Associations between habitual school-day breakfast

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Aug 4, 2010 - index (BMI), physical activity (PA) and cardiorespiratory fitness (CRF). Methods: .... The Progressive Aerobic Capacity Endurance Run (PACER).
European Journal of Clinical Nutrition (2010), 1–7

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ORIGINAL ARTICLE

Associations between habitual school-day breakfast consumption, body mass index, physical activity and cardiorespiratory fitness in English schoolchildren GRH Sandercock1, C Voss2 and L Dye2 1 2

Department of Biological Sciences, Centre for Sports and Exercise Science, University of Essex, Colchester, UK and Human Appetite Research Unit, Institute of Psychological Sciences, University of Leeds, Leeds, UK

Objectives: The aim of this study was to assess associations between habitual school-day breakfast consumption, body mass index (BMI), physical activity (PA) and cardiorespiratory fitness (CRF). Methods: BMI, PA and CRF were measured in 4326 schoolchildren aged 10–16 years. Participants were classified as obese or non-obese, as having low or high PA and CRF. Habitual school-day breakfast consumption was assessed by a questionnaire and classified as never, sometimes or always. Results: Participants who sometimes ate breakfast were more likely to be obese than those who always did (Po0.05). Boys who never ate breakfast were more likely to have low PA odds ratio (OR) 2.17, 95% CI 1.48–3.18) and low CRF (OR 2.02, 95% CI 1.40–2.93) than those who always did. Compared with those who always did so, girls were more likely to have low PA if they sometimes (OR 1.39, 95% CI 1.13–1.70) or never (1.48 95% CI 1.06–2.05) ate breakfast, but the likelihood of low CRF was not different between groups. Conclusions: Habitual breakfast consumption is associated with healthy BMI and higher PA levels in schoolchildren. In boys, regularly eating breakfast is also associated with higher levels of CRF. The higher PA observed in habitual breakfast eaters may explain the higher CRF values observed. These positive health behaviours and outcomes support the encouragement of regular breakfast eating in this age group.

European Journal of Clinical Nutrition advance online publication, 4 August 2010; doi:10.1038/ejcn.2010.145 Keywords: breakfast; physical activity; fitness

Introduction Children who regularly eat breakfast have a lower body mass index (BMI) (Rampersaud et al., 2005; Utter et al., 2007; Timlin et al., 2008; Croezen et al., 2009) and better long-term weight control (Timlin et al., 2008) compared with those who tend to miss this meal. However, the mechanism by which eating breakfast is linked to BMI remains elusive (Utter et al., 2007). There appears to be a greater likelihood of health-compromising behaviours in children who miss breakfast, including increased prevalence of smoking, poorer food choices and greater energy intake from snacks (Aarnio

Correspondence: Dr GRH Sandercock, Department of Biological Sciences, Centre for Sports and Exercise Science, University of Essex, Wivenhoe Park, Colchester, Essex CO43SQ, UK. E-mail: [email protected] Received 14 August 2009; revised 24 May 2010; accepted 24 May 2010

et al., 2002; Cohen et al., 2003; Keski-Rahkonen et al., 2003). Several studies have shown, however, that children who eat breakfast may actually have a higher daily energy intake than those who do not (Nicklas et al., 2000; Sjoberg et al., 2003; Dubois et al., 2009). To maintain lower BMI with higher energy intake, children who eat breakfast must have greater energy expenditure than those who miss breakfast. Studies have examined whether children who eat breakfast are more active than those who do not but have provided somewhat mixed results. A variety of self-report methods have been used to examine the relationship between physical activity (PA) and breakfast, including activity frequency (Cohen et al., 2003; Keski-Rahkonen et al., 2003), frequency of activity and exercise during leisure time, frequency of exercise outside school (Aarnio et al., 2002) or hours devoted to sport (Henriquez Sanchez et al., 2008). Two studies using wellvalidated PA assessment tools showed no relationship

Relationship between breakfast, BMI, PA and fitness in schoolchildren GRH Sandercock et al

