Safety of a Fat-reduced Diet: The Dietary Intervention Study in Children (DISC)
Objective. To assess the relationship between energy intake from fat and anthropometric, biochemical, and dietary measures of nutritional adequacy and safety.
Design. Three-year longitudinal study of children participating in a randomized controlled trial; intervention and usual care group data pooled to assess effects of self-reported fat intake; longitudinal regression analyses of measurements at baseline, year 1, and year 3.
Participants. Six hundred sixty-three children (362 boys and 301 girls), 8 to 10 years of age at baseline, with elevated low-density lipoprotein cholesterol, who are participants of the Dietary Intervention Study in Children.
Measures. Energy intake from fat assessed from three 24-hour recalls at each time point was the independent variable. Outcomes were anthropometric measures (height, weight, body mass index, and sum of skinfolds), nutritional biochemical determinations (serum ferritin, zinc, retinol, albumin, β-carotene, and vitamin E, red blood cell folate, and hemoglobin), and dietary micronutrients (vitamins A, C, E, thiamin, riboflavin, niacin, vitamins B-6, B-12, folate, calcium, iron, zinc, magnesium, and phosphorus).
Results. Lower fat intake was not related to anthropometric measures or serum zinc, retinol, albumin, β-carotene, or vitamin E. Lower fat intake was related to: 1) higher levels of red blood cell folate and hemoglobin, with a trend toward higher serum ferritin; 2) higher intakes of folate, vitamin C, and vitamin A, with a trend toward higher iron intake; 3) lower intakes of calcium, zinc, magnesium, phosphorus, vitamin B-12, thiamin, niacin, and riboflavin; 4) increased risk of consuming less than two-thirds of the Recommended Dietary Allowances for calcium in girls at baseline, and zinc and vitamin E in boys and girls at all visits.
Conclusions. Lower fat intakes during puberty are nutritionally adequate for growth and for maintenance of normal levels of nutritional biochemical measures, and are associated with beneficial effects on blood folate and hemoglobin. Although lower fat diets were related to lower self-reported intakes of several nutrients, no adverse effects were observed on blood biochemical measures of nutritional status. Current public health recommendations for moderately lower fat intakes in children during puberty may be followed safely.
To reduce risk of coronary heart disease, health organizations recommend that children older than the age of two years consume no more than 30% of kcal from total fat, less than 10% of kcal from saturated fat, and less than 300 mg of dietary cholesterol.1-4 Surveys indicate that dietary fat intake in children has been decreasing gradually throughout the past two decades, from 36.3% to 34.0% of energy in children 6 to 11 years of age.5-7 This trend toward lower fat diets is viewed favorably8 and continues to be promoted nationally.9
Some concerns, however, have been raised as to the safety of reduced-fat diets in growing children.10,11 Case studies of poor growth12,13 and warnings of nutritional inadequacy, particularly for iron and calcium, from reduced fat diets have been reported.14 Cross-sectional analyses15indicating significantly lower intakes of essential vitamins and minerals in children who reported consuming lower fat diets have been cited as cause for concern.11 In contrast, higher fat intakes have been associated with obesity16,17 and greater weight gain in children,18,19 and overweight in children has been increasing in prevalence.20
The Dietary Intervention Study in Children (DISC) is a randomized trial investigating the long-term efficacy and safety of a diet reduced in total fat, saturated fat, and cholesterol in prepubertal children 8 to 10 years of age with elevated low-density lipoprotein (LDL) cholesterol.21 There were no differences among the 663 participants at baseline between the intervention and usual care groups in height, weight, body mass index (BMI), sum of skinfolds, and nutritional biochemical measures.21,22 As previously reported,21 after three years, intervention children reduced their mean total fat intake to 28.6% of energy, compared with 33.0% for the usual care group, and had a mean 3.3 mg/dL greater reduction (P = .02) in LDL-cholesterol than did usual care children. There were no significant differences between the intervention and usual care children in growth, serum ferritin levels, and other measures of safety including: dietary intakes of vitamins A, C, B-6, calcium, iron, and zinc; serum levels of retinol, zinc, and albumin and red blood cell folate levels; or on a battery of psychosocial tests.21
The DISC main results at 3 years compared the intervention and usual care groups, regardless of whether or not the intervention children adhered to the diet, or whether or not the usual care children changed their diet to one that was reduced in fat. The present article describes the anthropometric measures, biochemical determinations, and dietary intakes in the boys and girls, and examines measures of nutritional adequacy and safety in relation to self-reported fat intake in the pooled intervention and usual care groups. Pooling the intervention and usual care groups allows asessment of these relationships throughout a wide range of fat intake; however, it is based on reported intake rather than randomized group assignment, and does not guarantee control for all factors that could be related to the outcomes of interest. Nutritional adequacy and safety are examined longitudinally, based on objective anthropometric and biochemical measurements as well as self-reported diet, to interpret better the DISC results regarding nutritional status.23,24 This report also examines the relationship of dietary fat intake with body fat based upon BMI and the sum of three skinfolds.
