Association of Serum Cholesterol and History of School Suspension among School-age Children and Adolescents in the United States

Jian Zhang1, Matthew F. Muldoon2, Robert E. McKeown3 and Steven P. Cuffe4

1 Division of Health and Family Studies, Institute for Families in Society, University of South Carolina, Columbia, SC
2 Center for Clinical Pharmacology, University of Pittsburgh School of Medicine, Pittsburgh, PA
3 Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC
4 Department of Neuropsychiatry and Behavioral Science, Division of Child and Adolescent Psychiatry, University of South Carolina School of Medicine, Columbia, SC

Correspondence to Dr. Jian Zhang, 4770 Buford Highway, MS K-24, Atlanta, GA 30341 (e-mail: bvw2{at}cdc.gov).

Received for publication June 16, 2004. Accepted for publication October 14, 2004.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The dietary guidelines developed for adults have been extended to children, but the role of serum cholesterol in the neurodevelopment of children is poorly understood. In the Third National Health and Nutrition Examination Survey (1988–1994), serum total cholesterol was measured in 4,852 children aged 6–16 years. Psychosocial development was evaluated by interviewing the mother regarding the child's history of school suspension or expulsion and difficulty in getting along with others. After adjustment for family socioeconomic status, maternal marital status and education, children's nutrition, and academic performance, the odds ratios of children with various concentrations of total cholesterol showed the children to be equally comfortable in their own peer subculture and not to be different in the proportion that had seen a mental health professional. However, non-African-American children with a serum total cholesterol concentration below the 25th percentile (<145 mg/dl) were almost threefold more likely to have been suspended or expelled from schools than their peers with total cholesterol at or above the 25th percentile (odds ratio = 2.96, 95% confidence interval: 1.55, 5.64). The authors concluded that, among non-African-American children, low total cholesterol is associated with school suspension or expulsion and that low total cholesterol may be a risk factor for aggression or a risk marker for other biologic variables that predispose to aggression.

adolescent psychology; child psychology; cholesterol; juvenile delinquency; United States


Abbreviations: CI, confidence interval; DISC, Dietary Intervention Study in Children; NHANES III, Third National Health and Nutrition Examination Survey; STRIP, Special Turku Coronary Risk Factor Intervention Project; WRAT-R, Wide Range Achievement Test, Revised


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Evidence from several large epidemiology and postmortem studies (1Go) reveals that serum cholesterol predicts coronary disease incidence and mortality. Therefore, a number of professional organizations endorsed recommendations restricting dietary intake of fat and cholesterol for children aged 2 years and up in order to keep cholesterol levels low from an early age and to prevent the development of arteriosclerosis in adulthood (2Go). However, the role of serum cholesterol in the neurodevelopment of children is uncertain, and associations between low serum cholesterol levels and negative mood, decrements in cognitive function, and various types of aggressive behavior have been noted in adults and nonhuman primates (3Go–8Go). Cholesterol is now thought to be required for synaptic growth (9Go), and genetic disorders of cholesterol synthesis are associated with mental retardation and suicidality (10Go, 11Go). Such issues and concerns have tended (12Go–15Go) to hamper implementation of the fat recommendations to children in the general population.

Results from the Dietary Intervention Study in Children (DISC) (16Go), the Special Turku Coronary Risk Factor Intervention Project (STRIP) (17Go, 18Go), and others (19Go, 20Go) have suggested that a low-saturated-fat, low-cholesterol diet decreases the concentration of serum low density lipoprotein cholesterol in children without detrimental effects on growth and psychosocial health. However, certain limitations in these studies constrain the validity of these conclusions as well as their generalizability to a broader population. All study subjects in STRIP were younger than 5 years of age; minor neurodevelopment deficits are difficult to recognize during the first few years of life. The subjects in DISC were children with hyperlipemia (low density lipoprotein cholesterol levels greater than the 80th percentile of children in the general population). Both STRIP and DISC were conducted in select volunteer samples under intensive surveillance and lowered serum cholesterol by no more than 5 percent compared with control subjects (21Go). Population-wide longitudinal studies about the effects of blood cholesterol on neurodevelopment in children would be highly informative, but such data are unlikely to be available in the near future because of prohibitive logistics and cost (22Go). Therefore, we examined the associations between serum cholesterol concentrations and psychosocial development of noninstitutionalized school-age children and adolescents using data from the Third National Health and Nutrition Examination Survey (NHANES III).


