RESEARCH

Original Research

Meets Learning Need Codes 3000, 3020, 4000, and 4160. To take the Continuing Professional Education quiz for this article, log in to the Academys Online Business Center at www.eatright.org/obc, click the Journal Article Quiz button, click Additional Journal CPE Articles, and select this articles title from a list of available quizzes.

Relationship between Whole-Grain Intake, Chronic Disease Risk Indicators, and Weight Status among Adolescents in the National Health and Nutrition Examination Survey, 1999-2004
IN YOUNG HUR, PhD, RD; MARLA REICKS, PhD, RD able, adjusted for demographic characteristics, smoking, physical activity, and food group/energy intake. Results Fewer than one third consumed 0.5 whole grain ounce equivalents per day. Higher whole-grain intake was associated with lower rened-grain and higher carbohydrate, ber, folate, and energy intakes. Higher whole-grain intake was associated with lower body mass index and waist, thigh, and arm circumferences among boys only but not on further adjustment for food group intake. In models adjusted for food group intake, higher whole-grain intake was associated with lower fasting insulin levels and higher serum and red blood cell folate levels for boys and girls, with lower C-peptide concentrations for girls and lower homocysteine concentrations for boys. Conclusions Whole-grain intake was not associated with body mass index after adjusting for food group intake but was related to positive nutrient proles and chronic disease risk factors, which supports current recommendations to promote greater intake of whole grains among adolescents. J Acad Nutr Diet. 2012;112:46-55. ost adolescents are not eating the recommended three or more servings of whole-grain foods per day (1-4). Nationally representative and populationbased intake data documented an estimated daily intake of approximately 0.6 to 0.8 servings of whole-grain foods by adolescents (1-4), in contrast to the recommended three or more daily servings (5). Four food sources (ready-to-eat and hot cereals, yeast breads, and popcorn), accounted for 80% of whole-grain intake by Americans in 2001-2002 (6). Although rened versions of these foods are commonly available for adolescents through school meal feeding programs, whole-grain counterparts are offered less frequently (7). Longitudinal and cross-sectional studies in adults show an association between higher intake of whole-grain foods and lower risk of type 2 diabetes (8,9), cardiovascular ABSTRACT Background Although whole-grain intake has been associated with improved chronic disease risk factors and weight status in adults, similar studies are limited among adolescents. Objective To determine the relationship among chronic disease risk factors, weight status, and whole-grain intake among adolescents (aged 12 to 19 years) by sex. Design Analysis of the relationship between dietary, anthropometric, and chronic disease risk factors/laboratory measures and whole-grain intake groups (none, low [0 to 0.5 oz equivalents/day], high [0.5 oz equivalents/ day]) among US adolescents (based on cross-sectional data from the National Health and Nutrition Examination Survey, 1999-2004). Participants/setting Data from 4,928 adolescents (2,495 boys, 2,433 girls) collected in person at home and mobile examination centers. Main outcome variables Adjusted least-squares means for dietary, anthropometric, and chronic disease risk factors/ laboratory measures by whole-grain intake groups. Statistical analyses performed Outcome variables were examined in separate multiple linear regression models with categories of whole-grain intake as the independent vari-

I. Y. Hur is a postdoctoral associate, and M. Reicks is a professor, Department of Food Science and Nutrition, University of Minnesota, St Paul. Address correspondence to: Marla Reicks, PhD, RD, Department of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, St Paul, MN 55018. E-mail: mreicks@umn.edu Manuscript accepted: July 27, 2011. Copyright 2012 by the Academy of Nutrition and Dietetics. 2212-2672/$36.00 doi: 10.1016/j.jada.2011.08.028

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disease (CVD) (10,11), and metabolic syndrome (12). These ndings support national dietary recommendations for consuming at least half of all grains as whole grains (5). Whole grains include various bioactive components, such as dietary ber, phytoestrogens, minerals, antioxidants, vitamin E, and folate, which may act synergistically to reduce risk of chronic disease (13,14). Higher whole-grain intake was associated with improvements in CVD risk factors in cross-sectional studies, including lower triacylglycerol, total and low-density lipoprotein cholesterol concentrations in adults (12,15), and lower homocysteine levels in adolescents (16). Improvements in markers of glycemic control such as insulin, C-peptide, and leptin were also observed with higher whole-grain intake in adults (17,18). However, mechanistic studies to explain the relationship between wholegrain intake and health benets have produced contradictory results in adults (19) and are limited in adolescents. Among adolescents, results from several cross-sectional studies have shown an inverse association between whole- and rened-grain intake and central obesity (1) and between whole-grain intake and body mass index (BMI) and BMI z score (3) and BMI and waist circumference (20). Results from research studies suggest that high ber consumption may suppress appetite, reduce energy intake, and enhance satiety (21,22). Wholegrain foods can be a good source of ber, which may explain why whole-grain consumption was linked to better weight outcomes in these previous studies (1,3,20). Intakes of ber, carbohydrate, and energy were signicantly higher, and total fat and protein intakes were signicantly lower among adolescents consuming a high level of daily whole-grain servings (3.0 servings/day) compared to those consuming 3.0 servings/day (23). However, the previous studies reporting inverse associations between whole-grain intakes and measures of body size (1,3,20) failed to adequately account for other dietary factors that may also explain the association (eg, total fat intake and fruit and vegetable intakes). The increased prevalence of obesity in adolescents during the past several decades (24) is of concern because of associations between obesity and risk factors for type 2 diabetes and CVD among adolescents (25,26). Nationally representative cross-sectional data (1999-2006) for adolescents (aged 12 to 19 years) showed a 20.3% prevalence of abnormal lipid levels that varied by BMI with 43% of adolescents with obesity having at least one abnormal lipid level (27). A cross-sectional study showed that CVD risk factors, such as lipid abnormalities, were associated with the presence of overweight or elevated insulin among obese adolescents attending an obesity treatment program (28). Some differences may exist in disease risk indicators by sex among adolescents. Based on data from the National Health and Nutrition Examination Survey (NHANES) 2007-2008, the prevalence of high BMI (BMI-for-age 97% percentile) was slightly higher for adolescent boys aged 12 to 19 years (14.3%) than for girls (10.4%), with a larger discrepancy observed in Hispanic boys (18.1%) than in girls (12.1%) (24). Insulin resistance data from NHANES 1999-2002 showed that adolescent girls aged 12 to 19 years had signicantly higher mean

