Advertisement

Recommended Levels of Physical Activity to Avoid an Excess of Body Fat in European Adolescents

The HELENA Study

      Background

      It is unclear how much physical activity is necessary to prevent obesity during adolescence.

      Purpose

      The purpose of this study was to examine whether the current physical activity guidelines for youth are associated with a lower risk of excess of body fat in European adolescents.

      Methods

      A sample of 2094 adolescents from the HELENA cross-sectional study was selected. Levels of moderate, vigorous, and moderate to vigorous physical activity (MVPA) were assessed using accelerometers. BMI and percentage of body fat (skinfolds) were calculated and used to categorize the adolescents as normal-weight/normal-fat, overweight/overfat, and obese. Data were collected during 2006–2007. Receiver operating characteristic (ROC) analysis, performed in 2009, was used to determine thresholds that best discriminate between weight and body fat categories.

      Results

      ROC analysis showed that ≥18 minutes/day in vigorous physical activity and ≥55 minutes/day in MVPA significantly discriminated between normal-weight and overweight+obesity categories. Moreover, ≥9 minutes/day of vigorous physical activity and ≥49 minutes/day of MVPA discriminated between normal-fat and overfat/obese adolescents. Adolescents who did not meet the current physical activity guidelines for youth of 60 minutes/day in MVPA increased the risk of having overweight+obesity (OR=1.24, 95% CI=1.01, 1.534) and overfat+obesity (OR=1.79, 95% CI=1.33, 2.42). ORs increased when adolescents did not meet the guidelines of at least 15 minutes/day in vigorous physical activity.

      Conclusions

      Current physical activity guidelines seem to be appropriate to prevent excess of body fat in European adolescents. However, participation in vigorous physical activity might have additional importance in preventing obesity.

      Introduction

      Many years have passed since the first recommendation of physical activity for children and adolescents stated by the American College of Sports Medicine in 1988
      American College of Sports Medicine
      Opinion statement on physical fitness in children and youth.
      up to the more recent physical activity guidelines for youth from the USDHHS in December 2008.
      USDHHS
      2008 Physical activity guidelines for Americans Be active, healthy and happy!.
      During these years, findings from cross-sectional, longitudinal, and experimental studies have contributed to the development of different physical activity guidelines. Several experimental studies helped to examine the dose–response effect of physical activity on pediatric obesity.
      • Connelly J.B.
      • Duaso M.J.
      • Butler G.
      A systematic review of controlled trials of interventions to prevent childhood obesity and overweight: a realistic synthesis of the evidence.
      On the other hand, cross-sectional studies have also evaluated dose–response associations
      • Marshall S.J.
      • Biddle S.J.
      • Gorely T.
      • Cameron N.
      • Murdey I.
      Relationships between media use, body fatness and physical activity in children and youth: a meta-analysis.
      • Jiménez-Pavón D.
      • Kelly J.
      • Reilly J.J.
      Associations between objectively measured physical activity and adiposity in children and adolescents: systematic review.
      and adherence to physical activity recommendations.
      • Troiano R.P.
      • Berrigan D.
      • Dodd K.W.
      • Mâsse L.C.
      • Tilert T.
      • McDowell M.
      Physical activity in the U.S. measured by accelerometer.
      • Riddoch C.J.
      • Bo Andersen L.
      • Wedderkopp N.
      • et al.
      Physical activity levels and patterns of 9- and 15-yr-old European children.
      • Martínez-Gómez D.
      • Welk G.J.
      • Calle M.E.
      • Marcos A.
      • Veiga O.L.
      AFINOS Study Group
      Preliminary evidence of physical activity levels measured by accelerometer in Spanish adolescents The AFINOS Study.
      In spite of this, the question about how much physical activity is necessary to prevent obesity in young people remains to be elucidated.
      • Reichert F.F.
      • Baptista Menezes A.M.
      • Wells J.C.
      • Carvalho Dumith S.
      • Hallal P.C.
      Physical activity as a predictor of adolescent body fatness: a systematic review.
      Several physical activity recommendations suggest that youth should engage in at least 60 minutes/day in moderate to vigorous physical activity (MVPA).
      USDHHS
      2008 Physical activity guidelines for Americans Be active, healthy and happy!.
      • Strong W.B.
      • Malina R.M.
      • Blimkie C.J.
      • et al.
      Evidence based physical activity for school-age youth.
      • Janssen I.
      Physical activity guidelines for children and youth.
      • Kushi L.H.
      • Byers T.
      • Doyle C.
      • et al.
      American Cancer Society Guidelines on Nutrition and Physical Activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity.
      USDHHS
      Physical activity.
      • Biddle S.J.
      • Cavill N.A.
      • Sallis J.F.
      Policy framework for young people and health-enhancing physical activity.
      • Corbin C.B.
      • Pangrazi R.P.
      Physical activity for children: a statement of guidelines for children aged 5–12.
      Department of Health and Ageing
      National physical activity guidelines for Australians.
      Public Health Canada
      Family guide to physical activity for youth 10–14 years of age.
      However, Health Canada promoted a recommendation among Canadian children and adolescents that reached 90 minutes/day in MVPA.
      Public Health Canada
      Family guide to physical activity for youth 10–14 years of age.
      Another concern is that these physical activity recommendations do not distinguish between children and adolescents
      • Hallal P.C.
      • Victora C.G.
      • Azevedo M.R.
      • Wells J.C.
      Adolescent physical activity and health: a systematic review.
      despite the well-documented biological differences between the two life periods
      • Malina R.M.
      • Bouchard C.
      • Bar-Or O.
      Growth, maturation, and physical activity.
      as well as the decrease of physical activity from childhood to adolescence.
      • Nader P.R.
      • Bradley R.H.
      • Houts R.M.
      • McRitchie S.L.
      • O'Brien M.
      Moderate-to-vigorous physical activity from ages 9 to 15 years.
      • Malina R.M.
      Tracking of physical activity and physical fitness across the lifespan.
      Therefore, specific recommendations for children and adolescents are warranted. To date, only one old physical activity recommendation has been specifically developed for adolescents,
      • Sallis J.F.
      • Patrick K.
      Physical activity guidelines for adolescents: consensus statement.
      and it is stated that adolescents should participate in at least 20 minutes/day of MVPA.
      The aim of the present study was to examine whether the current physical activity guidelines are associated with a low risk of having excess of body fat in European adolescents participating in the Healthy Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study (HELENA-CSS).