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Study population
The NHANES III is a cross-sectional survey of the US civilian noninstitutionalized population living in households, conducted from 1988 to 1994. The sampling scheme was a stratified, multistage probability design with oversampling of African Americans and Mexican Americans to allow more precise estimates for these subpopulations. Detailed descriptions of the survey have been published elsewhere (23Go). The NHANES III included medical and cognitive examinations and interviews conducted with survey children and proxy respondents. The sample for Household Youth Questionnaires and Youth and Proxy Questionnaires consists of 7,961 children aged 6–16 years. Of these children, 1,540 were excluded since validated hematologic data were not available. Proxy reports from someone other than the child's mother may not be as valid as, or comparable with, a mother's report; therefore, an additional 791 children were further excluded because the proxy respondents were not their mothers. Because the behavioral problems and school experience of mentally or physically handicapped children are likely different from those of other children, we excluded 757 children who attended special schools or classes as a result of impairment (including learning disabilities) or health problems, such as cerebral palsy, epilepsy/fit/convulsion, mental retardation, or muscle weakness (n = 185), or who had trouble seeing with one or both eyes even when wearing glasses or contact lenses or had trouble hearing with one or both ears (n = 572). We analyzed the data from the remaining 4,852 children and adolescents.

Measurements and variable definitions
Serum cholesterol.
Total cholesterol was measured enzymatically (measurement of triglycerides and the calculation of low density lipoprotein cholesterol require use of fasting samples, whereas less than half of the children were fasting at the time of phlebotomy). Initial exploratory analyses indicated that a linear or U- or J-shaped association did not exist and that using a single cutoff to dichotomize the total cholesterol concentration was able to present the association sufficiently. We examined various cutoffs of the total cholesterol concentration and observed that the 25th percentile (≥145 mg/dl) of the total cholesterol distribution among the weighted study population was the optimal one.

Psychosocial development.
During the Youth and Proxy Questionnaires interview, mothers were asked a series of questions about their children's behaviors and social skills. Psychosocial development was measured by four dichotomous variables constructed from the mothers' answers to these questions: 1) whether the child had ever seen a psychiatrist, psychologist, or psychoanalyst about any emotional, mental, or behavioral problems (affirmed answer: n = 296); 2) whether the child had ever been suspended, excluded, or expelled from school (n = 341); 3) whether the child was somewhat shy and slow to make a new friend (n = 949); and 4) whether the child had difficulties in getting along with others (n = 907).

Major covariates.
The covariates were selected from the literature (24Go–30Go) and included the following: the child's ethnicity as reported by the mother, maternal education (high school or below vs. above high school), number of times the family had moved (three or more vs. less than three), crowded dwelling (more than one person per room), and rural/urban classification of residence area (central or fringe counties of metropolitan areas of 1 million population or more vs. other counties). Since there were only 171 non-White, non-African-American children and since the majority of the characteristics examined were similar between these children and the White children, we collapsed these 171 children with the White children into one group (non-African-American children). Maternal marital status was collapsed into two categories: single-parent household (included mothers who were married but their spouses were not living in the household, widowed, divorced, separated, or never married) and married mothers with their spouses living in the household. Total family income for the previous 12 months was reported for categories ranging from less than $1,000 to $80,000 and over, in $1,000 increments at or below $19,999 and in $5,000 increments between $20,000 and $79,999. A poverty index ratio was then calculated by comparing the midpoint for the category and the child's family size with the federal poverty line (poverty index ratio = 1). These analyses used a three-level variable of poverty status: low income (poverty index ratio < 1.30, the federal cutpoint for eligibility for the Food Stamp Program); middle income (poverty index ratio = 1.30–2.99); and high income (poverty index ratio ≥ 3.0) (25Go). 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.

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 with excellent, very good, or good health. During Household Family and Household Youth Questionnaires interviews, the children were asked a series of questions about their own substance abuse behaviors. Children were classified as substance abusers (n = 220) if they answered affirmatively to at least one of these questions: 1) Have you ever used marijuana? (n = 139); 2) have you ever used crack or cocaine in any form? (n = 11); 3) have you smoked at least 100 cigarettes during your entire life? (n = 66); 4) in the past 12 months did you have at least 12 drinks of any kind of alcoholic beverage? (n = 141). We used standing height (in meters) measured at the time of the examination as an indicator of past nutrition status and z scores of age-adjusted body mass index as a surrogate variable of body image. Daily dietary energy intake was obtained from a 24-hour dietary recall performed by mothers. Other nutrition covariates were serum albumin and total proteins. Data on these two variables were available for children older than 11 years only and were used in the secondary analysis.

