ -
10.5 (7.7 10.1 (8.7
1.9 11.7) 0.97 10.7)
48.5 (35.2 46.7 (39.7
• 8.9 -- 54.0) -4- 5.0 -- 50.6)
Rice
• • -
Concentration in diluted cow's milk (gm/dl)
25
1.7 ___0.43 (1.2 - 2 . 3 ) 1.9 • 0.36 (1.6 - 2 . 5 ) 1.7 • 0.34 (1.3 - 2 . 2 )
9.2 55.1) 5.4 60.0) 7.0 54.7)
1.7 (1.3 1.6 (1.5
111.8 _+ 6.8 (102.0--117.9)
• -• --
0.28 1.9) 0.14 1.7)
4.5 • 0.28 (4.2--4.9)
Glucose
Starch 0.05 (0.02 0.02 (0.009 0.04 (0.01
_ 0.04 - 0.12) +_ 0.02 - 0.067) • 0.03 - 0.08)
0
(0.01 (0 0.02 (0.01
• 0.00) - 0.01) • 0.01 -- 0.03)
(0 -- 0.01) 0
0.33 • 0.34 (0.03--0.66)
0.01 • 0.01 (0--0.02)
0 (0 - 0.01) 0 _ 0.01 (0 - 0.02) 0
T a b l e III. A b s o r p t i o n o f v a r i o u s s t a r c h e s in 3 - m o - o l d i n f a n t s ( m e a n v a l u e s +_ 1 S D a n d o b s e r v e d r a n g e s in
Starch in diet
No. of subjects 5
Kind of starch Wheat Corn Tapioca
Rice Potato
Quantity (gm/day)
Stool findings (gm/day) Concentration in the diluted cow's milk (gm/dl)
Quantity (gm/m2/day)
21.9 ( 13.4 24.4 ( 15.9 22.3 (18.0
_ • -• -
4.8 24.3) 4.9 28.2) 2.5 24.3)
83.2 (47.8 92.2 (57.1 84.1 (65.9
• -_ -• --
21.7 103.4) 20.9 105.0) 13.2 96.3)
24.0 (23.5 21.9 (19.6
• 0.44 - 24.3) ___ 1.4 - 23.0)
89.1 (80.7 81.5 (76.7
• -_ --
6.5 97.2) 4.4 87.8)
3.2 ( 1.7 3.5 (2.1 3.2 (2.3 3.4 (2.8 3.1 (0.02
• • • -
Starch
1.1 4.2) 1.0 4.6) 0.69 3.9)
0.18 (0.01 0.13 (0.01 0.04 (0
• 0.15 - 0.34) • 0.16 -- 0.41) ___0.03 - 0.08)
___0.44 - 4.0) • 0.29 - 0.1)
0.02 (0.01 0.05 (0.02
• 0.02 -- 0.05) + 0.03 -- 0.1)
Glucose 0.03 (0.01 0.03 (0 0.01 (0
• 0.01 -- 0.04) • 0.03 -- 0.08) • 0.01 -- 0.02)
0.01 _+ 0.01 (0 -- 0.02) 0
in t h e fecal e x c r e t i o n o f fat a n d n i t r o g e n ( T a b l e s II a n d
c o w ' s m i l k in a c o n c e n t r a t i o n o f 6 g m / d l ; t h e q u a n t i t y o f s t a r c h f e d to t h e s e i n f a n t s w a s a p p r o x i m a t e l y 40 g m / day (178 g m / m 2 / d a y ) . T w o i n f a n t s d e v e l o p e d a f e r m e n -
III). D u r i n g t h e s e c o n d m o n t h o f life, larger a m o u n t s o f
glucose, dextrins, and starch (Table IV; Subjects 4 and
c o o k e d rice s t a r c h w e r e well t o l e r a t e d : 110 g m / m 2 / d a y
5).
