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Infant nutrient supplementation
Infant nutrient supplementation D o n n a M. Curtis, PhD, RD This review addresses vitamin and mineral supplementation recommendations, practices and rationales, patterns of supplement use, and the relationship between supplementation and nutrient concerns for older infants. According to current recommendations, healthy infants do not need supplements if vitamin D-fortified milk is used, the diet includes a d e q u a t e vitamin C, and iron-fortified cereals or formula are used. Infants fed human milk exclusively may need vitamin D supplements. Nevertheless, approximately one third to one half of 6- to 12-month-old U.S. infants receive nutrient supplements, as liquid vitamin A, D, and C preparations or multivitamin preparations, with or without iron or fluoride. Recent surveys suggest that most infants have more than a d e q u a t e vitamin and mineral intakes, with the possible exception of iron. The risk of poor vitamin A status is less likely than the risk of poor water-soluble-vitamin or iron status in the United States. Possibly marginal intakes of zinc and copper (not in currently available infant supplements) suggest the need for further research. Research, infant supplement formulation reevaluation, and education are suggested so that nutrient supplements for prophylaxis can be used most effectively and appropriately. (J PEDIATR1990;117:$410-8)
Vitamin preparations are widely available and used by many people in the United States; vitamin supplementation is especially common during the first few years of life. Infancy is a critical period for growth and development, and nutrient deficiencies, excesses, or imbalances may have significant long-term effects on health, but there is little information that can be used to assess the impact of supplement use on the nutriture of infants. The purpose of this review is to describe current nutrient supplementation recommendations and rationales, supplementation practices, prevalence and patterns of supplement use, and the relationship between supplementation and nutrient status of healthy infants during the second 6 months of life. The information available for this specific age group is limited, so data that encompass older or younger age groupings or apply to other ages are included when they might provide relevant insights. The American Academy of Pediatrics (AAP) Committee on Nutrition t has stated that vitamin and mineral supplements are "usually not required" by normal, healthy infants during the second 6 months of life, although they do point Reprint requests: Donna M. Curtis, PhD, RD, 1700 Princeton Drive, Columbia, MO 65203. 9/0/19675 SI10
out that it is important that the milk used during this time be fortified with vitamin D, and that the diet include an "adequate" source of vitamin C. It is recommended that iron be supplied by iron-fortified infant cereals or iron-fortified formula, both of which are more convenient and reliable than iron supplements. They state, however, that infants "at special nutritional risk as a result of lifestyle, economic disadvantage, or intercurrent illness may require multivitamin and mineral supplements." 1 It is assumed NHANES RDA RNI
National Health and Nutrition Examination Survey Recommended dietary allowance Recommended nutrient intakes (Canadian)
that during the second 6 months of life, human milk-fed and formula-fed infants are receiving a variety of solid foods. 2 Older infants may continue to receive the same supplements that they received in early infancy, so it is also relevant to review the recommendations for normal formulafed infants and breast-fed infants born at term. It is assumed that no additional supplementation is needed during the first 6 months of life if adequate amounts of commercial infant formulas are consumed, because these formulas are fortified with vitamins and minerals. 1
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The AAP Committee on Nutrition recommends vitamin D supplementation for breast-fed infants in certain situations, including inadequate vitamin D nutrition of the mother during pregfmncy and lactation, and low exposure to ultraviolet light. 2 The National Research Council3 recommends a daily supplement of 5 to 7.5 ug cholecalciferol or vitamin D (200 to 300 IU) for breast-fed infants not exposed to sunlight. The need for vitamin D supplementation of exclusively breast-fed infants is an area of controversy.4' 5 Several recent studies 6, 7 have shown no differences in bone mineralization between supplemented and unsupplemented breastfed infants during the first 6 months of life. The vitamin D content of human milk is very low, but other factors may be present that enhance vitamin D activity.8 Moreover, maternal vitamin D supplementation or regular exposure of the mother to ultraviolet light can affect human milk's antirachitic properties. 8 Nevertheless, rickets caused by vitamin D deficiency still occurs in some breast-fed infants.4,5,9 These cases are usually associated with prolonged, unsupplemented breast-feeding and with unconventional lifestyles and dietary practices, such as strict vegetarianism of the mother or infant, or prematurity. Some pediatricians advocate prophylactic vitamin D supplementation for all breast-fed infants, because there is little likelihood of harm from such a practice and it may be difficult to identify which infants are at risk) ~ 11 The Council on Scientific Affairs 12 recommends vitamin B12 supplementation for breast-fed infants whose mothers are strict vegetarians. Alternatively, the mother could take supplements or alter her diet. Certain sea vegetables may contain significant quantities of vitamin B12 and may be acceptable to mothers adhering to strict vegetarian diets) 3 The supplements specifically designed for use during the first year of life are liquid preparations that are either a combination of vitamins A, D, and C, with or without iron, or a multivitamin mixture, with or without iron. (These preparations may also contain fluoride.) Currently (1989) the levels of nutrients provided per daily dose are in voluntary compliance with the 1976 Food and Drug Administration (FDA) regulations, which specified minimum and maximum amounts of nutrients in supplements designed for use by infants or children. 14 (These regulations were revoked in 1979.1, 15) Daily doses of vitamin A, D, and C preparations supply 1500 IU vitamin A, 400 IU vitamin D, and 35 mg vitamin C. These levels are the U. S. recommended daily allowances for infants, which are based on the 1968 RDAs, as specified in the 1976 FDA regulations. The multivitamin preparations for infants provide the same daily amounts of vitamins A, D, and C and, in addition, 5 IU vitamin E, 0.5 mg thiamin, 0.6 mg riboflavin, 8 mg niacin, 0.4 mg vitamin B6, and 1.5 #g vitamin B12. Iron-containi.ng preparations provide 10 mg iron daily) 6 Folic acid
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is relatively unstable in liquid preparations and thus is not included. The vitamin A, D, and C preparations provide vitamin D for breast-fed infants or vitamin C for bottle-fed infants not receiving a commercial formula or a good food source of vitamin C. Today there is not as much concern for vitamin D as there was in the past, except in some exclusively breastfed infants, because nearly all cow milk (including low-fat and nonfat milk), infant formulas, and many foods are fortified with vitamin D in the United States. Even though scurvy is very rare in breast-fed infants,4 the idea that human milk is an inadequate source of vitamin C, like cow milk, has been expressed, 17 and has no doubt influenced supplementation recommendations. Human milk contains approximately 3 to 10 times as much vitamin C as cow milk, 3 and infants who'are exclusively breast fed for up to 12 months without maternal or infant nutrient supplementation mantain relatively high plasma vitamin C concentrations) 8 Apparently, vitamin A is present in the vitamin A, D, and C formulation for historical reasons, l Cod liver oil or other fish liver oils were given to infants to prevent rickets, and the fish liver oils also supplied considerable quantities of vitamin A. Milk is a good source of vitamin A; currently, even the use of low-fat and nonfat milk (which is not recommended during the first year of life) does not necessitate vitamin A supplementation, because most of the low-fat milks available in the United States are fortified with vitamin A. Vitamin A deficiency rarely occurs in breast-fed infants. Thus the current recommendations of the AAP Committee on Nutrition state that there would be "no harm in omitting vitamin A" from supplements designed to provide vitamin D to breast-fed infantsJ P A T T E R N S OF S U P P L E M E N T THE UNITED STATES
U S E IN
In 1981 a Child Health Supplement, which included questions about nutrient supplement use, was added to the National Health Interview Survey.19 It was administered to a national probability sample of approximately 42,000 families, and the data were weighted to represent all children of the United States. Nearly half (46.3%) of all children up to 2 years of age had received some type of vitamin or mineral preparation during the 2-week period before the interview. The percentage of 3- to 6-year-old children receiving supplements was similar (48.6%); a smaller percentage of older children had received supplements (34.4% of children 7 to 11 years and 26.4% of children 12 to 17 years of age). This study also found that supplement use was highest (41% of all ages) during the first quarter (January through March) and lowest (33.7% of all ages) during the third quarter (July through September). These results are in agreement with those of a Canadian study in which a
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The Journal of Pediatrics August 1990
100
90 ao 7o
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6o 50
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40 3o
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1-2
3-4
5-10
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11-19 25'-44 45-64 65-74
Age in Years Fig. 4. Percent•fp•pu•ati•nusingvitamin•rminera•supp•ementsasfuncti•n•fageandgenderacc•rdingt•NHANES II (1976-1980), based on interviews of national probability sample of noninstitutionalized U.S. population. Solid bars represent subjects who used vitamin or mineral supplements regularly; hatched bars represent those who used vitamin or mineral supplementsirregularly. (Respondents or their guardians were asked, "Are you currently taking vitamins or minerals?" Possible responses were "yes, regularly [i.e., daily]"; "irregularly"; or "no.") Data for boys and girls for three youngest age groupings were combined. (Data from an analysis of NHANES II data by Looker AC, Sempos CT, Johnson CL, Yetley EA. Am J Clin Nutr 1987;46:665-72and J Am Diet Assoc 1988;88:808-14.)
