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,2
* Division of Health and Family Studies, the Institute for Families in Society, University of South Carolina, Columbia, SC;
Department of Epidemiology and Biostatistics, the Arnold School of Public Health, University of South Carolina and the South Carolina Statewide Cancer Prevention and Control Program, Medical University of South Carolina Charleston, SC; and
** Center for Clinical Pharmacology, University of Pittsburgh School of Medicine, Pittsburgh, PA
2To whom correspondence should be addressed. E-mail: bvw2{at}cdc.gov.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • dietary fat • psychosocial functioning • cognitive functioning • children and adolescents • NHANES III
The customary diet of American children and adults is considered to be excessively high in total fat, saturated fat, and cholesterol—a dietary pattern widely thought to contribute to the development of obesity, cardiovascular disease, and cancer (1). As a result, many government agencies and health organizations have endorsed the fat restriction recommendations of the U.S. Dietary Guidelines for children 
2 y old (2,3), the key component of which calls for a reduction in cholesterol and saturated fat consumption (4). Prominent among anticipated health benefits of lower serum cholesterol levels during childhood is the prevention of arteriosclerosis in adulthood. However, this extension of adult dietary recommendations to children remains controversial (5,6). Dietary fat restriction during childhood may affect the central nervous system during rapid growth and development when it is more susceptible to environmental influences. In adults, very low serum cholesterol is associated with cognitive decrements (7–10), and in nonhuman primates fat restriction appears to have deleterious effects on social behavior (11,12).
The results of 2 randomized clinical trials in children (13,14) suggest that a low-saturated fat, low-cholesterol diet decreases serum LDL cholesterol (LDL-C)3 concentration without effects on growth or psychosocial development. However, broad conclusions from these studies may be premature. Children in one study were all <6 y old, and minor effects on neurodevelopment may be difficult to detect in that age group (13). The other trial was restricted to children whose age-specific LDL-C was in the highest quintile. Also, dietary fat was not substantially reduced in the intervention children in either trial, i.e., the difference in serum cholesterol between intervention and control subjects averaged no more than 3%. Some dietary guidelines for adults and children advise increased intake of mono- and polyunsaturated fats (4). However, the putative developmental benefits of unsaturated fat were shown primarily in studies of premature infants or children and adolescents with developmental disorders (15). The dearth of information may reflect methodological, logistical, and ethical issues in this field. In any case, whether and how specific dietary fats may affect social and cognitive development in normal children remain unclear. Given the clinical importance of these issues, we conducted this analysis to examine the potential associations between dietary intake of fats and cholesterol in relation to psychosocial, cognitive functioning in a population-based sample of school-aged children using data from the Third National Health and Nutrition Examination Survey (NHANES III).
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The NHANES III is a cross-sectional survey of the U.S. civilian noninstitutionalized population living in households, conducted from 1988 to 1994. The sampling scheme was a stratified, multistage probability design with oversampling of African- and Mexican-Americans to allow more precise estimates for these subpopulations. Detailed descriptions of the survey were published elsewhere (16). NHANES III included medical and cognitive examinations and interviews conducted with survey children and proxy respondents. A total of 5367 children aged 6–16 y participated in the Household Youth Interview. Of these, 212 did not complete a 24-h dietary recall interview. We excluded 128 children whose daily intakes were extreme [highest 1% or lowest 1% of the weighted distribution, total energy < 2.3 MJ/d or 21 MJ/d, or percentage of energy from total fat < 11 or 60%, or percentage of energy from polyunsaturated fat 25% or cholesterol intakes 144 mg/(MJ · d)]. Additionally, 643 children whose proxy respondents were not their mothers were excluded. Finally, 714 children were further excluded because they had to attend special schools or classes due to impairment (including learning disabilities, n = 36) or health problems, such as cerebral palsy, epilepsy/fit/convulsion, mental retardation, or muscle weakness (n = 104), trouble seeing with one or both eyes even when wearing glasses or contact lenses, or trouble hearing with one or both ears (n = 574). After these exclusions, a total of 3666 children and adolescents remained for primary analyses.