homeostasis model assessment of insulin resistance compared to boys after adjusting for race, age, and weight status (29). Most of the evidence for the relationship between whole-grain intake and risk factors for type 2 diabetes, CVD, and weight status is based on studies in adults, whereas only limited studies are available for adolescents. Thus, this study was conducted to evaluate associations among whole-grain intake, nutrient intake, weight status, chronic disease risk factors, and other laboratory measures among adolescents stratied by sex using cross-sectional data from NHANES 1999-2004. Results from this analysis will assist with providing direction for public health efforts about whole-grain intakes among adolescents. METHODS Participants NHANES 1999-2004 data were derived from a crosssectional survey with a nationally representative, stratied, multistage probability sample of the noninstitutionalized US population (30). In general, each survey participant is interviewed at home and also undergoes a physical examination conducted by trained personnel at a mobile examination center (31). NHANES data sets are released on a 2-year basis and are designed to be combined. In this study, 1999-2000, 2001-2002, and 2003-2004 data sets were combined to form one 1999-2004 data set. The combined data set included data from 6,418 different adolescents for whom demographic, anthropometric, dietary intake, and physical activity data were available based on both a home interview and a physical examination. Youth between the ages of 12 and 19 years were selected to represent adolescents for this study based on age categories used in the NHANES 1999-2000 sample design (32). Participants were excluded if they reported extreme energy intakes (6,000 kcal both for girls and boys, and 400 kcal for boys and 300 kcal girls) (n51), were pregnant or breastfeeding (n124), were taking insulin (n16), were taking oral medication for diabetes (n2), or had been prescribed medication for hypertension (n8). The cutoff values for energy intakes reected 20% or 200% of the estimated total energy expenditure for youth aged 12 to 18 years with sedentary or very active physical activity levels, respectively, according to 2005 Dietary Reference Intakes for energy (33). Participants with missing data for disease risk indicators, including C-reactive protein, systolic blood pressure, total cholesterol, high-density lipoprotein cholesterol, serum folate, or homocysteine (n1,289) were also excluded. For participants with nonfasting blood samples, data for insulin, glucose, C-peptide, low-density lipoprotein cholesterol, and triglycerides were missing (n1,073 to 1,130 for boys and 993 to 1,043 for girls). However, these participants were not excluded from the nal study population to maintain a large sample size. Therefore, the nal study population included 4,928 adolescents (2,495 boys and 2,433 girls). The study was approved by the University of Minnesotas Institutional Review Board as exempt because the

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research involved existing, deidentied, publicly available data. Dietary Intake Dietary intake data from NHANES 1999-2000 and 20012002 data sets were based on one 24-hour dietary recall, while intake data for 2003-2004 were collected on 2 days. Mean values for the 2 days of intake data (2003-2004) were used in the analysis. Food group intake data were obtained from US Department of Agriculture (USDA) Food Pyramid data based on NHANES 1999-2002 data and NHANES 2003-2004 data. Food group consumption was quantied as number of cup equivalents or ounce equivalents based on the MyPyramid Equivalents Database for USDA Survey food codes 1994-2002 version 1 (MPED 1.0) (34) and MyPyramid Equivalents Database for USDA Survey food codes 2003-2004 version 2 (MPED 2.0) (35). The MPED 1.0 and 2.0 provide food group information for total grain, whole-grain, and nonwholegrain. The MPED 1.0 and 2.0 also provide food group information for total vegetables (ie, dark-green leafy vegetables, orange vegetables, white potatoes, other starchy vegetables, tomatoes, and other vegetables), total fruits (ie, citrus fruits, melons, berries, and other fruits), total milk (ie, milk, yogurt, and cheese), and the meat and beans group (ie, beef, pork, veal, lamb, game, organ meats, chicken, turkey, frankfurters, sausage, luncheon meats, sh and shellsh, eggs, cooked dry beans and peas, soybean products, and nuts and seeds). Sugarsweetened beverages (SSBs) included soda, sports drinks, fruit drinks and punches, low-energy drinks, sweetened tea, and other sweetened beverages according to Bleich and colleagues (36). Dietary outcome variables included intake of total and rened grain, carbohydrate, dietary ber, folate, energy, total food consumption (grams), and energy density (kilocalories per gram).

