Cereal is a popular breakfast choice for children. Children who consume cereal, relative to other breakfast foods, are less likely to be overweight or obese and evidence lower BMI(Reference Albertson, Anderson and Crockett1–Reference Williams6). One study of Greek children aged 12–17 years indicated that youth who ate cereal had 33 % lower probability of being overweight or obese, regardless of age, gender or degree of physical activity(Reference Kosti, Panagiotakos and Zampelas3). Williams(Reference Williams6) reported that the lowest mean BMI and mean waist circumference were found in children (aged 1–12 years) who consumed cereal at breakfast when compared with those who ate other types of breakfasts or skipped breakfast.
Although weight is a useful indicator of health, it is not necessarily optimal. In fact, recent research has shown that waist-to-height ratio (WHtR) is a better predictor of health and disease outcomes than BMI, although most of these studies have been conducted with adults(Reference Aekplakorn, Kosulwat and Suriyawongpaisal7–Reference Lin, Lee and Chen10). Notably, a recently published meta-analysis concluded that ‘statistical evidence supports the superiority of …. WHtR over BMI, for detecting cardiovascular risk factors in both men and women’(Reference Lee, Huxley and Wildman11).
The advantage of WHtR as a discriminator for CVD risk has also been found in children, although the studies are fewer in number. Kahn et al.(Reference Kahn, Imperatore and Cheng12) analysed data from 4- to 17-year-olds who participated in the Third National Health and Nutrition Examination Survey (NHANES III) in a population-based comparison of BMI and WHtR to predict CVD risk. This large-scale study found that WHtR was a significantly better predictor of adverse cardiovascular risk factors than BMI. McCarthy and Ashwell(Reference McCarthy and Ashwell13) reported that WHtR is more closely linked to childhood morbidity than BMI, and suggested it to be used as an ‘additional or alternative measure to BMI’ (p. 988) in studies of health.
A second useful indicator of CVD risk is cholesterol level(Reference Moran, Jacobs and Steinberger14). Elevated LDL cholesterol levels are a major risk factor for CVD and the need for management of high cholesterol levels in children was recently highlighted(Reference Kwiterovich15). Because cholesterol levels can be altered by changes in eating habits, increasing our understanding of the relationship between dietary factors and cholesterol levels may have important implications for prevention. Although several studies have examined the relationship between cereal consumption and cholesterol levels in adults(Reference Kelly, Summerbell and Brynes16), very few have focused on children(Reference Spiotta and Luma17). In one large study of 4–18-year-olds, Gibson(Reference Gibson18) reported that relative to low or average consumers, high consumers of breakfast cereals had lower total and LDL cholesterol. Nicklas et al.(Reference Nicklas, von Duvillard and Berenson19) provided evidence that serum lipid and lipoprotein levels continue to track from childhood into young adulthood, suggesting the need for preventive measures aimed at developing healthy lifestyles early in life. Thus, furthering our understanding of the relationship between health risk markers, such as WHtR and cholesterol, and dietary behaviour, such as cereal consumption, is important for both predicting and potentially managing early risk factors for CVD.
The goal of the current study was to examine associations between cereal consumption and WHtR as well as total LDL and HDL, cholesterol. Based on previous research, we hypothesized that greater cereal consumption would be associated with lower WHtR as well as lower total and LDL cholesterol.
Experimental methods
As previously reported, the National Heart, Lung, and Blood Growth and Health Study (NGHS) is a 10-year longitudinal study of 2379 girls who were 9 or 10 years old at study entry(20). Participants (all female) were recruited from three study sites in the USA: University of California at Berkeley, University of Cincinnati/Cincinnati Children’s Hospital Medical Center and Westat Inc./Group Health in Rockville, MD. The study protocol was approved by the Institutional Review Boards of all participating sites. All girls who entered the NGHS had assented and a parent or guardian consented to their participation.