MATERIALS AND METHODS
The design of the DISC trial has been described.21,22 Briefly, the study includes 663 children (362 boys and 301 girls, 86.6% white, 9.4% black, and 4.0% other minority) 8 to 10 years of age at baseline with LDL-cholesterol levels between the 80th and 98th age- and sex-specific percentiles. Children were recruited from schools, prepaid health plans, and physicians' offices at six clinical centers. Children were eligible if they were 8 to 10 years of age, prepubertal, had normal psychosocial and cognitive development, had no medical conditions or were taking no medications that affect growth or blood lipids, and did not have a family history of premature heart disease. Informed consent was obtained from the parent or guardian of each child. Details on eligibility and recruitment have been described.21,22
Eligible children were randomly assigned to either a dietary intervention or usual care group. Usual care children received general health education materials on diet and heart disease. The intervention group received a family-oriented behavioral and educational intervention throughout a period of 3 years to lower total fat intake to 28% of calories, saturated fat intake to less than 8% of calories, and dietary cholesterol to 75 mg/1000 kcal not to exceed 150 mg/d, and to raise polyunsaturated fat intake to 9% of calories as a partial replacement for saturated fat. Details on the intervention have been described.25,26
Clinic measurements were conducted at baseline, year 1, and year 3, with examiners blinded to treatment assignment. The two primary safety outcome measurements were mean height and mean serum ferritin levels at year 3. Secondary safety measurements included other nutritional biochemical assessments, including serum zinc, retinol, and albumin, and red blood cell folate. Other serum micronutrients measured were β-carotene and vitamin E. Blood samples for the micronutrients were collected after a 12-hour fast. Hemoglobin was assessed and analyzed locally at each center. The serum and red blood cell micronutrients were analyzed by the Nutritional Biochemistry Branch, Division of Environmental Health Laboratory Sciences, Centers for Disease Control and Prevention, except for albumin, which was measured by Johns Hopkins Clinical Laboratory. The analytic methods used for micronutrient determinations were the same as those used for the third National Health and Nutrition Survey (1988 to 1994) with similar quality control methods.27
Anthropometric measurements were taken by trained and certified staff. At each time point, at least two readings were made of height, weight, and skinfolds at the triceps, subscapular, and suprailiac sites. BMI was calculated as weight (kg) divided by the square of height (m).
Because physical activity has been related to body fatness and may also be related to dietary fat intake, physical activity levels were analyzed as an adjustment factor for the relationship between energy intake from fat and body fatness. Physical activity levels were assessed by interview using a modified seven-day physical activity recall questionnaire.28 An overall score based on intensity and duration of physical activities performed throughout the week was calculated.