for determination of glucose, insulin, C-peptide, and Creactive protein (39-41). Serum total cholesterol, highdensity lipoprotein cholesterol, and triglycerides were measured with standard assays for blood lipid measurements, whereas low-density lipoprotein cholesterol levels were calculated using the Friedewald formula (39-42). Homocysteine concentrations were measured in plasma using a uorescence polarization immunoassay (39-41). After resting quietly in a sitting position for 5 minutes and determining the maximum ination level, systolic blood pressure was measured with three and sometimes four determinations with a mercury sphygmomanometer using the right arm. Serum and red blood cell folate and serum folate were measured by Centers for Disease Control and Prevention laboratories using standard assay procedures (39-41). Outcome variables for chronic disease risk factors/laboratory measures included plasma glucose, insulin, C-peptide, C-reactive protein, serum total cholesterol, high-density liporotein cholesterol, low-density lipoprotein cholesterol and triglycerides, serum and red blood cell folate, and homocysteine concentrations and systolic blood pressure. Physical Activity and Smoking Physical activity data were collected via a questionnaire about daily activities, leisure-time activities, and sedentary activities according to NHANES data collection protocols (43-45). These activities were categorized as vigorous activity, moderate activity, and nonactivity including television viewing or computer use. Vigorous activity was dened as causing heavy sweating or large increases in breathing or heart rate; examples are running, aerobics classes, or swimming during the past 30 days. Moderate activity was dened as activity that caused light sweating or an increase in breathing or heart rate, such as walking, bicycling, golf, and dancing during the past 30 days. Television or video viewing was recorded in exact number of hours per day and was categorized into four groups: 1 hour, 1 to 2 hours, 3 to 4 hours, and 5 hours/day. Computer use was categorized into three groups: 1 hour, 1 to 2 hours, and 3 hours. Smoking was assessed by questionnaire wherein adolescents indicated the number of cigarettes smoked per day during the past month. The frequency of smoking cigarettes was categorized into three groups: none, 10/day, and 10/day (43-45). Statistical Analysis Data were examined with SUDAAN software (Windows individual user SAS-callable version 9.0.1, 2005, Research Triangle Institute, Research Triangle Park, NC) and SAS version 9.1.3 software (2003, SAS Institute, Inc, Cary, NC). Appropriate sampling weights were used to account for differential probabilities of selection and complex sampling design. To examine relationships among individual dietary, anthropometric, chronic disease risk factors/laboratory measures, and whole-grain intake, separate multiple linear regression models were constructed for each outcome variable. Dietary, anthropometric, and chronic disease risk factors/laboratory measures were modeled as dependent variables, and wholegrain consumption (none, low [0 to 0.5 oz equivalents/

Anthropometric Measures Height; weight; waist, arm, and thigh circumferences; and subscapular skinfold thickness were measured as part of the physical examination process according to the Anthropometry Procedures Manual for NHANES data collection (37). BMI was calculated as weight in kilograms divided by height in meters squared. Age and sex-specic BMI z scores were calculated according to Centers for Disease Control and Prevention growth charts (38). Anthropometric outcome variables included BMI, BMI z score; weight; waist, arm, and thigh circumferences; and subscapular skinfold thickness. Chronic Disease Risk Factors/Laboratory Measures All blood and urine samples were collected at the mobile examination centers according to NHANES data collection protocols (39-41). Samples were collected from fasting participants (8.5 hours and 24 hours) in the morning examination session only. Complete blood count and pregnancy analyses were conducted in the mobile examination center laboratory, whereas the remaining laboratory analyses were performed at designated public and private institutions. Standard clinical assays were used

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day], or high [0.5 oz equivalents/day], entered as 0, 1, or 2, respectively) was modeled as the independent variable. All models were adjusted for age, race/ethnicity, family income, smoking, and physical activity (rst set of models). Age (12 to 14 years, 15 to 17 years, or 18 to 19 years), family income ($25,000, $25,000 to $55,000, or $55,000), daily computer use (1 hour, 1 to 2 hours, or 3 hours), and smoking level (none, 1 to 10, or 10) were modeled as three-level categorical variables; vigorous and moderate activity levels were dichotomized as 1yes and 0no, and daily television/video viewing ( 1 hour, 1 to 2 hours, 3 to 4 hours, or 5 hours) was modeled as a four-level categorical variable. Race/ethnicity was modeled using indicator variables. In the rst set of models, the models for specic nutrients (eg, folate) and anthropometric factors were additionally adjusted for energy intake. Anthropometric models for weight; waist, thigh, and arm circumferences; and subscapular skinfold thickness were also additionally adjusted for height (rst set of models). Chronic disease risk factor/ laboratory measures models were also adjusted for BMI and energy intake (rst set of models). Fruit, vegetable, milk, meat and beans, and SSB intakes were added to account for the effect of foods consumed in combination (second set of models). Results of independent two sample t tests are displayed showing the differences between least-square means for whole-grain consumption groups when regression models indicated signicant associations with chronic disease risk factors/ laboratory measures (second set of models only). Dietary intake data (food, nutrient, and energy intake), anthropometric data, and chronic disease risk indicator/laboratory measures data are presented according to three levels of whole-grain intake (none, low, high) as adjusted leastsquares meansstandard error of the means. Statistical signicance levels were set at P0.05. RESULTS Characteristics of the Sample Characteristics of the sample are shown in Table 1. Few differences were observed between those meeting all inclusion criteria and those excluded. Boys that were excluded were slightly younger (P0.002) and had a lower BMI (P0.05) than boys that were included. Excluded girls were somewhat more likely to spend more time watching television or videos (P0.037) and consumed slightly less energy than included girls (P0.05). Food, Nutrient, and Energy Intake Mean intakes for food, nutrients, and energy are presented by sex in Table 2. About half of adolescent boys (52%) and girls (50%) did not consume any whole grains on the days that intake was measured. About one third of boys (31%) and one fourth of girls (27%) consumed 0.5 oz equivalents/day (P0.003). For boys and girls, whole-grain intake was positively associated with intakes of carbohydrate, dietary ber, and total folate. Even with additional ber from whole grain intake, girls and boys with high whole-grain intakes were still far from meeting recommendations for ber intake (14 g vs 26 g and 17 g vs 31 to 38 g) (33). For

