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Eating Habits and Total and Abdominal Fat in Spanish Adolescents: Influence of Physical Activity. The AVENA Study

  • Sonia Gómez-Martínez
    Correspondence
    Address correspondence to: Sonia Gómez-Martínez, Ph.D., Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science, Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Calle José Antonio Novais, 10, 28040 Madrid, Spain
    Affiliations
    Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science and Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain
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  • David Martínez-Gómez
    Affiliations
    Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science and Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain

    Department of Physical Education, Sport and Human Movement, Faculty of Education and Teaching Training, Autonomous University of Madrid, Madrid, Spain
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  • Fatima Perez de Heredia
    Affiliations
    Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science and Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain

    Department of Medical Physiology, University of Murcia, Murcia, Spain
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  • Javier Romeo
    Affiliations
    Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science and Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain
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  • Magdalena Cuenca-Garcia
    Affiliations
    Department of Physical Education, University of Granada, Granada, Spain
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  • Miguel Martín-Matillas
    Affiliations
    Department of Physical Education and Sport, Faculty of Physical Activity and Sport Sciences, University of Granada, Granada, Spain
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  • Manuel Castillo
    Affiliations
    Department of Physical Education, University of Granada, Granada, Spain
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  • Juan-Pablo Rey-López
    Affiliations
    Department of Pediatrics, School of Health Sciences, University of Zaragoza, Zaragoza, Spain

    GENUD, “Growth, Exercise, Nutrition and Development” Research Group, Universidad de Zaragoza, Zaragoza, Spain
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  • German Vicente-Rodriguez
    Affiliations
    GENUD, “Growth, Exercise, Nutrition and Development” Research Group, Universidad de Zaragoza, Zaragoza, Spain

    Faculty of Health and Sport Science (FCSD), Department of Physiotherapy and Nursing, Universidad de Zaragoza, Ronda Misericordia 5, Huesca, Spain
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  • Luis Moreno
    Affiliations
    Department of Pediatrics, School of Health Sciences, University of Zaragoza, Zaragoza, Spain

    GENUD, “Growth, Exercise, Nutrition and Development” Research Group, Universidad de Zaragoza, Zaragoza, Spain
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  • Ascensión Marcos
    Affiliations
    Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science and Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain
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      Abstract

      Objective

      To evaluate the association between specific dietary habits and body fatness in Spanish adolescents, and to analyze the role of leisure-time physical activity (LTPA) in this association.

      Methods

      In this cross-sectional study, 1,978 adolescents (1,017 girls) aged 13.0–18.5 years from the AVENA (Alimentación y Valoración del Estado Nutricional en Adolescentes) study were included. Particular dietary habits (breakfast, mid-morning snack, lunch, afternoon snack, dinner, and nighttime snack, as well as time spent eating, number of meals, consumption of soft drinks, and ready-to-eat foods) and LTPA were self-reported and analyzed as dichotomic variables (yes/no). The sum of six skinfold thicknesses and waist circumference (WC) values were the main body fatness variables.

      Result

      Skinfolds and WC values were lower in adolescents who reported consumption of mid-morning snack, afternoon snack, more than four meals per day, and an adequate speed of eating, independently of participation in LTPA. Moreover, a beneficial influence of breakfast consumption on skinfolds and WC values was observed in those adolescent boys who did not participate in LTPA (p for interactions = .044 and .040, respectively).

      Conclusions

      In Spanish adolescents, certain healthy dietary habits (i.e., mid-morning snack, afternoon snack, > 4 meals per day, adequate eating speed) are associated with lower body fatness, independently of engaging in LTPA. In addition, among boys with non-LTPA, those who skipped breakfast showed the highest body fatness values, indicating a beneficial influence of daily breakfast on body fat in this particular group.