2 between eating breakfast and PA (Utter et al., 2007; Albertson et al., 2008). Definitions of eating or skipping breakfast also vary between these studies. Most studies use a two-group classification to assess breakfast habits (Cohen et al., 2003; Godin et al., 2005; Utter et al., 2007; Henriquez Sanchez et al., 2008) whereas others create three groups such as almost never, sometimes or always eating breakfast (Aarnio et al., 2002; Keski-Rahkonen et al., 2003). Assessing PA in children can also be problematic. Selfreported PA is a useful measure of health behaviour. Low PA in childhood tracks into adulthood where it is an important prognosticator for chronic disease (Williams, 2001). Selfreported PA is, however, open to recall difficulties, biases and dishonesty. Objective measures of children’s habitual PA such as pedometer counts and accelerometry correlate well with cardiorespiratory fitness (CRF) when assed by indirect calorimetry (Ekelund et al., 2001; Dencker et al., 2006). Assessing CRF, therefore, provides an objectively measurable alternative to self-assessed PA in large cohorts of children. CRF also offers a superior measure of health status compared with self-reported PA. CRF relates more closely with markers or cardiovascular disease than PA in children (Hurtig-Wennlof et al., 2007). CRF also tracks from childhood to adulthood (Kristensen et al., 2006; Boreham et al., 2004). In adults, CRF is significantly better as a predictor of cardiovascular disease than PA (Blair et al., 2001; Williams, 2001). The aims of this study were, therefore, threefold. First, to confirm the relationship between BMI and breakfast consumption in a sample of English schoolchildren using a three-group definition of school-day breakfast consumption (always, sometimes or never). Second, to assess differences in self-reported PA between these groups using a validated selfassessment tool. Third, to assess differences in objectively measured CRF between groups.

Methods After receiving ethical approval and parental consent, measurements were made in 4326 (2336 boys and 1990 girls) English schoolchildren aged 10–16 years. All procedures complied with the Declaration of Helsinki Principles. Participants were recruited through their school physical education (PE) departments. Schools were selected to provide a sample representative of the east of England in terms of urban and rural location, and levels of deprivation. We studied 10–16 year olds to include both primary and secondary schoolchildren. Children younger than 10 years were not studied due to difficulties in accurate self-reported PA and application of the aerobic capacity test. Over 90% of the available participants took part in some part of the study. Parents could withdraw consent from parts of the protocol (weighing for instance) and overall, 88% of the pupils completed the whole protocol. European Journal of Clinical Nutrition

Researchers trained in anthropometric assessment measured height to the nearest 1 mm and weight to the nearest 0.1 kg, with participants dressed in standard PE clothing without shoes. BMI was calculated (kg/m2) and converted to z-scores using UK reference data (Cole et al., 1995). BMI was categorized as underweight, normal weight, overweight or obese according to the criteria of the International Obesity Task Force (IOTF) (Cole et al., 2000). All measurements were made in PE lessons with screens for privacy, with boys and girls measured separately. All data were included in the analysis by comparing obese individuals with the remaining sample (which included normal-weight and overweight individuals). This approach differs from much of the existing literature. The reason for this choice is that obesity tracks strongly into adulthood (Kristensen et al., 2006; Boreham et al., 2004), whereas there tends to be more movement between normal-weight and overweight groups during adolescence (Wardle et al., 2006). PA was assessed by 7-day recall (Physical Activity Questionnaire for Children/Adolescents (PAQ-C/A) depending on the age of the participant. Those under 11 years completed the PAQ-C whereas those over 11 years completed the PAQ-A. Participants completed the questionnaire in a PE lesson, before exercise testing. The answers were checked during testing and incomplete questionnaires were returned for completion. The completion rate was 98% overall. The questionnaire is valid and correlates well with objective measures of PA (Kowalski et al., 1997; Janz et al., 2008). Aerobic capacity is often used as an objective proxy for PA. In our sample the correlation between PAQ score and aerobic capacity was r ¼ 0.3–0.5 (depending on age and sex). The PAQ assesses PA according to sports participation and PA at school, including PE and leisure time activities. The questionnaire is scored from 1 (no activity) to 5 (highly active). Numerous cut-points to classify children as active or inactive are available in the literature and these are often common between boys and girls. Due to significant between-sex differences in PA, participants were classified as having either low or high PA using a sex-specific median split. The Progressive Aerobic Capacity Endurance Run (PACER) test was used to assess CRF. Participants were required to run 20-m shuttles in time with an audible signal until they could no longer maintain the required pace. The test started at 8.5 km/h and increased by 0.5 km/h each minute. Performance was recorded as number of shuttles completed and expressed as a percentage of published minimum health criterion values for CRF (Meredith and Welk, 2005). These criterion-referenced standards for children are retro-extrapolated from adult data showing association between CRF and cardiovascular disease risk (Blair et al., 1989). The cutoffs take into account physiological changes such as maturation, as well as lifestyle changes such as PA (Cureton and Plowman, 2007). School-day breakfast habits were assessed by a single question: ‘On how many school days per week do you normally eat breakfast at home,’ with numerical responses