number of parents stated that they thought that infants needed additional vitamins during the winter months to prevent colds. 2~ The National Health and Nutrition Examination Survey of 1976 to 1980 (NHANES II) included a question about whether or not the respondent was taking vitamin or mineral supplements regularly or irregularly.21 The supplements were classified into 29 different groups, but no attempt was made to quantify nutrient contributions from these supplements. In contrast to N H A N E S I (19711974), this survey did include 6- to 12-month-old infants. However, the data for this age group have not yet been analyzed in relation to supplement use, according to a conversation with C. Johnson, of the National Center for Health Statistics (September 1989). Looker et al. 22' 23 examined more closely the data related to supplement use in other age groups, and one can make limited inferences based on these data; 41.7% of the children in the 1- to 2-year age group used supplements regularly. The total percentage of users in this age group, which included those who took supplements irregularly, was 55.4% 22 (Fig. 1). This is comparable to the data from the National Health Interview Survey, discussed above, which was done a few years later and which used a different criterion for supplement use. In the older age groups (5 to 19 years of age), there were significantly fewer
(p <0.05) children who used supplements, suggesting that supplement use is highest in the early years. Supplement use was relatively low in the teenage groupings but was greater in the adult age groupings.22, 23 In 1986 the National Center for Health Statistics 24 conducted another survey that focused on adults and children aged 2 to 6 years. They excluded those persons who were taking only prescription vitamin and mineral products--3% of the total sample. The results indicated that 43.3% of the children in this age group took supplements. This suggests that the use of supplements has not changed greatly since the late 1970s or early 1980s. The Gerber Nutrition Surveys25 collected information on supplement use of U.S. infants and also quantified the nutrient contribution from these supplements. For the most recent survey, in 1986, a representative sample of mothers with infants 2 to 12 months old were contacted by telephone in 20 cities throughout the United States. Mothers of 637 infants completed a 4-day diary and a questionnaire that were returned by mail (personal communication from S. J. Bartholmey, PhD, Gerber Products Co., Fremont, Mich., September 1989). Among all the infants surveyed, 31% were using supplements, and 33% of infants 6 months of age or older were using supplements (unpublished data, Gerber Products Co.). As Table I indicates, the number of supple-
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Table I. Infants using supplements according to the Gerber Nutrition Survey, 1986" Age (mo)
N Supplement users (%)
2
3
4
5
6
7
8
9
10
11
12
53 28
67 22
64 36
61 30
66 24
57 33
62 31
57 35
60 25
53 43
37 46
*From data providedby S. J. Bartholmey,PhD, GerberProducts Co., Fremont,Mich.Personalcommunication,September 1989. N, Total numberof infantsparticipatingin the survey.
ment users in the older age groups, the 11- and 12-monthold samples, was greatest, and these percentages, 43% and 46%, respectively, are comparable to the percentages derived from the other surveys cited above. Information is not available on the demographics of infant supplement users in the United States, but the data for older children give some insights into which groups are more likely to use supplements. Looker et al. 22 examined the demographics of supplement users 1 to 19 years of age by means of N H A N E S II data. Supplement users in two or more age groups were more likely to be white, have economic status above the poverty level, and have a household head with a higher level of education. Users in all age groups were more likely to reside in the Northeast. The data from the 1986 National Center for Health Statistics survey24 indicated the same trends. Among 2- to 6-year-old children, 46.3% of white children, but only 30.3% of black children, used supplements. Socioeconomic level also was related to supplement use, with only 22.8% of children in families whose income was less than $7000 using supplements, compared with 50.3% of children in families with incomes of $40,000 or more. Furthermore, 26.9% of children whose responsible parent had an educational level of less than 12 years used supplements, in comparison with 51% of children whose responsible parent had 13 years or more of education. In this 1986 survey the regional differences were less dramatic than in the N H A N E S II survey, ranging from 39.2% users in the Northeast to 47.2% users in the West. One can only speculate on the relationship of these data to the demographics of supplement use in infancy. Another study also suggested that low socioeconomic status might be associated with less nutrient supplementation. The regular supplement use by children (in 1980) in households receiving Aid to Families with Dependent Children in northern Mississippi was only about 11%.26 This contrasts with the overall percentage of 36% of children younger than 18 years of age who had used supplements according to the National Health Interview Survey. 19 The ages of the Mississippi children were not presented.
According to the Gerber Nutrition Survey of 1986, approximately 64% of supplement users (2 to 12 months old) were receiving a vitamin A, D, and C preparation (unpublished data, Gerber Products Co.). In a study of Canadian children less than 3 years old, 94% of those receiving supplements were receiving a combination of vitamins A, D, and C. 27 As children get older, a larger percentage consume multivitamin preparations. According to the recent National Center for Health Statistics survey,24 74.8% of supplement users, 2 to 6 years of age, consume multivitamin preparations and more than 85% use only one nutrient supplementation product. Of all the nutients, vitamin C was included in supplementation more than any other nutrient, with 94% of these children taking vitamin C in some form. 24 There is very little information that addresses the reasons that parents give supplements. In a Canadian study 2~ the two main reasons indicated for giving supplements to infants 6 months of age or older were "to supplement the diet" (41%) and "to follow advice of the doctor" (29%). Another reason indicated was "perceived importance for infants or that they needed additional vitamins in the winter months to ward off colds" (7%). They also assessed the reasons for not giving supplements, which were as follows: "Infants were eating well and therefore vitamin supplements were not necessary" (37%); "Physicians considered them unnecessary" (10%); "Infants refused to eat vitamin supplements or were 'intolerant'" (8%); and Vitamin supplements are ',fattening or costly" (2%). Thirty percent of those categorized as nonusers did use vitamin supplements occasionally (mainly in the winter months). A survey of the infant feeding recommendations of Nebraska family practice physicians indicated the gap between current recommendations and practice. 28 All the physicians who responded indicated that they recommended a commercially prepared formula for bottle-fed infants, and 64% recommended an iron-fortified formula. However, 80% reported that they were also recommending a vitamin supplement for bottle-fed infants. Eighty-five percent reported recommending vitamin supplements, and 60% reported
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T a b l e II. Mean and percentile nutrient intakes of infants 6 to 11 months of age according to N H A N E S II (1976-1980) Percentiles
Vitamin A (IU) Male (n = 179) Female (n = 177) Thiamin (mg) Male Female Riboflavin (mg) Male Female Niacin (preformed) (mg) Male Female Vitamin C (mg) Male Female Iron (mg) Male Female
Mean intake
5th
10th
25th
50th
95th
5567 4237
1011 1250
1305 1539
2032 2047
3370 3052
18,874 13,122
0.82 0.83
0.31 0.31
0.36 0.35
0.49 0.54
0.72 0.73
1.81 1.75
1.83 1.73
0.57 0.57
0.85 0.79
1.28 1.17
1.65 1.61
3.55 3.22
8.92 8.55
2.84 2.66
3.64 3.20
4.73 4.89
8.39 7.93
19.16 16.98
63 72
11 9
14 13
23 31
51 51
170 261
12.81 12.88
2.23 2.21
2.58 3.37
4.26 4.83
8.25 9.36
43.79 40.18
Data from dietary intake sourcedata: UnitedStates, 1976-80. Hyattsville,Md.: National Center for Health Statistics, 1983; DHHS publication no (PHS) 831681.
recommending iron supplements for breast-fed infants. Supplements with added iron were being recommended by physicians who were routinely prescribing iron-fortified formula. In an earlier nationwide survey of breast-feeding practices conducted in 1980, 88% of pediatricians and 90% of family practitioners indicated that they were recommending vitamin supplementation always or sometimes for breast-fed infants. 29 Iron supplements were sometimes or always recommended for breast-fed infants by 71% of the pediatricians and 86% of the family practitioners. INFANT NUTRIENT STATUS AND ITS RELATIONSHIP TO S U P P L E M E N T USE The available data suggest that most infants and young children receive more than adequate intakes of vitamins without the need for additional supplementation. However, a small percentage of infants may be receiving less than the RDAs 3 for certain nutrients. Nutrient consumption at less than RD A levels does not necessarily imply nutrient deficiency, because RDAs are set above average requirement levels, but it does imply an increased risk of deficiency. According to Montalto and Benson's analyses of the N H A N E S II data, 3~ solid foods supplied 52% of infants' energy intakes at 7 to 8 months of age, and 64% of the energy at 11 to 12 months of age. The median intakes of vitamin A, thiamin, riboflavin, niacin, and vitamin C exceeded the RDAs for infants 7 to 12 months of age. 3~
With the exception of vitamin C for the 9- to 10-month-old infants, the median intakes from solid foods alone met or exceeded the RDAs. 3~ Similar results have been obtained from other surveys, including the Ross Laboratories Infant Nutrition Survey, 32 the Nationwide Food Consumption Survey (1977-1978), 33 and the Gerber Nutrition Surveys. 25 In the Nationwide Food Consumption Survey, 33 the intakes of vitamins B6 and B12 were also quantified, and the median intakes by 7- to 12-month-old infants also exceeded the RDAs. Vitamin E and folacin were not measured in these surveys. A recent survey indicated that 1- to 3-year-old children had a mean vitamin E intake of 5.6 mg atocopherol equivalents per day and a mean folacin intake of 180 #g/day. 34 The 1989 RDAs for these children are 6 mg a-tocopherol equivalents and 50 #g folacin. 3 In contrast to the other surveys, the Gerber Nutrition Surveys 25 quantified and included the contribution to nutrient intakes from supplements and human milk, and the discussion that follows includes both supplemented and unsupplemented infants. The Gerber Nutrition Survey of 1986 indicated that 6% of the 2- to 12-month-old infants surveyed consumed less than the 1980 RD A 35 for vitamin A, and 1% consumed less than two thirds of the 1980 RDA. (The 1980 RDAs for vitamin A for infants up to 6 months of age and for infants from 6 months to 1 year of age were 420 and 400 retinol equivalents, respectively, whereas the 1989 RD A is 375 retinol equivalents for the entire first year.l, 3, 35 Eight percent received less than the RDA for vi-
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I n f a n t nutrient supplementation
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roUser Total I DUser-ExcludingSupplement r]Non User
oot
6 Months of Age
400 ]
~
200-
~
100-
OOll 400
200 I00]~/
o
o Vitamin A Thiamin "Riboflavin" Niacin Vitamin C"
12 Months of Age
, i
[_
Vitamin A Thiamin .Riboflavin Niacin Vit.aminC
Fig. 2.