      Keywords

      Obesity is a chronic disease associated with early development of cardiovascular diseases, diabetes, and cancer, which are among the most prevalent derived pathologies. The etiology of obesity has a multifactor origin, in which apart from genetic factors, lifestyle habits seem to play an important role in both its triggering and its development [
      • Lobstein T.
      • Baur L.
      • Uauy R.
      IASO International Obesity TaskForce
      Obesity in children and young people: A crisis in public health.
      ,
      • Moreno L.A.
      • Rodríguez G.
      Dietary risk factors for development of childhood obesity.
      ]. Special attention needs to be given to childhood obesity because many studies have pointed out that obese children are more likely to become obese adults [
      • Lobstein T.
      • Baur L.
      • Uauy R.
      IASO International Obesity TaskForce
      Obesity in children and young people: A crisis in public health.
      ]. It is noteworthy that obesity risk factors in children are particularly related to dietary factors [
      • Lobstein T.
      • Baur L.
      • Uauy R.
      IASO International Obesity TaskForce
      Obesity in children and young people: A crisis in public health.
      ,
      • Moreno L.A.
      • Rodríguez G.
      Dietary risk factors for development of childhood obesity.
      ]. The main reason for this alarming trend is the shift in nutritional and lifestyle habits caused by the increased popularity of fast foods, soft drinks, and diminished physical activity (PA). Presently, all these common upward trends are adopted by children and adolescents [
      • Lobstein T.
      • Baur L.
      • Uauy R.
      IASO International Obesity TaskForce
      Obesity in children and young people: A crisis in public health.
      ,
      • Moreno L.A.
      • Rodríguez G.
      Dietary risk factors for development of childhood obesity.
      ]. Thus, nowadays, the scientific community has begun to devote growing attention to examine the factors that influence eating behaviors and dietary quality, particularly in the most susceptible populations, such as adolescents [
      • Patrick H.
      • Nicklas T.A.
      A review of family and social determinants of children's eating patterns and diet quality.
      ].
      It is important to highlight that childhood and adolescence are decisive periods in human life within which body composition and psychosociologic changes determine nutritional requirements, as well as eating and PA behavior variability [
      • Rodríguez G.
      • Moreno L.A.
      • Blay M.G.
      • et al.
      Body composition in adolescents: Measurements and metabolic aspects.
      ]. The characteristic behavior patterns that show up during adolescence may produce energy unbalance and nutritional status disturbances. Prospective controlled trials to assess the protective potential of promoting regular and frequent meals in children and their families are highly desirable to strengthen the evidence base for such preventive approaches, which should explore the feasibility and effects of interventions [
      • Oude Luttikhuis H.
      • Baur L.
      • Jansen H.
      • et al.
      Interventions for treating obesity in children.
      ]. Data from cross-sectional studies have identified several dietary patterns associated with early obesity development, such as meal frequency and distribution, skipping meals, soft drink and fast food consumption, as well as high eating speed [
      • Moreno L.A.
      • Rodriguez G.
      • Fleta J.
      • et al.
      Trends of dietary habits in adolescents.
      ].
      On the other hand, regular PA seems to offer protection against a wide variety of these chronic disease-related risk factors during childhood and adolescence [
      • Must A.
      • Tybor D.J.
      Physical activity and sedentary behavior: A review of longitudinal studies of weight and adiposity in youth.
      ,
      • Christodoulos A.D.
      • Flouris A.D.
      • Tokmakidis S.P.
      Obesity and physical fitness of pre-adolescent children during the academic year and the summer period: Effects of organized physical activity.
      ,
      • Christodoulos A.D.
      • Douda H.T.
      • Polykratis M.
      • Tokmakidis S.P.
      Attitudes towards exercise and physical activity behaviours in Greek schoolchildren after a year long health education intervention.
      ]. Moreover, the combination of adequate PA together with healthy dietary habits has also been shown to help prevent obesity and other nutrition-related alterations common in adolescence, such as poor bone mineralization [
      • Moreno L.A.
      • Rodriguez G.
      • Fleta J.
      • et al.
      Trends of dietary habits in adolescents.
      ,
      • Vicente-Rodríguez G.
      • Ezquerra J.
      • Mesana M.I.
      • et al.
      Independent and combined effect of nutrition and exercise on bone mass development.
      ].
      Studies have shown that both dietary habits and PA independently affect the development of obesity. The current tendency is to perform cluster analyses, for example, to evaluate the combined effect of health-related factors related to a common trait; for instance, certain lifestyle habits that may increase the individual obesity risk. In this context, the specific contribution of each dietary and PA factors should be determined, but then it is necessary to know the interactions between them. However, to our knowledge, this information is lacking, and no data are available in this respect for adolescents in Spain. Therefore, the present study is aimed to evaluate the association between specific dietary habits and body fatness in Spanish adolescents, analyzing the role of leisure-time PA (LTPA) in this association.

      Methods

      Design and participants

      The AVENA study (Alimentación y Valoración del Estado Nutricional de los Adolescentes/Feeding and assessment of nutritional status of Spanish adolescents) is a cross-sectional and multicenter study performed on a representative sample of urban Spanish adolescents aged between 13.0 and 18.5 years. The complete and detailed methodology of the AVENA study has been published in other studies [
      • González-Gross M.
      • Castillo M.J.
      • Moreno L.
      • et al.
      Alimentación y Valoración del Estado Nutricional de los Adolescentes Españoles (Proyecto AVENA) Evaluación de riesgos y propuesta de intervención. I. Descripción metodológica del estudio.
      ,
      • Moreno L.A.
      • Mesana M.I.
      • Fleta J.
      • et al.
      Overweight, obesity and body fat composition in Spanish adolescents The AVENA Study.
      ]. Briefly, 2,859 adolescents were assessed in five Spanish cities (Granada, Madrid, Murcia, Santander, and Zaragoza) between 2000 and 2002. The AVENA study was designed to evaluate dietary patterns, anthropometry, lifestyle habits, health markers, biomarkers, and genetic markers in adolescents. Participants lacking the complete and valid PA and anthropometric measurements were excluded, and thus, the final sample for the present study was 961 boys and 1,017 girls (n = 1,978). The protocol for the study was approved by the Review Committee for Research Involving Human Subjects from Marqués de Valdecilla University Hospital (Santander, Spain).

      Anthropometric assessment

      Harmonization and standardization of anthropometric measurements within the AVENA study have been detailed elsewhere [
      • Moreno L.A.
      • Joyanes M.
      • Mesana M.I.
      • et al.
      Harmonization of anthropometric measurements for a multicenter nutrition survey in Spanish adolescents.
      ]. Anthropometric measurements were taken on barefoot participants wearing only undergarments. Therefore, body weight (kg) was estimated without shoes and with light clothing, and measured to .05 kg by using a standard beam balance. Body height was measured using a stadiometer SECA 714 (range, 60–200 cm [Seca, Hamburg, Germany]). Skinfold thickness was measured on the left side of the body with a Holtain caliper at the following sites: (1) triceps, halfway between the acromion process and the olecranon process; (2) biceps, at the same level as the triceps skinfold, directly above the center of the cubital fossa; (3) subscapular, approximately 20 mm below the tip of the scapula, at an angle of 45 degrees to the lateral side of the body; (4) suprailiac, about 20 mm above the iliac crest and 20 mm toward the medial line; (5) thigh, in the midline of the anterior aspect of the thigh, midway between the inguinal crease and the proximal border of the patella; (6) calf, at the level of maximum calf circumference, on the medial aspect of the calf. Waist circumference (WC) was measured with an inelastic tape between the lowest rib and iliac crest, at the end of a gentle expiration. In the present study, the sum of six skinfolds (sum6) was used as a marker of total body fat, whereas WC was used as a marker of abdominal fat.

      Dietary habits

      Adolescents' eating behaviors were assessed by questionnaire. The participants were asked whether they usually consumed commercially ready-to-eat foods (yes or no), about their eating speed (medium or quick), and about the frequency and distribution of the following meals: breakfast, mid-morning snack, lunch, afternoon snack, dinner, and nighttime snack. Soft drink consumption was assessed using a 24-hour diet recall. The 24-hour recall was administered throughout the year to avoid seasonal variations; questionnaires were administered homogeneously from Monday to Friday. A nutrient database software (Grunumur, Murcia, Spain) [
      • Pérez-Llamas F.
      • Garaulet M.
      • Herrero F.
      • et al.
      Multivalent informatics application for studies of the nutritional status of the population Assessment of food intake.
      ] was used to define soft drinks as caloric soft drinks, colas, and isotonic drinks. Sugar-free soft drinks were not included in the analysis. Data were categorized as “yes” (when participants consumed any kind of soft drinks) or “no” (when consumption of these drink was null).