Measurements and variable definitions
Psychosocial and cognitive functioning. During the Youth and Proxy Interview, mothers were asked a series of questions about their children’s behaviors and social skills. Psychosocial functioning was measured by 5 dichotomous variables constructed from mothers’ answers to these questions: 1) had the child ever seen a psychiatrist, psychologist, or psychoanalyst about any emotional, mental, or behavioral problems? 2) had the child ever been suspended, excluded, or expelled from school? 3) was the child somewhat shy and slow to make new friends? 4) did the child have difficulties in getting along with others? and 5) had the child repeated any grades for any reason. The surveyed children also were administered the Arithmetic and Reading Subtests of the Wide Range Achievement Test, Revised (WRAT-R) and the block design and digit span subtests of the Wechsler Intelligence Scale for Children, Revised (WISC-R) (16). The WRAT-R arithmetic subtest consists of oral and written problems ranging from simple addition to calculus; the Reading subtest assesses letter recognition and word reading skills. In the block design subtest, the child replicates 2-dimensional geometric patterns using a set of 3-dimensional cubes; this subtest is a measure of nonverbal reasoning. Digit span assesses short-term and working memory by asking the child to repeat a series of increasingly long number sequences forward and then backward. WRAT-R Arithmetic and Reading scores were age-standardized to a mean of 100, with an SD of 15. The WISC-R block design and digit span subtests were age-standardized to a mean of 10 (SD = 3) (16).
Dietary intake. A single 24-h diet recall interview was administered to the children’s mothers by a trained dietary interviewer using the Dietary Data Collection System. The system was designed specifically to probe for fat and salt used in the preparation of foods. The type and amount of foods consumed were prompted using recall aids such as special charts, measuring cups, and rulers to help in quantifying the amounts consumed. Special probes were also used to help the recall of commonly forgotten items such as condiments, accompaniments, fast foods, or alcoholic beverages. The interviewees were asked to report all foods and beverages consumed during the previous day, spanning 24 h from midnight to midnight. Data retrieval for day care and school lunch were carefully planned and executed. The food database was linked to the USDA’s Survey Nutrition Database and produced an estimate of total energy intake. In addition to total fat, specific categories of fatty acids assessed include SFA, monounsaturated fatty acids (MUFAs), and PUFAs.
Nondietary variables.
The covariates were selected from the literature (17,18) and included: the child’s ethnicity as reported by the mother [African-American, vs. Non-African-American (including Hispanic or other ethnicities)], maternal education (<12 y vs. 12 y), and rural/urban classification of residence area (central or fringe counties of metro areas of 1 million population or more vs. other areas). Maternal marital status was collapsed into 2 categories: single-parent household (including mothers who were married but whose spouses were not living in the household and those who were widowed, divorced, separated, or never married) vs. mothers who reported being married with their spouses living in the household. Total family income for the previous 12 mo was reported for categories ranging from <$1000 to $80,000, in $1000 increments below $19,999, in $5000 increments between $20,000 and $79,999. A poverty index ratio (PIR) was then calculated by comparing the midpoint for the category and the family size with the federal poverty line (PIR = 1). These analyses used a 3-level variable of poverty status: low (PIR < 1.30, the federal cutoff point for eligibility for the Food Stamp Program), middle (1.30 
PIR < 3.00) and high income (17). A child was classified as food insufficient if the mother reported that the family either sometimes or often did not get enough food to eat. We used stature-for-age Z-score and BMI-for-age measured at the time of the examination as indicators of past nutrition status (19). We also used the definitions of iron deficiency proposed by Looker et al. (20) based on laboratory tests of transferrin saturation, free erythrocyte protoporphytin, and serum ferritin. A child was considered as suffering from iron deficiency if any 2 of these 3 values of iron status were abnormal for age and gender.
Mothers rated their children’s health as excellent, very good, good, fair, or poor. A dichotomous variable was used in the analyses, comparing children in fair or poor health with children having excellent, very good, or good health. During Household Family and Household Youth interviews, the children were asked a series of questions about substance abuse. Respondents were classified as substance abusers if they answered affirmatively to at least 1 of these questions: 1) have you ever used marijuana? 2) have you ever used cocaine in any form? 3) have you smoked at least 100 cigarettes during your entire life? and 4) in the past 12 mo did you have at least 12 drinks of any kind of alcoholic beverage? Children aged 8–16 y were also asked: "How many times per week do you play or exercise enough to make you sweat or breathe hard?" These activities included school-related involvements such as physical education.