      Methods

      Design and Participants

      The HELENA-CSS is a multicenter investigation carried out in 10 European cities: Athens (Greece); Dortmund (Germany); Ghent (Belgium); Heraklion (Greece); Lille (France); Pécs (Hungary); Rome (Italy); Stockholm (Sweden); Vienna (Austria); and Zaragoza (Spain). The main aim of the HELENA-CSS was to obtain reliable and comparable data on a broad battery of relevant nutrition- and health-related parameters.
      • Moreno L.A.
      • De Henauw S.
      • González-Gross M.
      • et al.
      HELENA Study Group
      Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence cross-sectional study.
      The sampling and recruitment processes were detailed in a previous report.
      • Moreno L.A.
      • De Henauw S.
      • González-Gross M.
      • et al.
      HELENA Study Group
      Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence cross-sectional study.
      In brief, a multiple-stage cluster random sample of adolescents, stratified for geographic location, age, and SES, was obtained, striving for representativeness on the level of these cities. Data collection from the HELENA-CSS took place in 2006−2007.
      A total of 3865 adolescents were recruited at schools and met the general HELENA-CCS inclusion criteria: aged 12.5–17.5 years, not participating simultaneously in another clinical trial, free of any acute infection 1 week before the inclusion, and having information on weight and height.
      • Moreno L.A.
      • De Henauw S.
      • González-Gross M.
      • et al.
      HELENA Study Group
      Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence cross-sectional study.
      Adolescents and their parents or guardians were informed of the nature and characteristics of the study, and all provided a written informed consent. Ethics committees from each country approved the HELENA-CSS protocols.
      • Béghin L.
      • Castera M.
      • Manios Y.
      • et al.
      HELENA Study Group
      Quality assurance of ethical issues and regulatory aspects relating to good clinical practices in the HELENA cross-sectional study.

      Body Fat Measurements

      Measurements were performed with the adolescent barefoot and in underwear. Body weight was measured to the nearest 0.1 kg with an electronic scale and height was measured with a telescopic stadiometer to the nearest 0.1 cm.
      • Nagy E.
      • Vicente-Rodriguez G.
      • Manios Y.
      • et al.
      HELENA Study Group
      Harmonization process and reliability assessment of anthropometric measurements in a multicenter study in adolescents.
      BMI was calculated as body weight divided by the square of height (kg/m2). Skinfold thickness was measured to the nearest 0.2 mm in triplicate in the left with a Holtain caliper.
      • Nagy E.
      • Vicente-Rodriguez G.
      • Manios Y.
      • et al.
      HELENA Study Group
      Harmonization process and reliability assessment of anthropometric measurements in a multicenter study in adolescents.
      Body fat percentage (%BF) was calculated from triceps and subscapular skinfolds using Slaughter's equations.
      • Slaughter M.H.
      • Lohman T.G.
      • Boileau R.A.
      • et al.
      Skinfold equations for estimation of body fatness in children and youth.
      • Rodríguez G.
      • Moreno L.A.
      • Blay M.G.
      • et al.
      AVENA-Zaragoza Study Group
      Body fat measurement in adolescents: comparison of skinfold thickness equations with dual-energy X-ray absorptiometry.
      Age- and gender-standardized BMI cutoff points were used to define overweight and obesity.
      • Cole T.J.
      • Bellizzi M.C.
      • Flegal K.M.
      • Dietz W.H.
      Establishing a standard definition for child overweight and obesity worldwide: international survey.
      In addition, age- and gender-specific 85th and 95th percentile of %BF in the study sample were used to define overfat and obese adolescents.

      Physical Activity Measurements

      Levels of physical activity were objectively measured using the ActiGraph GT1M accelerometer. This accelerometer is a compact, small, lightweight, and uniaxial monitor designed to detect vertical acceleration movements. This accelerometer has been widely validated in youth.
      • Freedson P.
      • Pober D.
      • Janz K.F.
      Calibration of accelerometer output for children.
      Adolescents were instructed to place the accelerometer at the lower back using an elastic waistband. They were also instructed to wear the accelerometer at all times for 7 consecutive days and to remove it only during water-based activities and sleeping. The interval of time (epoch) was set at 15 seconds in concordance with consensus recommendations for assessing physical activity in these ages.
      • Ward D.S.
      • Evenson K.R.
      • Vaughn A.
      • Rodgers A.B.
      • Troiano R.P.
      Accelerometer use in physical activity: best practices and research recommendations.
      The data were downloaded onto a computer using the manufacturer's software and later were analyzed by a software based on Visual Basic. The analyzer excluded from the analysis bouts of 20 continuous minutes of zeros output, considering these periods as nonwearing time. Inclusion criteria of at least 3 days of valid recording and a minimum of 8 hours' registration per day were necessary to be included in the study.
      The time spent (minutes/day) in moderate and vigorous physical activity was calculated based on cutoffs of 500 counts per 15 seconds and 1000 counts per 15 seconds, respectively. Further, MVPA was calculated using the cutoff point of ≥500 counts per 15 seconds that is equivalent to walking at 3 km/hour.
      • Brage S.
      • Wedderkopp N.
      • Anderson L.B.
      • Froberg K.
      Influence of step frequency on movement intensity predictions with the CSA accelerometer: a field validation study in children.
      These cutoff points to define the intensity categories are similar to those used in previous studies
      • Andersen L.B.
      • Harro M.
      • Sardinha L.B.
      • et al.
      Physical activity and clustered cardiovascular risk in children: a cross-sectional study (The European Youth Heart Study).
      • Ekelund U.
      • Anderssen S.A.
      • Froberg K.
      • et al.
      Independent associations of physical activity and cardiorespiratory fitness with metabolic risk factors in children: the European youth heart study.
      with European children and adolescents.