      Physical activity patterns

      Participation in LTPA was determined from the following question: “Do you undertake any physical sporting activity after school?” Adolescents had to select “yes” or “no.”

      Statistical analysis

      Data are presented as mean ± standard deviation unless otherwise stated. First, the distribution of continuous variables was assessed for normality before analyses. Differences between adolescent boys and girls were determined by the Student t test for continuous variables, and χ2 test was used for categorical data.
      Differences in body fatness levels between groups of LTPA (yes or no) were assessed by analysis of covariance adjusted by age. Additionally, a binary logistic regression analysis was performed to determine whether participation in LTPA was associated with dietary habits.
      Differences in body fatness levels according to some dietary habits were assessed by analysis of covariance using three different models: model 1 was adjusted by age, model 2 was adjusted by age and LTPA, and model 3 was focused on the interactions between dietary habits and LTPAs. Statistical analyses were performed using the SPSS statistical software release 17 for Windows XP (Chicago, IL). Statistical significance was set at p < .05 for all the analyses, with the exception of interactions that was set at p < .1.

      Results

      Descriptive characteristics

      Characteristics and dietary habits of the adolescent sample are shown in Table 1. The boys showed higher weight, height, and WC than girls, although their sum6 was lower than that found in girls. The percentage of boys reporting participation in LTPA was also higher than that reported by girls (81.5% vs. 51.5%; p < .001); 89% of all adolescents reported having breakfast, the proportion of boys being significantly higher than that of girls (91.1% vs. 87.1%; p = .011). Although no gender differences were observed for mid-morning snack consumption, afternoon and nighttime snack intakes were more widespread in boys than in girls (73.2% vs. 68.9%, p = .034; 30.4% vs. 21.4%, p = .009, respectively). Boys also reported a lower percentage of eating speed adequacy than girls (58.4% vs. 65.6%; p = .002). The proportion of boys and girls who consumed both soft drinks and commercially ready-to-eat foods was similar (Table 1).
      Table 1Description of the adolescent population from the AVENA study, Spain
      NAllnBoysnGirlsp for sex
      Age (year)1,97815.3 ± 1.396115.2 ± 1.31,01715.4 ± 1.3.008
      Weight (kg)1,97859.8 ± 11.896163.7 ± 12.61,01756.2 ± 9.6<.001
      Height (cm)1,978166.2 ± 8.7961171.0 ± 8.51,017161.8 ± 6.2<.001
      Body mass index (kg/m2)1,97821.6 ± 3.496121.7 ± 3.61,01721.4 ± 3.3.095
      Sum of 6 skinfolds (mm)1,97887.1 ± 35.696174.8 ± 36.31,01798.7 ± 30.1<.001
      Waist circumference (cm)1,97873.9 ± 9.096176.6 ± 9.21,01771.0 ± 8.0<.001
      Participation in LTPA (%)1,97866.196181.51,01751.5<.001
      Dietary habits (%)
       Breakfast (yes)1,64989.076391.188687.1.011
       Mid-morning snack (yes)1,55867.671366.584568.5.391
       Lunch (yes)1,66698.377398.289398.4.700
       Afternoon snack (yes)1,56771.272873.283968.9.034
       Dinner (yes)1,59782.874083.469482.4.598
       Nighttime snack (yes)1,38427.165130.473324.1.009
       Eating speed (adequate)1,68362.377658.490765.6.002
       More than four meals/day (yes)1,31678.061180.470575.9.051
       Soft drinks consumption (yes)1,19229.953930.665329.4.650
       Ready-to-eat foods consumption1,68883.577884.391082.7.386
      Data are presented as mean ± SD or percentage. p denotes statistical significance between genders.
      LTPA = leisure-time physical activity.

      Association of LTPA with body fatness and dietary habits

      LTPA significantly affected body fatness markers in boys, with lower values of skinfolds in those who practiced LPTA (73.4 ± 35.5 vs. 81.0 ± 39.5; p = .005), and a similar trend was observed for WC (76.3 ± 9.0 vs. 77.9 ± 10.2; p = .089). This effect was not observed in girls. Dietary habits did not influence significantly the practice of LTPA (data not shown), except for the consumption of ready-to-eat foods in girls, which was related to less LTPA participation (odds ratio = .68; 95% confidence interval: .476–.962).