Dietary assessment was conducted by trained and certified dietitians blinded to treatment assignment. The assessment method was validated before the study.29 Three nonconsecutive 24-hour recalls were collected at each time point. The first recall was conducted in an interview at the clinic and the subsequent two recalls were obtained on the telephone within 2 weeks of the clinic visit. Coding and nutrient calculation (database version 20) were performed at the Nutrition Coordinating Center at the University of Minnesota,30 and the nutrient intakes for the three recalls were averaged. In DISC dietary micronutrients measured to assess safety were vitamins A, C, B-6, calcium, iron, and zinc. Dietary intakes of thiamin, niacin, riboflavin, folate, vitamins E and B-12, magnesium, and phosphorus were also analyzed for this report, because these nutrients previously have been reported to be low in children consuming low-fat diets or among children in general.15,31
Descriptive statistics (means and standard deviations) were calculated for anthropometric, dietary, and nutritional biochemical measures at baseline, year 1, and year 3. Longitudinal linear regression models using data from all three time points and taking into account the correlation between measurements on the same person32 were performed to examine the relationship between fat intake and anthropometric measures, micronutrient intake, and nutritional biochemical measures. To assess dietary adequacy, several dietary measures were examined further using longitudinal logistic regression to model the relationship between fat intake and the probability of meeting two-thirds of the Recommended Dietary Allowances (RDAs).33 Two-thirds of the RDAs, a commonly used cutpoint,31 were used in the analyses because RDAs overestimate nutrient requirements,33 three 24-hr recalls do not represent an individual's habitual intake,31,33 and 24-hr recalls tend to underestimate caloric and consequently nutrient intakes.34
Separate analyses were performed using each measure of nutritional adequacy and safety as the response variable. The independent variable of interest was energy intake from fat, which was represented as fat energy (fat in grams multiplied by 9 kcal/g). Fat energy was used in the models rather than percent of energy from fat to avoid ambiguous interpretation associated with nutrient densities.35,36Energy intake in the statistical models was controlled for with a variable that included all sources of energy other than fat. Other control variables in all models were sex, treatment group, and indicator variables used to represent visit number (baseline, year 1, and year 3). The first order interaction terms that a priori were considered plausible and important to control for were retained in all models; these included fat intake-by-treatment, fat intake-by-sex, fat intake-by-visit number, and visit-number-by treatment. For the anthropometric variables (except height) physical activity was controlled for with the overall physical activity score.
These analyses assess the relationship between fat intake and nutritional parameters. To test whether the intervention increased the probability of having a nutritionally inadequate diet, an interaction term between treatment assignment and energy intake from fat was tested in the linear regression models. When lower fat intakes were related to lower micronutrient intakes, the analysis was repeated with the categories of fatty acids (saturated, monounsaturated, and polyunsaturated fat) to examine any relation with the dependent dietary variable.
None of the results presented in this article have been adjusted for multiple comparisons because these analyses are secondary to the main safety hypotheses that have been previously published21 and because in assessing safety it is more conservative to risk accepting a false hypothesis than to risk failing to detect a true hypothesis.
Data collection follow-up rates were 93% at year 1 and 94% at year 3. Missing data for specific measures from children who attended the follow-up visits averaged 3% and 5% for the dietary and biochemical measures, respectively.
Neither treatment assignment nor interactions between treatment assignment and energy intake from fat were significant for any of the dependent variables (anthropometric, dietary, and nutritional biochemical measures). This indicates that there were no differences between the intervention and usual care groups in the relationships between energy intake from fat and the nutritional adequacy and safety measures, and that the intervention had no significant adverse effect on nutritional parameters. Therefore, the data from the intervention and usual care groups were pooled for the regression analyses. Other first-order interaction terms also were not significant.
Table 1 and Figs 1 and 2 present unadjusted mean anthropometric measures, energy and macronutrient intakes, vitamin and mineral intakes, and nutritional biochemical levels at baseline, year 1, and year 3 for the intervention and usual care groups combined. Percent of energy from fat ranged from a low of 12.2% to a high of 52.0%. Despite lower mean energy intakes from fat in boys and girls in year 1 and year 3 compared with baseline (Fig 1), mean micronutrient intakes met two-thirds of the RDAs (Fig2) for calcium, iron, zinc (except for baseline and year 1 in boys), magnesium, and phosphorus (data not shown).