Relationship between breakfast, BMI, PA and fitness in schoolchildren GRH Sandercock et al

3 more likely to always (w2 ¼ 82.4, Po0.001) eat breakfast. Girls were more likely to sometimes (w2 ¼ 8.0, P ¼ 0.005) or never (w2 ¼ 9.0, P ¼ 0.003) eat breakfast. Except for age and levels of obesity, boys and girls differed on all measures. Table 2 contains data according to breakfast group separately for boys and girls for all measures expressed as continuous variables. Analysis of variance with post hoc tests showed differences in age between all groups in both sexes with decreased breakfast frequency with increasing age. In boys who always ate breakfast, BMI was lower compared with those who sometimes did (P ¼ 0.043) but was not lower than in those who never did so. PA was higher in boys who always (Po0.001) or sometimes (P ¼ 0.001) ate breakfast compared with those who never did so. CRF was different between all groups, with levels increasing with greater breakfast frequency. Girls who always ate breakfast had a lower mean BMI than those who sometimes did (P ¼ 0.017). PA and CRF were different between all groups, with levels increasing with greater breakfast frequency. Table 3 shows the results of multinomial logistic regression analysis and gives the likelihood of participants being classified as being obese, having low PA and low CRF according to breakfast habits. In each case, those who always ate breakfast are used as the reference category (odds ratio (OR)1.00). Compared with boys who always ate breakfast, boys who sometimes ate breakfast were more likely to be obese (P ¼ 0.002). There was a trend towards an increased likelihood of obesity in boys who never did so (P ¼ 0.18). Boys who never ate breakfast were more than twice as likely to be classified as having low PA compared with those who always did. Boys who never ate breakfast were twice as likely to have low CRF compared with those who always did. Girls who never ate breakfast were nearly twice as likely to be obese compared with those who always did. Girls who never ate breakfast were more likely to report PA below the

from 0 to 5. We tested the reliability and validity of this questionnaire in a group of children and adolescents (n ¼ 64) similar to the sample (age 12.7±0.7 years) who visited the University for exercise testing. Two-day reliability was good (r ¼ 0.81, Po0.001) as was validity, assessed by comparing answers with those from a one-to-one interview (Cronbach’s alpha ¼ 0.89). The question was designed to provide habitual information, hence the use of word normally. School-day breakfast consumption was assessed as habits often differ on weekend days. We assessed eating breakfast at home only as none of the schools had breakfast clubs. As habitual breakfast consumption patterns were of interest in this study, answers were classified to create groups of participants who Always (5), Sometimes (1–4) or Never (0) ate breakfast.

Statistics Differences in the reported frequency of breakfast consumption and prevalence of obesity were assessed by Pearson’s w2 analysis. Differences in continuous variables were assessed by independent t-tests. Differences in BMI, PA and fitness were examined by one-way analysis of variance with post hoc (Tukey). Analysis of categorical variables was performed using multinomial logistic regression analyses. Always eating breakfast was used as the referent value and odds (±95% confidence interval (CI)) for being classified as obese, inactive and unfit were calculated in separate analyses controlling for age.

