Associations between substitution of sedentary behavior patterns to physical activity and cardiovascular risk factors in adolescents: a 3-year longitudinal study

doi:10.21203/rs.3.rs-3311397/v1

Background: Little is known on how the substitutions of time from sedentary behavior patterns to physical activity (PA) impacts cardiovascular risk factors during adolescence. In this sense, the study aimed to investigated the associations between substitutions of sedentary behavior (SB) and SB patterns to different PA intensities and changes in cardiovascular risk factors during adolescence in analyses stratified by sex.

Methods: Prospective cohort study whit mean follow-up period of 3.2 (± 0.34) years, involving Brazilian adolescents. Body mass index (BMI), waist circumference (WC) and cardiorespiratory fitness (CRF) were the cardiovascular risk factors considered. SB patterns, light physical activity (LPA) and moderate to vigorous physical activity (MVPA) were measured by accelerometers. Multivariate linear regression models adopting the isotemporal substitution were used to analyze the association between substitution of 30 min.day^-1of SB patterns to LPA and MVPA and risk factors. All analyses considered 5% significance levels.

Results: Substitutions of sedentary time, short and long bouts to MVPA were associated with higher CRF in boys (β = 0.228, 95%CI = 0.040-0.416, β = 0.213, 95%CI = 0.019-0.406 and β = 0.287, 95%CI = 0.077-0.497, respectively). No associations were observed when analyses involved substitution of SB patterns to LPA, adiposity and girls.

Conclusion: Substituting SB patterns to MVPA appears to favorably influence changes of CRF in boys during adolescence. Greater benefits appear to occur when longer sedentary bouts are substituted by MVPA.

Sedentary lifestyle

Motor activity

Obesity

Physical fitness

Youth

Epidemiology

The increasing prevalence of sedentary behavior (SB) has become a growing public health concern (1). Worryingly, the recent pandemic caused by SARS-Cov-2 has contributed to an exacerbated increase in time spent in this behavior (2, 3). Among adolescents, the high volume of time spent in sedentary activities is considered an important cardiovascular risk factor and is associated with negative health outcomes (4). In addition, SB patterns accumulated in bouts (uninterrupted periods in SB) also appears to impact cardiovascular risk factors in distinct ways (5–7).

SB, together with physical activity (PA) and sleep, are the movement behaviors and are mutually exclusive to the full 24-h period. These behaviors are codependent and finite over 24 hours, which means that change in the duration of one behavior will inevitably lead to change in the duration of another behavior (8). In addition, each behavior may show distinct associations with cardiovascular risk factors depending on the behavior being substituted (9, 10). In this way, the isotemporal substitution model (ISM) (9) is a technique used to analyze the theoretical effects on health outcomes by substituting the time spent in one behavior to another. Studies using ISM can provide relevant information for developing strategies to interrupt SB and promote PA, as well to provide evidence for creating specific recommendations on the substitution of SB and its patterns.

Previous studies investigating time substitutions have suggested that substitution of SB to moderate to vigorous physical activity (MVPA) is associated with reduced adiposity indicators and increased cardiorespiratory fitness (CRF) levels in adolescents (11, 12). Additionally, substitution of sedentary bouts to MVPA also appears to be associated with better adiposity (13, 14) and CRF indicators (13). However, most studies available in literature adopted cross-sectional design, which imposes important limitation on findings and does not allow determining the causality of results. Among prospective studies on this topic, most of them investigated adiposity (15–20) and only one investigated CRF (21). In addition, prospective studies investigating substitutions of SB patterns and stratifying analyses by sex are still scarce. Finally, most studies did not include changes in behavioral and cardiovascular risk factors that occur during adolescence in the statistical analyses, since this is a period marked by important behavioral changes.

In this way, using ISM, the present study aims to analyze associations between substitutions of SB and SB patterns to different PA intensities and changes in cardiovascular risk factors during adolescence in analyses stratified by sex.

