Abstract

BACKGROUND

Studies in youth show an association between systolic blood pressure (SBP) reactivity to acute psychological stress and carotid artery intima-media thickness (CIMT). Submaximal exercise produces similar cardiovascular responses as acute psychological stress and may be a valuable tool to assess SBP reactivity in youth. However, it has not yet been determined whether SBP reactivity during submaximal exercise in youth is associated with CIMT, as it is during psychological stress.

METHODS

Fifty-four adolescents aged 13–16 years completed 3 visits. On one visit, adolescents completed three, 4-minute stages of increasing intensity on a treadmill. On another visit, adolescents completed measures of acute psychological stress reactivity (star tracing, speech preparation, speech). On a third visit, adolescents completed an ultrasound scan to measure CIMT.

RESULTS

SBP reactivity during lower- (β = 0.29, P = 0.03) and higher-intensity (β = 0.31, P = 0.02) submaximal exercise was associated with greater CIMT. SBP reactivity during higher-intensity submaximal exercise was positively associated with SBP reactivity during star tracing (β = 0.34, P = 0.01), speech preparation (β = 0.37, P = 0.007), and speech (β = 0.41, P = 0.003).

CONCLUSIONS

Greater SBP reactivity during submaximal exercise in healthy adolescents was associated with greater CIMT, similar to SBP reactivity during acute psychological stress. Adolescents who had greater SBP reactivity during exercise also demonstrated greater SBP reactivity during the psychological stress tasks. Given that exercise testing can be standardized for comparison across studies, submaximal exercise tests may be a valuable tool to assess SBP reactivity in youth.

Cardiovascular disease (CVD) is the leading cause of death in the United States.1 Advances in noninvasive imaging technology have allowed in vivo study of the structural and functional properties of the arterial system and can be used in pediatric populations to identify youth at greater risk for developing CVD later in life.2–6 Studying CVD risk factors in children and adolescents is important because the antecedents of CVD occur in youth,7–9 decades before any clinical signs or symptoms appear.4,8

A growing literature shows an association between cardiovascular reactivity (CVR) to acute psychological stress and subclinical CVD risk in youth, with several studies showing an association between systolic blood pressure (SBP) reactivity to laboratory psychological stress tasks and carotid artery intima-media thickness (CIMT) in independent samples of children9 and adolescents.10,11 However, the mechanisms by which transient increases in blood pressure (BP) may contribute to future CVD are not well understood. A limitation of assessing CVR in a laboratory setting is that CVR is greatly influenced by the characteristics of the stressor.12 A majority of studies in both adults and youth utilize psychological stress tasks to assess CVR. However, the use of different tasks between studies, in addition to subject factors that can affect CVR to psychological stressors (e.g., ability, motivation, previous experience with task), makes comparisons between studies challenging and may hinder identification of the precise mechanisms whereby CVR is associated with CVD risk.

To most efficiently increase our understanding of how CVR in youth contributes to future CVD, it will be important to employ stressors that can be replicated for comparison across studies, that produce cardiovascular responses similar in magnitude to those encountered in a natural environment, and that are useful in identifying individuals at greater risk for CVD throughout the lifespan.13 Submaximal exercise produces cardiovascular adjustments similar to that produced by acute psychological stress. Notably, the workload of submaximal exercise tests can be objectively determined, and BPs during submaximal intensities are comparable with the range of BPs encountered during everyday activities in youth. Moreover, in children, SBP reactivity to running has been shown to be more reliable over time than SBP reactivity to psychological stress.13 If SBP reactivity during submaximal exercise can identify youth at risk for future CVD as well as or better than traditional psychological stress tasks, the use of standardized exercise protocols may increase the reliability of CVR measurement. However, it is not yet known whether SBP reactivity during submaximal exercise is associated with CIMT in youth, as it is during psychological stress.

The purpose of this study was to test the following hypotheses: (i) SBP reactivity during submaximal exercise is associated with CIMT, similar to SBP reactivity during acute psychological stress and (ii) SBP reactivity during submaximal exercise is associated with SBP reactivity during psychological stress tasks.

METHODS

Participants

Fifty-four adolescents (n = 27 boys, n = 27 girls), aged 13–16 years served as subjects. Subjects included 47 white adolescents and 7 adolescents of other or mixed race. Adolescents were lower than the 85th percentile for body mass index (BMI). Adolescents did not have any conditions and were not taking any medications that would affect cardiovascular responses to exercise or psychological stress. Additionally, adolescents who had previously participated in a stress reactivity study were excluded. Parents provided written informed consent for their child’s participation, and the adolescent provided written assent. The study was approved by the University at Buffalo Social and Behavioral Sciences Institutional Review Board. Adolescents were debriefed after completing the study.