Results Table 1 shows the descriptive characteristics of the sample and breakfast frequency data. Overall, 68% of participants always ate breakfast. Of the remainder, 25% sometimes missed this meal and 7% reported never eating this meal according to our definition. Compared with girls, boys were

Table 1 Basic descriptive characteristics of sample as means (±s.d.) for continuous variables and percentages (n) for categories Total Breakfast: Always Breakfast: Sometimes Breakfast: Never Age (years) BMI (z-score) Obese PAQ CRF (% minimum) Low CRF

67.9% 24.9% 7.2% 12.3 0.66 5.6% 2.9 176 21.0%

(2938) (1077) (311) (1.4) (1.1) (242) (0.7) (105) (908)

Boys 73.4% 21.1% 5.5% 12.3 0.73 6.0% 3.0 149 27.7%

(1715) (492) (129) (1.4) (1.1) (139) (0.7) (73) (648)

Girls

t-test or w2 P-value

61.4% (1223) 29.3% (585) 9.3% (182) 12.3 (1.4) 0.59 (1.1) 5.2% (103) 2.7(0.6) 209 (126) 13.1% (260)

Po0.001* P ¼ 0.003* P ¼ 0.005* P ¼ 0.13 Po0.001 P ¼ 0.15* Po0.001 Po0.001 Po0.001*

Abbreviations: BMI, body mass index; CRF, cardiorespiratory fitness; PAQ, physical activity questionnaire. Breakfast groups: Always, normally eaten on five school days per week; Sometimes, normally eaten on one to four school days per week; Never, not normally eaten on any school days. BMI, expressed as age- and sex-related z-scores on the basis of UK reference data; Obesity—based on IOTF classification (Cole et al., 2000); PAQ for Children or Adolescents (score 1–5 arbitrary units) (Kowalski et al., 1997); Low PA, determined by median split of 2.7 for girls and 3.0 for boys (not shown); CRF (% minimum), expressed as percentage of minimum cardiorespiratory fitness level for future adult health (Meredith and Welk, 2005); Low CRF, frequency (%) of participants with cardiorespiratory fitness o100% of level required for future adult health (Meredith and Welk, 2005). *P-value for w2-test.

European Journal of Clinical Nutrition

Relationship between breakfast, BMI, PA and fitness in schoolchildren GRH Sandercock et al

4 Table 2 Differences in age, BMI, PA and CRF between breakfast habit groups in boys and girls separately Breakfast Always

ANOVA F-value for main effect

Sometimes

Never

Boys Frequency Age (years) BMI (z-scores) PAQ (units 1–5) CRF (% minimum)

73.4% 12.3 0.69 3.04 152%

(1715) w (1.4)*** (1.14)** (0.71)* (73.2)***

21.1% 12.6 0.84 3.00 144%

(492) w (1.5)* (1.16) (0.72)* (73.4)*

5.5% 13.0 0.75 2.77 120%

(129)w (1.3) (1.16) (0.74) (60.1)

F ¼ 25.0 F ¼ 2.94 F ¼ 7.60 F ¼ 11.4

(Po0.001) (P ¼ 0.05) (P ¼ 0.001) (Po0.001)

Girls Frequency Age (years) BMI (z-scores) PAQ (units 1–5) CRF (% minimum)

61.4% 12.0 0.54 2.78 219%

(1223) (1.35)*** (1.11)** (0.624)*** (126)***

29.3% 12.5 0.69 2.66 194%

(584) (1.36)* (1.05) (0.597)* (120)*

9.3% 13.1 0.64 2.55 179%

(182) (1.23) (1.08) (0.649) (95.2)

F ¼ 65.7 F ¼ 4.07 F ¼ 14.1 F ¼ 11.2

(Po0.001) (P ¼ 0.017) (Po0.001) (Po0.001)

Abbreviations: ANOVA, analysis of variance; BMI, body mass index; CRF, cardiorespiratory fitness; PAQ, physical activity questionnaire. Breakfast groups: Always, normally eaten on five school days per week; Sometimes, normally eaten on one to four school days per week; Never, not normally eaten on any school days. BMI expressed as age- and sex-related z-scores on the basis of—UK reference data (Cole et al., 2000); PAQ for Children or Adolescents (score 1–5 arbitrary units) (Kowalski et al., 1997); CRF (% minimum) expressed as percentage of minimum cardiorespiratory fitness level for future adult health (Meredith and Welk, 2005). wSignificantly different frequency to girls (w2 Po0.05); *Different to Never group (Po0.05); **Different to Sometimes group (Po0.05); ***Different to Sometimes and Never groups (Po0.05).