      Association of dietary habits with body fatness, independently of LTPA

      Table 2 shows the association between dietary habits and markers of total and abdominal body fatness. Overall, the levels of sum6 and WC were lower in those adolescents reporting consumption of mid-morning snacks, afternoon snacks, and more than four meals per day than in those who did not show these habits. In addition, those adolescents who reported quick eating showed higher levels of both total and abdominal body fatness markers than those who reported adequate eating speed. The results did not substantially change when LTPA was included as a covariate (model 2) (Table 2).
      Table 2Differences in total and central body fat according to dietary habits in Spanish adolescents
      Sum of 6 skinfolds (mm)Waist circumference (cm)
      nBoysnGirlsnBoysnGirls
      Breakfast76375.0 ± 36.288698.8 ± 30.776376.5 ± 9.088671.2 ± 8.0
       No6876.8 ± 37.1114101.8 ± 31.76877.0 ± 9.711472.0 ± 9.5
       Yes69574.8 ± 36.177298.4 ± 30.669576.4 ± 977271.1 ± 7.8
      pmodel 1.594.280.729.279
      pmodel 2.621.306.742.288
      Mid-morning snack71374.5 ± 36.284598.5 ± 30.771376.4 ± 8.984571.2 ± 8.0
       No23983.2 ± 40.8266101.6 ± 29.223977.7 ± 9.826671.8 ± 8.2
       Yes47470.1 ± 32.857997.1 ± 31.347475.7 ± 8.957971.0 ± 7.9
      pmodel 1<.001.047.001.192
      pmodel 2<.001.040<.001.181
      Lunch77375.2 ± 36.489398.7 ± 30.677376.5 ± 9.189371.2 ± 8.0
       No1487.2 ± 38.11496.7 ± 35.01481.2 ± 8.91473.1 ± 10.2
       Yes75975.0 ± 36.487998.8 ± 30.575976.4 ± 9.187971.2 ± 7.9
      pmodel 1.180.825.062.367
      pmodel 2.190.795.065.374
      Afternoon snack72874.5 ± 36.283998.4 ± 30.472876.3 ± 9.083971.2 ± 8.0
       No19188.3 ± 41.4261104.0 ± 33.019180.7 ± 10.226172.4 ± 8.3
       Yes53769.6 ± 32.857895.9 ± 28.853774.8 ± 8.057870.7 ± 7.7
      pmodel 1<.001<.001<.001.005
      pmodel 2<.001<.001<.001.005
      Dinner74075.1 ± 36.485798.5 ± 30.574076.5 ± 9.185771.1 ± 7.9
       No12377.3 ± 36.4151101.0 ± 32.512377.0 ± 9.515170.8 ± 7.5
       Yes61774.7 ± 36.470698.0 ± 30.061776.4 ± 9.170671.2 ± 8.0
      pmodel 1.521.271.379.559
      pmodel 2.514.284.376.551
      Nighttime snack65174.1 ± 36.073397.4 ± 29.865176.2 ± 8.973370.9 ± 7.7
       No45375.3 ± 37.055698.2 ± 30.045376.4 ± 9.355671.2 ± 7.8
       Yes19871.3 ± 33.417794.9 ± 29.219876.0 ± 8.017769.9 ± 7.0
      pmodel 1.257.205.444.062
      pmodel 2.332.202.497.062
      Speed of eating77675.2 ± 36.490798.5 ± 30.477676.5 ± 9.190771.2 ± 7.9
       Adequate45373.0 ± 35.859596.3 ± 29.445375.5 ± 8.959570.6 ± 7.7
       Quick32378.2 ± 37.0312102.6 ± 31.932377.9 ± 9.231272.3 ± 8.3
      pmodel 1.037.003<.001.002
      pmodel 2.027.003<.001.002
      More than 4 meals/day61174.2 ± 36.270597.5 ± 29.961176.2 ± 9.070570.9 ± 7.7
       No12091.7 ± 42.1170106.8 ± 32.012081.6 ± 10.817072.8 ± 9.3
       Yes49170.0 ± 33.453594.5 ± 28.649174.9 ± 8.053570.3 ± 7.0
      pmodel 1<.001<.001<.001<.001
      pmodel 2<.001<.001<.001<.001
      Soft drinks53975.6 ± 37.665399.8 ± 30.253976.7 ± 9.265371.6 ± 8.1
       No37474.1 ± 36.746199.3 ± 30.137476.2 ± 8.746171.8 ± 8.3
       Yes16579.1 ± 39.5192101.1 ± 30.416577.7 ± 10.319271.0 ± 7.5
      pmodel 1.168.488.056.259
      pmodel 2.174.479.057.272
      Ready-to-eat foods77875.2 ± 36.391098.5 ± 30.477876.5 ± 9.191071.2 ± 7.9
       No12271.5 ± 32.7157101.1 ± 29.612275.4 ± 8.915771.9 ± 7.9
       Yes65675.9 ± 37.075397.9 ± 30.565676.7 ± 9.175371.0 ± 7.9
      pmodel 1.208.210.133.184
      pmodel 2.204.169.132.165
      Data are presented as mean ± SD. Model 1: adjusted for age. p denotes statistical significance between groups.
      Model 2: adjusted for age + LTPA.
      To assess possible interactions between dietary habits and LTPA on body fatness, respective interaction terms were included in the analyses (e.g., breakfast × LTPA). According to model 3, participation in LTPA seems to be capable of modulating the relationship between dietary habits and body fatness. Specifically, when analyzing the interactions between participation in LTPA and dietary habits, skipping breakfast had a negative impact on sum6 and WC (p < .05) among those boys who reported non-LTPA. However, the practice of LTPA attenuated the negative influence of skipping breakfast on body fatness markers in adolescent boys (p for interaction = .044 for sum6 and .040 for WC) but not in girls (both p for interaction > .1) (Figure 1) .
      Figure thumbnail gr1
      Figure 1Differences in total and central body fat across breakfast consumption and leisure-time physical activity groups in Spanish adolescents. Values are mean ± SE. *p < .05 compared with the skipping breakfast/non–leisure-time physical activity group.