Procedures and measures
Three-day food records that had been previously validated(Reference Crawford, Obarzanek and Morrison21) were collected at visits (study years) 1–5 and then again at years 7, 8 and 10. Dietitians used age-appropriate materials to instruct girls to record all food and drink, type of meal (breakfast, snack, lunch, etc.) and time of intake for three consecutive days that included two weekdays and one weekend day. Dietitians rated each eating event reported in the food diaries as either a ‘meal’ or a ‘snack’. Food records were coded and analysed for nutrient content(Reference Schakel, Sievert and Buzzard22). Nutrient values were updated annually to reflect changes in the nutrient composition of individual foods. The predictor of interest was the number of days (out of 3 d reported annually) that each girl consumed cereal, either ready-to-eat or cooked. Cereal food codes were identified using labels in the data. The outcome variables were WHtR (waist and height (cm) were measured in all study years except year 1) and total LDL and HDL, cholesterol (mg/dl) derived from 12 h fasting blood specimens obtained in the morning in study years 1, 3, 5, 7 and 10(Reference DeLong, DeLong and Wood23, Reference Friedewald, Levy and Fredrickson24). Cut-off values indicating risk for children include (i) >0·49 for WHtR(Reference Maffeis, Banzato and Talamini25); (ii) total cholesterol >200 mg/dl; (iii) HDL cholesterol <35 mg/dl; and (iv) LDL cholesterol >130 mg/dl(Reference Lee, Gebremariam and Card-Higginson26).
Girls’ age was recorded as age at last birthday. Race (black or white) was self-reported. Girls were categorized as being from one- or two-parent households. The highest level of parental education for either parent (an indicator of socio-economic status) was categorized as ≥4 years of college v. <4 years. The number of parents in the household was one or two. Age of menarche was calculated as the difference in years between a girl’s date of birth and the date when she started having her periods. Physical activity was assessed using the habitual activity questionnaire(Reference Ku, Shapiro and Crawford27). A physical activity score was computed by multiplying an estimate of ‘metabolic equivalents’ for the recorded activities by the weekly frequency, duration and fraction of the year during which activities were performed.
Statistical analysis
The number of days when cereal was eaten in each visit (out of 3 d possible) was the primary measure of the quantity of cereal consumed. There were two reasons for using the number of days when cereal was eaten as the measure of the quantity consumed. First, gram amounts of the cereal consumed were available only in visit three and after; in earlier visits, participants recorded cereal amounts in a variety of units. Second, the amount of cereal consumed varied within a relatively narrow range – for visits when gram amounts of cereal consumed were available, the widest interquartile range was 28–66 g/d(Reference Albertson, Thompson and Franko28).
Analyses estimated the association of days eating cereal with each outcome variable: WHtR, total cholesterol, HDL cholesterol and LDL cholesterol. Mixed models were used to take full advantage of the longitudinal data(Reference Verbeke and Molenberghs29). Briefly, for each girl, an intercept and slope of days eating cereal with each outcome was estimated (the intercept and slope are random effects, potentially varying across girls), using data for all visits; then the mean slope of days eating cereal with each outcome was computed, averaging across girls and visits. To ensure that the association between cereal consumption and the outcomes did not vary across visits, cereal-by-visit interactions were tested in preliminary models, but the interactions were left out of the final models because they did not approach significance. Mixed models accounted for the correlation among repeated measures within girls and enabled unbiased estimation in the presence of missing data arising from girls’ occasional failure to participate in study visits(Reference Verbeke and Molenberghs29, Reference Beunckens, Molenberghs and Kenward30).
A separate model was estimated for each outcome. Cereal consumption was the predictor of primary interest. All models adjusted for potential confounds of the cereal/outcome associations, namely age, study site, race, age of menarche, parental education, number of parents in the household, physical activity, average daily energy intake, average daily intake of fibre, fruit, vegetables and milk, respectively, and the number of days eating breakfast (because meal labels were not obtained in the study, breakfast was defined as eating between 5 am and 10 am on weekdays or 5 am and 11 am on weekends, based on previous study(Reference Affenito, Thompson and Barton31)). Parameter estimates, 95 % CI and hypothesis tests are reported for cereals; the other covariates were viewed as adjustment variables (potential confounds of the cereal effects), and therefore estimates for these are not reported but are available from the authors upon request.
Statistical tests compared the lowest level of cereal consumption (0 d eating cereal in a visit, or infrequent cereal consumption) with each higher level of cereal consumption. All tests were two-sided; P < 0·05 was the criterion of statistical significance. Analyses were performed with the SAS statistical software package version 9·1 (SAS Institute, Cary, NC, USA).
