Background
Although young people do not typically present with cardiometabolic diseases such as cardiovascular disease and type 2 diabetes [
1], the risk factors for these conditions are present during the early years of life [
1,
2] and track into adulthood and influence lifelong health [
3]. During adolescence, the body undergoes many developmental changes [
4], which can lead to a state of insulin resistance, and is further complicated by excess adiposity during this period [
5]. Indeed, the number of adolescents with type 2 diabetes is increasing each year [
6]. Thus, adolescence is a crucial time to identify the prevalence of risk factors for cardiometabolic disease, and their associations with related behaviours and characteristics, such as adiposity and physical fitness, which are modifiable. In addition to cardiometabolic health, the importance of cognition during adolescence has been recognised, as it is related to lifelong physical and mental health [
7], as well as academic performance [
8]. However, despite the importance of cardiometabolic health and cognition during adolescence, the associations between key modifiable lifestyle factors (such as physical activity, physical fitness, and adiposity) and risk factors for cardiometabolic disease and cognitive function during adolescence are relatively unexplored.
The role of device-measured physical activity is of particular interest, given that physical activity is central to UK national [
9] and global [
10] guidelines for well-being. Whilst it is generally accepted that physical activity has beneficial effects on traditional risk factors for cardiometabolic disease such as blood pressure [
11,
12] and insulin sensitivity [
12] in boys and girls between 10–19 years of age; much less is known about the impact of physical activity on novel risk factors for cardiometabolic disease. A key novel risk factor for cardiometabolic disease that has been studied more recently is elevated cytokine concentrations, a marker of low-grade chronic inflammation [
1,
13]. In the few studies conducted to date, no association was found between physical activity and IL-6 concentration in boys and girls aged 13 – 17 y [
14,
15] and no studies have examined other cytokines related to low-grade inflammation (such as IL-1β, IL-10, IL-15). Additionally, the association between habitual physical activity and cognitive function during adolescence is unclear, with some studies suggesting a beneficial association with the domains of inhibitory control and cognitive flexibility in boys and girls [
16,
17], whilst others did not find such associations [
18]. A recent omnibus review highlighted the benefits of planned/structured physical activity for cognitive function in young people, however the associations between device-measured physical activity and cognitive function were equivocal [
19]. To the author’s knowledge, no studies have examined whether age group (i.e. younger, 11–12 years; older, 14–15 years) moderate the associations with risk factors for cardiometabolic disease and cognitive function during adolescence.
One possible explanation for the lack of association between device-measured physical activity and cardiometabolic health, and cognitive function, is the challenge of assessing device-measured physical activity; including the divergent methodologies used and the numerous protocols for processing and categorising accelerometery data [
20,
21]. To address this, Rowlands et al. [
22] have proposed two new metrics that continuously capture the volume (average acceleration) and intensity (intensity gradient) of physical activity, overcoming some of the limitations of the more traditional cut-point based approaches. Recent studies have shown that these new metrics (both the average acceleration and intensity gradient) are negatively and independently associated with BMI in 9–11 year-old boys and girls [
23,
24] and a composite score of metabolic syndrome risk in boys and girls aged 9–10 years [
24]. Despite these initial promising findings, there are currently no data in older adolescents (14–18 years) and no data on the associations between these two new physical activity metrics (average acceleration and intensity gradient physical activity), and traditional metabolic risk factors such as insulin sensitivity. Furthermore, no studies have examined the associations between the new physical activity metrics and inflammatory risk factors for cardiometabolic disease (such as low-grade chronic inflammation), and no studies have examined the associations between the novel physical activity metrics and cognitive function.
There is a strong evidence base that physical fitness is beneficially associated with traditional risk factors for cardiometabolic disease, such as blood lipids [
11,
25], HOMA-IR [
14,
25,
26] and blood pressure [
11] in boys and girls across adolescence. In addition, a small number of previous studies in boys and girls aged 13–14 y [
27] and 11–12 y [
28] have shown that lower physical fitness is associated with increased pro-inflammatory IL-6 [
27,
28] and IL-1β [
28] concentrations, as well as a lower anti-inflammatory IL-10 concentration [
28]. However, there are no data on how the effect of physical fitness on traditional and novel risk factors for cardiometabolic disease may change across adolescence or if there are relationships between physical fitness and other cytokines which reflect cardiometabolic disease risk. For example, IL-15 is an anti-inflammatory cytokine which is involved in adipose tissue regulation [
29] and improved insulin sensitivity [
30], yet has not been examined in association with physical fitness.