boys and girls, a positive association existed between whole-grain intake and daily energy intake. For girls, whole-grain intake was positively associated with total food consumption (grams) and total dietary energy density (grams per kilocalorie). Anthropometric Measures After adjusting for age, race/ethnicity, family income, smoking, physical activity, and energy intake (rst set of models), anthropometric characteristics of girls were not signicantly associated with level of daily whole-grain intake (Table 3). However, whole-grain intake among boys was inversely associated with BMI, BMI z score, weight, and waist, thigh, and arm circumferences. After further adjustment for food group intake in the second set of models (fruits, vegetables, meat and beans, milk, and SSBs), a signicant inverse association only existed between wholegrain intake and arm circumference among boys (Table 3). Chronic Disease Risk Factors/Laboratory Measures In the rst set of models for boys, fasting insulin levels were inversely associated with whole-grain intake (Table 4). An inverse association existed between C-peptide levels of girls and whole-grain intake, whereas a positive association was observed between daily whole-grain intake and high-density lipoprotein cholesterol levels. For boys, homocysteine levels were inversely associated with whole-grain intake. A positive association existed for both serum and red blood cell folate levels for boys and girls with daily whole-grain intake. After further adjustment for food group intake (fruits, vegetables, meat and beans, milk, and SSBs), in the second set of models, an inverse association was observed between whole-grain intake and fasting insulin levels in girls, whereas fasting insulin levels were lower in boys with low whole-grain intake compared to boys with no whole-grain intake. C-peptide levels in girls were lower among those with high wholegrain intake compared to those with no or low intake, and C-reactive protein levels were higher in girls with low intake compared to those with no or high intake. Homocysteine concentrations were lower for boys with high whole-grain intake compared to those with no or low intake. Serum and red blood cell folate levels in boys and girls were positively associated with whole-grain intake. DISCUSSION This cross-sectional study addresses the associations between whole-grain intake and weight status and chronic disease risk indicators among adolescents. In the second set of models, which were adjusted for food group intake, whole-grain intake was not associated with BMI, contrary to other cross-sectional studies in adolescents (1,3) where whole-grain intake was inversely associated with indicators of weight status such as BMI and waist circumference. In the second set of models, positive results were observed for associations among whole-grain intake, nutrient intake, and chronic disease risk indicators that relate to protection from chronic disease. High intake of whole grain was positively associated with indicators of adiposity in other cross-sectional stud-

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Table 1. Characteristics of adolescents ages 12 to 19 years from the National Health and Nutrition Examination Survey data (1999-2004) who met all inclusion criteria and those excluded by sex in a study of the relationship among chronic disease risk factors, weight status, and whole-grain intake Sex Male Characteristic Age (y) Body mass index Energy intake (kcal) Race-ethnicity Hispanic Non-Hispanic white Non-Hispanic black Other Family income $0-$24,999 $25,000-$54,999 $55,000 Vigorous activity during the past 30 d Yes No Moderate activity during the past 30 d Yes No Daily television/video viewing 1 h 1-2 h 3-4 hours 5 h Daily computer use 1 h 1-2 h 3 h No. cigarettes/d over the past 30 d 0 10 10
a 2 b

Female Excluded (n657) P valuea 0.002 0.050 0.325 0.185 Included (n2,433) Excluded (n632) P value 0.345 0.089 0.050 0.205 11.0 (881) 61.6 (640) 14.1 (720) 13.4 (192) n2,257 36.5 (1,020) 26.7 (649) 36.8 (588) n2,392 65.5 (1,445) 34.5 (947) n2,392 67.7 (1,494) 32.3 (898) n1,620 19.8 (256) 45.2 (710) 23.6 (426) 11.4 (228) n1620 51.2 (921) 37.2 (546) 11.6 (153) n2,433 81.1 (2,098) 16.1 (295) 2.8 (40) 8.9 (194) 60.3 (169) 14.5 (200) 16.4 (69) n577 33.9 (266) 26.3 (147) 39.8 (164) n603 62.5 (352) 37.4 (251) n603 65.6 (370) 34.4 (233) n436 13.3 (67) 45.8 (192) 24.0 (102) 16.9 (75) n436 49.5 (240) 41.4 (157) 9.1 (39) n632 85.3 (554) 11.9 (68) 2.8 (10)

Included (n2,495)