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, were administered to all subjects (23Go). The WRAT-R Arithmetic Subtest consists of oral and written problems ranging from simple addition to calculus, while the Reading Subtest assesses letter recognition and word reading skills. In the Block Design Subtest, the child replicates two-dimensional geometric patterns using a set of three-dimensional cubes; this subtest is a measure of nonverbal reasoning. The Digit Span Subtest assesses short-term and working memory by asking the child to repeat a series of increasingly long number sequences forward and then backward. The WRAT-R Arithmetic and Reading test scores were age standardized to a mean of 100 (standard deviation: 15), while the Block Design and Digit Span test scores of the Wechsler Intelligence Scale for Children, Revised, were age standardized to a mean of 10 (standard deviation: 3).

Statistical methods
As recommended by the National Center for Health Statistics, we used SUDAAN software (31Go) (SAS version 7.5; SAS Institute, Inc., Research Triangle Park, North Carolina) with appropriate weighting and nesting variables. We used logistic regression to estimate multivariable-adjusted odds ratios of a negative psychosocial indicator and corresponding 95 percent confidence intervals. Before multivariable modeling, we examined the age-adjusted association between each psychosocial indicator and each covariate. For illustration purposes only, all continuous variables were categorized using quartiles or clinically recommended cutoffs, if available. A multivariable model was generated in a stepwise fashion for each psychosocial indicator. In the first step, the main effect and covariates, for which the overall p values of age-adjusted odds ratios were less than 0.25, were entered into the model. In the second step, the covariates with a p value greater than 0.10 were dropped, and the interactions among main effect and gender, urbanization of residence area, and ethnicity were tested. We kept the covariates with p values of regression coefficients less than 0.05 (two sided) in multivariable models. However, to avoid overadjusting and to increase the precision of estimates, we removed any covariate whose addition to the multivariable model changed the odds ratio of interest by less than 10 percent. Because preliminary analysis indicated that a strong interaction (p < 0.01) existed between serum total cholesterol and race for the history of school suspension, we present the results of multivariable-adjusted logistic regression for the entire sample as well as by race. At the final stage of the analysis, we conducted secondary regression analyses including the following: 1) daily energy intakes (with or without log transformation) in children 8–16 years of age and 2) serum albumin and total protein measurements in children 12–16 years of age to examine whether inclusion of these variables altered the findings. Regressions on all subjects who had valid data on serum cholesterol were also performed to examine potential biases caused by exclusion of a large portion of the subjects due to learning disability or other health problems.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Among the 4,852 children included in the analyses, the weighted average age was 10.0 (standard error: 0.1) years, 51.3 (standard error: 1.4) percent were boys (table 1), and 15.5 (standard error: 1.3) percent were African Americans. Of these children, 22.7 (standard error: 1.3) percent were living with single mothers, 5.7 (standard error: 0.6) percent did not have enough food to eat sometimes, and 8.4 (standard error: 0.9) percent had ever been suspended from school. Children excluded from analyses differed from those included in several respects. Compared with the participants included, those excluded were less healthy and more likely to live below the federal poverty line. As expected, the children and adolescents excluded were more likely to have seen a mental health professional for emotional or behavioral problems, and they were more likely to have been suspended or expelled from school.


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TABLE 1. Characteristics of participants excluded from analysis and those included among 7,961 children aged 6–16 years, Third National Health and Nutrition Examination Survey, 1988–1994

 
Of the four psychosocial indicators, a history of school suspension or expulsion was associated with most of the covariates analyzed (table 2), including low socioeconomic status, being male, being African American, reporting substance abuse, having poor health, and living with a single mother. Having seen a psychiatrist or psychologist was associated with male gender, food insufficiency, and maternal marital status (single). Feeling shy or being slow to make friends was significantly associated with living with a single mother, low maternal education, and being African American. Substance abuse was associated with increased odds of a history of school suspension and having seen a psychologist or psychiatrist but with reduced odds of feeling shy or being slow to make new friends.


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TABLE 2. Age-adjusted odds ratios* of negative psychosocial indicators by major categorized covariates of 4,852 children aged 6–16 years, Third National Health and Nutrition Examination Survey, 1988–1994

 
After adjustment for age and gender (table 3), children having low serum cholesterol levels did not differ from other children in whether or not they had ever seen a psychologist or psychiatrist, in their mother-rated social skills with peers, and in their level of comfort in their own peer subculture. However, children with low serum total cholesterol levels were more likely than other children to have been suspended or expelled from school. When subjects were separated by race, this association held specifically for non-African-American children. For the children with high total cholesterol levels, the suspension prevalence among non-African Americans was much lower than that of African Americans. Among children with low total cholesterol levels, suspension prevalence did not differ by race (table 3).