Mean vitamin intakes expressed as percentage of RDAs (National Research Council, 19893) of non-breast-fed Canadian infants, 6 and 12 months of age, who were users and nonusers of vitamin supplements. Solid bars represent mean daily vitamin intakes of supplement users according to 4-day dietary records and including contribution of supplements. Hatched bars represent mean daily intakes of supplement users excluding intakes from supplements. Open bars represent mean daily intakes of supplement nonusers. Data were from 217 users and 61 nonusers at 6 months of age, and 240 users and 72 nonusers at 12 months of age. (Data at 12 months include many of the same infants who were assessed at 6 months. Additional infants who were being fed human milk at 6 months of age were included in the 12-month-old cohort.) (Calculations based on data of Yeung DL, Pennell MD, Leung M. Nutr Res 1984;4:811-8.)
tamin C. The ages of the infants who received less than the R D A were not presented, but the mean intakes of both of these nutrients were higher during the later part of infancy. The mean intakes of B vitamins were less in 1986 than in 1972, and part of this difference could be attributed to decreased intakes from supplements. In addition, more infants' intakes were less than the 1980 R D A s for B vitamins than for vitamins A or C; 26% received less than the 1980 R D A for thiamin, 19% received less than the 1980 R D A for riboflavin, and 48% received less than the 1980 (and 1989) R D A for vitamin B 6. Twenty-four percent received less than two thirds of the R D A for vitamin B6. (The 1980 R D A s for thiamin and riboflavin for 6- to 12-month-old infants were 0.5 mg and 0.6 mg, respectively, and the 1989 R D A s are 0.4 and 0.5 mg, respectively. The R D A s for these nutrients during the first 6 months and the vitamin B6 R D A for infancy were not changed.) The fact that more supplement users were receiving vitamins A and C than the B vitamins can account for only a small part of these differences. The data from N H A N E S 1136 also show that intakes at the low end of the spectrum for vitamin A are not as much of a concern as intakes of some of the water-soluble vitamins (Table II). At least 95% of 6- to 11-month-old infants consumed more than two thirds of the 1989 R D A for vitamin
A. Toxicity would seem to be a greater concern, because the 95th percentile intake for male infants was 18,874 IU; this included only the contribution from foods, so the actual intakes were higher for those taking supplements. The 5th percentile intakes of vitamin C and niacin were tess than two thirds of the 1989 R D A . However, the niacin equivalents that could be derived from dietary tryptophan were not included. Vitamin C and the B vitamins are more likely than fat-soluble vitamins to be affected by storage and preparation losses, such as losses into cooking water, so actual intakes of unsupplemented persons may be lower than intakes calculated from food composition data. Because cow milk is a poor source of vitamin C, intakes of this vitamin during the second 6 months of life were affected by the type of milk feeding. Montalto et al. 31 found that the 25th, 50th, and 75th percentile vitamin C intakes of formula-fed infants were 49, 64, and 103 mg, respectively. These contrast with the 25th, 50th, and 75th percentile intakes of 20, 39, and 63 mg of cow milk-fed infants. The study by Yeung et al. 2~ of young children in Canada quantified vitamin intakes of supplement users and nonusers. This analysis included only those subjects who were not breast fed, because no attempt was made to quantify intakes from human milk. The nutrient intakes of most in-
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T a b l e III. Mean serum levels of vitamins A, E, and C, and folic acid according to feeding practice at 6 and 12 months Age
Vitamin
Vitamin A (~g/dl) Vitamin E (mg/dl) Vitamin C (mg/dl) Folic acid (ng/dl)
6 mo
12 mo
Feeding practice
No.
Mean
SD
No.
Mean
SD
Bottle Breast* Bottle Breast Bottle Breast Bottle Breast
200 98 202 99 195 99 126 64
79.3 84.7 0.44] 0.49]" 0.52]" 0.62]" 14.7 16.7
32.7 35.8 0.11 0.1 ! 0.21 0.22 6.6 7.5
193 88 194 88 186 90 145 64
67.5 65.5 0.47 0.47 0.58 0.61 15.1:~ 17.0:~
33.2 29.1 0.14 0.13 0.25 0:24 5.9 6.9
Reprinted with permissionfrom VobeckyJS, VobeckyJ, Shapcott D, DemacrsP, BlanehardR, FischC. lnt J VitamNutr Res 1985;55:205-16. *Breast fed longerthan 2 weeks. "~p<0.001. Sp <0.05. fants were ample, and vitamin intakes from foods for supplement users and nonusers were similar (Fig. 2). In addition, this study determined the percentage of infants who were not receiving the Canadian Recommended Nutrient Intakes. Of 314 one-year-old infants, the percentages not receiving the RNIs for vitamin A, thiamin, riboflavin, and vitamin C were 1.9%, 5.1%, 0%, and 2.5%, respectively. If vitamin supplements had not been consumed, these percentages would have increased only slightly to 7.3%, 6.1%, 0, and 6.7%, respectively. This finding reflects the general adequacy of these infants' diets. Another Canadian study 27 investigated the relationship between intakes and serum levels of vitamins A, C, and E and folates. This study followed 325 apparently healthy infants from birth to 3 years of age. The dietary data were based on 24-hour recalls. By 12 months of age, 95% of the infants consumed more than 120% of the RNI for vitamin C, and a similar trend was noted for vitamin A. However, the majority of infants consumed less than 80% of the RNI for folates and vitamin E at all ages. At 6 months of age, those infants who had been breast fed had higher mean serum vitamin levels than those who had been bottle fed, regardless of vitamin supplementation (Table III). The types of bottle feedings used were not reported. The investigators found no deficient serum values for vitamin A in any infant at any age. Ninety percent of these infants were receiving vitamin supplements at 6 months, and usage decreased to 36% at 24 months. Most of those taking supplements were taking the combination of vitamins A, D, and C. Those infants taking supplements had higher serum levels of vitamins A and C. The authors stated that more unsupplemented infants had suboptimal serum values of one or more vitamins than supplemented infants had, but the data were not presented. Intakes of calcium and phosphorus by most 6- to 12-
month-old infants appear to be adequate, according to N H A N E S II, 31 the Nationwide Food Consumption Survey,33 the Ross Laboratories Infant Nutrition Survey,32 and the Gerber Nutrition Surveys. 25 Magnesium intakes are adequate according to the Nationwide Food Consumption Survey33 and the Gerber Nutrition Surveys.25 Calcium intakes can be less than RDAs if insufficient dairy products are consumed. According to the 1986 Gerber Nutrition Survey,25 10% of the infants were consuming less than two thirds of the 1980 RDA for calcium. Since the 1989 RDAs for calcium are higher, this percentage might be higher if intakes had been compared with the latter RDAs. Iron is most likely to be consumed at inadequate levels in this age group. The estimated prevalence of iron deficiency of children aged 1 to 2 years in the United States, based on NHANES II biochemical data, is about 9%, which is one of the highest prevalence rates among the gender and age groups sampled. 37 The prevalence of iron deficiency anemia is decreasing in the United States, indicating that this problem is preventable. The decrease is attributed to favorable changes in infant feeding practices. 3s Montalto et a130. 31 found that the choice of weaning foods and milk can have a considerable impact on the iron intake of infants during the second 6 months of life, according to the NHANES II data. The median iron intake of infants fed cow milk was 7.8 mg, or 78% of the 1989 RDA, whereas the median iron intakes of infants fed iron-fortified formula were 14.7 mg at 7 to 8 months, 17 mg at 9 to 10 months, and 15.8 mg at 11 to 12 months of age. Cow milk is not only a poor source of iron; it also may increase iron losses. 39 Montalto et al. 31 also found that fewer cow milk-fed infants, who could most benefit from the extra iron, than formula-fed infants consumed dry infant cereal. The Ross Laboratories Infant Nutrition Survey32 and the Nationwide
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Food Consumption Survey33 also indicated that the median iron intakes of older infants who received iron-fortified formula exceeded the RDA, whereas the median intakes of infants given regular formula or cow milk were generally less than the RDA. From the Ross Laboratories Infant Nutrition Survey, Martinez et al. 32 found that only 27.6% of infants (6.5 to 13.4 months of age) fed cow milk and 9.3% of infants fed regular formula received iron supplementation on a regular basis. Of those fed cow milk who received less than the RDA of iron from the diet, only 23.1% received iron supplementation, and the proportion receiving supplemental iron decreased with age. Trace elements other than iron have been largely ignored in infant nutrition, and little is known about optimal intake amounts. Zinc supplementation, for example, merits further investigation because marginal zinc deficiencies have been associated with slower growth rates in young children.4~ A recent double-blind, controlled study42 demonstrated significant effects on weight when zinc sulfate was administered to young children 8 to 27 months of age who had poor growth rates and no known medical cause of growth failure. According to the Gerber Nutrition Surveys, 25 zinc intakes were close to the RDAs for all infant age groups, and 27% consumed less than two thirds of the 1980 RDA in the 1986 survey. (The 1980 zinc RDAs were 3 mg for the first 6 months and 5 mg for the second 6 months of life35; the 1989 zinc RDA is 5 mg for the entire first year3.) Zinc supplementation (or any trace element supplementation) must be approached with caution, however, because of the interaction between elements and other dietary constituents. Festa et al. 43 found that the copper status of adult men was impaired when 18.5 mg of zinc was ingested. (The zinc RDA for men is 15 mg3.) Copper deficiency has been documented in infants fed cow milk-based diets while recovering from malnutrition.44 Because of the uncertainty about the requirements for copper, RDAs have not been established, but the estimated safe and adequate range of dietary copper intake for infants 6 to 12 months of age was set at 0.6 to 0.7 mg/day; this level is believed to include a considerable margin of safety. 3 Typical diets of 6- to 11-month-old infants, according to the Total Diet Study, 45 contain about 0.45 mg copper. CONCLUSIONS AND RECOMMENDATIONS On the basis of extrapolations from several national surveys, approximately one third to one half of infants in the second half year of life are receiving nutrient supplementation, even though the AAP Committee on Nutrition suggests that most healthy children at this age do not need them. According to the Gerber Nutrition Surveys, infants