Procedures

Adolescents were tested on 3 days: exercise day, stress day, and CIMT measurement day. The order of the exercise day and stress day were counterbalanced across subjects. CIMT was measured on a separate day at least 24 hours after participants completed the exercise and stress protocols. Adolescents were instructed not to eat anything in the 3 hours prior to each lab visit and not to participate in any intense physical activity or consume any caffeine the day of or the day before each lab visit. The exercise day and stress day were scheduled at least 24 hours apart and at the same time of day.

At the first appointment, adolescents were measured for height and weight. Girls reported the date of their last menstrual cycle. On both the exercise and the stress days, adolescents were fitted with a Suntech Tango BP cuff (Morrisville, NC). Adolescents rested for 10 minutes. BP was taken twice during the last 2 minutes of baseline on both days. The average BP on each day served as the baseline BP value.

Measurement

Medical history and demographic variables.

Current medical problems, psychiatric diagnoses, and medications were assessed by phone screen. Socioeconomic status (SES) was assessed by the parent completing a questionnaire.14

Anthropometrics.

Body weight was measured to the nearest 0.01kg. Height was measured with a stadiometer. BMI was calculated according to the following formula: BMI = kg/m2. BMI percentile was calculated in relationship to the 50th BMI percentile for adolescents based on sex and age.

Blood pressure.

During exercise and stress protocols, BP was measured with a Suntech Tango monitor. Adhesive electrodes were attached to the adolescent’s chest (one below each collar bone and one below right rib area). The Suntech Tango is a valid and reliable measure of BP during rest and exercise.15 Measurement of BP followed published guidelines16 regarding cuff length and width, placement of the cuff around the arm 2.5cm above the antecubital space, and seating of the cuff on the arm by inflating and deflating the cuff before taking any measurements.

Submaximal exercise.

Adolescents completed three, 4-minute stages of increasing intensity (3–5 metabolic equivalents (METs)) on a treadmill. Four-minute stages were used to ensure the subject reached a steady state. Before beginning the protocol, subjects were given a three-minute warm-up. BP was measured twice during the last 2 minutes of each exercise stage. The average BP during the last 2 minutes of each exercise stage was used as data.

Psychological stress tasks.

Adolescents completed a mirror star tracing task and an interpersonal speech task. The order of the stress tasks was counterbalanced across subjects. Subjects were given a 5-minute rest between tasks.

For the mirror star tracing task, adolescents were instructed to slide a computer mouse to control a cursor to trace a 5-sided star. Both horizontal and vertical movements of the cursor were programmed to be reversed relative to movement of the mouse. Adolescents were instructed to trace the star as quickly as possible without allowing the cursor to stray out-of-bounds. Errors were noted with a red X that flashed on the screen and a beeping sound. Adolescents were instructed to complete as many stars as possible with as few errors as possible in 4 minutes. BP was measured twice during the last 2 minutes of the task.

For the interpersonal speech task, adolescents were given 4 minutes to prepare and 3 minutes to deliver a speech about why they were a good friend. Adolescents were informed that their speeches would be recorded and judged for honesty, believability, and confidence. After adolescents stop speaking, an additional ad lib period was provided in which adolescents were encouraged to continue talking by adding any additional information that others should know about them. BP was measured twice during the last 2 minutes of the speech preparation period and the actual speech.

Carotid artery intima-media thickness.

Utrasound measures were performed with the Biosound Esaote (MyLab 25 Gold) ultrasound imaging machine (Biosound Esaote, Inc., Indianapolis, IN) and with a 7.5 MHz transducer. The images were recorded on super VHS videotapes using an S-VHS cassette recorder and analyzed offline. Standardized longitudinal images were acquired of the near and far walls of the distal 1.0cm portion of the common carotid, 1.0cm of the carotid bifurcation, and the proximal 1.0cm of the internal carotid arteries. The maximum intima-media thickness was measured in the common carotid artery, bulb, and internal carotid artery from 3 interrogation angles on the right and left side. After selection of the single maximum intima-media thickness from the 3 angles of the near and far wall in each anatomical segment (1×2 × 3 = 6 on right and left), the mean values of these 12 single maximum intima-media thickness values were computed as the mean maximum CIMT.