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TABLE 3. Prevalence of negative psychosocial indicators and age- and gender-adjusted odds ratios by levels* of serum total cholesterol among 4,852 children aged 6–16 years, Third National Health and Nutrition Survey, 1988–1994

 
These analyses were repeated with adjustment of additional psychosocial covariates (table 4). No new findings emerged, and the association between a low serum cholesterol level and a history of school suspension or expulsion tended to strengthen. Among non-African Americans, a history of school suspension or expulsion was approximately threefold higher for children with total cholesterol below the 25th percentile than for children with total cholesterol at or above the 25th percentile. All the estimates for children aged 6–16 years remained essentially the same when including daily energy intakes (with or without log transformation) from children aged 8–16 years, serum total protein, and albumin from children aged 12–16 years as additional variables in supplementary analyses (data not shown). Estimates from the regression on all subjects who had valid serum cholesterol data (n = 6,392) differed slightly from the results presented above but remain statistically significant for the history of school suspension among non-African Americans for whom the odds ratio = 2.11 (95 percent confidence interval (CI): 1.27, 3.49). The odds ratio for all ethnicities together was 1.54 (95 percent CI: 1.03, 2.29) and for African Americans was 0.94 (95 percent CI: 0.58, 1.53).


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TABLE 4. Multivariable adjusted odds ratios* of negative psychosocial indicators by levels of serum total cholesterol among 4,852 children aged 6–16 years, Third National Health and Nutrition Examination Survey, 1988–1994

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
From a large national sample of children and adolescents, we observed that, of four psychosocial development indicators, a history of school suspension was significantly associated with low serum total cholesterol and that this association existed among non-African-American children only. These results are important because they are the first to demonstrate a statistically significant, ethnicity-dependent association between serum total cholesterol and aggressive behaviors from a national sample of noninstitutionalized, school-age children. This association persists even after adjustment for many other factors, including cognitive and academic performance and nutrition status, which are known to place children's emotional and behavioral development at risk.

The behaviors that lead to school suspension have been seen as "red flags" to identify students with serious behavioral problems. Prior studies reveal that over two thirds of school suspensions and expulsions are ordered in response to acts of physical aggression (27Go, 30Go). Therefore, the results of the current study are consistent with the majority of previous studies examining the associations between low serum cholesterol and various forms of aggression in adults. With few exceptions (32Go), significant associations have been observed from cross-sectional studies (7Go, 33Go), cohort samples (5Go), general population studies (5Go), psychiatric patients and criminals (13Go–15Go), and controlled dietary studies conducted in nonhuman primates (34Go). In particular, low total cholesterol has been associated with the onset of conduct disorder during childhood among male criminals (7Go). The current study extends prior literature by showing an ethnicity-dependent association among children and adolescents. Research across the age spectrum and including other ethnicities might be helpful in disentangling the mystery of the association between serum cholesterol and violence. As of today, almost all studies examining the association between serum cholesterol levels and violence were carried out among Caucasian adults. Researchers have speculated that the observed association of low cholesterol with violence may be a product of confounding. However, it is unlikely that confounding effects from occult factors would selectively affect non-African-American children only.

From prior literature on adults, it is unclear whether there is a temporal association between serum cholesterol and violent behavior. By showing a statistically significant association from children and adolescents, the current study provides indirect evidence that a low serum cholesterol level precedes aggressive behaviors. This study used school suspension as a marker of early aggression. Early aggression has been identified as one of the strongest predictors of later aggression and criminal involvement (35Go, 36Go). Children who exhibited aggressive behavior at age 8 years were more likely to report higher levels of physical aggression, to have more criminal convictions as adults, and to engage in more serious criminal acts (28Go). Almost half of those who initiated violent behavior between 10 and 12 years of age eventually became chronic violent offenders (37Go). However, temporality is just one of Hill's criteria for a causal connection as described by Golomb (4Go), and a putative cause-effect relation between low serum cholesterol and violence awaits further study. Low total cholesterol may represent a biologic marker rather than a risk factor for childhood-onset conduct disorder and violent behavior. Cholesterol and aggressive behavior may not be causally related to one another.