Infant nutrient supplementation
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are receiving the liquid products specifically designed for them, the preparations of vitamins A, D, and C or the multivitamin preparations (with or without iron). The survey data for older children suggest that supplements are being used most by persons in the upper socioeconomic groups; these may be the persons who are least likely to benefit from supplementation. The choice of supplements also may be inappropriate. Both the nutrient survey data and the Nebraska survey of physicians suggest that supplementation practices are not consistent with the risks of nutrient deficiency. Large numbers of infants are receiving the preparations of vitamins A, D, and C, even though there may be less risk of deficiency in infancy for these nutrients than for some of the B vitamins or, possibly, vitamin E. The use of cow milk rather than iron-fortified formula during the second 6 months of life increases the risk for inadequate intakes of vitamin C and iron. Certain infants may be at particular risk for nutrient deficiencies during the second 6 months. These include infants with erratic or poor food intakes, those who consume cow milk during the first year of life, and those who Consume unconventional diets such as vegetarian diets. For all these groups, a multivitamin preparation would be the supplement of choice. On the basis of what is known, it appears that physicians and parents can be better informed about the appropriate use and choice of supplements for prophylaxis during infancy. More information is needed about the intake during infancy of nutrients that are not found in infant nutrient supplements, such as folacin, zinc, and copper, and about the effect of these nutrients on growth and other measures of health. There is also a need to identify the infant feeding patterns that increase the risk of nutrient inadequacy so that appropriate dietary recommendations can be made and supplementation can be provided in a rational way. Appreciation is expressed to Sandra Bartholmey, of Gerber Products, for supplying data from the 1986 Gerber Survey and to Julia Boetteher and David Irons for their assistance in obtaining references and in the preparation of figures. REFERENCES 1. Committee on Nutrition, American Academy of Pediatrics. Vitamin and mineral supplement needs in normal children in the United States. Pediatrics 1980;66:1015-21. 2. Committee on Nutrition, American Academy of Pediatrics. Vitamin and mineral supplement needs of normal children in the United States. In: Pediatric nutrition handbook. Elk Grove, I11.:American Academy of Pediatrics, 1985:37-48. 3. National Research Council, Subcommittee on the Tenth Edition of the RDAs. Recommendeddietary allowances. 10th ed. Washington, D.C.: National Academy Press, 1989. 4. Orzalesi M. Do breast and bottle fed babies require vitamin supplements? Acta Paediatr Scand 1982;299(suppl):77-82. 5. Coveney J. Is breast milk the best food for all infants? Hum Nutr: Appl Nutr 1985;39A:179-88.
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Curtis
6. Greer FR, Marshall S. Bone mineral content, serum vitamin D metabolite concentrations, and ultraviolet B light exposure in infants fed human milk with and without vitamin D2 supplements. J PEDIATR 1989;114:204-12. 7. Roberts CC, Chan GM, Folland D, Rayburn C, Jackson R. Adequate bone mineralization in breast-fed infants. J PEDIATR 1981;99:192-6. 8. Greer FR, Tsang RC. Vitamin D in human milk: is there enough? J Pediatr Gastroenterol Nutr 1983;2:$277-81. 9. Hanning RM, Zlotkin SH. Unconventional eating practices and their health implications. Pediatr Clin North Am 1985; 32:429-45. 10. Hayward I, Stein MT, Gibson MI. Nutritional rickets in San Diego. Am J Dis Child 1987;141:1060-2. 11. Finberg L. Human milk feeding and vitamin D supplementation-1981. J PEDIATR 1981;99:228-9. 12. Council on Scientific Affairs. Vitamin preparations as dietary supplements and as therapeutic agents. JAMA 1987;257:1929-36. 13. Specker BL, Miller D, Norman E J, Greene H, Hayes KC. Increased urinary methylmalonic acid excretion in breast-fed infants of vegetarian mothers and identification of an acceptable dietary source of vitamin BL2.Am J Clin Nutr 1988;47:89-92. 14. Title 21: Part 80. Definitions and standards of identity for foods for special dietary uses. Part 125. Label statements concerning dietary properties of food purporting to be or represented for special dietary uses (vitamin and mineral products). Federal Register 1976(Oct 19);41:46156-76. 15. Foods for special dietary use: vitamin and mineral products-revocation of regulations. Federal Register 1979(March t 6);44:16005-6. 16. Physician's desk reference. 43rd ed. Oradell, N.J.: Medical Economics, 1989. 17. Nelson WE, ed. Textbook of pediatrics. 6th to 9th eds. Philadelphia: WB Saunders, 1954, 1959, 1964, 1969. 18. Salmenpera L. Vitamin C nutrition during prolonged lactation: optimal in infants while marginal in some mothers. Am J Clin Nutr 1984;40:1050-6. 19. Kovar MG. Use of medications and vitamin-mineral supplements by children and youth. Public Health Rep 1985;100: 470-3. 20. Yeung DL, Pennell MD, Leung M. Vitamin supplements: are they necessary for infants and preschoolers? Nutr Res 1984;4:811-8. 21. Plan and operation of the second National Health and Nutrition Examination Survey, 1976-1980: programs and collection procedures. Hyattsville, Md.: National Center for Health Statistics, 1981; U.S. Department of Health and Human Services publication no (PHS) 81-1317. (Vital and health statistics; series 1-15.) 22. Looker AC, Sempos CT, Johnson CL, Yetley EA. Comparison of dietary intakes and iron status of vitamin-mineral supplement users and nonusers, aged 1-19 years. Am J Clin Nutr 1987;46:665-72. 23. Looker A, Sempos CT, Johnson C, Yetley EA. Vitamin-mineral supplement use: association with dietary intake and iron status of adults. J Am Diet Assoc 1988;88:808-14. 24. Moss A J, Levy AS, Kim I, Park YK. Use of vitamin and mineral supplements in the United States: current users, types of products, and nutrients. Advance data. Hyattsville, Md.: National Center for Health Statistics, 1989. (Vital and health statistics; no. 174.) 25. Purvis GA, Bartholmey SJ. Infant feeding practices: commercially prepared baby foods. In: Tsang RC, Nichols BF, eds.
The Journal of Pediatrics August 1990
Nutrition during infancy. Philadelphia: Hanley & Belfus, 1988:399-417. 26. Sharpe TR, Smith MC. Use of vitamin-mineral supplements by AFDC children. Public Health Rep 1985;100:321-4. 27. Vobecky JS, Vobecky J, Shapcott D, Demars P, Blanchard R, Fisch C. The vitamin status of infants in a free living population. lnt J Vitam Nutr Res 1985;55:205-16. 28. Auerbach KG, Walburn J. Nebraska family practitioners' infant feeding recommendations. Fam Pract Res J 1987;6:18999. 29. Lawrence RA. Practices and attitudes toward breast-feeding among medical professionals. Pediatrics 1982;70:912-20. 30. Montalto MB, Benson JD. Nutrient intakes of older infants: effect of different milk feedings. J Am Coil Nutr 1986;5:33141. 31. Montalto MB, Benson JD, Martinez GA. Nutrient intakes of formula-fed infants and infants fed cow's milk. Pediatrics 1985;75:343-51. 32. Martinez GA, Ryan AS, Malec DJ. Nutrient intakes of American infants and children fed cow's milk or infant formula. Am J Dis Child 1985;139:1010-8. 33. Martinez GA, Ryan AS. Nutrient intake in the United States during the first 12 months of life. J Am Diet Assoc 1985;85:82630. 34. Nationwide Food Consumption Survey. Continuing survey of food intakes by individuals: women 19-50 years and their children 1-5 years, 4 days, 1985. Hyattsville, Md.: Information Service, U.S. Department of Agriculture, 1987; Report No. 85-4. 35. National Research Council National Academy of Sciences. Recommended dietary allowances. 9th ed. Washington, D.C.: National Academy Press, 1980. 36. Dietary intake source data: United States, 1976-80. Hyattsville, Md.: National Center for Health Statistics, 1983; DHHS publication no (PHS) 83-1681. 37. Yip R. Iron nutritional status defined. In: Filer LJ Jr, ed. Dietary iron: birth to two years. New York: Raven Press, 1989:19-36. 38. Yip R. The changing characteristics of childhood iron nutritional status in the United States. In: Filer LJ Jr, ed. Dietary iron: birth to two years. New York: Raven Press, 1989:37-56. 39. Ziegler EE. Intestinal blood loss by normal infants fed cow's milk. In: Filer LJ Jr, ed. Dietary iron: birth to two years. New York: Raven Press, 1989:75-80. 40. Hambidge KM, Hambidge C, Jacobs M, Gaum JD. Low levels of zinc in hair, anorexia, poor growth, and hypogeusia in children. Pediatr Res 1972;6:868-74. 41. Walravens PA, Krebs NF, Hambidge KM. Linear growth of low-income preschool children receiving a zinc supplement. Am J Clin Nutr 1983;38:195-201. 42. Walravens PA, Hambidge KM, Koepfer DM. Zinc supplernentation in infants with a nutritional pattern of failure to thrive: a double-blind, controlled study. Pediatrics 1989; 38:532-8. 43. Festa MD, Anderson HL, Dowdy RP, Ellersieck MR. Effect of zinc intake on copper excretion and retention in men. Am J Clin Nutr 1985;41:285-92. 44. Castillo-Duran C, Uauy R. Copper deficiency impairs growth of infants recovering from malnutrition. Am J Clin Nutr 1988;47:710-4. 45. Pennington JAT, Young BE, Wilson DB. Nutritional elements in U.S. diets: results from the Total Diet Study, 1982 to 1986. J Am Diet Assoc 1989;89:659-64.