in t h e diet, n o d i f f e r e n c e w a s a p p a r e n t in d i g e s t i b i l i t y among various starches. No differences were observed
o f this s t a r c h w e r e a b s o r b e d a l m o s t c o m p l e t e l y ( T a b l e II). T h e t o l e r a n c e for still larger q u a n t i t i e s o f c o o k e d rice s t a r c h w a s s t u d i e d in five i n f a n t s d u r i n g t h e s e c o n d m o n t h o f life ( T a b l e I V ) . I n t h e diet o f t h e s e i n f a n t s , s t a r c h w a s t h e o n l y c a r b o h y d r a t e a d d e d to t h e d i l u t e d
tative diarrhea
with high excretion
of lactic acid,
DISCUSSION M a l a b s o r p t i o n o f s t a r c h is a s s o c i a t e d w i t h t h e fecal e x c r e t i o n o f t h e p o l y s a c c h a r i d e a n d its i n t e r m e d i a r y p r o d u c t s o f i n t e s t i n a l h y d r o l y s i s ; t h e latter, e x p e c i a l l y
Volume 86 Number 1
Starch digestibility in infants
53
parentheses)
Absorption coefficient (%)
Lactic acid 0.02 0 0.02 (0.01 0.02
Fat
Nitrogen
Starch
___0.02 - 0.04 • 0.02 - 0.07) • 0.02 - 0.04)
0.99 (0.65 0.84 (0.46 0.98 (0.44
• • • -
0.32 1.4) 0.32 1.2) 0.58 1.9)
0.22 (0.14 0.19 (0.11 0.16 (0.10
• • • -
0.01 • 0.01 ( 0 - 0.02) 0.01 • 0.01 (0 - 0.03)
0.93 (0.51 1.1 (0.73
• • -
0.34 1.2) 0.35 1.6)
0.18 (0.12 0.15 (0.07
_• 0.06 - 0.26) _ 0.08 - 0.27)
0.19 • 0.04 (0.14 - 0.23)
(0
0.06 • 0.04 (0.03 - 0.12)
1.2 • 0.50 (0.63 - 1.7)
0.10 0.39) 0.05 0.25) 0.06 0.25)
99.4 (98.4 99.8 (99.4 99.6 (99.2
• • • -
Fat
0.6 99.7) 0.2 99.9) 0.2 99.8)
92.6 (90.1 93.5 (90.0 92.9 (88.0
• • • -
2.4 95.4) 2.8 96.9) 3.6 97.0)
99.8 _ 0.1 (99.7 - 99.9)
93.0 (90.8 91.6 ( 88.0
• • -
2.5 96.0) 2.6 94.0)
98.7 • 1.4 (97.3 - 99.9)
90.1 • 3.9 (86.0 - 94.7)
99.9
parentheses)
Absorption coefficient (%)
Fat
Lact& acid 0.06 (0.01 0.09 (0.01 0.02
+ + •
Nitrogen
Starch
Fat
0.04 0.1) 0.11 0.3) 0.01 0.03)
0.91 (0.56 1.3 (0.83 0.97 (0.20
+ 0.45 - 1.7) +__0.64 - 2.3) _ 0.79 - 2.0)
0.18 (0.10 0.23 (0.14 0.13 (0.05
+ • • -
0.08 0.28) 0.07 0.32) 0.05 0.20)
99.1 (98.4 99.4 (98.3 99.8 (99.6
+ • • -
0.67 99.9) 0.66 99.9) 0.17 100)
95.7 (92.6 94.5 (91.8 95.6 (90.6
+ • • -
1.8 97.3) 2.3 96.6) 3.5 98.6)
0.01 + 0.01 ( 0 - 0.03) 0.01 + 0.02 (0 - 0.04)
1.50 (0.46 1.4 (0.36
_ + -
0.26 (0.15 0.17 (0.07
• _ -
0.09 0.37) 0.06 0.20)
99.9 (99.8 99.8 (99.5
+ + -
0.05 99.9) 0.17 99.9)
91.5 (82.0 91.9 (85.6
+ + -
6.1 96.9) 4.1 97.0)
(0 -
1.1 3.1) 0.78 2.5)
those of lower molecular weights, are transformed i n t e s t i n a l b a c t e r i a i n t o lactic acid. 12 W h e n
by
feeding of
a n d 23 g m / d a y ( 4 5 a n d 85 g m / m 2 / d a y )
s t a r c h is n o t f o l l o w e d b y e x c e s s i v e f e c a l e x c r e t i o n o f
corresponds
lactic a c i d as well as o f g l u c o s e , d ~ x t r i n s , a n d p o l y s a c -
fed milk formulas
char•
•
it c a n b e c o n c l u d e d c o n f i d e n t l y t h a t s t a r c h is
in 1- a n d 3 - m o -
o l d i n f a n t s , r e s p e c t i v e l y ; t h e q u a n t i t y o f 10 g m o f s t a r c h to t h e q u a n t i t y g i v e n to 1 - m o - o l d i n f a n t s containing
not only sucrose
but also small amounts
and