Table 3 Multinomial logistic regression analysis of obesity, low PA and low CRF according to breakfast habits (age-adjusted OR, 95% CI) in boys and girls Always

Sometimes

Never

Boys Obesity (6.0%) Low PA Low CRF (27.7%)

1 (reference) 1 (reference) 1 (reference)

1.82 (1.24–2.67)* 1.07 (0.88–1.31) 1.15 (0.92–1.44)

1.62 (0.82–3.22) 2.17 (1.48–3.18)* 2.02 (1.40–2.93)*

Girls Obesity (5.2 %) Low PA Low CRF (13.1%)

1 (reference) 1 (reference) 1 (reference)

1.12 (0.71–1.77) 1.39 (1.13–1.70)* 1.11 (0.83–1.50)

1.92 (1.01–3.61)* 1.51 (1.08–2.11)* 0.949 (0.61–1.48)

Abbreviations: CI, confidence interval; CRF, cardiorespiratory fitness; OR, odds ratio; PA, physical activity. Breakfast groups: Always, normally eaten on five school days per week; Sometimes, normally eaten on 1–4 school days per week; Never, not normally eaten on any school days. Obesity, on the basis of IOTF classification (Cole et al., 2000); Low PA on the basis of a median split PAQ score of 3.03 in boys and 2.80 in girls; Low CRF on the basis of non-achievement of the recommended minimum cardiorespiratory fitness level for future adult health (Meredith and Welk, 2004). *Significantly greater likelihood than the Always group.

median value compared with those who sometimes or always did. Low CRF was much less common in girls (13%) than in boys (28%) and there was no association between CRF and breakfast habits in girls.

Discussion The aim of this study was to determine differences in BMI, PA and, for the first time, CRF in children grouped according to their breakfast habits. These three outcomes will be discussed in turn. The relationship between breakfast and BMI is well investigated and in agreement with the existing European Journal of Clinical Nutrition

literature; there was a general trend towards healthier BMI values in habitual breakfast eaters. Breakfast skipping may be linked to an increased risk of obesity due to dietary factors such as increased snacking frequency, unhealthy food choices and greater energy consumption later in the day (Sjoberg et al., 2003; Moreno and Rodriguez, 2007; Giovannini et al., 2008; Dubois et al., 2009), but previous findings regarding the relationship between breakfast habits and energy intake are heterogeneous and lower daily energy consumption has been reported (Berkey et al., 2003). Such heterogeneous findings in breakfast skippers suggest that the mechanism by which eating breakfast is associated with lower BMI is unlikely to be purely dietary nature.

Relationship between breakfast, BMI, PA and fitness in schoolchildren GRH Sandercock et al

5 Albertson et al. (2008) and Giovannini et al. (2008) have proposed that eating breakfast may be a marker for other positive health behaviours and Albertson et al. (2008) showed a significant association between eating breakfast and PA over a short (3-day) assessment period. If, as some studies suggest, children who regularly eat breakfast have a higher energy intake but maintain a BMI lower or similar to their peers who skip breakfast, it follows that they must have greater energy expenditure. The present data support this notion as the highest PA levels were found in boys and girls who always ate breakfast. These data are in agreement with a number of previous studies, which show higher PA in children who are regular breakfast eaters (Aarnio et al., 2002; Cohen et al., 2003; Keski-Rahkonen et al., 2003; Godin et al., 2005; Henriquez Sanchez et al., 2008). Despite the wide variety of definitions used to classify children as physically active and the widely varying categorization of breakfast frequencies the positive relationship between eating breakfast and PA is becoming increasingly apparent. Assessing PA by means of self-report is problematic, particularly in children. It is of note that only this study and two others (Utter et al., 2007; Albertson et al., 2008) have used a validated questionnaire to assess PA. Using the habitual activity questionnaire, Albertson et al. (2008) found no association between daily energy expenditure (metabolic equivalents) and frequency of breakfast consumption (0–3 times) over three study days. The authors did, however, find that children who ate a cereal-based breakfast on all three study days were more active than those who did not, and suggested that eating cereal for breakfast may serve as a proxy for a healthy lifestyle. Utter et al. (2007) found that children who sometimes or never ate breakfast were no less likely to be in the top quartile of PA as measured using the PAQ-A/C (OR 0.75; CI 0.5–1.1). Utter et al.’s cohort in New Zealand comprised mainly immigrant children from the Pacific Islands or of indigenous Maori decent, the majority of the study participants also fell within the most deprived quintile of the population. Deprivation and ethnicity were both strongly associated with PA and breakfast consumption. Such results are, therefore, difficult to generalize from and to compare with the present data. The present data are the first, therefore, to show an association between eating breakfast and PA using a validated self-report tool. In both sexes, the largest difference was between children who always and never ate breakfast, supporting the notion that habitual breakfast eating is associated with positive health behaviours. One weakness of this study, as that of all previous work on this topic, is the use of selfreported PA. As well as poor recall and potential bias, the tool used here (PAQ-A/C) does not provide information on exercise intensity, which is important as current guidelines suggest that moderate and vigorous activity is needed to promote health in children. The correlation between PA and objectively measured CRF suggests the latter may be able to serve as a proxy for habitual vigorous PA (Dencker et al., 2006). CRF has the