      Statistical Analyses

      A sample of 2199 adolescents had valid data on physical activity and BMI. Both samples were equivalent to the full HELENA-CSS sample according to age, gender distribution, and anthropometric measures. Further, because the aim of this study was to study the excess of body fat, those adolescents classified as underweight
      • Cole T.J.
      • Flegal K.M.
      • Nicholls D.
      • Jackson A.A.
      Body mass index cutoffs to define thinness in children and adolescents: international survey.
      were not included (n=105), even though there were no differences in levels of physical activity between underweight and normal-weight adolescents (all p>0.05). Thus, the present study sample comprised 2094 adolescents (973 boys and 1121 girls), and a total of 1994 (902 boys and 1092 girls) had valid data on skinfold thicknesses.
      Study sample characteristics are presented as mean (SD), unless otherwise stated. Differences between genders were analyzed by ANOVA for continuous variables and by the chi-square test for nominal variables. Receiver operating characteristic (ROC) curves
      • Zweig M.H.
      • Campbell G.
      Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine.
      were used to calculate the optimal physical activity cutoff points for moderate physical activity, vigorous physical activity, and MVPA that best discriminate between the normal-weight/normal-fat and overweight+obesity/overfat+obesity categories. Additional analyses were performed to discriminate between normal-weight/normal-fat and obesity using both classifications.
      An ROC curve provides the whole spectrum of specificity/sensitivity values for all the possible cutoffs. Sensitivity was considered as the probability to correctly identify an overweight/overfat or obese adolescent (true-positive proportion). Specificity was considered to be the probability of correctly identifying a normal-weight/normal-fat adolescent. The false-positive proportion were those normal-weight/normal-fat adolescents who were incorrectly identified as being overweight/overfat or obese.
      To identify the best cutoff, the distance between the ideal test and each sensitivity and 100-specificity pair was calculated with the MedCalc statistical software, version 10.4.5). The area under ROC curve (AUC) and 95% CIs were calculated using the same software. The AUC represents the ability of the test to correctly classify adolescents according to their weight/body-fat category. Values of AUC range from 0.5 (noninformative test) to 1.0 (ideal test). The cutoffs, AUC, and the sensitivity/specificity pairs were also calculated for the total sample and for each gender.
      Finally, the percentages of adolescents meeting different definitions of physical activity recommendations for youth (20, 60, and 90 minutes/day in MVPA, 60 minutes/day in MVPA with 30 minutes/day in vigorous physical activity, and the recommendation obtained in this study from the ROC analysis) were calculated. Further, the relationship between not meeting the physical activity recommendations and an unhealthy weight or body fat status was examined by binary logistic regression analysis. These analyses were conducted using SPSS, version 15.0, for Windows, and the level of significance was set at <0.05. All the analyses were performed in 2009.