4 meanstandard error 3 15.50.1 15.00.1 23.30.2 22.70.3 2,57831 2,52348 4 % (n)b 3 11.7 (903) 60.7 (631) 13.9 (767) 13.7 (194) n2,289 33.6 (1,003) 28.2 (686) 38.2 (600) n2,467 79.0 (1,888) 21.0 (579) n2,465 64.8 (1,472) 35.2 (993) n1,584 14.1 (205) 44.1 (636) 29.4 (497) 12.4 (246) n1,586 50.8 (880) 34.9 (517) 14.4 (189) n2,495 82.2 (2,085) 13.6 (343) 4.2 (67) 9.4 (207) 63.0 (168) 15.0 (229) 12.7 (53) n587 31.3 (241) 26.0 (170) 42.7 (176) n629 78.5 (490) 21.5 (139) n626 68.1 (377) 31.9 (249) n439 16.4 (72) 46.4 (185) 25.0 (120) 12.3 (62) n439 49.4 (235) 33.5 (145) 17.1 (59) n657 84.6 (569) 10.4 (71) 5.0 (17)

4 meanstandard error 3 15.40.1 15.30.2 23.30.2 23.80.3 1,97921 1,88446 4 % (n) 3

0.510

0.553

0.828

0.394

0.277

0.444

0.633

0.037

0.592

0.360

0.306

0.083

P comparing included vs excluded boys or included vs excluded girls. Column percentage within demographic or physical activity category (number of subjects).

ies in adolescents where an inverse association was reported between whole-grain intake and BMI and waist circumference (1,3); however, these associations were not examined by sex in one of these studies (3). Among Greek adolescents, intake of whole-grain bread by normal weight boys was higher compared to overweight and obese boys, but not among girls (46). Vgstrand and colleagues (47) reported an inverse association between body fatness in adolescents boys (derived from densitometry via air-displacement plethysmography measurements) and breakfast cereal intake, an important food source of whole grain (6). However, in these studies, po-

tentially confounding factors included in the analysis were age, sex, ethnicity, total energy intake, Tanner stage, parental education, and physical activity, but not other dietary factors, such as intake of fruits, vegetables, meat and beans, dairy, and SSBs. Adjusting for food group intake may be a positive means to accurately identify relationships between intakes of a food group (whole grains) and weight status. Newby and colleagues (48) reported that factors associated with diets high in whole grains among adults included greater fruit and vegetable intake and lower meat intake. Intake of certain food groups has also been associated with overweight and

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Table 2. Daily food, nutrient, and energy intake by whole-grain consumption among adolescent boys and girls ages 12 to 19 years from the National Health and Nutrition Examination Survey (1999-2004) data in a study of the relationship among chronic disease risk factors, weight status, and whole-grain intake Whole-Grain Consumptiona Boys Food/nutrient Whole-grain median (oz eq) Total grain (oz eq)c Whole grain (oz eq)c Nonwhole grain (oz eq)c Carbohydrate (g)c Dietary ber (g)c Total folate (g)c Total energy intake (kcal)d Total food consumption(g)d Energy density (kcal/g)d
a b

Girls High (n672) P value None (n1,278) 0 4 adjusted 6.10.1 0 6.10.1 2643 10.90.2 2946 1,87423 1,72128 1.140.01 Low (n568) High (n587) P value

None (n1,354) 0 4 adjusted 8.40.2 0 8.40.2 3384 13.60.3 3998 2,50443 2,38440 1.140.02

Low (n469)

0.2 1.2 meanbstandard error 3 8.50.2 8.80.2 0.20.0 1.60.1 8.30.2 7.20.2 3465 3575 14.40.4 17.30.5 42518 54319 2,61956 2,70451 2,44969 2,51362 1.140.02 1.170.01

0.419 0.001 0.001 0.018 0.001 0.001 0.019 0.121 0.163

0.2 1.0 meanstandard error 3 6.60.2 7.30.2 0.20.0 1.30.1 6.40.2 6.00.2 2644 2853 11.70.2 14.50.3 36313 45215 1,90937 2,20334 1,73334 1,94839 1.170.02 1.190.02

0.001 0.001 0.263 0.001 0.001 0.001 0.001 0.001 0.002

None0 oz eq/d; low0 and 0.5 oz eq/d; high0.5 oz eq/d. Adjusted least squares means based on multiple regression models as described in the methods section. c Means were adjusted for age, race/ethnicity, family income, energy intake, smoking, and physical activity. d Means were adjusted for age, race/ethnicity, family income, smoking, and physical activity. NOTE: Information from this table is available online at www.andjrnl.org as part of a PowerPoint presentation.