Sample selection and experimental design

This is an observational prospective cohort study involving adolescents from public schools in the city of Londrina/PR, Brazil. Details about the sample selection process have been previously described (22). At baseline, 690 adolescents were monitored by accelerometers and 394 had valid measurements (57%). Follow-up was conducted three years later and only participants with valid accelerometer data were screened for the second phase of the project. Of these, 155 participated in all assessments and were included in the final sample. Both phases of the research were approved by the local ethics committee (Ethics Committee of the State University of Londrina according to opinion No. 1.281.324 and No. 3.389.373 for baseline and follow-up, respectively) according to resolution 466/2012 of the National Health Council on research involving human beings. Informed Consent was obtained from legal guardians of the participants involved in the study. The experimental design is presented in Fig. 1.

The inclusion criteria adopted for both phases were: (I) to present valid accelerometer data; (II) delivery of the informed consent term signed by parent/ guardian; (III) adolescents regularly enrolled in public schools in the city of Londrina/PR. Participants younger than ten years and older than 14 years at baseline; those with less than four days of valid accelerometer data; with incomplete measures of cardiovascular risk factors and covariates; those who had any physical limitation or were under treatment for any disease or injury during the study and those who were not present on all days of data collection were excluded from the study.

Cardiovascular risk factors assessment

Body mass was measured using portable digital reading scale (Seca, model 831, 0.1 kg precision) and height using portable stadiometer (Harpenden Holtain Ltd, 0.1 cm precision). Based on this information, body mass index (BMI) was calculated and converted into z-score according to normative values proposed by De onis et al. (23). Waist circumference (WC) was determined using metal tape measure according to procedures described by Katzmarzyk et al. (24) and converted into z-score according to normative values proposed by Fryar; Gu; Ogden, (25).

The 20-m shuttle run test (SR-20m) was applied to assess CRF, according to Léger et al. (26). SR-20 m is an intermittent 20-m run test with initial speed of 8.5 km/h, and increment of 0.5 km/h per minute. The test was interrupted if the participant could no longer achieve the 20-m distance on three consecutive times. CRF values were converted into z-score according to sex and age-specific normative values proposed by Tomkinson et al. (27). The same protocols and procedures were used in both phases of the study.

Sedentary behavior and physical activity assessment

SB and PA were objectively measured using ActiGraph (ActiGraph, Pensacola, FL, USA) accelerometers, models GT3X and GT3X+. Participants were instructed to wear the accelerometer on the right side of the hip (at the level of the anterior iliac crest) and to use the equipment for seven consecutive days, except during water activities, bathing and sleep periods. Data were recorded at frequency of 30Hz (GT3X+) or one second (GT3X) and reintegrated into 15-second epoch length for analyses (ActiLife software, version 6.13.4).

Adolescents with at least four valid days recorded by accelerometers were included in analyses (≥480 min/d). The criterion of 30 minutes of consecutive zeros was used to determine the non-wear time (28). SB, light physical activity (LPA) and MVPA were estimated using cut-off points developed for ActiGraph vector magnitude in Brazilian adolescents (29). Sedentary bouts were defined as uninterrupted periods in SB (drop time = 0) with duration of 1–14 minutes (short bouts), 15–29 (middle bouts) and ≥ 30 minutes (long bouts). For analysis purposes, time spent in SB, SB patterns and PA were converted into minutes per day (min.day^− 1).

Covariables

Sex, socioeconomic status, peak height velocity (PHV), sleep period and percentage of time in MVPA were adopted as covariates in this study. Socioeconomic status was assessed through questionnaire developed by the Brazilian Association of Research Companies (30), in which the highest score indicates the highest economic level. Somatic maturation was estimated by the equation proposed by Mirwald et al. (31). Sleep period was obtained from self-administered questionnaire and calculated through the mean sleep time, considering weekdays and weekends. Information obtained at baseline was considered for all covariates.

Statistical analyses

Descriptive statistics were presented as mean and standard deviation. Comparisons between baseline and follow-up were computed using the student t-test for paired samples. Differences between sex were estimated using the t-test for independent samples. Multivariate linear regression models analyzed associations between substitution of SB and SB patterns to PA determined between baseline and follow-up (Δ = behavior at follow-up – behavior at baseline) and changes in cardiovascular risk factors (Δ = risk factor at follow-up – risk factor at baseline). In ISM analyses (9), the behavior of interest is removed from the regression model, while total activity (sum of all behaviors), other behaviors and covariates remained in the model. Thus, the corresponding coefficients represent associations of substituting the removed behavior by the remaining behaviors, maintaining the other variables constant.