Physical fitness is also beneficially associated with a range of cognitive function domains in healthy children [
16,
31], children living with obesity [
32] and adults [
33]. Less is known about adolescents, but a small number of studies have shown that physical fitness is positively associated with academic performance [
34], inhibitory control [
35,
36] and working memory [
36] in boys and girls aged 11–15 y. Furthermore, it is interesting that the relationships between device-measured moderate-to-vigorous physical activity (MVPA) and cognitive function found by Aadland et al. [
16] no longer remained when physical fitness was considered; suggesting that physical fitness may be more important than habitual physical activity for cognition in adolescents. Thus, it is important to address the possible independent impacts of both physical activity and physical fitness on cognitive function across adolescence.
Adiposity is recognised as an important risk factor for the development of cardiovascular disease and type 2 diabetes [
37]. In boys and girls aged 11–12, sum of four skinfolds was positively related to HOMA-IR and mean arterial pressure [
28], and in boys and girls aged 13–17 the sum of six skinfolds was positively related with C-reactive protein (CRP) [
14]. Adiposity, measured by waist circumference, has also previously been assessed as an outcome related to cardiometabolic disease in adolescents – commonly used in the formation of a composite risk score [
11,
12,
25]. There has, however, been less consideration as to how waist circumference influences novel risk factors for cardiometabolic disease in adolescents, such as low-grade chronic inflammation. Furthermore, there is growing evidence to suggest that adiposity may be detrimental for cognitive function, with worse executive function task performance seen in young adults with a higher BMI [
38]. On top of this, focus on the association between adiposity and cognitive function has been centred on children [
39], with less attention in an adolescent population. Some limited data in adolescents show that boys and girls, aged 13–15, with a higher BMI had worse performance on an attention and cognitive flexibility task [
40].
Therefore, the purpose of the present study was to examine the associations between physical activity, physical fitness and adiposity, and risk factors for cardiometabolic disease and cognitive function in a sample of adolescents (age 11–15 years). Furthermore, the present study will also examine if these associations are modified by year group (year 7 (age 11–12 years) and year 10 (age 14–15 years).
Discussion
The main findings of the present study were that: physical fitness (distance covered on the MSFT) was positively associated with anti-inflammatory IL-15 concentration and accuracy on the congruent and incongruent Stroop tasks, and negatively associated with response times across cognitive domains (indicating that higher fit participants displayed faster response times); and that physical activity volume (average acceleration) and physical activity intensity (intensity gradient) were negatively associated with blood pressure (systolic, diastolic and MAP). Furthermore, the present study also demonstrates that boys spent more time in high intensity physical activity compared to girls (as reflected by a less negative intensity gradient value), and that boys and year 10 participants had a higher physical fitness (as measured by distance covered on the MSFT) compared to girls and year 7 participants respectively. Furthermore, the difference in physical fitness between boys and girls was greater in year 10 participants than year 7 participants. In addition, year 7 girls had higher cytokine concentrations (IL-6 and IL-10) in comparison with boys of the same age. Blood pressure and blood glucose concentration were higher in year 10 participants compared to year 7, and year 10 participants were consistently quicker across a range of cognitive function domains (attention, inhibitory control, working memory and visual processing).
A key novel finding of the present study is that physical fitness (distance covered on the MSFT) is positively associated with IL-15 concentration in adolescents. IL-15 has a recognised role in adipose tissue regulation [
29] as well as skeletal muscle insulin sensitivity, oxidative metabolism and angiogenesis [
30]. Data from animal models suggest that IL-15 activates PPAR-δ which is responsible for a subsequent improvement in endurance capacity through regular training [
30]. Our findings extend the previously reported increase in skeletal muscle IL-15 content after 12 weeks of endurance training in adult males [
57], by reporting a positive association between physical fitness (MSFT performance) and IL-15 concentration, which may contribute to chronic training adaptations as a result of repeated physical activity. However, longitudinal data following a training intervention in adolescents is required to confirm this suggestion.
Another key finding of the present study was the positive relationships between higher levels of physical fitness and cognitive function in adolescents. Specifically, the present study is also the first to demonstrate that physical fitness is beneficially associated with indices of simple and complex visual processing speed (response times on the visual search test) in adolescents. Higher physical fitness was also associated with faster response times across the domain of executive function (specifically inhibitory control and working memory), which is consistent with much of the evidence base in adolescents [
16,
35,
58]. It has been stated that adolescents may be more sensitive to the effects of physical fitness on cognition, particularly with regards to executive function, as the associated brain regions are still developing at this stage [
59]. A hypothesised mechanism of these beneficial effects is through the release of neurotrophins, such as brain-derived neurotrophic factor (BDNF) [
59]. However, the present study did not support this and found no associations between physical fitness and BDNF concentration. Nonetheless, the data from the present study demonstrate a beneficial association between physical fitness and cognitive function. Future work should seek to explore the potential mechanistic links between physical fitness and cognition, an understanding of which would allow such mechanisms to be targeted in the design of future interventions.