of the polysac-
w e l l d i g e s t e d a n d a b s o r b e d . It is p o s s i b l e , h o w e v e r , t h a t
char•
the intestinal microflora might utilize starch without
a p p r o x i m a t e l y to t h a t g i v e n to 3 - m o - o l d i n f a n t s r e c e i v -
T h e q u a n t i t y o f 23 g m o f s t a r c h c o r r e s p o n d s
p r o d u c i n g a n i n c r e a s e in fecal e x c r e t i o n o f lactic a c i d o r
i n g , in a d d i t i o n to s u c h m i l k , c o m m e r c i a l l y
Of h y d r o l y t i c p r o d u c t s o f t h e p o l y s a c c h a r i d e .
cereals.
W i t h t h i s l i m i t a t i o n in m i n d , w e s t u d i e d t h e d i g e s t ibility o f v a r i o u s s t a r c h e s in a m o u n t s a p p r o x i m a t i n g
10
The results clearly demonstrate
prepared
that young infants
are capable of digesting the quantities of the starches
54
De Vizia et al.
The Journal of Pediatrics January 1975
Table IV. Absorption of rice starch in 1-mo-old infants Starch in diet Subject No. 1 2 3 4 5
Quantity Quantity (gm/day) (gmlm2/day) 39.6 31.7 48.6 39.7 40.0
137.7 156.9 186.9 182.1 180.2
Stool findings (gm/day)
Absorption coefficient (%) r 84
Starch 0.07 0.04 0.04 1.1 1.14
G l u c o s e Lactic acid 0 0.27 0 0.46 0.37
which were studied. This may be explained by the fact that the c~-amylase of the intestinal secretions, although low, may still be sufficient to digest dietary starch, or that digestion of starch and of the intermediary products of a-amylolysis might be provided, at least in part, by the glucamylase activity of the maltase, which splits starch and dextrins directly into glucose. 4,6,7In this way mucosal maltases not only complete but also provide alternative pathways for intestinal digestion of starch .7 These results cannot be extended to other kinds of starches or to the same starches which are Processed in a different way. Native granular starches are hydrolyzed b y enzymes t-o different degrees, depending on their botanical origin. Starches whose granular structure has been destroyed by cooking are much more readily hydrolyzed, and differences between varieties are almost eliminated. 13 In this report it is interesting that the absorption of potato starch given as biscuits to 1-yr-old children was improved when biscuits were cooked in water for 10 min (Table I). Larger quantities of rice starch (110 gm/m2/day) are well absorbed by 1-mo-old infants (Table II); it should therefore be possible to provide a large part of carbohydrate requirements of infants from the first months of life with cooked starchesl Further research is necessary before formulas containing starch (and high-molecularweight dextrins) can be utilized instead of formulas containing disaccharides for the feeding of infants. Since the intraluminal hydrSlysis is slow, starch feeding in young infants results in lpwer and more prolonged increases of blood glucose, as compared to feeding with sucrose or other disaccharides. 13-t5Whether or not this is an advantage for the intermediary metabolism remains to be established. Also, long-term experiments are required to study whether starch feeding is compatible with a normal growth in young infants. It should be finally pointed out that the tolerance of y o u n g i n f a n t s to very large quantities of starch is limited, probably as a consequence of low levels of ~-