      Results

      Characteristics of the study sample are shown in Table 1. ROC analysis using BMI categories (Table 2) showed that moderate physical activity does not discriminate among weight status categories, whereas vigorous physical activity significantly discriminated between normal-weight and overweight+obesity, and between normal-weight and obesity. The significant cutoff points of vigorous physical activity associated with normal-weight were 18 minutes/day for all, 18–19 minutes/day in boys, and 10 minutes/day in girls. The optimal cutoffs for time spent in MVPA were also significant between normal-weight and overweight+obesity and between normal-weight and obesity. These cutoffs were with 55–71 minutes/day in MVPA for all, 56 minutes/day of MVPA for boys, and 49–51 minutes/day of MVPA for girls.
      Table 1Physical characteristics, body fat, and levels of physical activity in European adolescents
      CharacteristicsAllBoysGirlspgender
      n20949731121
      Age (years)14.7 (1.2)14.7 (1.2)14.7 (1.2)0.683
      Weight (kg)59.0 (11.7)61.7 (13.0)56.6 (9.9)<0.001
      Height (cm)165.5 (9.2)169.6 (9.8)162.0 (7.0)<0.001
      BMI21.4 (3.4)21.3 (3.5)21.5 (3.3)0.257
      Overweight (%)
      Overweight and obese adolescents were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      17.818.617.10.060
      Obesity (%)
      Overweight and obese adolescents were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      5.36.44.40.042
      Overweight+obesity (%)
      Overweight and obese adolescents were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      23.125.021.50.060
      Body fat (%)
      n=1994, 902, and 1092 for all, boys, and girls, respectively.
      23.8 (9.2)20.2 (10.2)26.7 (6.9)<0.001
      Accelerometer wearing time (minutes/day)772 (93)778 (97)766 (90)<0.005
      Moderate physical activity (minutes/day)39 (15)42 (16)37 (14)<0.001
      Vigorous physical activity (minutes/day)19 (14)24 (14)14 (11)<0.001
      MVPA (minutes/day)58 (25)66 (26)50 (25)<0.001
      Note: Values are M (SD) unless otherwise specified.
      MVPA, moderate to vigorous physical activity
      a Overweight and obese adolescents were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      b n=1994, 902, and 1092 for all, boys, and girls, respectively.
      Table 2Physical activity cutoff points to identify the risk of an excess of body fat according to BMI categories
      BMI categories were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      in adolescents by ROC analysis
      SubjectsNormal-weight vs overweight+obesityNormal-weight vs obesity
      Cutoff (minutes/day)Se (%)Sp (%)AUC (95% CI)p-valueCutoff (minutes/day)Se (%)Sp (%)AUC (95% CI)p-value
      All
       Moderate physical activity4729.174.90.48 (0.46, 0.51)0.2874635.173.20.48 (0.42, 0.53)0.390
       Vigorous physical activity1867.146.90.58 (0.55, 0.61)<0.0011880.247.20.66 (0.61, 0.71)<0.001
       MVPA7179.826.70.53 (0.51, 0.56)0.0225564.949.80.57 (0.51, 0.62)0.012
      Boys
       Moderate physical activity4736.269.40.48 (0.44, 0.52)0.3634548.464.00.47 (0.39, 0.54)0.365
       Vigorous physical activity1853.566.70.61 (0.57, 0.65)<0.0011975.862.90.70 (0.63, 0.77)<0.001
       MVPA5644.965.30.55 (0.51, 0.59)0.0225653.264.40.58 (0.50, 0.65)0.030
      Girls
       Moderate physical activity3846.159.40.50 (0.46, 0.54)0.8812834.773.10.51 (0.43, 0.60)0.784
       Vigorous physical activity1055.659.20.59 (0.55, 0.63)<0.0011079.656.20.70 (0.63, 0.77)<0.001
       MVPA5162.245.10.54 (0.50, 0.58)0.0394971.449.30.61 (0.54, 0.69)0.003
      Note: p-values indicate AUC significantly >0.50.
      AUC, area under the ROC curve; MVPA, moderate to vigorous physical activity; ROC, receiver operating characteristic; Se, sensitivity; Sp, specificity
      a BMI categories were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      Receiver operating characteristic analysis using %BF categories (Table 3) showed that a cutoff point of 29 minutes/day in moderate physical activity discriminated between the normal-fat and excess-of-body-fat categories in girls. Vigorous physical activity and MVPA cutoffs significantly discriminated between the normal-fat and excess-of-body-fat categories. The vigorous physical activity cutoffs were 11–12 minutes/day for all, 17–18 minutes/day for boys, and 9–10 minutes/day for girls. The MVPA cutoffs were 49–52 minutes/day for the total sample, 47–55 for boys, and 41–42 for girls. The higher AUC values were always found when comparing the normal-weight/normal-fat and obesity categories.
      Table 3Physical activity cutoff points to identify the risk of an excess of body fat according to body fat categories
      Body fat categories were classified according to age- and gender-specific 85th and 95th percentile.
      in adolescents by ROC analysis
      SubjectsNormal-fat vs overfat+obesityNormal-fat vs obesity
      Cutoff (minutes/day)Se (%)Sp (%)AUC (95% CI)p-valueCutoff (minutes/day)Se (%)Sp (%)AUC (95% CI)p-value
      All
       Moderate physical activity2827.278.90.51 (0.46, 0.55)0.7493448.562.50.56 (0.49, 0.62)0.054
       Vigorous physical activity1153.070.30.65 (0.61, 0.69)<0.0011269.766.20.73 (0.69, 0.78)<0.001
       MVPA4952.362.40.59 (0.56, 0.63)<0.0015270.757.30.66 (0.60, 0.72)<0.001
      Boys
       Moderate physical activity4542.263.10.51 (0.45, 0.57)0.6943853.355.50.49 (0.40, 0.58)0.792
       Vigorous physical activity1760.768.20.68 (0.62, 0.74)<0.0011877.867.30.77 (0.70, 0.83)<0.001