The present study is also the first to demonstrate that the newly proposed physical activity metrics, both the physical activity volume and intensity of the activity, are negatively associated with mean arterial pressure. It is well known that higher physical activity levels are associated with reductions in blood pressure [
11,
12] and have protective effects against the development of hypertension [
60]. However, the present study provides novel insight across adolescence in that the association for both physical activity variables was dependent on year group, whereby a stronger negative association was observed in year 10 participants, when compared to year 7 participants, for both volume and intensity. This highlights the importance of physical activity for older adolescents, who are typically less active [
61] and also subject to an age-related increase in blood pressure [
62]. The present study also adds further novel insights with regards to the relationship between the activity volume metric and IL-6 concentration, as well as the intensity gradient and IL-1β concentration. Interestingly, the negative association observed between average acceleration and IL-6 concentration, as well as intensity gradient and IL-1β concentration, was exclusive to year 7 participants. The present study is the first to report that these relationships may be moderated by age across adolescence and thus future research should aim to replicate such findings and also examine the potential mechanism responsible.
The present study is also the first to examine the associations between the newly proposed physical activity metrics, average acceleration and intensity gradient, and cognitive function in adolescents. These data from the present study did not suggest there were any associations between average acceleration and intensity gradient with cognitive function. Whilst previous studies have reported that device-measured physical activity is beneficially associated with measures of cognitive function [
16,
17], others do not [
18]. Discrepancies amongst these findings may be explained by the different processing techniques used, as well as the summary metrics used to represent physical activity. Indeed, previous work focused solely on moderate-to-vigorous physical activity from self-report measures [
17], whereas the present study utilised novel metrics that consider the whole physical activity intensity spectrum [
22]. Despite the use of these new metrics, the present study may be limited by a small sample size (particularly for older adolescents; 14–15 y). Indeed, more work using these metrics with much larger samples is required to fully establish the nature of relationship between physical activity and cognition in adolescents.
It has been argued that physical fitness, as a state (which to some extent reflects chronic physical activity), is a better measure to use than physical activity itself which varies greatly from day-to-day, when examining the relationship with cognitive function [
18]. This is supported by evidence showing that the associations between moderate-to-vigorous physical activity and cognitive function do not hold when physical fitness was accounted for [
16]. This suggests that it is physical fitness, rather than physical activity per se, which is important for cognitive function and only some physical activities, of a sufficient intensity to enhance physical fitness, will contribute to enhanced cognition. Indeed, when considering physical fitness, physical activity and adiposity (waist circumference), the findings of the present study only found associations between physical fitness and cognitive performance, suggesting that interventions to enhance cognition in adolescents should focus on improving physical fitness, rather than simply increasing physical activity, or reducing adiposity.
The present study found that adiposity was important for cardiometabolic health, whereby waist circumference was positively associated with IL-6 concentration, although interestingly this was exclusive to year 10 participants. The findings of the present study support the empirical findings of Dring et al. [
28], whereby sum of skinfolds (also indicative of greater adiposity) was positively associated with IL-6 concentration. Indeed, it is generally recognised that adolescents who display greater adiposity have higher concentrations of inflammatory cytokines [
63]. Waist circumference is a recommended proxy of visceral adipose tissue, which is known as an endocrinological tissue that secretes inflammatory mediators, particularly IL-6 [
64]. It is thought that the adipose tissue-derived IL-6 is mechanistically involved in the development of insulin resistance [
5] and subsequent occurrence of cardiometabolic diseases, such as cardiovascular disease and type 2 diabetes [
65]; with the present study providing novel evidence of a positive relationship between waist circumference and IL-6 concentration, indicative of poorer cardiometabolic health.
Whilst the present study provides novel insight as previously discussed, it is not without limitations. Firstly, the present study is cross-sectional in nature which precludes any inference of causality in the observed associations. Furthermore, although a commonly used field-based measurement of physical fitness was used (MSFT), a different version (15 m shuttles) than what is typically used (20 m shuttles) in paediatric exercise research was used, due to facility constraints at participating schools. The present study also recruited fewer year 10 participants compared to year 7, which may limit the conclusions in these older adolescents. As a result of this, the models created were parsimonious in nature and did not account for other important independent variables. Indeed, future work utilising large samples should seek to replicate such findings whilst accounting for additional independent variables.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.