Analytic plan.

Separate 1-way analyses of variance were used to test differences between boys and girls for participant characteristics. Separate 2-way repeated measures analyses of variance (sex, day) were used to test differences in baseline SBP of the boys and girls on the exercise and stress days, with day treated as a repeated measures factor. To determine SBP reactivity during exercise, change scores were calculated by subtracting the average value taken during the last 2 minutes of baseline on the exercise day from the average value during the last 2 minutes of the exercise stage. Separate change scores were calculated for the lowest- (3 METs) and highest-intensity (5 METs) exercise that all subjects completed. To calculate SBP reactivity during the psychological stress tasks, the average baseline SBP on the stress day was subtracted from the average value taken during the last 2 minutes of each psychological stress task (star tracing, speech preparation, speech). Sequential regression was used to determine whether SBP reactivity during submaximal exercise significantly predicted CIMT, independent of age, sex, SES, BMI percentile, and baseline SBP. These covariates were selected based on research indicating these factors are correlated with CVD pathogenesis, exercise responses, and cardiovascular reactivity to psychological stress in youth.17–19 Menstrual cycle of the girls was also considered as a covariate but was not included in the final analyses because it was not significantly associated with girls’ CIMT or exercise SBP reactivity and would preclude analyses using the full sample of boys and girls. Linear regression was used to determine the association of SBP reactivity during exercise with SBP reactivity during each of the psychological stress tasks. In exploratory fashion, we used separate sequential regression analyses to determine whether SBP reactivity during submaximal exercise significantly predicted CIMT beyond psychological stress SBP reactivity by including covariates and SBP reactivity of 1 psychological stress task in the model. We then used backwards stepwise regression including all tasks (star tracing, speech preparation, speech, 3 METs exercise, 5 METs exercise) to determine which task or set of tasks best predicted CIMT. An alpha of 0.05 for was used for all analyses.

RESULTS

Participant characteristics are shown in Table 1. Boys had greater CIMT (P = 0.005) than girls. There were no other sex differences for any physical or demographic characteristics. Baseline SBP was not different on the exercise and stress days between the boys and girls. SBP data was missing for 1 subject during 3 METs exercise and for 2 subjects during 5 METs exercise.

Table 1.

Participant characteristics of the boys and girls

Characteristics  Boys, n = 27 Girls, n = 27 
Age, y 14.3 ± 1.1 14.4 ± 1.1 
Weight, kg 56.1 ± 12.7 56.3 ± 6.0 
Height, cm 167.1 ± 16.1 163.0 ± 14.4 
BMI% 40.6 ± 21.7 52.8 ± 21.7 
SES 48 ± 11 51 ± 9 
CIMTa, mm 0.663 ± 0.040 0.630 ± 0.043 
Stress baseline SBP, mmHg 106 ± 11 108 ± 10 
Exercise baseline SBP, mmHg 108 ± 11 108 ± 8 
Characteristics  Boys, n = 27 Girls, n = 27 
Age, y 14.3 ± 1.1 14.4 ± 1.1 
Weight, kg 56.1 ± 12.7 56.3 ± 6.0 
Height, cm 167.1 ± 16.1 163.0 ± 14.4 
BMI% 40.6 ± 21.7 52.8 ± 21.7 
SES 48 ± 11 51 ± 9 
CIMTa, mm 0.663 ± 0.040 0.630 ± 0.043 
Stress baseline SBP, mmHg 106 ± 11 108 ± 10 
Exercise baseline SBP, mmHg 108 ± 11 108 ± 8 

Data are Mean ± SD.

Abbreviations: BMI%, body mass index percentile, calculated in relationship to the 50th BMI percentile for adolescents based on their age and sex; CIMT, carotid artery intima media thickness, measured as the mean maximum IMT; SES, socioeconomic status, an SES of 40 through 50 is equivalent to medium size business owners, minor professionals and technical jobs, such as computer programmers, real estate agents, sales managers, social workers and teachers.

aBoys were significantly different than girls (P < 0.05).

Table 2 shows the association between SBP reactivity during 3 METs exercise and CIMT. SBP reactivity during 3 METs exercise significantly added to the prediction of CIMT, when controlling for age, sex, SES, BMI percentile, and baseline SBP (β = 0.29, P = 0.03, R2 change = 0.08). Table 3 shows the association between SBP reactivity during 5 METs exercise and CIMT. SBP reactivity during 5 METs exercise significantly added to the prediction of CIMT, when controlling for step 1 covariates (β = 0.30, P = 0.03, R2 change = 0.09).