For the substitution of sedentary time to LPA or MVPA, total activity was considered as the sum of the differences of these behaviors between follow-up and baseline (total activity = Δ SB + Δ LPA + Δ MVPA). For substitution of SB patterns to LPA or MVPA, the total activity calculation involved the sedentary time fractionation (total activity = Δ short bouts + Δ middle bouts + Δ long bouts + Δ LPA + Δ MVPA + SB residuals). All models considered substitution blocks of 30 min.day^− 1 and were adjusted for study covariates. All analyses were conducted in the SPSS statistical package, version 28.0 (IBM Corporation, USA), with significance set at 5%.

A total of 394 adolescents with mean age of 11.78 ± 0.89 years had valid accelerometer measurements at baseline. Of these, 155 participated in follow-up procedures. Among the 155 participants monitored by accelerometers who participated in the follow-up, 109 provide complete data for the variables of interest in both phases of the study and were included in the final analyses. No significant differences were observed in behavioral variables, adiposity indicators and CRF values between included and excluded participants.

** INSERT FIGURE 1**

Sociodemographic, cardiovascular risk factors and accelerometry information are presented in Table 1. The sample was mostly composed of girls (54.1%). In absolute terms, significant increase in BMI and WC was observed between baseline and follow-up in both sexes, while increase in CRF values was observed only among boys. In relative terms, significant decrease in BMI z-score values was observed among boys and increase in WC z-score values among girls. No differences in relative CRF values were observed between baseline and follow-up.

Significant differences were observed for SB and PA estimates. For both sexes, significant reduction in time spent in LPA and MVPA was observed. Regarding sedentary time, significant increase in time spent in bouts of 1–14 and 15–29 min.day^− 1 was observed for boys, while among girls, increase in sedentary time, short, middle and long bouts was observed. Considering comparisons between sexes, boys had higher CRF values, time spent in long bouts and MVPA at baseline, when compared to girls. At follow-up, significant differences remained only in CRF values.

** INSERT Table 1**

Associations between substitutions of SB and SB patterns to PA and BMI, WC, CRF during adolescence and stratified by sex are presented in Table 2. Substitution of sedentary time (β = 0.228, 95%IC = 0.040–0.416), short bouts (β = 0.213, 95%IC = 0.019–0.406) and long bouts β = 0.287, 95%IC = 0.077–0.497) to MVPA were significantly associated with higher CRF values only in boys. No associations were observed between cardiovascular risk factors and girls. Additionally, no significant association was observed when analyses involved substitution of SB patterns to LPA, or when analyses involved BMI and WC for boys and girls.

** INSERT Table 2**

This is one of the first studies to investigate associations between substitutions of SB patterns to different PA intensities and cardiovascular risk factors in adolescents from a prospective cohort design and performing analyses stratified by sex. The present study found that substitution of sedentary time, short and long bouts to MVPA were associated with CRF only in boys. Our findings did not reveal positive effects of substituting SB patterns to MVPA on BMI and WC for both sexes. In addition, no associations were observed by substituting SB and SB patterns to LPA in all cardiovascular risk factors.

Previous studies on this topic mostly had cross-sectional design and few investigated substitutions of sedentary bouts and analyses stratified by sex (11, 12). Among prospective studies, some of them only considered associations between substitution of exposure variables at baseline and outcomes at follow-up (17, 18, 21). Thus, our study adds new information about how substituting SB patterns to LPA and MVPA impact changes in cardiovascular risk factors during adolescence and the respective differences between sexes. In addition, the prospective design with a three-year follow-up makes it possible determining the causality of findings.