0.04 0.16 0.01 0.41 0.53
Fat 0.49 0.61 2.2 1.6 1.02
Nitrogen 0.08 0.18 0.39 0.25 0.31
Starch
Fat
99.9 99.0 99.9 96.1 96.3
96.4 94.3 87.0 87.6 92.1
amylase activity in the intestinal juice16: in our experience 178 gm/ma/day of rice starch may cause malabsorption of starch and fermentative diarrhea in 1-moold infants. We thank Dr. N. Pisani of Industria Buitoni, Perugia, Italy, for the generous gift of the flours. REFERENCES
1. Auricchio S, Ciccimarra F, Della Pietra D, and Vegnente A: Intestinal hydrolysis of starch. Symposium on intestinal absorption and malabsorption, Mod Probl Pediatr 11:22, 1968. 2. Auricchio S, Della Pietra D, and Vegnente A: Studies on intestinal digestion of starch in man. II. Intestinal hydrolysis of amylopectin in infants and children, Pediatrics 39:853, 1967. 3. Auricchio S, Semenza G, and Rubino A: Multiplicity of human intestinal disaccharidases. II. Characterization of the individual maltases, Biochim Biophys Acta 96:498, 1965. 4. Thompson DL: Separation and characterization of human intestinal mucosal amylases, Gastroenterology 48:432, 1967. 5. Messer M, and Kerry KR: Intestinal digestion of maltotriose in man, Biochim Biophys Acta 132:432, 1967. 6. Eggermont E: The hydrolysis of the naturally occurring a-glucosides by the human intestinal mucosa, Europ J Biochem 9:483, 1969. 7. Auricchio S, and Ciccimarra F: Glucamylolytic digestion of starch in human intestinal mucosa, Proc 7th Int Congr Clin Chem, Geneva/Evian, 1969; in Digestion and intestinal absorption, Basel, 1970, S. Karger AG, vol 4, pp 45-50. 8. Auricchio S, Rubino A, and M~rset G: Intestinal glycosidase activities in the human embryo, foetus and newborn, Pediatrics 35:944, 1965. 9. Auricchio S, Ciccimarra F, Rubino A, and Prader A: Studies on intestinal digestion of starch in man. III.,The absorption coefficient of starch in infants and children, Enzymol Biol Clin 9:321, 1968. 10. Kamer JH van de, Bokkel Huinink H ten, and Weijers HA: Rapid method for the determination of fat in feces, J Biol Chem 177:347, 1969. 11. Weijers HA, Kamer JH van de, Dicke WK, and Ijsseling
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J: Diarrhea caused by deficiency of sugar splitting enzymes, I. Acta Paediatr 50:55, 1961. 12. Auricchio S, Ciccimarra F, and De Vizia B: Starch malabsorption, Proc XIII Int Congr Pediatr, Wien, 1971; in Nutrition and gastroenterology Wien, 1971, Wiener Medizinische Akademie, vol 2, pp 139-150, 13. Filer LJ: Modified food starches for use in infant foods, Nutr Rev 29:55, 1971. 14. Husband J, Husband P, and Mallinson CN: Gastric
Starch digestibility in infants
55
emptying of starch meals in the newborn, Lancet 2:290, 1970. 15. Anderson ThA, Fomon S, and Filer LJ: Carbohydrate tolerance studies with 3-day-old infants, J Lab Clin Med 79:31, 1972. 16. Lilibridge CB, and Townes PL: Physiologic deficiency of pancreatic amylase in infancy: A factor in iatrogenic diarrhea, J PEDIATR82:279, 1973.