Energy intake from fat was not associated with height, weight, BMI, or sum of skinfolds (all P > .40) (Table2). Lower energy intake from fat was associated with higher levels of red blood cell folate (P = .03) and hemoglobin (P = .025) and with a trend for higher levels of serum ferritin (P = .10) (Table2). Serum levels of β-carotene, retinol, vitamin E, zinc, and albumin were not related to fat intake. The interactions tested were not significant.
Lower energy intake from total fat was associated with higher dietary intakes of folate (P < .0001), vitamin C (P < .0001), and vitamin A (P < .002), and a trend for higher iron intake (P = .06) (Table 2). Lower fat intake was associated with lower intakes of calcium, zinc, magnesium, phosphorus, vitamin E, vitamin B-12, thiamin, niacin, and riboflavin (allP < .01). There was no relationship between energy intake from fat and vitamin B-6 intake. The only significant interaction occurred for vitamin E, in which the coefficients differed between the three visits (significant fat intake-by-visit number interaction).
The relationships of fat intake with iron and calcium, the two nutrients that were of most interest to DISC, and with zinc are illustrated in Fig 3. These figures are from prediction models that use the intervention group at year 3 as the reference and would be similar if the usual care children or other visits were used instead. As energy intake from fat increases, iron intake decreases, whereas calcium and zinc intakes increase. Iron intakes are greater than two-thirds of the RDAs along virtually the entire range of energy intake from fat in boys and along the lower range of fat intake in girls (Fig 3). Calcium intakes tend to remain greater than two-thirds of the RDAs in boys and girls along the entire range of fat intake. In contrast, zinc intakes tend to be below two-thirds of the RDAs in boys and girls at the lower range of fat intake.
Nutrient intake from supplement use was not included in these analyses, because nutritional adequacy of the diet was the primary focus. On average 18% of the DISC children were taking supplements at each visit. Neither treatment assignment, visit number, sex, nor energy intake from fat was related to the probability of taking supplements. In addition, no interactions were observed between energy intake from fat and supplement use with respect to blood biochemical measures. Results were consistent when analyses relating dietary fat intake with blood biochemical measures were performed in the subgroup of children who were not taking supplements. Thus relationships between energy intake from fat and nutritional biochemical measures were not modified by the use of supplements.
Examining the components of total fat (data not shown), lower intakes from saturated fat were associated with lower intakes of calcium, zinc, phosphorus, and riboflavin (P < .05). Lower intakes from polyunsaturated fat were associated with lower intakes of phosphorus (P < .05), magnesium (P < .0001), and thiamin in boys (P < .01). Lower intakes of monounsaturated fat were primarily associated with lower intakes of niacin (P < .0001) and thiamin in girls (P < .0001). There were no discernible relationships between the type of fatty acid intake and vitamin E or vitamin B-12.
In analyses assessing dietary adequacy by examining whether energy intake from fat was related to the risk of having dietary micronutrient intake less than two-thirds of the RDAs for calcium, zinc, magnesium, phosphorus, vitamin E, vitamin B-12, thiamin, niacin, or riboflavin, significant interactions of energy intake from fat with visit number or with sex, or with both, were observed. When interactions were significant, analyses were performed separately by visit number (baseline, year 1, and year 3) or by visit number and sex. There were no differences between the intervention and usual care groups in risk of having less than two-thirds of the RDAs associated with energy intake from fat (nonsignificant interaction). Lower fat intake was not related to the risk of consuming less than two-thirds of the RDAs for most of the nine nutrients. The exceptions were as follows: calcium in girls at baseline only (odds ratio [OR], 1.011, P < .0003); vitamin E for all visits (baseline OR, 1.009; year 1 OR, 1.007; and year 3 OR, 1.007; P < .0001 for all visits); and zinc at all visits for boys (baseline OR, 1.004; P < .05; year 1 OR, 1.003; P < .02; and year 3 OR, 1.004;P < .003) and girls (baseline OR, 1.007;P < .001; year 1 OR, 1.008; P < .0006; and year 3 OR, 1.005; P < .003).