      Discussion

      The present findings suggest that the main dietary habits associated with higher levels of body fat in Spanish adolescents are (i) skipping mid-morning snack, (ii) skipping afternoon snack, (iii) eating less than four meals per day, and (iv) quick eating, independently of participation in LTPA (Table 2). By contrast, LTPA alone was related to lower sum of skinfolds in boys, but not in girls. Moreover, an interesting interaction was observed between dietary habits (specifically, eating breakfast) and participation in LTPA concerning body fatness. Those boys who participated in LTPAs showed similar sum of skinfolds and WC values, regardless of having breakfast or not; in contrast, among less-active boys, skipping breakfast was associated with significantly higher body fatness markers. In view of our results, we could suggest that having breakfast might counteract the potential negative influence of not practicing LTPA on body fatness in boys (Figure 1).
      According to the recent literature, data regarding dietary and other lifestyle habits, such as PA levels, are necessary to understand the current trends in the increasing early obesity prevalence [
      • Moreno L.A.
      • Rodriguez G.
      • Fleta J.
      • et al.
      Trends of dietary habits in adolescents.
      ,
      • Must A.
      • Tybor D.J.
      Physical activity and sedentary behavior: A review of longitudinal studies of weight and adiposity in youth.
      ,
      • Christodoulos A.D.
      • Flouris A.D.
      • Tokmakidis S.P.
      Obesity and physical fitness of pre-adolescent children during the academic year and the summer period: Effects of organized physical activity.
      ,
      • Christodoulos A.D.
      • Douda H.T.
      • Polykratis M.
      • Tokmakidis S.P.
      Attitudes towards exercise and physical activity behaviours in Greek schoolchildren after a year long health education intervention.
      ]. Our results show that 81.5% of boys and 51.5% of girls practice some type of LPTA, which is in agreement with previous studies [
      • Roman B.
      • Serra-Majem L.
      • Ribas-Barba L.
      • et al.
      How many children and adolescents in Spain comply with the recommendations on physical activity?.
      ].
      Regarding eating habits, there has been much debate about the best criteria to define meals and snacks [
      • Gatenby S.J.
      Eating frequency: Methodological and dietary aspects.
      ]. In our opinion, the best definitions are those based on the time of the day when people eat, which may corroborate other findings [
      • Ziegler P.J.
      • Jonnalagadda S.S.
      • Nelson J.A.
      • et al.
      Contribution of meals and snacks to nutrient intake of male and female elite figure skaters during peak competitive season.
      ,
      • Kerr M.A.
      • Rennie K.L.
      • McCaffrey T.A.
      • et al.
      Snacking patterns among adolescents: A comparison of type, frequency and portion size between Britain in 1997 and Northern Ireland in 2005.
      ], and that is the criterion adopted for the current study, classifying meals as breakfast, mid-morning snack, lunch, afternoon snack, dinner, and nighttime snack (before going to bed).
      In the present study, adolescent boys showed a significantly higher percentage of breakfast habit than adolescent girls (91.1% vs. 87.1%), in concordance with previous studies [
      • Morgan K.J.
      • Zabik M.E.
      • Stampley G.L.
      Breakfast consumption patterns of US children and adolescents.
      ,
      • Hoglund D.
      • Samuelson G.
      • Mark A.
      Food habits in Swedish adolescents in relation to socioeconomic conditions.
      ,
      • Sjoberg A.
      • Hallberg L.
      • Höglund D.
      • et al.
      Meal pattern, food choice, nutrient intake and lifestyle factors in the Göteborg Adolescence Study.
      ,
      • Moreno L.A.
      • De Henauw S.
      • González-Gross M.
      • et al.
      Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study.
      ,
      • Moreno L.A.
      • González-Gross M.
      • Kersting M.
      • et al.
      Assessing, understanding and modifying nutritional status, eating habits and physical activity in European adolescents: The HELENA (Healthy Lifestyle in Europe by Nutrition in Adolescence) Study.
      ]. Other authors [
      • Sjoberg A.
      • Hallberg L.
      • Höglund D.
      • et al.
      Meal pattern, food choice, nutrient intake and lifestyle factors in the Göteborg Adolescence Study.
      ] have also reported a higher percentage of boys having dinner than girls. However, these gender differences have not been found in the current study. By contrast, girls reported a more suitable eating speed than boys, also in accordance to previous studies carried out in school-going adolescents aged 12–13 years [
      • Sun Y.
      • Sekine M.
      • Kagamimori S.
      Lifestyle and overweight among Japanese adolescents: The Toyama Birth Cohort Study.
      ]. In addition, 80.4% of boys and 75.9% of girls reported to consume four or more meals per day, which is lower than the values observed in a similar population (89.7% boys and 84.4% girls) [
      • Moreno L.A.
      • González-Gross M.
      • Kersting M.
      • et al.
      Assessing, understanding and modifying nutritional status, eating habits and physical activity in European adolescents: The HELENA (Healthy Lifestyle in Europe by Nutrition in Adolescence) Study.
      ] (Table 1). To date, there is little information about meal frequency in adolescents, although it is commonly accepted that skipping main meals may promote overweight [
      • Mota J.
      • Fidalgo F.
      • Silva R.
      • et al.
      Relationships between physical activity, obesity and meal frequency in adolescents.
      ,
      • Koletzko B.
      • Toschke A.M.
      Meal patterns and frequencies: Do they affect body weight in children and adolescents?.
      ]. Our results support this hypothesis, as significant correlations have been found between mid-morning and afternoon snack intakes and lower skinfolds and WC values. A recent study has reported that nighttime snack is negatively associated with being overweight in adolescent boys and girls [
      • Sun Y.
      • Sekine M.
      • Kagamimori S.
      Lifestyle and overweight among Japanese adolescents: The Toyama Birth Cohort Study.
      ], although this association has not been observed in the current study. In general, our results showed that adolescents eating more than four meals per day had lower skinfolds and WC, which is in agreement with previous studies that found negative association between meal frequency and body fatness [
      • Sun Y.
      • Sekine M.
      • Kagamimori S.
      Lifestyle and overweight among Japanese adolescents: The Toyama Birth Cohort Study.
      ,
      • Moore G.F.
      • Tapper K.
      • Murphy S.
      • et al.
      Associations between deprivation, attitudes towards eating breakfast and breakfast eating behaviours in 9–11-year-olds.