       MVPA4735.679.30.59 (0.53, 0.65)<0.0015562.265.20.63 (0.55, 0.72)<0.001
      Girls
       Moderate physical activity2939.372.60.55 (0.50, 0.61)0.0242950.072.60.62 (0.54, 0.70)0.001
       Vigorous physical activity963.863.20.65 (0.59, 0.71)<0.0011081.561.60.76 (0.69, 0.82)<0.001
       MVPA4147.268.80.61 (0.55, 0.67)<0.0014266.765.90.71 (0.64, 0.77)<0.001
      Note: p-values indicate AUC significantly >0.50.
      AUC, area under the ROC curve; MVPA, moderate to vigorous physical activity; ROC, receiver operating characteristic; Se, sensitivity; Sp, specificity
      a Body fat categories were classified according to age- and gender-specific 85th and 95th percentile.
      From the results obtained with the ROC analyses, cutoff points for MVPA could be slightly rounded to 60 minutes/day for boys and girls. However, the large differences between boys and girls in cutoff points for vigorous physical activity deserve emphasis. Therefore, three recommendations were proposed, based on the time spent in vigorous-intensity activity: (1) a combined recommendation for boys and girls of 60 minutes in MVPA with at least 15 minutes in vigorous physical activity; (2) a recommendation for boys of 60 minutes in MVPA with at least 20 minutes/day of vigorous physical activity; (3) a recommendation for girls of 60 minutes of MVPA with at least 10 minutes of vigorous physical activity. The percentages of adolescents meeting the physical activity recommendations by gender, weight, and body fat categories are displayed in Table 4.
      Table 4Percentage of adolescents meeting physical activity recommendations for youth stratified in body fat categories
      Categoriesn20 minutes/day MVPA60 minutes/day MVPA90 minutes/day MVPA90 minutes/day MPA with 30 minutes/day VPAThe present study
      60 minutes/day in MVPA with 15 minutes/day in VPA (all), 20 minutes/day in VPA (boys), or 10 minutes/day in VPA (girls)
      BMI CATEGORIES
      BMI categories were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      All
       Normal-weight161096.742.010.28.337.8
       Overweight37396.538.39.97.233.0
       Obesity11110031.59.05.423.4
      Boys
       Normal-weight73098.458.817.714.750.0
       Overweight18198.951.416.012.740.3
       Obesity6210045.214.58.122.6
      Girls
       Normal-weight88095.328.14.53.126.4
       Overweight19294.326.04.22.124.0
       Obesity4910014.32.02.014.3
      % BODY FAT CATEGORIES
      Percentage of body fat categories were classified according to age- and gender-specific 85th and 95th percentile.
      All
       Normal-fat169698.642.610.68.838.0
       Overfat19997.535.26.53.030.2
       Obesity9997.019.25.11.014.1
      Boys
       Normal-fat76799.758.517.715.549.7
       Overfat9098.953.510.05.638.9
       Obesity4510033.311.12.215.6
      Girls
       Normal-fat92997.729.54.73.227.8
       Overfat10996.320.23.70.916.5
       Obesity5494.47.4007.4
      MPA, moderate physical activity; MVPA, moderate to vigorous physical activity; VPA, vigorous physical activity
      a 60 minutes/day in MVPA with 15 minutes/day in VPA (all), 20 minutes/day in VPA (boys), or 10 minutes/day in VPA (girls)
      b BMI categories were classified according to age- and gender-reference values proposed by the International Obesity Task Force.
      c Percentage of body fat categories were classified according to age- and gender-specific 85th and 95th percentile.
      Figure 1a shows the OR of having overweight+obesity and overfat+obesity if the adolescent did not meet the physical activity recommendations for the total sample and by gender. In the whole sample, only those adolescents who did not meet the 60 minutes in MVPA recommendation and the recommendation of 60 minutes in MVPA with at least 15 minutes in vigorous physical activity had an increased risk of being in both the overweight+obesity (OR=1.24, 95% CI=1.01, 1.53, and OR=1.36, 95% CI=1.10, 1.70, respectively) and the overfat+obesity (OR=1.79, 95% CIs=1.33, 2.42, and OR=1.85, 95% CI=1.40, 2.45, respectively) categories. Similarly in boys, only the 60 minutes in MVPA recommendation and the recommendation of 60 minutes in MVPA with at least 20 minutes in vigorous physical activity obtained significant ORs of having both overweight+obesity and overfat+obesity. In girls, none recommendation obtained significant ORs for overweight+obesity. Despite this, the 60 minutes in MVPA recommendation and the recommendation of 60 minutes in MVPA with at least 10 minutes in vigorous physical activity obtained significant ORs of overfat+obesity in girls. All analyses were repeated by analyzing the risk of having obesity in normal-weight/normal-fat adolescents and results were similar (Figure 1b).
      Figure thumbnail gr1
      Figure 1OR and 95% CI for having overweight+obesity and overfat+obesity (a) and obesity (b) in adolescents not meeting the physical activity recommendation, compared to those meeting the recommendations for the total sample (■); boys (); and girls (☐)
      Note: The physical activity recommendations for youth are the following: A: 20 minutes/day in MVPA; B: 60 minutes/day in MVPA; C: 90 minutes/day in MVPA; D: 90 minutes/day in MVPA with 30 minutes/day in VPA; E: The present study: 60 minutes/day in MVPA with 15 minutes/day in VPA (all); or 20 minutes/day in VPA (boys); or 10 minutes/day in VPA (girls).
      MVPA, moderate to vigorous physical activity; VPA, vigorous physical activity