Vitamin preparations are widely available and used by many people in the United States; vitamin supplementation is especially common during the first few years of life. Infancy is a critical period for growth and development, and nutrient deficiencies, excesses, or imbalances may have significant long-term effects on health, but there is little information that can be used to assess the impact of supplement use on the nutriture of infants. The purpose of this review is to describe current nutrient supplementation recommendations and rationales, supplementation practices, prevalence and patterns of supplement use, and the relationship between supplementation and nutrient status of healthy infants during the second 6 months of life. The information available for this specific age group is limited, so data that encompass older or younger age groupings or apply to other ages are included when they might provide relevant insights. The American Academy of Pediatrics (AAP) Committee on Nutrition t has stated that vitamin and mineral supplements are "usually not required" by normal, healthy infants during the second 6 months of life, although they do point Reprint requests: Donna M. Curtis, PhD, RD, 1700 Princeton Drive, Columbia, MO 65203. 9/0/19675 SI10
out that it is important that the milk used during this time be fortified with vitamin D, and that the diet include an "adequate" source of vitamin C. It is recommended that iron be supplied by iron-fortified infant cereals or iron-fortified formula, both of which are more convenient and reliable than iron supplements. They state, however, that infants "at special nutritional risk as a result of lifestyle, economic disadvantage, or intercurrent illness may require multivitamin and mineral supplements." 1 It is assumed NHANES RDA RNI
National Health and Nutrition Examination Survey Recommended dietary allowance Recommended nutrient intakes (Canadian)
that during the second 6 months of life, human milk-fed and formula-fed infants are receiving a variety of solid foods. 2 Older infants may continue to receive the same supplements that they received in early infancy, so it is also relevant to review the recommendations for normal formulafed infants and breast-fed infants born at term. It is assumed that no additional supplementation is needed during the first 6 months of life if adequate amounts of commercial infant formulas are consumed, because these formulas are fortified with vitamins and minerals. 1
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The AAP Committee on Nutrition recommends vitamin D supplementation for breast-fed infants in certain situations, including inadequate vitamin D nutrition of the mother during pregfmncy and lactation, and low exposure to ultraviolet light. 2 The National Research Council3 recommends a daily supplement of 5 to 7.5 ug cholecalciferol or vitamin D (200 to 300 IU) for breast-fed infants not exposed to sunlight. The need for vitamin D supplementation of exclusively breast-fed infants is an area of controversy.4' 5 Several recent studies 6, 7 have shown no differences in bone mineralization between supplemented and unsupplemented breastfed infants during the first 6 months of life. The vitamin D content of human milk is very low, but other factors may be present that enhance vitamin D activity.8 Moreover, maternal vitamin D supplementation or regular exposure of the mother to ultraviolet light can affect human milk's antirachitic properties. 8 Nevertheless, rickets caused by vitamin D deficiency still occurs in some breast-fed infants.4,5,9 These cases are usually associated with prolonged, unsupplemented breast-feeding and with unconventional lifestyles and dietary practices, such as strict vegetarianism of the mother or infant, or prematurity. Some pediatricians advocate prophylactic vitamin D supplementation for all breast-fed infants, because there is little likelihood of harm from such a practice and it may be difficult to identify which infants are at risk) ~ 11 The Council on Scientific Affairs 12 recommends vitamin B12 supplementation for breast-fed infants whose mothers are strict vegetarians. Alternatively, the mother could take supplements or alter her diet. Certain sea vegetables may contain significant quantities of vitamin B12 and may be acceptable to mothers adhering to strict vegetarian diets) 3 The supplements specifically designed for use during the first year of life are liquid preparations that are either a combination of vitamins A, D, and C, with or without iron, or a multivitamin mixture, with or without iron. (These preparations may also contain fluoride.) Currently (1989) the levels of nutrients provided per daily dose are in voluntary compliance with the 1976 Food and Drug Administration (FDA) regulations, which specified minimum and maximum amounts of nutrients in supplements designed for use by infants or children. 14 (These regulations were revoked in 1979.1, 15) Daily doses of vitamin A, D, and C preparations supply 1500 IU vitamin A, 400 IU vitamin D, and 35 mg vitamin C. These levels are the U. S. recommended daily allowances for infants, which are based on the 1968 RDAs, as specified in the 1976 FDA regulations. The multivitamin preparations for infants provide the same daily amounts of vitamins A, D, and C and, in addition, 5 IU vitamin E, 0.5 mg thiamin, 0.6 mg riboflavin, 8 mg niacin, 0.4 mg vitamin B6, and 1.5 #g vitamin B12. Iron-containi.ng preparations provide 10 mg iron daily) 6 Folic acid
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is relatively unstable in liquid preparations and thus is not included. The vitamin A, D, and C preparations provide vitamin D for breast-fed infants or vitamin C for bottle-fed infants not receiving a commercial formula or a good food source of vitamin C. Today there is not as much concern for vitamin D as there was in the past, except in some exclusively breastfed infants, because nearly all cow milk (including low-fat and nonfat milk), infant formulas, and many foods are fortified with vitamin D in the United States. Even though scurvy is very rare in breast-fed infants,4 the idea that human milk is an inadequate source of vitamin C, like cow milk, has been expressed, 17 and has no doubt influenced supplementation recommendations. Human milk contains approximately 3 to 10 times as much vitamin C as cow milk, 3 and infants who'are exclusively breast fed for up to 12 months without maternal or infant nutrient supplementation mantain relatively high plasma vitamin C concentrations) 8 Apparently, vitamin A is present in the vitamin A, D, and C formulation for historical reasons, l Cod liver oil or other fish liver oils were given to infants to prevent rickets, and the fish liver oils also supplied considerable quantities of vitamin A. Milk is a good source of vitamin A; currently, even the use of low-fat and nonfat milk (which is not recommended during the first year of life) does not necessitate vitamin A supplementation, because most of the low-fat milks available in the United States are fortified with vitamin A. Vitamin A deficiency rarely occurs in breast-fed infants. Thus the current recommendations of the AAP Committee on Nutrition state that there would be "no harm in omitting vitamin A" from supplements designed to provide vitamin D to breast-fed infantsJ P A T T E R N S OF S U P P L E M E N T THE UNITED STATES
U S E IN
In 1981 a Child Health Supplement, which included questions about nutrient supplement use, was added to the National Health Interview Survey.19 It was administered to a national probability sample of approximately 42,000 families, and the data were weighted to represent all children of the United States. Nearly half (46.3%) of all children up to 2 years of age had received some type of vitamin or mineral preparation during the 2-week period before the interview. The percentage of 3- to 6-year-old children receiving supplements was similar (48.6%); a smaller percentage of older children had received supplements (34.4% of children 7 to 11 years and 26.4% of children 12 to 17 years of age). This study also found that supplement use was highest (41% of all ages) during the first quarter (January through March) and lowest (33.7% of all ages) during the third quarter (July through September). These results are in agreement with those of a Canadian study in which a
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The Journal of Pediatrics August 1990
100
90 ao 7o
~
6o 50
| | 1
40 3o
|
eo
lO o
I
I
I
I
1-2
3-4
5-10
I
I
I
I
11-19 25'-44 45-64 65-74
Age in Years Fig. 4. Percent•fp•pu•ati•nusingvitamin•rminera•supp•ementsasfuncti•n•fageandgenderacc•rdingt•NHANES II (1976-1980), based on interviews of national probability sample of noninstitutionalized U.S. population. Solid bars represent subjects who used vitamin or mineral supplements regularly; hatched bars represent those who used vitamin or mineral supplementsirregularly. (Respondents or their guardians were asked, "Are you currently taking vitamins or minerals?" Possible responses were "yes, regularly [i.e., daily]"; "irregularly"; or "no.") Data for boys and girls for three youngest age groupings were combined. (Data from an analysis of NHANES II data by Looker AC, Sempos CT, Johnson CL, Yetley EA. Am J Clin Nutr 1987;46:665-72and J Am Diet Assoc 1988;88:808-14.)