      ,
      • Franko D.L.
      • Striegel-Moore R.H.
      • Thompson D.
      • et al.
      The relationship between meal frequency and body mass index in black and white adolescent girls: More is less.
      ]. Quick eating also appeared to be related to higher body fatness markers, which corroborates other findings [
      • Sun Y.
      • Sekine M.
      • Kagamimori S.
      Lifestyle and overweight among Japanese adolescents: The Toyama Birth Cohort Study.
      ] (Table 2).
      A relatively high percentage of adolescents reported soft drink consumption (29.9%) (Table 1), which is in agreement with the trend of increasing consumption of sugar-sweetened beverages observed during the last decade [
      • Bere E.
      • Glomnes E.S.
      • te Velde S.J.
      • Klepp K.I.
      Determinants of adolescents' soft drink consumption.
      ]. As this increase in sugar drink consumption has been parallel to the rise in obesity prevalence, there might be a relationship between both events [
      • Harrington S.
      The role of sugar-sweetened beverage consumption in adolescents obesity: A review of the literature.
      ]. However, studies focused on this issue have obtained inconsistent results [
      • Striegel-Moore R.H.
      • Thompson D.
      • Affenito S.G.
      • et al.
      Correlates of beverage intake in adolescents girls: The National Heart, Lung, and Blood Institute Growth and Health Study.
      ,
      • Johnson L.
      • Mander A.P.
      • Jones L.R.
      • Emmett P.M.
      • Jebb S.A.
      Is sugar-sweetened beverage consumption associated with increased fatness in children?.
      ]. In fact, our results do not sustain a relationship between soft drinks and body fatness markers. Similarly, the increasing consumption of ready-to-eat food has been proposed as another contributor to the development of obesity, and recent data support this hypothesis [
      • Lobato J.C.
      • Costa A.J.
      • Sichieri R.
      Food intake and prevalence of obesity in Brazil: An ecological analysis.
      ]. In our study, a high percentage of adolescents reported ready-to-eat food consumption (83.5%; Table 1), in agreement with the global shift toward increased availability of this kind of food [
      • Adair L.S.
      • Popkin B.M.
      Are child eating patterns being transformed globally?.
      ]. Nevertheless, and similarly to what we observed for soft drinks, no relationship was found between the intake of ready-to-eat foods and body fatness in the adolescents evaluated.
      Together with dietary habits, the practice of PA is another key environmental factor influencing body fatness during adolescence [
      • Moreno L.A.
      • Rodriguez G.
      • Fleta J.
      • et al.
      Trends of dietary habits in adolescents.
      ,
      • Chermont Prochnik Estima C.
      • da Costa R.S.
      • Sichieri R.S.
      • et al.
      Meal consumption patterns and anthropometric measurements in adolescents from a low socioeconomic neighbourhood in the metropolitan area of Rio de Janeiro, Brazil.
      ]. In this direction, we have observed that total body fatness (skinfolds) was lower in boys (but not in girls) who reported participation in LTPA. Furthermore, certain dietary and PA patterns seem to be linked [
      • Keski-Rahkonen A.
      • Kaprio J.
      • Rissanen A.
      • et al.
      Breakfast skipping and health-compromising behaviors in adolescents and adults.
      ]. In the current study, dietary habits had little influence on the practice of LTPA; only in girls, a tendency toward less LTPA frequency was associated to the consumption of ready-to-eat foods (Table 2). Similarly, Corder et al [
      • Corder K.
      • van Sluijs E.M.
      • Steele R.M.
      • et al.
      Breakfast consumption and physical activity in British adolescents.
      ] could not find a direct correlation between breakfast frequency and PA in girls, but reported that both factors could probably build a cluster of healthy behaviors that are interacting. Nonetheless, it is worth noting that significant interactions between LTPA and dietary habits—in particular, skipping breakfast—were found in relation to body fatness markers. In the overall population tested, we did not find a significant effect of breakfast consumption on body fat markers. This outcome is in disagreement with other authors, who have associated breakfast consumption with lower body mass index [
      • Keski-Rahkonen A.
      • Kaprio J.
      • Rissanen A.
      • et al.
      Breakfast skipping and health-compromising behaviors in adolescents and adults.
      ]. However, in the current study when boys were classified according to the practice of LTPA, skipping breakfast was related to greater total (sum6) and abdominal (WC) body fat, but only in those individuals who reported no LTPA. Therefore, we suggest that the variation of body fatness values associated with having breakfast was minimized when boys practiced LTPA (Figure 1).
      Sandercock et al have recently proposed that heterogeneous findings regarding breakfast skippers indicate that the mechanisms by which eating breakfast is associated with lower body mass index are unlikely to be purely of a dietary nature [
      • Sandercock G.R.
      • Voss C.
      • Dye L.
      Associations between habitual school-day breakfast consumption, body mass index, physical activity and cardiorespiratory fitness in English schoolchildren.
      ]. Our data support this hypothesis, and present LTPA as an influencing factor in that relationship. The reason this interaction was not found in girls is still not clear. However, we would be tempted to speculate that it is not so much due to the frequency or habit of practicing PA, but due to the type of PA instead. For example, although in this study we could not analyze the type of PA, a recent study has reported that adolescent boys usually prefer more vigorous activities than girls [
      • De Cocker K.
      • Ottevaere C.
      • Sjöström M.
      • et al.
      Self-reported physical activity in European adolescents: Results from the Helena (Healthy Lifestyle in Europe by Nutrition in Adolescence) study.
      ,
      • Martinez-Gomez D.
      • Ruiz J.R.
      • Ortega F.B.
      • et al.
      Recommended levels of physical activity to avoid an excess of body fat in European adolescents: the HELENA Study.
      ]. This fact is important because vigorous PA seems to be associated with lower levels of body fat in adolescents [
      • Martinez-Gomez D.
      • Ruiz J.R.
      • Ortega F.B.
      • et al.
      Recommended levels of physical activity to avoid an excess of body fat in European adolescents: the HELENA Study.
      ].
      The current study has certain limitations. First, interpretation of our results is limited to association; due to its cross-sectional design, causal directionality cannot be inferred. Second, all the measures of nutrition and PA shown in this article are self-reported with the consequent subjectivity this may entail.