      Discussion

      The main result of the current study suggests that physical activity recommendations for youth that advise 60 minutes/day in MVPA are associated with reduced risk of overweight and obesity in European adolescents. Adolescents who did not meet 60 minutes/day in MVPA with at least 10–20 minutes/day in vigorous physical activity might have a higher risk of having an excess of body fat than adolescents who meet the daily overall 60 minutes in MVPA.
      The USDHHS together with several medical institutions recently launched the Physical Activity Guidelines for Children and Adolescents, where it is mentioned that this population group should participate in 60 minutes or more of physical activity daily.
      USDHHS
      2008 Physical activity guidelines for Americans Be active, healthy and happy!.
      This recommendation continues along the same lines as previous public health recommendations for this population. However, a final note in the USDHHS recommendation suggests that children and adolescents should do vigorous physical activity at least 3 days per week but none volume is stated.
      USDHHS
      2008 Physical activity guidelines for Americans Be active, healthy and happy!.
      The current results concur with these recommendations because it was also shown that between 10 and 20 minutes/day in vigorous physical activity might have a major benefit in reducing body fat in this life period. Only the Health Canada recommendation of 90 minutes/day in MVPA included a specific recommendation for vigorous physical activity (i.e., 30 minutes in vigorous physical activity).
      Public Health Canada
      Family guide to physical activity for youth 10–14 years of age.
      Conversely, the possibility to achieve this goal is questioned as observed in the current findings, and recently they have adhered to the standard 60 minutes in MVPA guidelines.
      • Janssen I.
      Physical activity guidelines for children and youth.
      In contrast, the old recommendation for adolescents of 20 minutes in MVPA
      • Sallis J.F.
      • Patrick K.
      Physical activity guidelines for adolescents: consensus statement.
      was achieved for most of adolescents independently of gender and body fat. According to the current results, the 20 and 90 minutes/day in MVPA thresholds do not seem to be adequate.
      A threshold of 60 minutes/day in MVPA might discriminate between normal-weight and overweight+obesity adolescents as well as between those in the normal-fat versus overfat+obesity category. Nevertheless, approximately 20 minutes/day in vigorous physical activity in boys, 10 minutes/day in girls, and 15 minutes/day combined for both genders discriminated more accurately between normal-weight/normal-fat and unhealthier weight and body fat categories. The key role of vigorous physical activity on overweight and obesity has been highlighted in a number of cross-sectional and experimental studies. For example, an earlier study
      • Eliakim A.
      • Makowski G.S.
      • Brasel J.A.
      • Cooper D.M.
      Adiposity, lipid levels, and brief endurance training in nonobese adolescent males.
      evaluated the effect of a vigorous physical activity training in 38 nonobese adolescents (18 control) and the results showed reductions in subcutaneous adipose tissue measured by magnetic resonance. Another study
      • Gutin B.
      • Yin Z.
      • Humphries M.C.
      • Barbeau P.
      Relations of moderate and vigorous physical activity to fitness and fatness in adolescents.
      examined the associations of objectively assessed physical activity with body fat measured by dual-energy x-ray absorptiometry (DXA), and only objectively assessed vigorous physical activity explained a significant proportion of the variance in body fat after controlling for potential confounders. Similarly, one study
      • Patrick K.
      • Norman G.J.
      • Calfas K.J.
      • et al.
      Diet, physical activity, and sedentary behaviors as risk factors for overweight in adolescence.
      found that insufficient vigorous physical activity estimated by accelerometry was the only risk factor for higher weight in 878 adolescents. Likewise, the authors have found similar results in previous reports.
      • Moliner-Urdiales D.
      • Ruiz J.R.
      • Ortega F.B.
      • et al.
      Association of objectively assessed physical activity with total and central body fat in Spanish adolescents; The HELENA Study.
      • Ruiz J.R.
      • Rizzo N.S.
      • Hurtig-Wennlöf A.
      • Ortega F.B.
      • Warnberg J.
      • Sjöström M.
      Relations of total physical activity and intensity to fitness and fatness in children; The European Youth Heart Study.
      • Ortega F.B.
      • Ruiz J.R.
      • Sjöström M.
      Physical activity, overweight and central adiposity in Swedish children and adolescents: the European Youth Heart Study.
      These and the current findings highlight the role of daily vigorous physical activity to prevent overweight and obesity during adolescence.
      When the thresholds were examined by intensities, in general, moderate physical activity cutoff points did not significantly discriminate among weight and body fat categories, whereas vigorous physical activity always found significant cutoffs. Interestingly, MVPA cutoffs also discriminated between weight status and body fat categories. Taken together, the current results suggest that MVPA is negatively associated with an excess of body fat as a result of the vigorous physical activity included into the MVPA threshold. Likewise, in a previous study with a subsample of 365 Spanish adolescents from the HELENA-CSS, where body fat was measured by DXA, BodPod, and anthropometry, MVPA and especially vigorous physical activity were negatively associated with indicators of body fat.
      • Moliner-Urdiales D.
      • Ruiz J.R.
      • Ortega F.B.
      • et al.
      Association of objectively assessed physical activity with total and central body fat in Spanish adolescents; The HELENA Study.
      Subsequently, the MVPA cutoff points found in the current study seem to represent the necessary time in MVPA to guarantee enough time in vigorous physical activity, in order to avoid excess of body fat in adolescents. Following this rationale, it is recommended that the guideline of 60 minutes in MVPA be maintained and that a specific period of vigorous physical activity be added as part of that time period instead of adding more overall time spent in physical activity (e.g., 60 minutes in MVPA plus 15 minutes in vigorous physical activity). Thus, an after-school intervention in black girls provided 80 minutes in MVPA in order to ensure enough vigorous physical activity, and the greatest decreases were found in those girls who maintained the highest heart rates during the training.
      • Barbeau P.
      • Johnson M.H.
      • Howe C.A.
      • et al.
      Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls.
      Differences observed between boys and girls in vigorous physical activity cutoff points allowed a different recommendation with 20 minutes/day for boys and 10 minutes/day for girls and a combined recommendation of 15 minutes/day for both genders. The obvious biological and physical activity differences between genders across adolescence may need to be reflected in the physical activity guidelines. Several recommendations based on steps measured by pedometer have suggested different thresholds for boys and girls related to a healthy weight status.
      • Tudor-Locke C.
      • Pangrazi R.P.
      • Corbin C.B.
      • et al.
      BMI-referenced standards for recommended pedometer-determined steps/day in children.
      • Duncan J.S.
      • Schofield G.
      • Duncan E.K.
      Step count recommendations for children based on body fat.
      • Laurson K.R.
      • Eisenmann J.C.
      • Welk G.J.
      • Wickel E.E.
      • Gentile D.A.
      • Walsh D.A.
      Evaluation of youth pedometer-determined physical activity guidelines using receiver operator characteristic curves.
      Nevertheless, a combined recommendation was included for both genders of 60 minutes/day in MVPA including 15 minutes/day in vigorous physical activity, similar to the recommendation made in a previous study.
      • Wittmeier K.D.
      • Mollard R.C.
      • Kriellaars D.J.
      Physical activity intensity and risk of overweight and adiposity in children.
      This study
      • Wittmeier K.D.
      • Mollard R.C.
      • Kriellaars D.J.
      Physical activity intensity and risk of overweight and adiposity in children.
      found that 45 minutes/day in moderate physical activity and 15 minutes/day in vigorous physical activity were independently associated with reduced body fat and BMI status in children. Unfortunately, the small sample did not allow an analysis by gender, but girls were engaged in less-vigorous physical activity than boys.
      In further analyses, an examination was made of the ORs of having overweight+obesity, overfat+obesity, and obesity in adolescents not meeting several physical activity recommendations, including the current proposals obtained by the ROC analysis. These analyses showed that the whole sample that did not meet the recommendation had a significantly greater risk of having an excess of body fat than other recommendations. These results were stronger in boys than in girls, for whom the current proposal obtained similar results compared with the overall 60 minutes/day in MVPA recommendation. All the other physical activity recommendations failed to detect significant risks of having both overweight+obesity and overfat+obesity if the adolescent did not meet such recommendations.
      Strengths of the current study include measurements by accelerometer and a relatively large sample of adolescents from 10 European cities. Also, two methods were used to estimate body fat (BMI and %BF by skinfolds). BMI is widely used for the screening of obesity both in children and adolescents; however, BMI seems to be associated with lean mass rather than with fat mass.
      • Maynard L.M.
      • Wisemandle W.
      • Roche A.F.
      • et al.
      Childhood body composition in relation to body mass index.
      Likewise, physical activity might have an effect on both lean and fat masses.
      USDHHS
      2008 Physical activity guidelines for Americans Be active, healthy and happy!.
      Moreover, BMI seems to be a better indicator of adiposity than %BF obtained by skinfolds in obese adolescents.
      • Castro-Piñero J.
      • Artero E.G.
      • España-Romero V.
      • et al.
      Criterion-related validity of field-based fitness tests in youth: a systematic review.
      These are the reasons why both BMI and %BF variables were included in this study.
      The current study has limitations as well. The cross-sectional design limits the possibility to infer directionality. Thus, although reverse causality might be considered, there is certain evidence with regard to the plausible effect of physical activity on body fat in youth.
      • Eliakim A.
      • Makowski G.S.
      • Brasel J.A.
      • Cooper D.M.
      Adiposity, lipid levels, and brief endurance training in nonobese adolescent males.
      • Barbeau P.
      • Johnson M.H.
      • Howe C.A.
      • et al.
      Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls.
      • Riddoch C.J.
      • Leary S.D.
      • Ness A.R.
      • et al.
      Prospective associations between objective measures of physical activity and fat mass in 12–14 year old children: the Avon Longitudinal Study of Parents and Children (ALSPAC).
      Another limitation of the study is that both BMI and %BF by skinfolds are indirect methods to assess body fat. In addition, there are inherent limitations when the current physical activity outcomes are compared with those of other studies because of several factors such as type of monitor, length of the epoch, and cutoff points selected.
      • Martínez-Gómez D.
      • Welk G.J.
      • Calle M.E.
      • Marcos A.
      • Veiga O.L.
      AFINOS Study Group
      Preliminary evidence of physical activity levels measured by accelerometer in Spanish adolescents The AFINOS Study.
      In summary, the physical activity recommendation of 60 minutes/day in MVPA may be enough to avoid excess of body fat in adolescents. However, vigorous physical activity seems to be a key factor for decreasing the possibility of being obese. Therefore, public health recommendations should include a specific amount of vigorous physical activity for adolescents. In this framework, these results need to be contrasted in experimental designs.
      We acknowledge the help of all the adolescents who took part in the Helena study. The writing group takes sole responsibility for the content of this article. The content of this article reflects the views of the authors only, and the European Community is not liable for any use that may be made of the information contained therein. The HELENA study was supported by the European Community 6th RTD Framework Programme (Contract FOOD-CT-2005-007034 ). This study is also being supported by grants from the Spanish Ministry of Education ( EX-2007-1124 , EX-2008-0641 , AP2006-02464 ), the Spanish Ministry of Health (Maternal, Child Health and Development Network , RD08/0072 ), the Swedish Council for Working Life and Social Research , and the Swedish Heart Lung Foundation ( 20090635 ).
      No financial disclosures were reported by the authors of this paper.