number of parents stated that they thought that infants needed additional vitamins during the winter months to prevent colds. 2~ The National Health and Nutrition Examination Survey of 1976 to 1980 (NHANES II) included a question about whether or not the respondent was taking vitamin or mineral supplements regularly or irregularly.21 The supplements were classified into 29 different groups, but no attempt was made to quantify nutrient contributions from these supplements. In contrast to N H A N E S I (19711974), this survey did include 6- to 12-month-old infants. However, the data for this age group have not yet been analyzed in relation to supplement use, according to a conversation with C. Johnson, of the National Center for Health Statistics (September 1989). Looker et al. 22' 23 examined more closely the data related to supplement use in other age groups, and one can make limited inferences based on these data; 41.7% of the children in the 1- to 2-year age group used supplements regularly. The total percentage of users in this age group, which included those who took supplements irregularly, was 55.4% 22 (Fig. 1). This is comparable to the data from the National Health Interview Survey, discussed above, which was done a few years later and which used a different criterion for supplement use. In the older age groups (5 to 19 years of age), there were significantly fewer
(p <0.05) children who used supplements, suggesting that supplement use is highest in the early years. Supplement use was relatively low in the teenage groupings but was greater in the adult age groupings.22, 23 In 1986 the National Center for Health Statistics 24 conducted another survey that focused on adults and children aged 2 to 6 years. They excluded those persons who were taking only prescription vitamin and mineral products--3% of the total sample. The results indicated that 43.3% of the children in this age group took supplements. This suggests that the use of supplements has not changed greatly since the late 1970s or early 1980s. The Gerber Nutrition Surveys25 collected information on supplement use of U.S. infants and also quantified the nutrient contribution from these supplements. For the most recent survey, in 1986, a representative sample of mothers with infants 2 to 12 months old were contacted by telephone in 20 cities throughout the United States. Mothers of 637 infants completed a 4-day diary and a questionnaire that were returned by mail (personal communication from S. J. Bartholmey, PhD, Gerber Products Co., Fremont, Mich., September 1989). Among all the infants surveyed, 31% were using supplements, and 33% of infants 6 months of age or older were using supplements (unpublished data, Gerber Products Co.). As Table I indicates, the number of supple-
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Infant nutrient supplementation
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Table I. Infants using supplements according to the Gerber Nutrition Survey, 1986" Age (mo)
N Supplement users (%)
2
3
4
5
6
7
8
9
10
11
12
53 28
67 22
64 36
61 30
66 24
57 33
62 31
57 35
60 25
53 43
37 46
*From data providedby S. J. Bartholmey,PhD, GerberProducts Co., Fremont,Mich.Personalcommunication,September 1989. N, Total numberof infantsparticipatingin the survey.
ment users in the older age groups, the 11- and 12-monthold samples, was greatest, and these percentages, 43% and 46%, respectively, are comparable to the percentages derived from the other surveys cited above. Information is not available on the demographics of infant supplement users in the United States, but the data for older children give some insights into which groups are more likely to use supplements. Looker et al. 22 examined the demographics of supplement users 1 to 19 years of age by means of N H A N E S II data. Supplement users in two or more age groups were more likely to be white, have economic status above the poverty level, and have a household head with a higher level of education. Users in all age groups were more likely to reside in the Northeast. The data from the 1986 National Center for Health Statistics survey24 indicated the same trends. Among 2- to 6-year-old children, 46.3% of white children, but only 30.3% of black children, used supplements. Socioeconomic level also was related to supplement use, with only 22.8% of children in families whose income was less than $7000 using supplements, compared with 50.3% of children in families with incomes of $40,000 or more. Furthermore, 26.9% of children whose responsible parent had an educational level of less than 12 years used supplements, in comparison with 51% of children whose responsible parent had 13 years or more of education. In this 1986 survey the regional differences were less dramatic than in the N H A N E S II survey, ranging from 39.2% users in the Northeast to 47.2% users in the West. One can only speculate on the relationship of these data to the demographics of supplement use in infancy. Another study also suggested that low socioeconomic status might be associated with less nutrient supplementation. The regular supplement use by children (in 1980) in households receiving Aid to Families with Dependent Children in northern Mississippi was only about 11%.26 This contrasts with the overall percentage of 36% of children younger than 18 years of age who had used supplements according to the National Health Interview Survey. 19 The ages of the Mississippi children were not presented.
According to the Gerber Nutrition Survey of 1986, approximately 64% of supplement users (2 to 12 months old) were receiving a vitamin A, D, and C preparation (unpublished data, Gerber Products Co.). In a study of Canadian children less than 3 years old, 94% of those receiving supplements were receiving a combination of vitamins A, D, and C. 27 As children get older, a larger percentage consume multivitamin preparations. According to the recent National Center for Health Statistics survey,24 74.8% of supplement users, 2 to 6 years of age, consume multivitamin preparations and more than 85% use only one nutrient supplementation product. Of all the nutients, vitamin C was included in supplementation more than any other nutrient, with 94% of these children taking vitamin C in some form. 24 There is very little information that addresses the reasons that parents give supplements. In a Canadian study 2~ the two main reasons indicated for giving supplements to infants 6 months of age or older were "to supplement the diet" (41%) and "to follow advice of the doctor" (29%). Another reason indicated was "perceived importance for infants or that they needed additional vitamins in the winter months to ward off colds" (7%). They also assessed the reasons for not giving supplements, which were as follows: "Infants were eating well and therefore vitamin supplements were not necessary" (37%); "Physicians considered them unnecessary" (10%); "Infants refused to eat vitamin supplements or were 'intolerant'" (8%); and Vitamin supplements are ',fattening or costly" (2%). Thirty percent of those categorized as nonusers did use vitamin supplements occasionally (mainly in the winter months). A survey of the infant feeding recommendations of Nebraska family practice physicians indicated the gap between current recommendations and practice. 28 All the physicians who responded indicated that they recommended a commercially prepared formula for bottle-fed infants, and 64% recommended an iron-fortified formula. However, 80% reported that they were also recommending a vitamin supplement for bottle-fed infants. Eighty-five percent reported recommending vitamin supplements, and 60% reported
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The Journal of Pediatrics August 1990
T a b l e II. Mean and percentile nutrient intakes of infants 6 to 11 months of age according to N H A N E S II (1976-1980) Percentiles
Vitamin A (IU) Male (n = 179) Female (n = 177) Thiamin (mg) Male Female Riboflavin (mg) Male Female Niacin (preformed) (mg) Male Female Vitamin C (mg) Male Female Iron (mg) Male Female
Mean intake
5th
10th
25th
50th
95th
5567 4237
1011 1250
1305 1539
2032 2047
3370 3052
18,874 13,122
0.82 0.83
0.31 0.31
0.36 0.35
0.49 0.54
0.72 0.73
1.81 1.75
1.83 1.73
0.57 0.57
0.85 0.79
1.28 1.17
1.65 1.61
3.55 3.22
8.92 8.55
2.84 2.66
3.64 3.20
4.73 4.89
8.39 7.93
19.16 16.98
63 72
11 9
14 13
23 31
51 51
170 261
12.81 12.88
2.23 2.21
2.58 3.37
4.26 4.83
8.25 9.36
43.79 40.18
Data from dietary intake sourcedata: UnitedStates, 1976-80. Hyattsville,Md.: National Center for Health Statistics, 1983; DHHS publication no (PHS) 831681.
recommending iron supplements for breast-fed infants. Supplements with added iron were being recommended by physicians who were routinely prescribing iron-fortified formula. In an earlier nationwide survey of breast-feeding practices conducted in 1980, 88% of pediatricians and 90% of family practitioners indicated that they were recommending vitamin supplementation always or sometimes for breast-fed infants. 29 Iron supplements were sometimes or always recommended for breast-fed infants by 71% of the pediatricians and 86% of the family practitioners. INFANT NUTRIENT STATUS AND ITS RELATIONSHIP TO S U P P L E M E N T USE The available data suggest that most infants and young children receive more than adequate intakes of vitamins without the need for additional supplementation. However, a small percentage of infants may be receiving less than the RDAs 3 for certain nutrients. Nutrient consumption at less than RD A levels does not necessarily imply nutrient deficiency, because RDAs are set above average requirement levels, but it does imply an increased risk of deficiency. According to Montalto and Benson's analyses of the N H A N E S II data, 3~ solid foods supplied 52% of infants' energy intakes at 7 to 8 months of age, and 64% of the energy at 11 to 12 months of age. The median intakes of vitamin A, thiamin, riboflavin, niacin, and vitamin C exceeded the RDAs for infants 7 to 12 months of age. 3~
With the exception of vitamin C for the 9- to 10-month-old infants, the median intakes from solid foods alone met or exceeded the RDAs. 3~ Similar results have been obtained from other surveys, including the Ross Laboratories Infant Nutrition Survey, 32 the Nationwide Food Consumption Survey (1977-1978), 33 and the Gerber Nutrition Surveys. 25 In the Nationwide Food Consumption Survey, 33 the intakes of vitamins B6 and B12 were also quantified, and the median intakes by 7- to 12-month-old infants also exceeded the RDAs. Vitamin E and folacin were not measured in these surveys. A recent survey indicated that 1- to 3-year-old children had a mean vitamin E intake of 5.6 mg atocopherol equivalents per day and a mean folacin intake of 180 #g/day. 34 The 1989 RDAs for these children are 6 mg a-tocopherol equivalents and 50 #g folacin. 3 In contrast to the other surveys, the Gerber Nutrition Surveys 25 quantified and included the contribution to nutrient intakes from supplements and human milk, and the discussion that follows includes both supplemented and unsupplemented infants. The Gerber Nutrition Survey of 1986 indicated that 6% of the 2- to 12-month-old infants surveyed consumed less than the 1980 RD A 35 for vitamin A, and 1% consumed less than two thirds of the 1980 RDA. (The 1980 RDAs for vitamin A for infants up to 6 months of age and for infants from 6 months to 1 year of age were 420 and 400 retinol equivalents, respectively, whereas the 1989 RD A is 375 retinol equivalents for the entire first year.l, 3, 35 Eight percent received less than the RDA for vi-
Volume 117 Number 2, Part 2
I n f a n t nutrient supplementation
S 115
roUser Total I DUser-ExcludingSupplement r]Non User
oot
6 Months of Age
400 ]
~
200-
~
100-
OOll 400
200 I00]~/
o
o Vitamin A Thiamin "Riboflavin" Niacin Vitamin C"
12 Months of Age
, i
[_
Vitamin A Thiamin .Riboflavin Niacin Vit.aminC
Fig. 2.