additional benefit of objective measurement and not being open to recall bias. Finally, CRF is more closely related to childhood health status (Hurtig-Wennlof et al., 2007) and onset of chronic disease in adulthood than self-reported PA (Williams, 2001). In short, it is useful from a health perspective to think of PA as a behaviour and target for intervention. CRF, however, should be considered as an important health outcome. Given the importance of CRF as a measure of health, it is surprising that this is the first study to examine its relationship with eating breakfast. We found that boys and girls who never ate breakfast had lower mean CRF than those who sometimes or always did, although this was not evident in girls. Boys who never ate breakfast were also twice as likely to be classified as unfit compared with those who always did. Like BMI, CRF is a health outcome and we can only hypothesize as to the mechanism by which the health behaviour of eating breakfast is linked to higher CRF. A potential mechanism is again, by means of PA and Table 2 shows that between-group differences in CRF closely mirror those for PA. The health behaviour of eating breakfast is associated with higher PA and the meal itself provides sufficient energy requirements for morning activity (Vermorel et al., 2003). Boys and girls who always eat breakfast show higher mean PA levels than their peers who skip this meal. Higher PA is associated with higher CRF. As high CRF is an important, positive health outcome this interrelationship may be yet another reason to encourage children to eat breakfast.

Limitations The cross-sectional nature of the study prevents us from inferring causality from these data and it may simply be that parents who encourage their children to eat breakfast also encourage PA. We also only analysed school-day breakfast consumption. This limits the generalizability of the data but was necessary for clarity. Breakfast habits on weekends are likely to differ and to complicate responses. As most of the PA assessed was during school days and because we wanted to look only at habitual patterns, it was deemed necessary to omit weekend breakfast data. Further studies might benefit from assessing weekend and weekday breakfast habits separately. For simplicity we did not choose to define breakfast except for being eaten at home and this limits our findings as participants given a healthy cereal-based meal may classify themselves similarly to those who are given perhaps and energy-dense snack before school. Further research is needed to determine how breakfast composition may be associated with PA and aerobic capacity. The lack of association between CRF and eating breakfast in girls is most likely due to the cut-points for achieving satisfactory CRF (being fit) on the PACER being much lower in girls than boys. This is due to the lower incidence of cardiovascular disease in adult females (Cureton and European Journal of Clinical Nutrition

Relationship between breakfast, BMI, PA and fitness in schoolchildren GRH Sandercock et al

6 Plowman, 2005) as the cut points are retro-extrapolated from adult data, which relate CRF to chronic disease. In this study this means that less than half the number of girls were classified as having low CRF compared with boys. Using CRF cut-points on the basis of increasing risk factor prevalence in childhood might be a useful alternative, but such points have not yet been agreed.

Conclusions This study shows positive associations between school-day breakfast consumption, lower body mass index, PA and CRF in English schoolchildren. In agreement with previous data, those who always ate breakfast had a lower mean BMI and were less likely to be obese. We have shown for the first time that children who always eat breakfast have better CRF than those who habitually miss this meal. The higher PA observed in habitual breakfast eaters was also associated with better CRF. Given the importance of CRF as a marker of child health (Hurtig-Wennlof et al., 2007) and in preventing adult disease (Williams, 2001) children should be encouraged to eat breakfast regularly.

Conflict of interest The authors declare no conflict of interest.

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