Table 2.

Hierarchical linear regression to predict carotid artery intima-media thickness from systolic blood pressure (SBP) reactivity during lower intensity exercise

Predictors Regression coefficient Standard error Standardized regression coefficient P value ΔR2 
Step 1a     0.21 
 Age 0.006 0.005 0.14 0.30  
 Sex −0.04 0.01 −0.47 0.001  
 SES 0.001 0.001 0.12 0.37  
 BMI% 0.000 0.000 0.16 0.24  
 Baseline SBP 0.001 0.001 0.19 0.16  
Step 2b     0.08 
  ΔSBPc 0.001 0.000 0.29 0.03  
Predictors Regression coefficient Standard error Standardized regression coefficient P value ΔR2 
Step 1a     0.21 
 Age 0.006 0.005 0.14 0.30  
 Sex −0.04 0.01 −0.47 0.001  
 SES 0.001 0.001 0.12 0.37  
 BMI% 0.000 0.000 0.16 0.24  
 Baseline SBP 0.001 0.001 0.19 0.16  
Step 2b     0.08 
  ΔSBPc 0.001 0.000 0.29 0.03  

Abbreviations: BMI%, body mass index percentile; SES, socioeconomic status.

aPredictors: age, sex, SES, BMI%, baseline SBP. bPredictors: age, sex, SES, BMI%, baseline SBP, ΔSBP. cΔSBP = (average SBP during 3 metabolic equivalents) – (average baseline SBP on exercise day).

Table 3.

Hierarchical linear regression to predict carotid artery intima-media thickness from systolic blood pressure (SBP) reactivity during higher intensity exercise

Predictors Regression coefficient Standard error  Standardized regression coefficient P value ΔR2 
Step 1a     0.23 
 Age 0.006 0.005 0.16 0.23  
 Sex −0.04 0.01 −0.45 0.002  
 SES 0.001 0.001 0.13 0.34  
 BMI% 0.000 0.000 0.13 0.37  
 Baseline SBP 0.001 0.001 0.24 0.08  
Step 2b     0.09 
  ΔSBPc 0.001 0.000 0.31 0.02  
Predictors Regression coefficient Standard error  Standardized regression coefficient P value ΔR2 
Step 1a     0.23 
 Age 0.006 0.005 0.16 0.23  
 Sex −0.04 0.01 −0.45 0.002  
 SES 0.001 0.001 0.13 0.34  
 BMI% 0.000 0.000 0.13 0.37  
 Baseline SBP 0.001 0.001 0.24 0.08  
Step 2b     0.09 
  ΔSBPc 0.001 0.000 0.31 0.02  

Abbreviations: BMI%, body mass index percentile; SES, socioeconomic status.

aPredictors: age, sex, SES, BMI%, baseline SBP. bPredictors: age, sex, SES, BMI%, baseline SBP, ΔSBP. cΔSBP = (average SBP during 5 metabolic equivalents) – (average baseline SBP on exercise day).

The unadjusted relationships between SBP reactivity during 5 METs exercise and SBP reactivity during the psychological stress tasks is presented in Figure 1. SBP reactivity during 5 METs exercise was significantly associated with SBP reactivity during star tracing (β = 0.34, P = 0.01), speech preparation (β = 0.37, P = 0.007), and speech (β = 0.41, P = 0.003). When including age, sex, SES, and BMI percentile as covariates, SBP reactivity during star tracing (β = 0.32, P = 0.02), speech preparation (β = 0.40, P = 0.005), and speech (β = 0.44, P = 0.002) remained significantly associated with SBP reactivity during 5 METs exercise. Similar associations were observed between SBP reactivity during 3 METs exercise and SBP reactivity during star tracing (β = 0.28, P = 0.04), speech preparation (β = 0.36, P = 0.008), and speech (β = 0.26, P = 0.06). However, when covarying for age, sex, SES, and BMI percentile, only SBP reactivity during speech preparation (β = 0.35, P = 0.01) remained significantly associated with SBP reactivity during 3 METs exercise (data not shown).

Figure 1.

Unadjusted associations between systolic blood pressure (SBP) reactivity during exercise (5 metabolic equivalents) and (a) SBP reactivity during star tracing (β = 0.34, P = 0.01), (b) SBP reactivity during speech preparation (β = 0.37, P = 0.007), and (c) SBP reactivity during speech (β = 0.41, P = 0.003).