Mean vitamin intakes expressed as percentage of RDAs (National Research Council, 19893) of non-breast-fed Canadian infants, 6 and 12 months of age, who were users and nonusers of vitamin supplements. Solid bars represent mean daily vitamin intakes of supplement users according to 4-day dietary records and including contribution of supplements. Hatched bars represent mean daily intakes of supplement users excluding intakes from supplements. Open bars represent mean daily intakes of supplement nonusers. Data were from 217 users and 61 nonusers at 6 months of age, and 240 users and 72 nonusers at 12 months of age. (Data at 12 months include many of the same infants who were assessed at 6 months. Additional infants who were being fed human milk at 6 months of age were included in the 12-month-old cohort.) (Calculations based on data of Yeung DL, Pennell MD, Leung M. Nutr Res 1984;4:811-8.)
tamin C. The ages of the infants who received less than the R D A were not presented, but the mean intakes of both of these nutrients were higher during the later part of infancy. The mean intakes of B vitamins were less in 1986 than in 1972, and part of this difference could be attributed to decreased intakes from supplements. In addition, more infants' intakes were less than the 1980 R D A s for B vitamins than for vitamins A or C; 26% received less than the 1980 R D A for thiamin, 19% received less than the 1980 R D A for riboflavin, and 48% received less than the 1980 (and 1989) R D A for vitamin B 6. Twenty-four percent received less than two thirds of the R D A for vitamin B6. (The 1980 R D A s for thiamin and riboflavin for 6- to 12-month-old infants were 0.5 mg and 0.6 mg, respectively, and the 1989 R D A s are 0.4 and 0.5 mg, respectively. The R D A s for these nutrients during the first 6 months and the vitamin B6 R D A for infancy were not changed.) The fact that more supplement users were receiving vitamins A and C than the B vitamins can account for only a small part of these differences. The data from N H A N E S 1136 also show that intakes at the low end of the spectrum for vitamin A are not as much of a concern as intakes of some of the water-soluble vitamins (Table II). At least 95% of 6- to 11-month-old infants consumed more than two thirds of the 1989 R D A for vitamin
A. Toxicity would seem to be a greater concern, because the 95th percentile intake for male infants was 18,874 IU; this included only the contribution from foods, so the actual intakes were higher for those taking supplements. The 5th percentile intakes of vitamin C and niacin were tess than two thirds of the 1989 R D A . However, the niacin equivalents that could be derived from dietary tryptophan were not included. Vitamin C and the B vitamins are more likely than fat-soluble vitamins to be affected by storage and preparation losses, such as losses into cooking water, so actual intakes of unsupplemented persons may be lower than intakes calculated from food composition data. Because cow milk is a poor source of vitamin C, intakes of this vitamin during the second 6 months of life were affected by the type of milk feeding. Montalto et al. 31 found that the 25th, 50th, and 75th percentile vitamin C intakes of formula-fed infants were 49, 64, and 103 mg, respectively. These contrast with the 25th, 50th, and 75th percentile intakes of 20, 39, and 63 mg of cow milk-fed infants. The study by Yeung et al. 2~ of young children in Canada quantified vitamin intakes of supplement users and nonusers. This analysis included only those subjects who were not breast fed, because no attempt was made to quantify intakes from human milk. The nutrient intakes of most in-
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The Journal of Pediatrics August 1990
T a b l e III. Mean serum levels of vitamins A, E, and C, and folic acid according to feeding practice at 6 and 12 months Age
Vitamin
Vitamin A (~g/dl) Vitamin E (mg/dl) Vitamin C (mg/dl) Folic acid (ng/dl)
6 mo
12 mo
Feeding practice
No.
Mean
SD
No.
Mean
SD
Bottle Breast* Bottle Breast Bottle Breast Bottle Breast
200 98 202 99 195 99 126 64
79.3 84.7 0.44] 0.49]" 0.52]" 0.62]" 14.7 16.7
32.7 35.8 0.11 0.1 ! 0.21 0.22 6.6 7.5
193 88 194 88 186 90 145 64
67.5 65.5 0.47 0.47 0.58 0.61 15.1:~ 17.0:~
33.2 29.1 0.14 0.13 0.25 0:24 5.9 6.9
Reprinted with permissionfrom VobeckyJS, VobeckyJ, Shapcott D, DemacrsP, BlanehardR, FischC. lnt J VitamNutr Res 1985;55:205-16. *Breast fed longerthan 2 weeks. "~p<0.001. Sp <0.05. fants were ample, and vitamin intakes from foods for supplement users and nonusers were similar (Fig. 2). In addition, this study determined the percentage of infants who were not receiving the Canadian Recommended Nutrient Intakes. Of 314 one-year-old infants, the percentages not receiving the RNIs for vitamin A, thiamin, riboflavin, and vitamin C were 1.9%, 5.1%, 0%, and 2.5%, respectively. If vitamin supplements had not been consumed, these percentages would have increased only slightly to 7.3%, 6.1%, 0, and 6.7%, respectively. This finding reflects the general adequacy of these infants' diets. Another Canadian study 27 investigated the relationship between intakes and serum levels of vitamins A, C, and E and folates. This study followed 325 apparently healthy infants from birth to 3 years of age. The dietary data were based on 24-hour recalls. By 12 months of age, 95% of the infants consumed more than 120% of the RNI for vitamin C, and a similar trend was noted for vitamin A. However, the majority of infants consumed less than 80% of the RNI for folates and vitamin E at all ages. At 6 months of age, those infants who had been breast fed had higher mean serum vitamin levels than those who had been bottle fed, regardless of vitamin supplementation (Table III). The types of bottle feedings used were not reported. The investigators found no deficient serum values for vitamin A in any infant at any age. Ninety percent of these infants were receiving vitamin supplements at 6 months, and usage decreased to 36% at 24 months. Most of those taking supplements were taking the combination of vitamins A, D, and C. Those infants taking supplements had higher serum levels of vitamins A and C. The authors stated that more unsupplemented infants had suboptimal serum values of one or more vitamins than supplemented infants had, but the data were not presented. Intakes of calcium and phosphorus by most 6- to 12-
month-old infants appear to be adequate, according to N H A N E S II, 31 the Nationwide Food Consumption Survey,33 the Ross Laboratories Infant Nutrition Survey,32 and the Gerber Nutrition Surveys. 25 Magnesium intakes are adequate according to the Nationwide Food Consumption Survey33 and the Gerber Nutrition Surveys.25 Calcium intakes can be less than RDAs if insufficient dairy products are consumed. According to the 1986 Gerber Nutrition Survey,25 10% of the infants were consuming less than two thirds of the 1980 RDA for calcium. Since the 1989 RDAs for calcium are higher, this percentage might be higher if intakes had been compared with the latter RDAs. Iron is most likely to be consumed at inadequate levels in this age group. The estimated prevalence of iron deficiency of children aged 1 to 2 years in the United States, based on NHANES II biochemical data, is about 9%, which is one of the highest prevalence rates among the gender and age groups sampled. 37 The prevalence of iron deficiency anemia is decreasing in the United States, indicating that this problem is preventable. The decrease is attributed to favorable changes in infant feeding practices. 3s Montalto et a130. 31 found that the choice of weaning foods and milk can have a considerable impact on the iron intake of infants during the second 6 months of life, according to the NHANES II data. The median iron intake of infants fed cow milk was 7.8 mg, or 78% of the 1989 RDA, whereas the median iron intakes of infants fed iron-fortified formula were 14.7 mg at 7 to 8 months, 17 mg at 9 to 10 months, and 15.8 mg at 11 to 12 months of age. Cow milk is not only a poor source of iron; it also may increase iron losses. 39 Montalto et al. 31 also found that fewer cow milk-fed infants, who could most benefit from the extra iron, than formula-fed infants consumed dry infant cereal. The Ross Laboratories Infant Nutrition Survey32 and the Nationwide
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Food Consumption Survey33 also indicated that the median iron intakes of older infants who received iron-fortified formula exceeded the RDA, whereas the median intakes of infants given regular formula or cow milk were generally less than the RDA. From the Ross Laboratories Infant Nutrition Survey, Martinez et al. 32 found that only 27.6% of infants (6.5 to 13.4 months of age) fed cow milk and 9.3% of infants fed regular formula received iron supplementation on a regular basis. Of those fed cow milk who received less than the RDA of iron from the diet, only 23.1% received iron supplementation, and the proportion receiving supplemental iron decreased with age. Trace elements other than iron have been largely ignored in infant nutrition, and little is known about optimal intake amounts. Zinc supplementation, for example, merits further investigation because marginal zinc deficiencies have been associated with slower growth rates in young children.4~ A recent double-blind, controlled study42 demonstrated significant effects on weight when zinc sulfate was administered to young children 8 to 27 months of age who had poor growth rates and no known medical cause of growth failure. According to the Gerber Nutrition Surveys, 25 zinc intakes were close to the RDAs for all infant age groups, and 27% consumed less than two thirds of the 1980 RDA in the 1986 survey. (The 1980 zinc RDAs were 3 mg for the first 6 months and 5 mg for the second 6 months of life35; the 1989 zinc RDA is 5 mg for the entire first year3.) Zinc supplementation (or any trace element supplementation) must be approached with caution, however, because of the interaction between elements and other dietary constituents. Festa et al. 43 found that the copper status of adult men was impaired when 18.5 mg of zinc was ingested. (The zinc RDA for men is 15 mg3.) Copper deficiency has been documented in infants fed cow milk-based diets while recovering from malnutrition.44 Because of the uncertainty about the requirements for copper, RDAs have not been established, but the estimated safe and adequate range of dietary copper intake for infants 6 to 12 months of age was set at 0.6 to 0.7 mg/day; this level is believed to include a considerable margin of safety. 3 Typical diets of 6- to 11-month-old infants, according to the Total Diet Study, 45 contain about 0.45 mg copper. CONCLUSIONS AND RECOMMENDATIONS On the basis of extrapolations from several national surveys, approximately one third to one half of infants in the second half year of life are receiving nutrient supplementation, even though the AAP Committee on Nutrition suggests that most healthy children at this age do not need them. According to the Gerber Nutrition Surveys, infants
Infant nutrient supplementation
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are receiving the liquid products specifically designed for them, the preparations of vitamins A, D, and C or the multivitamin preparations (with or without iron). The survey data for older children suggest that supplements are being used most by persons in the upper socioeconomic groups; these may be the persons who are least likely to benefit from supplementation. The choice of supplements also may be inappropriate. Both the nutrient survey data and the Nebraska survey of physicians suggest that supplementation practices are not consistent with the risks of nutrient deficiency. Large numbers of infants are receiving the preparations of vitamins A, D, and C, even though there may be less risk of deficiency in infancy for these nutrients than for some of the B vitamins or, possibly, vitamin E. The use of cow milk rather than iron-fortified formula during the second 6 months of life increases the risk for inadequate intakes of vitamin C and iron. Certain infants may be at particular risk for nutrient deficiencies during the second 6 months. These include infants with erratic or poor food intakes, those who consume cow milk during the first year of life, and those who Consume unconventional diets such as vegetarian diets. For all these groups, a multivitamin preparation would be the supplement of choice. On the basis of what is known, it appears that physicians and parents can be better informed about the appropriate use and choice of supplements for prophylaxis during infancy. More information is needed about the intake during infancy of nutrients that are not found in infant nutrient supplements, such as folacin, zinc, and copper, and about the effect of these nutrients on growth and other measures of health. There is also a need to identify the infant feeding patterns that increase the risk of nutrient inadequacy so that appropriate dietary recommendations can be made and supplementation can be provided in a rational way. Appreciation is expressed to Sandra Bartholmey, of Gerber Products, for supplying data from the 1986 Gerber Survey and to Julia Boetteher and David Irons for their assistance in obtaining references and in the preparation of figures. REFERENCES 1. Committee on Nutrition, American Academy of Pediatrics. Vitamin and mineral supplement needs in normal children in the United States. Pediatrics 1980;66:1015-21. 2. Committee on Nutrition, American Academy of Pediatrics. Vitamin and mineral supplement needs of normal children in the United States. In: Pediatric nutrition handbook. Elk Grove, I11.:American Academy of Pediatrics, 1985:37-48. 3. National Research Council, Subcommittee on the Tenth Edition of the RDAs. Recommendeddietary allowances. 10th ed. Washington, D.C.: National Academy Press, 1989. 4. Orzalesi M. Do breast and bottle fed babies require vitamin supplements? Acta Paediatr Scand 1982;299(suppl):77-82. 5. Coveney J. Is breast milk the best food for all infants? Hum Nutr: Appl Nutr 1985;39A:179-88.