Table 3. Anthropometric parameters by whole-grain consumption among adolescent boys and girls ages 12 to 19 years from the National Health and Nutrition Examination Survey (1999-2004) data in a study of the relationship among chronic disease risk factors, weight status, and whole-grain intake Whole-Grain Consumptiona Boys Anthropometric parameter First set of models Body mass indexc Body mass index z scorec Weight (kg)d Waist circumference (cm)d Thigh circumference (cm)d Arm circumference (cm)d Subscapular skinfold (mm)d Second set of models Body mass indexe Body mass index z scoree Weight (kg)f Waist circumference (cm)f Thigh circumference (cm)f Arm circumference (cm)f Subscapular skinfold (mm)f
a b

Girls High (n672) P value None (n1,278) Low (n568) High (n587) P value

None (n1,354)

Low (n469)

4 adjusted meanbstandard error 3 23.60.2 0.60.0 69.30.6 82.60.6 51.80.3 29.80.2 12.50.3 23.50.2 0.50.0 69.20.6 82.50.6 51.80.3 29.80.2 12.50.3 23.20.4 0.50.1 68.41.1 81.71.0 51.30.5 29.50.3 12.30.5 23.20.4 0.50.1 68.31.1 81.61.0 51.30.5 29.50.3 12.30.5 22.80.2 0.40.1 67.10.7 80.50.6 50.60.3 28.80.2 12.30.4 22.90.2 0.40.1 67.40.7 80.80.6 50.70.3 28.90.2 12.40.4 0.034 0.036 0.043 0.031 0.018 0.004 0.736 0.151 0.152 0.163 0.145 0.068 0.023 0.914

4 adjusted meanstandard error 3 23.60.2 0.50.0 61.70.7 80.10.6 50.30.3 27.90.2 15.30.4 23.50.3 0.50.0 61.60.7 80.00.6 50.30.3 27.90.2 15.30.4 23.00.2 0.40.1 60.30.6 79.20.5 49.70.3 27.40.2 14.50.4 23.00.2 0.40.1 60.20.6 79.20.5 49.60.3 27.40.2 14.40.4 22.90.3 0.40.1 59.90.7 78.70.6 49.90.4 27.40.2 14.70.4 23.00.3 0.40.1 60.00.7 78.90.6 49.90.4 27.40.2 14.70.4 0.227 0.515 0.187 0.226 0.319 0.246 0.262 0.281 0.547 0.250 0.373 0.319 0.296 0.259

None0 oz eq/d; low0 and 0.5 oz eq/d; high0.5 oz eq/d. Adjusted least-squares means based on multiple regression analysis as described in the methods section. c Means were adjusted for age, race/ethnicity, family income, energy intake, smoking, and physical activity. d Means were adjusted for age, race/ethnicity, family income, height, energy intake, smoking, and physical activity. e Means were adjusted for age, race/ethnicity, family income, energy intake, smoking, physical activity, and intake of food groups (meat and beans, milk, fruit, vegetable, and sugar-sweetened beverages). f Means were adjusted for age, race/ethnicity, family income, height, energy intake, smoking, physical activity, and intake of food groups (meat and beans, milk, fruit, vegetable, and sugar-sweetened beverages).

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Table 4. Chronic disease risk indicators and laboratory measures by whole-grain consumption among adolescent boys and girls ages 12 to 19 years from the National Health and Nutrition Examination Survey (1999-2004) data in a study of the relationship among chronic disease risk factors, weight status, and whole-grain intake Whole-Grain Consumptiona Chronic disease risk indicators and laboratory measures First set of models Fasting insulin level (IU/mL)de Glucose, plasma (mg/dL)df C-peptide (nmol/L)dg C-reactive protein (mg/dL)h Systolic blood pressure (mm Hg) Total cholesterol (mg/dL)i High-density lipoprotein cholesterol (mg/dL)i Low-density lipoprotein cholesterol (mg/dL)di Triglyceride (mg/dL)dj Homocysteine (mol/L)k Folate, serum (ng/mL)l Folate, red blood cell (ng/mL)l Second set of modelsm Fasting insulin level (IU/mL)de Glucose, plasma (mg/dL)df C-peptide (nmol/L)dg C-reactive protein (mg/dL)h Systolic blood pressure (mm Hg) Total cholesterol (mg/dL)i High-density lipoprotein cholesterol (mg/dL)i Low-density lipoprotein cholesterol (mg/dL)di Triglyceride (mg/dL)dj Homocysteine (mol/L)k Folate, serum (ng/mL)l Folate, red blood cell (ng/mL)l
a b

Boys None (n1,354) Low (n469) High (n672) P value None (n1,278) Low (n568)

Girls High (n587) P value

4 adjusted meanbstandard error 3 13.20.5 93.30.4 0.700.02 0.150.01 1121 1601 471 932 954 6.80.1 12.50.2 2363 13.20.5y 931 0.700.02y 0.150.01 1121 1601 471 932 963 6.70.1y 12.60.2y 2373y 10.10.6 92.00.8 0.650.02 0.170.04 1131 1622 481 973 934 6.70.2 12.40.3 2484 9.90.6z 921 0.640.02z 0.170.04 1131 1622 481 973 944 6.70.2y 12.50.2y 2494z 12.40.5 92.20.5 0.690.02 0.140.01 1121 1602 471 922 1004 6.30.1 14.30.3 2596 12.40.6y 921 0.700.02y 0.140.02 1131 1602 471 922 995 6.40.1z 14.10.3z 2565z 0.002 0.246 0.099 0.701 0.767 0.580 0.490 0.539 0.475 0.002 0.001 0.001 0.004 0.159 0.047 0.755 0.761 0.649 0.599 0.459 0.735 0.020 0.001 0.001