Our findings on the effect of substituting SB and sedentary time on CRF values during adolescence provides support to findings of previous studies that involved only sedentary time or SB patterns. For example, Santos et al. (21) found that replacing 30 min of sedentary time to vigorous physical activity (VPA) measure at baseline was associated with higher CRF values at follow-up. Jones et al. (13) observed beneficial associations in CRF replacing 30 min of short (< 10 minutes) and long (≥ 10 minutes) sedentary bouts to MVPA for boys and girls. Significant associations only for female adolescents were found by substituting sedentary time to MVPA. These results differ in part from those found in the present study. Analyses stratified by sex showed significant associations between substitution of sedentary time, short and long bouts to MVPA only for boys. We speculate that these results may be linked to longer time spent in MVPA for boys compared to girls and higher CRF levels over the follow-up period. It is also noteworthy that the highest magnitudes of associations were observed when long bouts were substituted by MVPA. This is an interesting finding, as if confirmed in subsequent studies, it may help establishing recommendations on PA and SB for the adolescent population.

The lack of association between substitution of sedentary time to LPA and adiposity indicators observed in the present study corroborates results from previous prospective cohort studies (15–17, 19, 20). Although LPA has the potential to be more easily achievable than MVPA, to reduce time spent in sedentary activies and, consequentely, and to increase PA levels, the potential benefits linked to this intensity are still poorly understood in the pediatric population.

In the present study, no associations were observed between substitutions of SB patterns to MVPA and BMI and WC in adolescents. Prospective studies have shown inconsistent results when adiposity is analyzed. While some studies point to benefits in adiposity when substituting SB to MVPA (15, 17) and VPA (18, 20, 32), others point to null associations (16, 19). A single study showed benefitial associations substituting sedentary bouts to VPA (20). Some hypotheses may explain the lack of association found in the present study. Inittialy, variables related do diet composition were not considered as covariates. In addition, BMI values showed unexpected behavior throughout the follow-up period (reduction of z-score values). Considering that weight indicators increase during adoelescence, this unexpected behavior may have introduced bias when determining the association between BMI and substituion of SB and SB patterns to PA. Finally, the integrated approach of moderate and vigorous physical activities may also have influenced associations, since VPA seems to have greater effect on obesity prevention compared to other PA intensities.

Some study limitations need to be considered and generalization of our findings should be carried out with caution. Many adolescents were excluded at baseline because they did not have valid accelerometer data and there were considerable follow-up losses. These losses and exclusions contributed to the low sample size, which may have affected the magnitude of associations and induced type II error. Despite follow-up losses, it was observed that body composition characteristics, health outcomes and time in SB, SB patterns and PA were similar between included and excluded individuals, which may have minimized possible bias in estimates. Therefore, future studies with more roust analyses stratified by sex should be carried out to confirm or not this finding. Finally, it is important to recognize the limitation of accelerometers in detecting postural transitions, which hinders a more accurate estimation of variables that compose SB patterns.

On the other hand, this study had positive points that should be highlighted. This is one of the first prospective cohort studies to investigated, using ISM, associations between changes in SB, SB patterns and PA and changes in cardiovascular risk factors throughout adolescence. The few prospective studies analyzed these associations predictively (i.e., considering time in SB and PA at baseline and outcomes at follow-up). In addition, the follow-up period was longer than periods found in previous studies. This allowed for a more comprehensive understanding of how the substitution of sedentary time and SB patterns to LPA and MVPA is related to risk factors during a period when these behaviors are unfavorably changing in adolescents (increased SB and decrease LPA and MVPA). The high accelerometer wear time (~ 14 hours) allowed for a more representative estimate of daily behaviors. Finally, our analyses considered many confounding variables, including somatic maturation, which is not usually considered in studies with adolescents.

The results of the present study provide relevant information for public policies for promoting PA and preventing cardiovascular risk factors in the pediatric population. Considering the high sedentary time during adolescence in schools (33), interventions implemented in the school environment replacing shorter (5 and 10 min.day^− 1) and/or longer (15 and 30 min.day^− 1) time intervals of SB and short, middle and long sedentary bouts to MVPA may promote improvements in CRF values. The use of stand desks (34), implementation of active breaks (35) and physically active classes (36) appear to be effective interventions for reducing unfavorable behavioral changes that occur throughout adolescence. Strategies targeting out-of-school and leisure time should also be considered, where opportunities for sedentary lifestyle are increasingly frequent.