Results
The analysis included the 2371 girls who completed a full 3 d food diary in at least one study year; of these girls, 98·2 % had food diaries available in two or more study years. Of the 2371 girls included in the analysis, 51·0 % were black, 35·1 % had a parent with ≥4 years of college education, 68·5 % were from two-parent households, 37·3 % were from the Berkeley site, 36·5 % from the Cincinnati site and 26·2 % from the Westat/Group Health site. Table 1 shows descriptive statistics for cereal consumption and the outcome variables, by age. Table 2 shows the basic sociodemographic characteristics, physical activity score and nutrition indicators (energy, fruit, vegetable and milk intake) by the average number of days eating cereal (out of 3 d possible) across all visits.
WHtR, waist-to-height ratio.
Gram amounts of cereal consumed were not collected during the first and second visits of the National Heart, Lung, and Blood Growth and Health Study, and therefore no data on this measure are available for 9-year-olds.
MET, metabolic equivalent units.
On average, girls who consumed cereal on 3 d had significantly lower WHtR than girls who consumed cereal on 0 d (Table 3). Girls who consumed cereal on 2 or 3 d had significantly lower total cholesterol than did those who consumed cereal on 0 d, on average. On average, girls who consumed cereal on 1, 2 or 3 d had significantly lower LDL cholesterol than did those who consumed cereal on 0 d. However, there was no significant association between cereal consumption and HDL cholesterol. These analyses adjusted for the measures of sociodemographic characteristics, physical activity and nutrition shown in Table 2 (as well as the study site, age and number of days eating breakfast). Therefore, the results are interpreted as the estimated association of days eating cereal with each outcome, holding these other factors constant.
* Significantly different from 0 d consuming cereal, P < 0·05.
† Estimates are from mixed models adjusting for age, study site, race, parental education, age of menarche, number of parents in the household, physical activity level, average daily energy intake, average daily intake of fibre, fruit, vegetables and milk and number of days of eating breakfast. The estimates are interpreted as the expected value of a given outcome variable, averaged over the other covariates, which were centre-coded to enable such interpretation.
The results indicate that adolescent girls who ate cereal more often had lower WHtR, as well as lower total cholesterol and lower LDL cholesterol, even after adjusting for differences in sociodemographic factors, physical activity, nutrition variables and total energy intake. However, it should be noted that none of the mean values fell into the at-risk range for the variables studied in this sample. Earlier study(Reference Barton, Eldridge and Thompson32) found that cereal consumption was related to BMI; the present study extends that finding to potentially include more powerful predictors of CVD risk and offers suggestive evidence that cereal eating is associated with markers of cardiovascular risk in adolescent girls.
Discussion
The variables that might influence the relationship between cereal consumption and indicators of health have only begun to be studied. Potential mediators of these links include dietary fat levels(Reference Gibson18), glycaemic index(Reference Backhouse, Williams and Stevenson33), nutrient fortification(Reference Rampersaud, Pereira and Girard34), consumption of whole grains(Reference Kochar, Djousse and Gaziano35) and breakfast frequency(Reference Timlin, Pereira and Story36). One recent study of adults(Reference Newby, Maras and Bakun37) found significant associations between cereal fibre and several health variables, including lower BMI, smaller waist circumference, and lower cholesterol and glucose levels, suggesting that fibre intake may be one important factor mediating the health effects of cereal consumption. Mozzaffarian et al.(Reference Mozaffarian, Kumanyika and Lemaitre38) found support for this hypothesis with an elderly sample for which cereal fibre consumption was inversely associated with cardiovascular incidents (i.e. stroke, myocardial infarction); individuals in the highest quintile of cereal fibre intake had a 21 % lower risk of cardiovascular events. Other studies have linked whole grains, including oat fibre, to lower cholesterol in adult samples(Reference Kelly, Summerbell and Brynes16, Reference Davy, Davy and Ho39). Research is needed to better understand the mechanisms by which cereal consumption may lower cholesterol in children and longer-term data will be necessary to determine whether this association continues into adulthood(Reference Srinivasan, Frontini and Xu40).