4 adjusted meanstandard error 3 13.60.7 88.90.4 0.740.02 0.170.01 1071 1631 521y 931 873 5.80.1 12.60.3 2475 13.60.6y 891 0.740.02y 0.170.01y 1071 1641 521 931 883 5.80.1 12.70.2y 2485y 12.60.5 89.10.8 0.740.02 0.250.03 1071 1652 531z 943 966 5.90.1 13.60.5 2446 12.60.5y 891 0.740.02y 0.250.03z 1071 1652 531 943 956 5.90.1 13.70.5yz 2446y 11.80.5 90.30.7 0.690.02 0.170.01 1061 1652 531z 902 895 5.80.2 14.80.5 2696 11.80.5z 901 0.690.02z 0.170.01y 1061 1652 531 902 895 5.80.2 14.50.4z 2665z 0.060 0.222 0.019 0.046 0.372 0.625 0.032 0.409 0.474 0.844 0.001 0.001 0.019 0.276 0.016 0.046 0.452 0.728 0.062 0.335 0.547 0.902 0.001 0.001

None0 oz eq/d; low0 and 0.5 oz eq/d; high0.5 oz eq/d. Adjusted least squares means based on multiple regression analysis as described in the Methods section. c Means were adjusted for age, race/ethnicity, family income, body mass index, energy intake, smoking, and physical activity. d Number of observations ranges from n1,073-1,130 for boys, n993-1,043 for girls due to missing data; differs from total n reported in columns. e To convert IU/mL insulin to pmol/L, multiply IU/mL by 6.945. To convert pmol/L insulin to IU/mL, multiply pmol/L by 0.143. Insulin of 13.2 IU/mL91.6 pmol/L. f To convert mg/dL glucose to mol/L, multiply mg/dL by 0.0555. To convert mol/L glucose to mg/dL, multiply mol/L by 18.02. Glucose of 93.3 mg/dL5.18 mol/L. g To convert nmol/L C-peptide to ng/mL, multiply nmol/L by 3.0. To convert ng/mL C-peptide to nmol/L, multiply ng/mL by 0.333. C-peptide of 0.70 nmol/L2.1 ng/mL. h To convert mg/L C-reactive protein to nmol/L, multiply mg/L by 9.524. To convert nmol/L C-reactive protein to mg/L, multiply nmol/L by 0.105. C-reactive protein of 0.15 mg/L1.43 nmol/L. i To convert mg/dL cholesterol to mmol/L, multiply mg/dL by 0.026. To convert mmol/L cholesterol to mg/dL, multiply mmol/L by 38.6. Cholesterol of 160 mg/dL4.16 mmol/L. j To convert mg/dL triglyceride to mmol/L, multiply mg/dL by 0.0113. To convert mmol/L triglyceride to mg/dL, multiply mmol/L by 88.6. Triglyceride of 96 mg/dL1.08 mmol/L. k To convert mol/L homocysteine to mg/L, multiply mol/L by 0.135. To convert mg/L homocysteine to mol/L, multiply mg/L by 7.397. Homocysteine of 6.7 mol/L0.9 mg/L. l To convert ng/mL folate to nmol/L, multiply ng/mL by 2.266. To convert nmol/L folate to ng/mL, multiply nmol/L by 0.441. Folate of 12.5 ng/L28.3 nmol/L. m Means were adjusted for age, race/ethnicity, family income, body mass index, energy intake, smoking, physical activity, and intake of food groups (meat and beans, milk, fruit, vegetable, and sugar sweetened beverages). yz Means not sharing the same superscript letter (y, z) within sex group are signicantly different (P0.05). NOTE: Information from this table is available online at www.andjrnl.org as part of a PowerPoint presentation.

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obesity among various population groups. For example, SSB intake was positively associated with increased energy intake and body weight in a meta-analysis of 88 longitudinal, experimental, and cross-sectional studies, including those involving children and adolescents (49). A review of cross-sectional studies also showed that intake of dairy products was inversely associated with weight status in adolescents (50). An inconsistent relationship was observed in our study between whole-grain intake and risk factors for type 2 diabetes, including fasting insulin and C-peptide levels in boys, whereas an inverse association was noted in girls. Sex differences regarding these risk factors will be discussed in the following paragraphs. Results among girls were consistent with previous cross-sectional studies indicating a favorable association between whole-grain intake and risk factors for type 2 diabetes and CVD in adults and adolescents, such as fasting insulin or insulin sensitivity (12,15,20). Adolescents with higher wholegrain intake in our study had higher intakes of dietary ber, which was expected because some whole-grain foods are a good source of ber. Fiber intake has been favorably linked to risk factors for type 2 diabetes and CVD (51,52). In longitudinal studies, the association between whole-grain intake and fasting insulin was attenuated after adjusting for dietary ber and magnesium (15), and the reduction in risk of type 2 diabetes was attributed to both whole-grain and cereal ber intake (8). Folate has the potential to reduce risk of coronary artery disease by lowering total homocysteine levels (53). Boys and girls in our study with higher intake of whole grains also had higher serum and red blood cell folate levels, and boys had lower homocysteine levels. Similarly, a previous study in adolescents also showed that higher intake of whole grains and rened grain was associated with lower homocysteine levels (16). A recent review regarding gender differences and obesity in children aged 0 to 18 years indicated that differences in body composition, weight-gain patterns, and involvement of hormones in growth and development are evident between girls and boys before and during puberty (54). These differences may account for the variation in how whole grains are associated with disease risk indicators according to sex. For example, sex hormones are thought to play a role in modulation of metabolic syndrome and risk factors for CVD in adolescents (55). However, in our study, it was not possible to control for Tanner stage of development because these data were not collected for adolescents in NHANES (1999-2004). Another potential explanation for inconsistent results between boys and girls and the lack of associations between some outcome variables and whole-grain intake may be that whole-grain intake was very low overall, which limited the range of intakes. Even in the high category, adolescents may not have been eating enough whole grain to observe signicant associations. In another study where a signicant association existed between wholegrain intake and BMI in adolescents (3), intake was divided into quartiles where some adolescents (n214) consumed three or more servings per day. However, in our study where whole-grain consumption was categorized as none, low, and high, the number of adolescents in each group was more evenly distributed.