Statistical methods
As recommended by the National Center of Health Statistics, we used SUDAAN software (SAS-callable version, 8.0.2) with appropriate weighting and nesting variables (21). We examined all 9 indicators of cognitive and psychosocial functioning as dichotomized variables. We defined a poor performance on each of the 4 cognitive tests as the lowest 10th percentile (inclusive) and compared poor performers to all others (i.e., the remaining 90%). Specifically, the following cutoff values were used: arithmetic score 71, reading score 65, nonverbal reasoning 4, and working memory 4. Using logistic regression, we estimated the multivariable-adjusted odds ratios (ORs) of a negative outcome and corresponding 95% CI.
Four regression models have been proposed to adjust for total energy intake: the nutrient-density, nutrient-residual, energy-partition models (or decomposition), and the model using standard multivariate regression techniques (22,23). Recent study indicates that the nutrient-residual and nutrient-density models provide good parameter stability, whereas other models may introduce spurious associations (24). In the nutrient-density model, all dietary variables are expressed as the percentage of energy in continuous form; total energy intake, the percentage of energy derived from protein, and subtypes of fat are included simultaneously. The coefficients from this model can be interpreted as the estimated effect of substituting a specific percentage of energy from one source for another (e.g., carbohydrate substituted for saturated fat) while "holding total energy intake constant." When estimating the effects of substituting one type of fat for another, the model includes total energy and the percentage of energy from the fat of interest, protein, and carbohydrate. The simple multivariable model answers questions about the absolute effect of each nutrient in the units expressed (as opposed to standardizing in terms of percentage of total energy). In the energy partition model, the regression coefficients compare the effect of each source of energy to one another, and make no assumption about holding total energy intake constant.
Energy per se is associated with an enhancement of cognitive performance (25). The nutrient-residual model accounts for total energy intake before considering the effect of specific macronutrients. In this sense, it provides information different from and supplementary to results obtained from the density models. In the nutrient-residual model, the fat residuals obtained by regressing nutrient intake (a continuous variable expressed as gram mass) on total energy intake are included as independent variables. Each coefficient in the nutrient-residual model can be interpreted as the effect of a given amount of fat after accounting for that amount that is associated with dietary energy from all sources (i.e., "regressing out" the effect of total energy intake). Dietary intake variables were first log-transformed to create residuals with a more constant variance across the levels of total energy intake.
Regressions were also run with the outcomes of 4 cognitive tests in continuous form to assess the changes in cognition scores associated with unit increment of fat intake. As supplementary analyses, we also repeated all of the regressions described above on all subjects (n = 5367) who had valid data of any indicator of psychosocial, cognitive functioning to examine potential biases caused by exclusion of a large portion of the subjects due to various reasons. For all multivariate regression models, potential nondietary confounders were screened in a stepwise fashion, and any covariate whose regression coefficient was associated with a P-value > 0.05 (two-sided) was excluded.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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25% were living with single mothers, and 5% reported sometimes not having enough food to eat. The characteristics of the children included in the primary analyses were similar to those excluded in term of dietary intakes of major macronutrients. However, the 2 groups differed on many variables, such as maternal marital status, overall health, substance abuse, and almost all cognitive and psychosocial indicators. The children excluded were less healthy, and more likely to live with single mothers and under the poverty line. Compared with the children included, those excluded from primary analyses more often performed poorly on the cognition tests, had seen a psychiatrist or psychologist, had to repeat a grade, and been suspended or expelled from school. Both groups consumed energy from fat in excess of the recommended 30% of total dietary energy.