This study provides evidence that substituting blocks of 30 min.day^− 1 of sedentary time and SB patterns to MVPA positively impact CRF levels in boys during adolescence. Greater benefits appear to occur when longer sedentary bouts (> 30 minutes) are replaced by MVPA. Future studies with longitudinal design, larger sample size and analyses stratified by sex may provide additional information on the impact of substituting SB patterns to PA on the health of adolescents. The use of devices able to distinguish posture transitions should also be considered, since they allow estimating SB patterns more reliably when compared to accelerometers.

BMI: Body Mass Index; CRF: Cardiorespiratory fitness; ISM: Isotemporal Substitution Model; LPA: Light Physical Activity; MVPA: Moderate to Vigorous Physical Activity; PA: Physical Activity; PHV: Peak Height Velocity; SB: Sedentary Behavior; VPA: Vigorous Physical Activity; WC: Waist Circumference.

Ethics approval and consent to participate

The study was approved by the Ethics Committee in Research with Human Beings of the State University of Londrina (according to opinion No. 1.281.324 dated the 09^th of October 2015 and No. 3.389.373 dated the 3^rd of November 2019) and complies with the Declaration of Helsinki on human research. Informed Consent was obtained from legal guardians of the participants involved in the study.

All participants signed the Free and Informed Consent Term and the Infant Assent Term.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

There is no funding source.

Authors´ contributions

LAV: Conception and design, methodology, data collection, analysis and interpretation of data, drafting the article, final approval; VMRW: Conception and design, data collection, drafting the article, final approval; WAL: Drafting the article, revising it critically, final approval; JES: Drafting the article, revising it critically, final approval; CLPR: Revising it critically, supervision, editing, final approval; ERVR: Revising it critically, supervision, editing, final approval; MR: Conception and design, methodology, analysis and interpretation of data, drafting the article, supervision, final approval.

Acknowledgments

The authors would like to thank all individuals that participated in the research and the researches that helped in the data collection. We also would like to thank the Brazilian research agency CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the doctor´s grant.

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Table 1 – Cardiovascular risk factors and time spent in sedentary behavior, sedentary bouts and physical activity at baseline and follow-up.

	Baseline			Follow-up
Variables	Boys (M ± SD)	Girls (M ± SD)	P	Boys (M ± SD)	Girls (M ± SD)	P
Age (years)	11.72 ± 0.57	11.67 ± 0.53	0.664	14.95 ± 0.73#	14.91 ± 0.59#	0.387
BMI (kg/m²)	20.20 ± 4.13	20.67 ± 4.75	0.568	21.90 ± 4.58#	23.01 ± 5.10#	0.212
BMI z-score	0.83 ± 1.37	0.70 ± 1.50	0.609	0.49 ± 1.33#	0.61 ± 1.32	0.597
WC (cm)	69.81 ± 8.77	67.88 ± 9.66	0.255	79.61 ± 12.44#	77.79 ± 13.04#	0.431
WC z-score	0.40 ± 0.89	0.14 ± 1.00	0.133	0.55 ± 0.86	0.36 ± 1.02#	0.271
CRF (km/h)	9.87 ± 0.78	9.34 ± 0.67	<0.001*	10.46 ± 0.92#	9.31 ± 0.62	<0.001*
CRF z-score	-0.42 ± 0.77	-0.53 ± 0.80	0.432	-0.44 ± 0.70	-0.62 ± 0.66	0.162
SB (min.day^-1)	576.61 ± 146.12	536.81 ± 118.54	0.098	616.51 ± 120.28	605.55±115.14#	0.607
Bouts 1-14 (min.day^-1)	356.20 ± 65.02	344.54 ± 59.78	0.302	382.87 ± 83.76#	372.73 ± 63.69#	0.448
Bouts 15-29 (min.day^-1)	100.15 ± 54.92	86.23 ± 47.18	0.133	127.04 ± 54.12#	125.54 ± 45.92#	0.868
Bouts ≥30 (min.day^-1)	58.15 ± 64.23	38.23 ± 36.41	0.041*	57.36 ± 46.47	53.53 ± 40.63#	0.627
LPA (min.day^-1)	172.64 ± 42.33	184.83 ± 39.03	0.099	145.80 ± 43.28#	151.33 ± 32.85#	0.423
MVPA (min.day^-1)	83.51 ± 29.76	71.09 ± 25.84	0.016*	64.91 ± 33.18#	55.28 ± 23.00#	0.068
Accelerometer wear time (min.day^-1)	832.77 ± 152.49	792.75 ± 128.27	0.724	827.24 ± 125.64	812.17 ± 119.24	0.905