A strength of our study is the use of nationally representative data based on a large number of subjects selected through a complex, multistage probability sampling design. Furthermore, use of the already established and tested food groupings in MPED 1.0 and 2.0 reduces potential bias. Limitations involve the use of self-reported, 24-hour, dietary recall procedures for 1 day to estimate dietary intake for 1999-2002 and the use of 2-day recalls for 2003-2004. Previous cross-sectional studies of associations between whole-grain intake and chronic disease risk factors used 1-year, semiquantitative food frequency questionnaires to assess usual whole-grain intake (12,1518,20). Recalls based on 24 hours may not reect habitual intake over time in the same manner as food frequency questionnaires. In addition, an assumption was made that intake based on 24-hour recalls collected at one point in time can be related to chronic disease risk factors and other laboratory measures, which may actually reect intake based on a period of several days to months. Several studies have also shown that about one third of adolescents were considered under- or over-reporters of energy intake, and the proportion of under-reporters increased among those adolescents with higher weight status (47,56). Methodologic issues regarding self-reported dietary intake need to be considered when interpreting results of studies determining an association between dietary intake and weight status. Furthermore, NHANES data are cross-sectional, which does not allow an examination of causal relationships. Thus, further longitudinal and clinical studies are needed to verify ndings regarding associations among whole-grain intake, weight status, and disease risk indicators in adolescents. Another limitation was the loss of the boys that were younger and had lower BMI measures and the girls that viewed more television/ video and had lower energy intakes after applying the exclusion criteria to the sample. Given that the results for BMI were not signicant after extensive adjustment, the loss of the boys with lower BMI and the girls with more television/video viewing likely would not have changed the results. Age was accounted for throughout the analysis, which likely remediated the loss of the younger boys. Because the excluded girls had lower energy intakes, but no differences in whole-grain intakes, the results of whole-grain intakes being associated with lower energy intakes were likely attenuated. CONCLUSIONS Although studies have examined the association among whole-grain intakes, weight status, and chronic disease risk factors in adults, this is one of only a few studies conducted for the same purpose in adolescents. Whereas whole-grain intake by adolescents was well below recommendations, consumption was favorably associated with intake of carbohydrate, dietary ber, and total folate. Results suggested that whole-grain intake may also be favorably associated with risk factors for type 2 diabetes and CVD, although results varied by sex. With higher whole-grain intake, fasting insulin levels were lower and serum and red blood cell folate levels were higher for boys and girls; however, C-peptide levels were lower for girls, and homocysteine concentrations were lower for boys. These ndings provide further support for current recom-

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mendations to promote greater intake of whole grains among adolescents. STATEMENT OF POTENTIAL CONFLICT OF INTEREST: No potential conict of interest was reported by the authors. FUNDING/SUPPORT: This project was funded through the Minnesota Agricultural Experiment Station. ACKNOWLEDGEMENTS: The authors thank Sarah Cusick, Department of Pediatrics, University of Minnesota, for editorial comments and Nort Holschuh, Bell Institute of Health and Nutrition, General Mills, Inc, Minneapolis, MN, for advice on using data analysis software. References
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40. National Health and Nutrition Examination Survey laboratory methodology and public data les. Centers for Disease Control and Prevention Web site. http://www.cdc.gov/nchs/data/nhanes/nhanes_01_02/lab_b_ generaldoc.pdf. Accessed April 7, 2010. 41. National Health and Nutrition Examination Survey laboratory methodology and public data les. Centers for Disease Control and Prevention Web site. http://www.cdc.gov/nchs/data/nhanes/nhanes_03_04/lab_c_ generaldoc.pdf. Accessed April 7, 2010. 42. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499-502. 43. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey 2003-2004 physical activity and smoking and tobacco use questionnaire les. Centers for Disease Control andPreventionWebsite.http://www.cdc.gov/nchs/nhanes/nhanes20032004/quex03_04.htm. Accessed August 25, 2011. 44. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey 2001-2002 physical activity and smoking and tobacco use questionnaire les. Centers for Disease Control and Prevention Web sitehttp://www.cdc.gov/nchs/nhanes/nhanes 2001-2002/quest01_02.htm. Accessed August 25, 2011 45. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey 1999-2000 physical activity and smoking and tobacco use questionnaire les. Centers for Disease Control and Prevention Web site. http://www.cdc.gov/nchs/nhanes/nhanes1999-2000/ quest99_00.htm. Accessed August 25, 2011. 46. Kosti RI, Panagiotakos DB, Mihas CC, et al. Dietary habits, physical activity and prevalence of overweight/obesity among adolescents in Greece: The Vyronas study. Med Sci Monit. 2007;13(10):CR437CR444. 47. Vgstrand K, Barkeling B, Forslund HB, et al. Eating habits in

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