      References

        • American College of Sports Medicine
        Opinion statement on physical fitness in children and youth.
        Med Sci Sports Exerc. 1988; 20: 422-423
        • USDHHS
        2008 Physical activity guidelines for Americans.
        USDHHS, Washington DC2008
        • Connelly J.B.
        • Duaso M.J.
        • Butler G.
        A systematic review of controlled trials of interventions to prevent childhood obesity and overweight: a realistic synthesis of the evidence.
        Public Health. 2007; 121: 510-517
        • Marshall S.J.
        • Biddle S.J.
        • Gorely T.
        • Cameron N.
        • Murdey I.
        Relationships between media use, body fatness and physical activity in children and youth: a meta-analysis.
        Int J Obes Relat Metab Disord. 2004; 28: 1238-1246
        • Jiménez-Pavón D.
        • Kelly J.
        • Reilly J.J.
        Associations between objectively measured physical activity and adiposity in children and adolescents: systematic review.
        Int J Pediatr Obes. 2010; 5: 3-18
        • Troiano R.P.
        • Berrigan D.
        • Dodd K.W.
        • Mâsse L.C.
        • Tilert T.
        • McDowell M.
        Physical activity in the U.S. measured by accelerometer.
        Med Sci Sports Exerc. 2008; 40: 181-188
        • Riddoch C.J.
        • Bo Andersen L.
        • Wedderkopp N.
        • et al.
        Physical activity levels and patterns of 9- and 15-yr-old European children.
        Med Sci Sports Exerc. 2004; 36: 86-92
        • Martínez-Gómez D.
        • Welk G.J.
        • Calle M.E.
        • Marcos A.
        • Veiga O.L.
        • AFINOS Study Group
        Preliminary evidence of physical activity levels measured by accelerometer in Spanish adolescents.
        Nutr Hosp. 2009; 24: 212-218
        • Reichert F.F.
        • Baptista Menezes A.M.
        • Wells J.C.
        • Carvalho Dumith S.
        • Hallal P.C.
        Physical activity as a predictor of adolescent body fatness: a systematic review.
        Sports Med. 2009; 39: 279-294
        • Strong W.B.
        • Malina R.M.
        • Blimkie C.J.
        • et al.
        Evidence based physical activity for school-age youth.
        J Pediatr. 2005; 146: 732-737
        • Janssen I.
        Physical activity guidelines for children and youth.
        Can J Public Health. 2007; 98: S109-S121
        • Kushi L.H.
        • Byers T.
        • Doyle C.
        • et al.
        American Cancer Society Guidelines on Nutrition and Physical Activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity.
        CA Cancer J Clin. 2006; 56: 254-281
        • USDHHS
        Physical activity.
        in: Dietary guidelines for Americans 2005. U.S. Government Printing Office, Washington DC2005: 19-22
        • Biddle S.J.
        • Cavill N.A.
        • Sallis J.F.
        Policy framework for young people and health-enhancing physical activity.
        in: Biddle S.J. Sallis J.F. Cavill N.A. Young and active? Young people and health-enhancing physical activity. Evidence and implications Health Education Authority, London1998: 3-16
        • Corbin C.B.
        • Pangrazi R.P.
        Physical activity for children: a statement of guidelines for children aged 5–12.
        2nd ed. National Association for Sport and Physical Education, Reston VA2004
        • Department of Health and Ageing
        National physical activity guidelines for Australians.
        Commonwealth of Australia, Canberra1999
        • Public Health Canada
        Family guide to physical activity for youth 10–14 years of age.
        Government of Canada, Ottawa2002
        • Hallal P.C.
        • Victora C.G.
        • Azevedo M.R.
        • Wells J.C.
        Adolescent physical activity and health: a systematic review.
        Sports Med. 2006; 36: 1019-1030
        • Malina R.M.
        • Bouchard C.
        • Bar-Or O.
        Growth, maturation, and physical activity.
        2nd ed. Human Kinetics, Champaign IL2004
        • Nader P.R.
        • Bradley R.H.
        • Houts R.M.
        • McRitchie S.L.
        • O'Brien M.
        Moderate-to-vigorous physical activity from ages 9 to 15 years.
        JAMA. 2008; 300: 295-305
        • Malina R.M.
        Tracking of physical activity and physical fitness across the lifespan.
        Res Q Exerc Sport. 1996; 67: S48-S57
        • Sallis J.F.
        • Patrick K.
        Physical activity guidelines for adolescents: consensus statement.
        Pediatr Exerc Sci. 1994; 6: 302-314
        • Moreno L.A.
        • De Henauw S.
        • González-Gross M.
        • et al.
        • HELENA Study Group
        Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence cross-sectional study.
        Int J Obes (Lond). 2008; 32: S4-S11
        • Béghin L.
        • Castera M.
        • Manios Y.
        • et al.
        • HELENA Study Group
        Quality assurance of ethical issues and regulatory aspects relating to good clinical practices in the HELENA cross-sectional study.
        Int J Obes (Lond). 2008; 32: S12-S18
        • Nagy E.
        • Vicente-Rodriguez G.
        • Manios Y.
        • et al.
        • HELENA Study Group
        Harmonization process and reliability assessment of anthropometric measurements in a multicenter study in adolescents.
        Int J Obes (Lond). 2008; 32: S58-S65
        • Slaughter M.H.
        • Lohman T.G.
        • Boileau R.A.
        • et al.
        Skinfold equations for estimation of body fatness in children and youth.
        Hum Biol. 1988; 60: 709-723
        • Rodríguez G.
        • Moreno L.A.
        • Blay M.G.
        • et al.
        • AVENA-Zaragoza Study Group
        Body fat measurement in adolescents: comparison of skinfold thickness equations with dual-energy X-ray absorptiometry.
        Eur J Clin Nutr. 2005; 59: 1158-1166
        • Cole T.J.
        • Bellizzi M.C.
        • Flegal K.M.
        • Dietz W.H.
        Establishing a standard definition for child overweight and obesity worldwide: international survey.
        BMJ. 2000; 320: 1240-1243