Note: * = differences between sex were tested by independent sample Student’s t-test. # = differences between baseline and follow-up were tested by paired Student’s t-test. BMI = Body mass index. CRF = Cardiorespiratory fitness. LPA = Light physical activity. M = mean. MVPA = Moderate to vigorous physical activity. SB = Sedentary behavior. SD = Standard deviation. WC = Waist circumference.

Table 2 – Associations between isotemporal substitution of sedentary behavior and sedentary bouts to different intensities of physical activity and body mass index, waist circumference and cardiorespiratory fitness during adolescence.

Variables removed	Girls		Boys
Variables removed	LPA β (95% IC)	MVPA β (95% IC)	LPA β (95% IC)	MVPA β (95% IC)
BMI
Sedentary time (min.day^-1)	-0.105 (-0.251; 0.042)	-0.053 (-0.155; 0.261)	-0.008 (-0.194; 0.179)	-0.007 (-0.250; 0.236)
Bouts 1-14 (min.day^-1)	0.164 (-0.443; 0.114)	0.102 (-0.136; 0.340)	0.000 (-0.370; 0.370)	-0.012 (-0.271; 0.247)
Bouts 15-29 (min.day^-1)	-0.192 (-0.527; 0.142)	0.073 (-0.179; 0.326)	-0.004 (-0.407; 0.415)	-0.008 (-0.315; 0.298)
Bouts ≥30 (min.day^-1)	-0.221 (-0.563; 0.120)	0.044 (-0.184; 0.273)	0.015 (-0.344; 0.374)	0.003 (-0.283; 0.288)
WC
Sedentary time (min.day^-1)	-0.097 (-0.245; 0.051)	0.102 (-0.099; 0.303)	-0.001 (-0.138; 0.135)	0.016 (-0.171; 0.202)
Bouts 1-14 (min.day^-1)	0.006 (-0.267; 0.279)	0.051 (-0.180; 0.282)	0.005 (-0.267; 0.276)	0.005 (-0.188; 0.199)
Bouts 15-29 (min.day^-1)	0.002 (-0.324; 0.329)	0.047 (-0.196; 0.291)	0.060 (-0.244; 0.365)	0.061 (-0.172; 0.294)
Bouts ≥30 (min.day^-1)	0.068 (-0.266; 0.401)	0.112 (-0.109; 0.333)	0.035 (-0.227; 0.297)	0.036 (-0.178; 0.250)
CRF
Sedentary time (min.day^-1)	-0.039 (-0.202; 0.124)	0.034 (-0.202; 0.271)	-0.107 (-0.255; 0.040)	0.228 (0.040; 0.416)
Bouts 1-14 (min.day^-1)	-0.086 (-0.418; 0.246)	0.059 (-0.233; 0.350)	-0.151 (-0.421; 0.118)	0.213 (0.019; 0.406)
Bouts 15-29 (min.day^-1)	-0.058 (-0.473; 0.357)	0.087 (-0.201; 0.375)	-0.143 (-0.443; 0.157)	0.221 (-0.006; 0.448)
Bouts ≥30 (min.day^-1)	-0.131 (-0.542; 0.279)	-0.014 (-0.255; 0.282)	-0.077 (-0.339; 0.185)	0.287 (0.077; 0.497)

Note: Bold values denote significant associations (P<0.05). β = beta coefficient. BMI = Body mass index. CRF = Cardiorespiratory fitness. IC = Confidence interval. LPA = Light physical activity. MVPA = Moderate to vigorous physical activity. SB = Sedentary behavior. WC = Waist circumference.

Results were adjusted for socioeconomic status at baseline. peak growth velocity at baseline. sleep period at baseline. percentage in MVPA at baseline. BMI z-score at baseline and CRF z-score at baseline.

No competing interests reported.

Associations between substitution of sedentary behavior patterns to physical activity and cardiovascular risk factors in adolescents: a 3-year longitudinal study

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