      Conclusion

      In view of these results, the consumption of mid-morning snack, afternoon snack, and eating more than four meals per day, and having an adequate eating speed are important dietary habits associated with lower body fatness in Spanish adolescents. Moreover, among boys with non-LTPA, those who skipped breakfast showed the highest body fatness markers, indicating that the beneficial influence of daily breakfast on body fat might be enhanced in adolescent boys with lower levels of LTPA. According to this outcome, we emphasize the need to take into account the interactions between different dietary habits and PA patterns, when the nutritional status is evaluated, and to elucidate and prevent the development of obesity in childhood and adolescence.

      Acknowledgments

      The authors express their sincere gratitude to the adolescents who participated in this study. The AVENA Study was supported by the Spanish Ministry of Health ( FIS 00/0015 ); and grants from Panrico S.A. , Madaus S.A. , and Procter & Gamble S.A. D.M.G. was supported by a grant from the Spanish Ministry of Education and Science ( AP2006-02464 ). J.P.R.L., G.V.R., M.G.F., and L.A.M. were also supported by a grant from the Spanish Ministry of Health: Maternal, Child Health and Development Network ( RD08/0072 ).
      Authors' contributions: Statistical analysis: S.G.M. and D.M.G.; Draft the manuscript: S.G.M. and D.M.G.; Funding and overall concept and design: A.M. and L.A.M. Interpretation and acquisition of data: S.G.M., D.M.G., F.P.H., J.R., M.C., M.M.M., M.J.C., J.P.L.R., G.V.R., L.A.M., and A.M. All authors read and approved the final manuscript.
      AVENA Study Group: Coordinator: A Marcos, Madrid. Local coordinators: M.J. Castillo, Granada; A. Marcos, Madrid; S. Zamora, Murcia; M. García Fuentes, Santander; M. Bueno, Zaragoza. Granada: M.J. Castillo, M.D. Cano, R Sola (Biochemistry); A. Gutiérrez, J.L. Mesa, J.R. Ruiz (Physical fitness); M. Delgado, P. Tercedor, P. Chillón (Physical activity), M. Martín-Matillas, F. Carreño, F.B. Ortega, G.V. Rodríguez, R. Castillo, F. Arellano (Collaborators). Universidad de Granada. E-18071 Granada. Madrid: A. Marcos, M. González-Gross, J. Wärnberg, S. Medina, F. Sánchez-Múniz, E. nova, A. Montero, B. de la Rosa, S. Gómez, S Samartín, J. Romeo, R. Álvarez (Coordination, immunology). A. Álvarez (Cytometric analysis). L. Barrios (Statistical analysis), A. Leyva, B, Payá (Psychological assessment). L. Martínez, E. Ramos, R. Ortiz, A. Urzanqui (Collaborators). Instituto de Nutrición y Bromatología. Consejo Superior de Investigaciones Científicas (CSIC). E-28040 Madrid. Murcia: S. Zamora, M. Garaulet, F. Pérez-Llamas, J.C. Baraza, J.F. Marine, F. Pérez de Heredia, M.A. Fernández, C. González, R. García, C. Torralba, E. Donat, E. Morales, M.D. García, J.A. Martínez, J.J. Hernández, A. Asensio, F.J. Plaza, M.J. López (Diet analysis). Dpto. Fisiología. Universidad de Murcia. E-30100 Murcia. Santander: M. García Fuentes, D. González-Lamuño, P. de Rufino, C. Redondo-Figuero, M.J. Noriega, R. Lanza-Saiz, T. Amigo (Genetic study). Dpto. Pediatría. Universidad de Cantabria. E −19,003 Santander. Zaragoza: M. Bueno, L.A. Moreno, A. Sarriá, J. Fleta, G. Rodríguez, C.M. Gil, M.I. Mesana, J.A. Casajús, Vicente Blay, María Guadalupe Blay (Anthropometric assessment). Escuela Universitaria de Ciencias de la Salud. Universidad de Zaragoza. E-50009 Zaragoza.