The main results of the DISC trial, which studied children with elevated LDL-cholesterol for 3 years, found that despite a significant reduction in fat intake by the intervention group, no differences in growth, blood biochemical measures, and dietary micronutrient intakes were found between intervention and usual care children.21 By pooling the intervention and usual care groups, this report examines further the nutritional adequacy and safety of a reduced-fat diet determined from anthropometric and blood biochemical measures and self-reported dietary intakes. The results show that growth and biochemical measures of nutritional status are not adversely related to lower dietary fat. The findings are consistent with other observational studies reporting no adverse associations with growth and nutritional biochemical measures in children consuming vegetarian diets31,37-39 and in nonvegetarian children consuming lower fat diets,15,40,41 and with other cholesterol-lowering intervention studies in children which reported no adverse effects on growth or serum measures of micronutrients.42-44 In addition, the results found that lower fat intakes did not result in differences in body fat.
In several case studies that have reported that lower fat diets in children resulted in adverse effects, the reported diets were not only low in fat but also low in energy.12,45,46 Thus, the observed growth failure was more likely attributable to the low energy intakes rather than to low fat intake per se.47,48
Studies based solely on self-reported dietary assessment have not shown any consistent pattern of low micronutrient intakes in children consuming lower fat diets.41,49 In a cross-sectional analysis based on single 24-hr recalls, Nicklas et al15found that a higher proportion of children with less than 30% of energy intake from total fat failed to meet the RDAs for a number of vitamins and minerals compared with those consuming more than 30% of their energy from total fat. However, in that study total energy intake decreased with decreasing percent of energy from fat, which could thus account for the lower intakes of vitamins and minerals found in the children on lower fat intakes. In studies in which energy intakes are similar across varying levels of fat consumption, no differences in vitamin and mineral intakes were observed.40,50 In the present study, relationships observed between dietary fat and dietary micronutrients were independent of energy intake.
In the present study, lower fat intakes were not related to adverse effects on objective growth or nutritional blood biochemical measures; however, lower fat intakes, independent of total energy intake, were associated with self-reported lower intakes of 9 micronutrients from among 14 investigated. Of these nine, assessment of nutritional adequacy showed that energy intake from fat was associated with increased risk of not meeting two-thirds of the RDAs for only zinc and vitamin E and inconsistently for calcium (at baseline in girls). The mean zinc, vitamin E, and calcium intakes of the DISC children were similar to those reported in children in the United States,51 particularly when expressed in terms of 4200 kJ (1000 kcal). In the present study, fat intake was not related to serum zinc or vitamin E levels, and there was no evidence of zinc or vitamin E deficiency in any individual child based on the distribution of serum levels. Because the risk of not meeting two-thirds of the RDAs for calcium occurred only at baseline in girls, the intervention did not result in further risk of inadequate calcium intake. Underreporting of food intake, including animal products and high-fat foods, may account for the relationships observed with dietary measures and not with biochemical measures. Also, because of paucity of source data, 74% of the vitamin E data in the nutrient database is imputed. Although the reported dietary intake data suggest that lower fat intakes may result in lower than RDA-recommended intakes of zinc and vitamin E, there is no evidence of any adverse effects on biochemical objective measures of nutritional status.