        • Freedson P.
        • Pober D.
        • Janz K.F.
        Calibration of accelerometer output for children.
        Med Sci Sports Exerc. 2005; 37: S523-S530
        • Ward D.S.
        • Evenson K.R.
        • Vaughn A.
        • Rodgers A.B.
        • Troiano R.P.
        Accelerometer use in physical activity: best practices and research recommendations.
        Med Sci Sports Exerc. 2005; 37: S582-S588
        • Brage S.
        • Wedderkopp N.
        • Anderson L.B.
        • Froberg K.
        Influence of step frequency on movement intensity predictions with the CSA accelerometer: a field validation study in children.
        Pediatr Exerc Sci. 2003; 15: 277-287
        • Andersen L.B.
        • Harro M.
        • Sardinha L.B.
        • et al.
        Physical activity and clustered cardiovascular risk in children: a cross-sectional study (The European Youth Heart Study).
        Lancet. 2006; 368: 299-304
        • Ekelund U.
        • Anderssen S.A.
        • Froberg K.
        • et al.
        Independent associations of physical activity and cardiorespiratory fitness with metabolic risk factors in children: the European youth heart study.
        Diabetologia. 2007; 50: 1832-1840
        • Cole T.J.
        • Flegal K.M.
        • Nicholls D.
        • Jackson A.A.
        Body mass index cutoffs to define thinness in children and adolescents: international survey.
        BMJ. 2007; 335: 194
        • Zweig M.H.
        • Campbell G.
        Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine.
        Clin Chem. 1993; 39: 561-577
        • Eliakim A.
        • Makowski G.S.
        • Brasel J.A.
        • Cooper D.M.
        Adiposity, lipid levels, and brief endurance training in nonobese adolescent males.
        Int J Sports Med. 2000; 21: 332-337
        • Gutin B.
        • Yin Z.
        • Humphries M.C.
        • Barbeau P.
        Relations of moderate and vigorous physical activity to fitness and fatness in adolescents.
        Am J Clin Nutr. 2005; 81: 746-750
        • Patrick K.
        • Norman G.J.
        • Calfas K.J.
        • et al.
        Diet, physical activity, and sedentary behaviors as risk factors for overweight in adolescence.
        Arch Pediatr Adolesc Med. 2004; 158: 385-390
        • Moliner-Urdiales D.
        • Ruiz J.R.
        • Ortega F.B.
        • et al.
        Association of objectively assessed physical activity with total and central body fat in Spanish adolescents; The HELENA Study.
        Int J Obes (Lond). 2009; 33: 1126-1135
        • Ruiz J.R.
        • Rizzo N.S.
        • Hurtig-Wennlöf A.
        • Ortega F.B.
        • Warnberg J.
        • Sjöström M.
        Relations of total physical activity and intensity to fitness and fatness in children; The European Youth Heart Study.
        Am J Clin Nutr. 2006; 84: 298-302
        • Ortega F.B.
        • Ruiz J.R.
        • Sjöström M.
        Physical activity, overweight and central adiposity in Swedish children and adolescents: the European Youth Heart Study.
        Int J Behav Nutr Phys Act. 2007; 4: 61
        • Barbeau P.
        • Johnson M.H.
        • Howe C.A.
        • et al.
        Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls.
        Obesity (Silver Spring). 2007; 15: 2077-2085
        • Tudor-Locke C.
        • Pangrazi R.P.
        • Corbin C.B.
        • et al.
        BMI-referenced standards for recommended pedometer-determined steps/day in children.
        Prev Med. 2004; 38: 857-864
        • Duncan J.S.
        • Schofield G.
        • Duncan E.K.
        Step count recommendations for children based on body fat.
        Prev Med. 2007; 44: 42-44
        • Laurson K.R.
        • Eisenmann J.C.
        • Welk G.J.
        • Wickel E.E.
        • Gentile D.A.
        • Walsh D.A.
        Evaluation of youth pedometer-determined physical activity guidelines using receiver operator characteristic curves.
        Prev Med. 2008; 46: 419-424
        • Wittmeier K.D.
        • Mollard R.C.
        • Kriellaars D.J.
        Physical activity intensity and risk of overweight and adiposity in children.
        Obesity (Silver Spring). 2008; 16: 415-420
        • Maynard L.M.
        • Wisemandle W.
        • Roche A.F.
        • et al.
        Childhood body composition in relation to body mass index.
        Pediatrics. 2001; 107: 344-350
        • Castro-Piñero J.
        • Artero E.G.
        • España-Romero V.
        • et al.
        Criterion-related validity of field-based fitness tests in youth: a systematic review.
        Br J Sports Med. 2009; ([Epub ahead of print])
        • Riddoch C.J.
        • Leary S.D.
        • Ness A.R.
        • et al.
        Prospective associations between objective measures of physical activity and fat mass in 12–14 year old children: the Avon Longitudinal Study of Parents and Children (ALSPAC).
        BMJ. 2009; 339: b4544

      Linked Article

      • Author Response
        American Journal of Preventive MedicineVol. 41Issue 1
        • Preview
          Drs. Guinhouya, Hubert, and Zitouni raise an important question for the field of accelerometry in their letter: Which is the best cut point to estimate moderate-to-vigorous physical activity (MVPA) using the ActiGraph accelerometer in youth?
        • Full-Text
        • PDF
      • Need for Unbiased Computation of the Moderate-Intensity Physical Activity of Youth in Epidemiologic Studies
        American Journal of Preventive MedicineVol. 41Issue 1
        • Preview
          Physical activity is recognized as a key health component. Thus, it is currently recommended that youth engage in a minimum of 60 minutes/day of an activity that is of moderate intensity or, ideally, a moderate-to-vigorous physical activity (MVPA).1 In order to quantify accurately the physical activity level of youth, and for a fair examination of the relationships between physical activity and health outcomes, devices such as the MTI Actigraph accelerometer are used increasingly among this population.
        • Full-Text
        • PDF