      References

        • Lobstein T.
        • Baur L.
        • Uauy R.
        • IASO International Obesity TaskForce
        Obesity in children and young people: A crisis in public health.
        Obes Rev. 2004; 5: 4-104
        • Moreno L.A.
        • Rodríguez G.
        Dietary risk factors for development of childhood obesity.
        Curr Opin Clin Nutr Metab Care. 2007; 10: 336-341
        • Patrick H.
        • Nicklas T.A.
        A review of family and social determinants of children's eating patterns and diet quality.
        J Am Coll Nutr. 2005; 24: 83-92
        • Rodríguez G.
        • Moreno L.A.
        • Blay M.G.
        • et al.
        Body composition in adolescents: Measurements and metabolic aspects.
        Int J Obes. 2004; 28: S54-S58
        • Oude Luttikhuis H.
        • Baur L.
        • Jansen H.
        • et al.
        Interventions for treating obesity in children.
        Cochrane Database Syst Rev. 2009; 1 (CD001872)
        • Moreno L.A.
        • Rodriguez G.
        • Fleta J.
        • et al.
        Trends of dietary habits in adolescents.
        Crit Rev Food Sci Nutr. 2010; 50: 106-112
        • Must A.
        • Tybor D.J.
        Physical activity and sedentary behavior: A review of longitudinal studies of weight and adiposity in youth.
        Int J Obes (Lond). 2005; 29: S84-S96
        • Christodoulos A.D.
        • Flouris A.D.
        • Tokmakidis S.P.
        Obesity and physical fitness of pre-adolescent children during the academic year and the summer period: Effects of organized physical activity.
        J Child Health Care. 2006; 10: 199-212
        • Christodoulos A.D.
        • Douda H.T.
        • Polykratis M.
        • Tokmakidis S.P.
        Attitudes towards exercise and physical activity behaviours in Greek schoolchildren after a year long health education intervention.
        Br J Sports Med. 2006; 40: 367-371
        • Vicente-Rodríguez G.
        • Ezquerra J.
        • Mesana M.I.
        • et al.
        Independent and combined effect of nutrition and exercise on bone mass development.
        J Bone Miner Metab. 2008; 26: 416-424
        • González-Gross M.
        • Castillo M.J.
        • Moreno L.
        • et al.
        Alimentación y Valoración del Estado Nutricional de los Adolescentes Españoles (Proyecto AVENA).
        Nutr Hosp. 2003; 18: 15-28
        • Moreno L.A.
        • Mesana M.I.
        • Fleta J.
        • et al.
        Overweight, obesity and body fat composition in Spanish adolescents.
        Ann Nutr Metab. 2005; 49: 71-76
        • Moreno L.A.
        • Joyanes M.
        • Mesana M.I.
        • et al.
        Harmonization of anthropometric measurements for a multicenter nutrition survey in Spanish adolescents.
        Nutrition. 2003; 19: 481-486
        • Pérez-Llamas F.
        • Garaulet M.
        • Herrero F.
        • et al.
        Multivalent informatics application for studies of the nutritional status of the population.
        Nutr Hosp. 2004; 19: 160-166
        • Roman B.
        • Serra-Majem L.
        • Ribas-Barba L.
        • et al.
        How many children and adolescents in Spain comply with the recommendations on physical activity?.
        J Sports Med Phys Fitness. 2008; 48: 380-387
        • Gatenby S.J.
        Eating frequency: Methodological and dietary aspects.
        Br J Nutr. 1997; 77: S7-S20
        • Ziegler P.J.
        • Jonnalagadda S.S.
        • Nelson J.A.
        • et al.
        Contribution of meals and snacks to nutrient intake of male and female elite figure skaters during peak competitive season.
        J Am Coll Nutr. 2002; 21: 114-119
        • Kerr M.A.
        • Rennie K.L.
        • McCaffrey T.A.
        • et al.
        Snacking patterns among adolescents: A comparison of type, frequency and portion size between Britain in 1997 and Northern Ireland in 2005.
        Br J Nutr. 2008; 5: 1-10
        • Morgan K.J.
        • Zabik M.E.
        • Stampley G.L.
        Breakfast consumption patterns of US children and adolescents.
        Nutr Res. 1986; 6: 635-646
        • Hoglund D.
        • Samuelson G.
        • Mark A.
        Food habits in Swedish adolescents in relation to socioeconomic conditions.
        Eur J Clin Nutr. 1998; 52: 784-789
        • Sjoberg A.
        • Hallberg L.
        • Höglund D.
        • et al.
        Meal pattern, food choice, nutrient intake and lifestyle factors in the Göteborg Adolescence Study.
        Eur J Clin Nutr. 2003; 57: 1569-1578
        • Moreno L.A.
        • De Henauw S.
        • González-Gross M.
        • et al.
        Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study.
        Int J Obes (Lond). 2008; 32: S4-S11
        • Moreno L.A.
        • González-Gross M.
        • Kersting M.
        • et al.
        Assessing, understanding and modifying nutritional status, eating habits and physical activity in European adolescents: The HELENA (Healthy Lifestyle in Europe by Nutrition in Adolescence) Study.
        Public Health Nutr. 2008; 11: 288-299
        • Sun Y.
        • Sekine M.
        • Kagamimori S.
        Lifestyle and overweight among Japanese adolescents: The Toyama Birth Cohort Study.
        J Epidemiol. 2009; 19: 303-310
        • Mota J.
        • Fidalgo F.
        • Silva R.
        • et al.
        Relationships between physical activity, obesity and meal frequency in adolescents.
        Ann Hum Biol. 2008; 35: 1-10
        • Koletzko B.
        • Toschke A.M.
        Meal patterns and frequencies: Do they affect body weight in children and adolescents?.
        Crit Rev Food Sci Nutr. 2010; 50: 100-105
        • Moore G.F.
        • Tapper K.
        • Murphy S.
        • et al.
        Associations between deprivation, attitudes towards eating breakfast and breakfast eating behaviours in 9–11-year-olds.
        Public Health Nutr. 2007; 10: 582-589
        • Franko D.L.
        • Striegel-Moore R.H.
        • Thompson D.
        • et al.
        The relationship between meal frequency and body mass index in black and white adolescent girls: More is less.
        Int J Obes (Lond). 2008; 32: 23-29
        • Bere E.
        • Glomnes E.S.
        • te Velde S.J.
        • Klepp K.I.
        Determinants of adolescents' soft drink consumption.
        Public Health Nutr. 2008; 11: 49-56
        • Harrington S.
        The role of sugar-sweetened beverage consumption in adolescents obesity: A review of the literature.
        J Sch Nurs. 2008; 24: 3-12
        • Striegel-Moore R.H.
        • Thompson D.
        • Affenito S.G.
        • et al.
        Correlates of beverage intake in adolescents girls: The National Heart, Lung, and Blood Institute Growth and Health Study.
        J Pediatr. 2006; 148: 183-187
        • Johnson L.
        • Mander A.P.
        • Jones L.R.
        • Emmett P.M.
        • Jebb S.A.
        Is sugar-sweetened beverage consumption associated with increased fatness in children?.
        Nutrition. 2007; 23: 557-563
        • Lobato J.C.
        • Costa A.J.
        • Sichieri R.
        Food intake and prevalence of obesity in Brazil: An ecological analysis.
        Public Health Nutr. 2009; 12: 2209-2215
        • Adair L.S.
        • Popkin B.M.
        Are child eating patterns being transformed globally?.
        Obes Res. 2005; 13: 1281-1299
        • Chermont Prochnik Estima C.
        • da Costa R.S.
        • Sichieri R.S.
        • et al.
        Meal consumption patterns and anthropometric measurements in adolescents from a low socioeconomic neighbourhood in the metropolitan area of Rio de Janeiro, Brazil.
        Appetite. 2009; 52: 735-739
        • Keski-Rahkonen A.
        • Kaprio J.
        • Rissanen A.
        • et al.
        Breakfast skipping and health-compromising behaviors in adolescents and adults.
        Eur J Clin Nutr. 2003; 57: 842-853
        • Corder K.
        • van Sluijs E.M.
        • Steele R.M.
        • et al.
        Breakfast consumption and physical activity in British adolescents.
        Br J Nutr. 2011; 105: 316-321
        • Sandercock G.R.
        • Voss C.
        • Dye L.
        Associations between habitual school-day breakfast consumption, body mass index, physical activity and cardiorespiratory fitness in English schoolchildren.
        Eur J Clin Nutr. 2010; 64: 1086-1092
        • De Cocker K.
        • Ottevaere C.
        • Sjöström M.
        • et al.
        Self-reported physical activity in European adolescents: Results from the Helena (Healthy Lifestyle in Europe by Nutrition in Adolescence) study.
        Public Health Nutr. 2010; 18: 1-9
        • Martinez-Gomez D.
        • Ruiz J.R.
        • Ortega F.B.
        • et al.
        Recommended levels of physical activity to avoid an excess of body fat in European adolescents: the HELENA Study.
        Am J Prev Med. 2010; 39: 203-211