The limitations of self-reported dietary assessments including possible differential underreporting bias are well-recognized.34,52-54 To maximize quality and accuracy, DISC dietary data were carefully ascertained. Staff were centrally trained to follow a standardized protocol, and interviewers were blinded to group assignment. Participants were guided through the interview process with great attention paid to details of ascertaining food intake. The findings that lower fat intake was related to higher intakes of folate (P < .0001) and iron (P = .06) were supported by the biochemical measures: lower fat intake was related to higher levels of red blood cell folate (P < .03), hemoglobin (P < .025), and possibly serum ferritin (P = .10). In contrast, the lower zinc intake associated with lower fat intake was not confirmed by lower levels of serum zinc. Although nutritional biochemical measures are not necessarily sensitive indicators of an individual's recent dietary nutrient intake, concordant relationships are suggestive of accurate dietary assessments.
Saturated fat accounted for most of the observed relationship between lower fat intake and lower intakes of zinc, calcium, riboflavin, and phosphorus. Although the DISC intervention emphasized use of lean meats and low-fat and non-fat dairy foods, reported changes in dairy and meat food groups, which are major sources of saturated fat for children, may account for the observed relationships. Analyses of food group patterns would better identify how consumption patterns changed and how those changes affected intakes of specific nutrients.
In this study, lower energy intake from fat was related to higher intakes of folate, vitamins C and A, and iron, and to higher concentrations of red blood cell folate, hemoglobin, and serum ferritin. The increased emphasis on fruits and vegetables that was part of the dietary counseling probably contributed to the higher intakes of folate, vitamin C and vitamin A. Increased emphasis on fortified breakfast cereals, whole grain breads, and other grains may have accounted for the higher levels of iron associated with lower fat intake. These findings on iron do not support the concerns that reduced fat diets may result in inadequate iron status, particularly when nutrition education accompanies the dietary changes.
In summary, observations from anthropometric measures, biochemical measures, and self-reported dietary intakes indicate that lower fat intakes in children during puberty are safe for growth and are nutritionally adequate. Furthermore, they are associated with beneficial effects on folate and iron status. Although dietary recall data indicate lower fat diets are related to lower intakes of several nutrients, no adverse effects were observed on blood biochemical measures of nutritional status. Adequate consumption of lean meats, fish, or poultry and non-fat dairy products when following a reduced-fat diet will help ensure adequate intakes of zinc and calcium. This study indicates that public health recommendations for moderately lower fat intakes in children during puberty may be followed safely.
This research was supported by the National Heart, Lung, and Blood Institute cooperative agreements HL-37947, HL-37948, HL-37954, HL-37962, HL-37966, HL-37975, and HL-38110.
We gratefully acknowledge Ms Elaine Gunter, Centers for Disease Control and Prevention, for conducting and reviewing the nutritional biochemical analyses.
- Received May 31, 1996.
- Accepted November 27, 1996.
- Address correspondence to: Eva Obarzanek, National Heart, Lung, and Blood Institute, Two Rockledge Centre, Room 8136, 6701 Rockledge Drive, MSC 7936, Bethesda, MD 20892–7936.
Reprint requests to (B.A.B.) DISC Coordinating Center, Maryland Medical Research Institute, 600 Wyndhurst Avenue, Baltimore, MD 21210
- DISC =
- Dietary Intervention Study in Children •
- LDL =
- low-density lipoprotein •
- BMI =
- body mass index •
- RDA =
- recommended dietary allowance •
- OR =
- odds ratio
- Weidman W,
- Kwiterovich P,
- Jesse MJ,
- et al.