It is possible that at least part of the association of low total cholesterol with school suspension is explainable by a reverse causation. School suspension appears to have serious negative psychiatric consequences, including elevated depressive symptoms and post-traumatic stress disorder (38Go). Post-traumatic stress disorder may result in a fall in cholesterol concentration, and depressed cholesterol may persist for years in chronic medical conditions (39Go). Low or lowered cholesterol has been linked to other biologic factors that predispose to nonatherosclerotic diseases (40Go). Low total cholesterol or lipoprotein concentrations may result in impaired delivery of lipids and fat-soluble nutrients to cells that are activated during the immune response and involved in tissue repair, thus possibly impairing defense against endotoxins and viruses (41Go–43Go). In any case, both psychological and biologic consequences (38Go) of school suspension or expulsion on children and adolescents deserve further examination.

Many biologic mechanisms have been postulated to explain the association between serum lipids and violence. Cholesterol and fats have many physiologic roles and may influence brain function and behavior through modification of membranes and through effects on production, reuptake, or metabolism of neurotransmitters. Several studies in nonhuman primates and humans suggest a specific connection between low or lowered fats or cholesterol levels and low or lowered serotonin activity (44Go, 45Go). In humans, the association between decreased serotonin and impulsivity and aggression is well documented (45Go, 46Go). Researchers therefore speculated that low cholesterol might increase impulsivity by lowering serotonin activity (47Go). Most children and adolescents suspended from school indeed attributed their infractions to a lack of self-control, rather than blaming others (30Go). This study, however, is unable to clarify whether the association of total cholesterol and aggression is a reflection of genetic covariance or a direct causal association. Though a difference in the association by race/ethnicity was found in the current study, we are not able to rule out the possibility that this difference was due to basal prevalence. The prevalence of school suspension is already high among African-American children, so the marginal impact from lower total cholesterol, if any, would be relatively small compared with that on non-African-American children, among whom the basal prevalence of school suspension is low.

The results of the current study should be viewed with caution. As in all research using self-report measures, the psychosocial indicators used in the current study represented the perceptions of the respondents or proxies (30Go). The survey format is subject to multiple biases, including social desirability. In addition, because the responses to the survey items were collapsed or originally designed as dichotomized variables, the range of possible responses was restricted, possibly resulting in misclassifications. For example, school suspension or expulsion is a highly contextualized decision, and the severity of rule violations leading to a school suspension varies case by case (29Go). The heterogeneity of measurement may lead to measurement errors, resulting in an attenuation of the true relations. Depressive symptoms and attention-deficit/hyperactivity disorder are two major reasons for children and adolescents to see psychiatrists or psychologists (48Go, 49Go). Because depressive symptoms and attention-deficit/hyperactivity disorder differ etiologically, grouping children with depressive symptoms, attention-deficit/hyperactivity disorder, or other developmental-behavioral problems together might account for the failure to identify an association between serum cholesterol and a history of seeing psychiatrists or psychologists.

This study has several other limitations. First, the findings were based on a cross-sectional survey. The duration of exposure to abnormal levels of serum cholesterol is unknown. Second, although the richness of NHANES III allows us to delineate the relation between serum cholesterol and psychosocial development after adjustment for many factors, we were unable to adjust for other important potential confounders, such as duration of poverty, maternal mental health, serum essential fatty acids, or long chain polyunsaturated fatty acids, which have been demonstrated to be associated with behavioral development (50Go). However, it was unlikely that these unmeasured factors selectively confounded the association for non-African-American children only. Finally, the samples of the current study may represent only minor offenders. Institutionalized children and children in special classes were excluded. Therefore, the ability to identify a strong association between total cholesterol and aggression may have been constrained by not sampling those who may have been institutionalized in the juvenile justice system because of serious violent offending.

The current study has several unique strengths as well. Existing data suggest that social skills are associated with micro- and macronutrients in animal or human adults (51Go). Many of these associations, however, are difficult to assess in infants or toddlers with the degree of reliability and precision that is possible in older children (52Go). Thus, if any, the relation of serum cholesterols and neurobehaviors in school-age children may be more cogent. Children of the NHANES III were randomly selected from the noninstitutionalized US population; therefore, our results should be fairly generalizable to children in the United States.

In summary, this study reports a statistically significant association between school suspension or expulsion and low total cholesterol among non-African-American children and adolescents from a multiethnic national sample. The finding corroborates and extends the existing literature linking low total cholesterol and aggressive behaviors in adults. Low cholesterol may be a risk factor for aggressive behavior, a risk marker for other biologic substances or genotypes that predispose to such behavior, or a biologic marker for poor prognosis. If well-designed prospective studies confirm the findings of this study, pediatricians will have an opportunity to make a significant contribution to schools and to violence prevention.


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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