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6. Greer FR, Marshall S. Bone mineral content, serum vitamin D metabolite concentrations, and ultraviolet B light exposure in infants fed human milk with and without vitamin D2 supplements. J PEDIATR 1989;114:204-12. 7. Roberts CC, Chan GM, Folland D, Rayburn C, Jackson R. Adequate bone mineralization in breast-fed infants. J PEDIATR 1981;99:192-6. 8. Greer FR, Tsang RC. Vitamin D in human milk: is there enough? J Pediatr Gastroenterol Nutr 1983;2:$277-81. 9. Hanning RM, Zlotkin SH. Unconventional eating practices and their health implications. Pediatr Clin North Am 1985; 32:429-45. 10. Hayward I, Stein MT, Gibson MI. Nutritional rickets in San Diego. Am J Dis Child 1987;141:1060-2. 11. Finberg L. Human milk feeding and vitamin D supplementation-1981. J PEDIATR 1981;99:228-9. 12. Council on Scientific Affairs. Vitamin preparations as dietary supplements and as therapeutic agents. JAMA 1987;257:1929-36. 13. Specker BL, Miller D, Norman E J, Greene H, Hayes KC. Increased urinary methylmalonic acid excretion in breast-fed infants of vegetarian mothers and identification of an acceptable dietary source of vitamin BL2.Am J Clin Nutr 1988;47:89-92. 14. Title 21: Part 80. Definitions and standards of identity for foods for special dietary uses. Part 125. Label statements concerning dietary properties of food purporting to be or represented for special dietary uses (vitamin and mineral products). Federal Register 1976(Oct 19);41:46156-76. 15. Foods for special dietary use: vitamin and mineral products-revocation of regulations. Federal Register 1979(March t 6);44:16005-6. 16. Physician's desk reference. 43rd ed. Oradell, N.J.: Medical Economics, 1989. 17. Nelson WE, ed. Textbook of pediatrics. 6th to 9th eds. Philadelphia: WB Saunders, 1954, 1959, 1964, 1969. 18. Salmenpera L. Vitamin C nutrition during prolonged lactation: optimal in infants while marginal in some mothers. Am J Clin Nutr 1984;40:1050-6. 19. Kovar MG. Use of medications and vitamin-mineral supplements by children and youth. Public Health Rep 1985;100: 470-3. 20. Yeung DL, Pennell MD, Leung M. Vitamin supplements: are they necessary for infants and preschoolers? Nutr Res 1984;4:811-8. 21. Plan and operation of the second National Health and Nutrition Examination Survey, 1976-1980: programs and collection procedures. Hyattsville, Md.: National Center for Health Statistics, 1981; U.S. Department of Health and Human Services publication no (PHS) 81-1317. (Vital and health statistics; series 1-15.) 22. Looker AC, Sempos CT, Johnson CL, Yetley EA. Comparison of dietary intakes and iron status of vitamin-mineral supplement users and nonusers, aged 1-19 years. Am J Clin Nutr 1987;46:665-72. 23. Looker A, Sempos CT, Johnson C, Yetley EA. Vitamin-mineral supplement use: association with dietary intake and iron status of adults. J Am Diet Assoc 1988;88:808-14. 24. Moss A J, Levy AS, Kim I, Park YK. Use of vitamin and mineral supplements in the United States: current users, types of products, and nutrients. Advance data. Hyattsville, Md.: National Center for Health Statistics, 1989. (Vital and health statistics; no. 174.) 25. Purvis GA, Bartholmey SJ. Infant feeding practices: commercially prepared baby foods. In: Tsang RC, Nichols BF, eds.
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Nutrition during infancy. Philadelphia: Hanley & Belfus, 1988:399-417. 26. Sharpe TR, Smith MC. Use of vitamin-mineral supplements by AFDC children. Public Health Rep 1985;100:321-4. 27. Vobecky JS, Vobecky J, Shapcott D, Demars P, Blanchard R, Fisch C. The vitamin status of infants in a free living population. lnt J Vitam Nutr Res 1985;55:205-16. 28. Auerbach KG, Walburn J. Nebraska family practitioners' infant feeding recommendations. Fam Pract Res J 1987;6:18999. 29. Lawrence RA. Practices and attitudes toward breast-feeding among medical professionals. Pediatrics 1982;70:912-20. 30. Montalto MB, Benson JD. Nutrient intakes of older infants: effect of different milk feedings. J Am Coil Nutr 1986;5:33141. 31. Montalto MB, Benson JD, Martinez GA. Nutrient intakes of formula-fed infants and infants fed cow's milk. Pediatrics 1985;75:343-51. 32. Martinez GA, Ryan AS, Malec DJ. Nutrient intakes of American infants and children fed cow's milk or infant formula. Am J Dis Child 1985;139:1010-8. 33. Martinez GA, Ryan AS. Nutrient intake in the United States during the first 12 months of life. J Am Diet Assoc 1985;85:82630. 34. Nationwide Food Consumption Survey. Continuing survey of food intakes by individuals: women 19-50 years and their children 1-5 years, 4 days, 1985. Hyattsville, Md.: Information Service, U.S. Department of Agriculture, 1987; Report No. 85-4. 35. National Research Council National Academy of Sciences. Recommended dietary allowances. 9th ed. Washington, D.C.: National Academy Press, 1980. 36. Dietary intake source data: United States, 1976-80. Hyattsville, Md.: National Center for Health Statistics, 1983; DHHS publication no (PHS) 83-1681. 37. Yip R. Iron nutritional status defined. In: Filer LJ Jr, ed. Dietary iron: birth to two years. New York: Raven Press, 1989:19-36. 38. Yip R. The changing characteristics of childhood iron nutritional status in the United States. In: Filer LJ Jr, ed. Dietary iron: birth to two years. New York: Raven Press, 1989:37-56. 39. Ziegler EE. Intestinal blood loss by normal infants fed cow's milk. In: Filer LJ Jr, ed. Dietary iron: birth to two years. New York: Raven Press, 1989:75-80. 40. Hambidge KM, Hambidge C, Jacobs M, Gaum JD. Low levels of zinc in hair, anorexia, poor growth, and hypogeusia in children. Pediatr Res 1972;6:868-74. 41. Walravens PA, Krebs NF, Hambidge KM. Linear growth of low-income preschool children receiving a zinc supplement. Am J Clin Nutr 1983;38:195-201. 42. Walravens PA, Hambidge KM, Koepfer DM. Zinc supplernentation in infants with a nutritional pattern of failure to thrive: a double-blind, controlled study. Pediatrics 1989; 38:532-8. 43. Festa MD, Anderson HL, Dowdy RP, Ellersieck MR. Effect of zinc intake on copper excretion and retention in men. Am J Clin Nutr 1985;41:285-92. 44. Castillo-Duran C, Uauy R. Copper deficiency impairs growth of infants recovering from malnutrition. Am J Clin Nutr 1988;47:710-4. 45. Pennington JAT, Young BE, Wilson DB. Nutritional elements in U.S. diets: results from the Total Diet Study, 1982 to 1986. J Am Diet Assoc 1989;89:659-64.