- Expert Panel on Blood Cholesterol Levels in Children and Adolescents
- ↵National Research Council Committee on Diet and Health. Diet and Health: Implications for Reducing Chronic Disease Risk. Food and Nutrition Board, National Research Council. Washington, DC: National Academy Press; 1989:670–672
- ↵US Department of Agriculture and the US Department of Health and Human Services. Nutrition and Your Health. Dietary Guidelines for Americans. Washington, DC: US Department of Agriculture, 1995
- ↵National Center for Health Statistics. Dietary Intake Findings. United States, 1971–1974. Publication No. (HRA) 77–1647, Series 11, No. 202, Hyattsville, MD: US Department of Health, Education, and Welfare; 1977
- ↵National Center for Health Statistics. Dietary Intake Source Data: United States, 1976–80. Publication No. (PHS) 83–1681, Series 11, No. 231, Hyattsville, MD: US Department of Health and Human Services; 1983
- ↵McDowell MA, Briefel RR, Alaimo K, et al. Energy and macronutrient intakes of persons ages 2 months and over in the United States: Third National Health and Nutrition Examination Survey, Phase 1, 1988–1991. Advance Data From Vital and Health Statistics, No. 255. Hyattsville, MD: National Center for Health Statistics, Centers for Disease Control and Prevention; 1994
- ↵Ernst ND, Sempos CT, Briefel RR, Clark MB. Consistency between the declines in dietary fat and cholesterol intake and serum total cholesterol levels among US adults: The National Health and Nutrition Examination Surveys. Am J Clin Nutr. In press
- ↵US Department of Health and Human Services. Healthy People 2000. National Health Promotion and Disease Prevention Objectives. DHHS Publication No. (PHS) 91–50212. Washington, DC: US Government Printing Office; 1991:117–118
- ↵Anderson GH. Factors affecting nutritional lifestyle changes in childhood. In: Filer LJ, Lauer RM, Luepker RV, eds. Prevention of Atherosclerosis and Hypertension Beginning in Youth. Philadelphia, PA: Lea Febiger; 1994:3–10
- Olson RE
- Pugliese MT,
- Weyman-Daum M,
- Moses N,
- Lifshitz F
- Nicklas TA,
- Webber LS,
- Koschak ML,
- Berenson GS
- Gazzaniga JM,
- Burns TL
- Obarzanek E,
- Schreiber GB,
- Crawford PB,
- et al.
- Klesges RC,
- Klesges LM,
- Eck LH,
- Shelton ML
- Troiano RP,
- Flegal KM,
- Kuczmarski RJ,
- Campbell SM,
- Johnson CL
- The Writing Group for the DISC Collaborative Research Group
- ↵Gibson RS. Principles of Nutritional Assessment. New York, NY: Oxford University Press; 1990:3–8
- Shank FR,
- Wilkening VL
- Hartmuller VW,
- Snetselaar L,
- Van Horn L,
- et al.
- ↵Gunter EW, Lewis BG, Koncikowski SM. Laboratory Methods Used for the Third National Health and Nutrition Examination Survey (1988–1994). Atlanta, GA: Centers for Disease Control and Prevention; 1995
- Sallis JF,
- Haskell WL,
- Wood PD,
- Fortmann SP,
- Rogers T,
- Blair SN,
- Paffenbarger RS
- Gibson RS,
- MacDonald CA,
- Smit Vanderkooy PD, McLennan CE, Mercer NJ
- ↵National Research Council, Food and Nutrition Board. Recommended Dietary Allowances. Tenth edition. Washington, DC: National Academy Press; 1989
- Beaton GH,
- Milner J,
- Corey P,
- et al.
- Willett W,
- Stampfer MJ
- Kipnis V,
- Freedman LS,
- Brown CC,
- Hartman A,
- Schatzkin A,
- Wacholder S
- Sanders TAB,
- Reddy S
- Shea S,
- Basch CE,
- Stein AD,
- Contento IR,
- Irigoyen M,
- Zybert P
- Friedman G,
- Goldberg SJ
- Davis DR,
- Apley J,
- Fill G,
- Grimaldi C
- ↵Alaimo K, McDowell MA, Briefel RR, et al. Dietary intake of vitamins, minerals, and fiber of persons ages 2 months and over in the United States: Third National Health and Nutrition Examination Survey, Phase 1, 1988–91. Advance Data From Vital and Health Statistics; No. 258. Hyattsville, MD: National Center for Health Statistics; 1994
- Bingham SA
- Thompson FE,
- Byers T
- Copyright © 1997 American Academy of Pediatrics