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In the supplementary analyses, in which we investigated the potential biases introduced by our exclusion criteria by repeating analyses including all study subjects with valid psychosocial or cognitive functioning data, all of the principal findings were retained.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The current report has several limitations. Its cross-sectional design prevented us from asserting causality. As in all research using self-reported measures, the information obtained from the interviewees may have been influenced by the perceived value of particular response choices (18,26). As previously reported (27,28), misreporting of diet intake can occur as a result of social desirability and social approval, and the same may be true for indicators of psychological health and adjustment. Whether each cognitive test measures what it purports to measure remains an issue for debate. These heterogeneities in both dependent and independent variables may lead to random measurement errors, resulting in an attenuation of the true relations. A single 24-h diet interview can provide only a rough estimation of an individual’s usual habitual intake (29). Nonetheless, data from a single 24-h diet recall had only slightly higher within-subject variances than those associated with FFQ, and the 24-h diet recall performed relatively well for estimating macronutrient intake (30,31). The current study was also limited by the absence of information on subtypes of PUFAs. Although derived from a true-population sample, participants in the current study may represent only "normal" children because the children with major behavioral or physical disabilities may have been institutionalized. Therefore, our ability to identify some associations may have been constrained by NHANES III sampling procedures.
Despite these shortcomings, the results of the current study are a substantive contribution to an incomplete literature. Two randomized clinical trials examined the effects of counseling to reduce total and saturated fat and cholesterol (13,14). Neither study observed effects on neurological or psychosocial development but, as noted, the results are inconclusive due to methodological considerations. In a cross-sectional study of school-aged boys, Kasl et al. (32) observed that lower serum cholesterol was associated with better academic performance. In the current study, we observed that poor performance on the digit span test but not the other cognitive test was significantly associated with a high intake of cholesterol. In adults, arteriosclerosis was hypothesized to be a potential link between high serum cholesterol and impaired memory (33). In contrast, other evidence from both observational studies and clinical trials suggested that cognitive function was poorer in individuals with either low (8–10) or lowered serum cholesterol (34,35). In any event, arteriosclerosis cannot underlie our observations in children and adolescents.
It is important to note that diet affects serum cholesterol concentration primarily through intake of saturated fat rather than cholesterol itself (36). Also, most studies examining the associations between fatty acids and psychological development and learning ability were conducted in animals, human fetuses, or infants, or in children and adolescents with learning disabilities or developmental/psychiatric disorders (15). In contrast, the current study was conducted among school-aged children and adolescents free of severe learning disabilities. Animal studies indicate that low intake of essential fatty acids (EFAs) and their long-chain PUFA derivatives can result in learning and behavioral problems that are reversed by supplementation of these fatty acids (37–42). The studies on human infants are consonant with the animal literature in suggesting that particular long-chain PUFAs are important for early cognitive development (43–47). In one study, scores on EFA deficiency symptoms were associated with psychometric measures of reading, spelling, and memory for children aged 8–12 y (48). Similar findings were reported for adults with dyslexia (49) and the elderly (50,51). The literature indicates that premature infants or children with developmental disorders appear to benefit from high intake of long-chain PUFAs (44,47,52). The current study suggests that normal school-aged children may benefit from consumption of PUFAs as well in terms of working memory and possibly reading ability.
In summary, the current investigation found that cognitive and psychosocial functioning in children was unrelated to total or saturated fat intake but that dietary cholesterol was associated with performance on 1 cognitive test, and increased PUFA consumption had somewhat broader beneficial effects. Due to the clinical relevance of diet on development in children, further research is clearly warranted.
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FOOTNOTES |
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3 Abbreviations used: EFA, essential fatty acid; LDL-C, LDL cholesterol; MUFA, monounsaturated fatty acid; NHANES III, the 3rd National Health and Nutrition Survey; PIR, poverty index ratio; WISC-R, Wechsler Intelligence Scale for Children, Revised; WRAT-R, Wide Range Achievement Test, Revised.
Manuscript received 26 January 2005. Initial review completed 1 April 2005. Revision accepted 4 May 2005.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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  A. S. Ryan and E. B. Nelson Assessing the Effect of Docosahexaenoic Acid on Cognitive Functions in Healthy, Preschool Children: A Randomized, Placebo-Controlled, Double-Blind Study Clinical Pediatrics, May 1, 2008; 47(4): 355 - 362. [Abstract] [PDF]
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The mean of the digit-span test score of the weighted population was 8.9 (SE: 0.1).