In the present study, cereal consumption was related to both lower total cholesterol and lower LDL cholesterol in adolescent girls. A previous study with a different sample of children found that higher ready-to-eat cereal consumption was associated with both lower total and LDL cholesterol in boys(Reference Albertson, Affenito and Bauserman41). The mechanisms that might explain this relationship in children are most likely complex and have not been well studied to date. It is possible that the nutrient content of cereal, particularly as related to whole grains, directly impacts the cholesterol levels(Reference Kelly, Summerbell and Brynes42). Another explanation is that the link with cholesterol is related to the connection between cereal consumption and physical activity. An earlier study found that children who were high cereal consumers also tended to engage in more physical activity(Reference Albertson, Thompson and Franko28), and recent data indicate that higher physical activity is associated with lower cholesterol levels in children and adolescents(Reference Owen, Nightingale and Rudnicka43). In a recent review, e.g., five of eight intervention-based studies found significant improvements in at least one lipid/lipoprotein variable in the children who received a physical activity programme, relative to controls(Reference Janssen and Leblanc44). Alternatively, previous studies of this cohort have indicated that girls who ate cereal also consumed less fat in their diets, which most likely relates to cholesterol levels(Reference Barton, Eldridge and Thompson45, Reference Albertson, Thompson and Franko46). For example, in a study of 7-year-old children in Finland, serum cholesterol concentrations were found to be lower in those who had diets lower in saturated fat(Reference Räsänen, Lehtinen and Niinikoski47), suggesting the possibility of intervention targets. Further study is needed to determine exactly how cereal consumption might influence risk for CVD in children and to develop programmes for reducing cholesterol levels in children at risk.
The relationship between dietary intake, body composition, sexual maturation during adolescence and lipid levels is complex(Reference Kwiterovich, Barton and McMahon48). Studies of the effects of diet on HDL cholesterol in children have been less consistent than those on LDL cholesterol(Reference Gibson18, 49–Reference Polonsky, Bellet and Specher51), suggesting that dietary changes may have a stronger effect on LDL than HDL cholesterol, as was seen in the present study. Future research exploring interventions to decrease LDL cholesterol and raise HDL cholesterol is needed(Reference Newfield, Dewan and Jain52).
There are several limitations to the present study. Due to the large sample size, NGHS had excellent statistical power to detect associations between cereal consumption and health outcomes, and therefore statistically significant differences do not necessarily represent practically large effects. As is typical of epidemiological studies, dietary information was based on self-report and may therefore be subject to recall errors or under-reporting. Because meal labels were not collected in the study, breakfast was defined based on the time of consumption, but these times could include snacks as well as breakfast meals. Finally, although demographically diverse in terms of geography and socio-economic status, the NGHS is not a nationally representative sample of girls. These limitations are offset by several strengths, such as the low attrition rate and the availability of 3 d of food intake data.
The present study adds to the growing body of evidence indicating that cereal consumption is associated with a number of positive health benefits that should be studied further.
Acknowledgements
The present study was supported by the General Mills Inc. and by a grant from the National Heart, Lung, and Blood Institute (NHLBI) (HL/DK71122). Drs Franko, Thompson and Barton are paid consulting fees by General Mills Inc. The present study was also supported by contracts HC55023-26 and cooperative agreements U01-HL-48941-44. Participating NGHS centers included Children’s Medical Center, Cincinnati, OH, USA (Stephen R Daniels, MD, Principal Investigator and John A Morrison, PhD, Co-Investigator); Westat Inc., Rockville, MD, USA (George B Schreiber, ScD, Principal Investigator and Ruth Striegel-Moore, PhD, Co-Investigator); and University of California, Berkeley, CA, USA (Zak I Sabry, PhD, Principal Investigator, Patricia B Crawford, MPH, Dr PH, RD, Co-Investigator); Maryland Medical Research Institute, Baltimore, MD (Bruce A Barton, PhD, Principal Investigator) served as the data coordinating centre. Program Office: NHLBI (Eva Obarzanek, PhD, MPH, RD, Project Officer 1992–2007, Gerald H Payne, MD, Project Officer 1985–1991). The authors have no conflict of interest to declare. D.L.F. and A.M. designed the study and wrote the manuscript; D.R.T. designed the study, analysed the data and wrote the manuscript; and B.A.B. designed the study and analysed the data. Portions of the present manuscript were completed while one of the authors (D.L.F.) was a distinguished research fellow at the Institute for Advanced Study and the School of Psychological Science at La Trobe University, Melbourne, Australia.