Figure 1.

Unadjusted associations between systolic blood pressure (SBP) reactivity during exercise (5 metabolic equivalents) and (a) SBP reactivity during star tracing (β = 0.34, P = 0.01), (b) SBP reactivity during speech preparation (β = 0.37, P = 0.007), and (c) SBP reactivity during speech (β = 0.41, P = 0.003).

Additional analyses tested whether exercise SBP reactivity significantly predicted CIMT when one of the psychological stress SBP reactivity measures was included in the model. For 5 METs exercise, the association between SBP reactivity and CIMT was largely unchanged when including any one of the psychological stress tasks in the model. However, for 3 METs exercise, including speech preparation into the model significantly attenuated the relationship between 3 METs SBP reactivity and CIMT. When SBP reactivity to all tasks was considered in a backwards regression analysis, only SBP reactivity to 5 METs exercise was selected as a significant (β = 0.001, P = 0.004) predictor of CIMT.

DISCUSSION

To our knowledge, this was the first study to demonstrate that SBP reactivity during submaximal exercise was associated with greater CIMT in youth, similar to acute psychological stress. In addition, we have demonstrated that SBP during submaximal exercise is associated with SBP reactivity during acute psychological stress in healthy adolescents. Notably, SBP reactivity during 5 METs exercise demonstrated the strongest and most consistent associations with both psychological stress SBP reactivity and CIMT.

Similar cardiovascular adjustments are observed during both submaximal exercise and acute psychological stress. However, few studies have examined whether CVR during submaximal exercise is associated with greater CVD risk, similar to CVR reactivity during psychological stress. Based on previous research demonstrating that greater SBP reactivity during acute psychological stress is associated greater CIMT in youth,9–11 we hypothesized that a similar relationship would exist between submaximal exercise SBP reactivity and CIMT in our sample of healthy adolescents. As we hypothesized, greater SBP reactivity during submaximal exercise was significantly associated with greater CIMT. Additionally, when we included SBP reactivity during both exercise and psychological stress in regression models predicting CIMT, 5 METs exercise emerged as the strongest and most consistent predictor of CMIT. Thus, submaximal exercise may be a valuable tool to assess CVR and identify youth at greater risk for future CVD.

Adolescents who had a greater increase in SBP during submaximal exercise were also more likely to have a greater increase in SBP during the psychological stress tasks. This is consistent with previous work in youth demonstrating similarities in CVR between psychological stress and other types of physical stress (e.g., hand grip, postural change, running).13,20,21 The high correlation between SBP reactivity during submaximal exercise and psychological stress and their similar associations with CIMT suggest that similar systemic reactions to both submaximal exercise and psychological stressors are being observed.

The mechanisms whereby greater SBP reactivity in youth may contribute to subclinical CVD are not well understood. One proposed mechanism is that repeated exposure to transient increases in BP and resultant shear stress over time may cause damage to the arterial system, eventually altering arterial structure and function.22 However, most studies assessing the relationship between CVR and subclinical CVD in youth, including this study, use cross-sectional study designs, which prohibit conclusions about causality. Only 1 study23 that we are aware of has examined the relationship between CVR and CIMT longitudinally over a 3year period in adolescents. Future work is needed to determine how CVR in youth is associated prospectively with CIMT in adulthood and the directionality of this relationship.

Adolescents encounter numerous stressors in their daily lives (e.g., academic, social, physical). BP responses during laboratory stress tasks are considered stable individual characteristics24,25 and are hypothesized to reflect an individual’s BP response to stressors in the natural environment. Thus, utilizing valid and reliable stressors to capture this BP response in a laboratory setting is crucial. Although psychological stress tasks are commonly used to assess CVR, the responses to these tasks can be affected by numerous factors related to the subject, the task, and the environment. Moreover, although CVR to psychological stress tasks has been shown to be reliable over time in youth for periods up to 4 years,24,26 few studies have assessed CVR longitudinally over longer time periods and into adulthood. The relevance or perception of psychological stressors in youth may change from youth to adulthood, which could reduce reliability of CVR measurement over longer time periods. A methodological advantage of submaximal exercise tests to assess CVR is that factors known to influence cardiovascular responses during exercise (e.g., caffeine, smoking, medications) are relatively easy to control for or measure in experimental studies. Additionally, the workload of submaximal exercise tests can be objectively determined. Utilization of submaximal exercise to assess CVR in future studies could help standardize protocols and facilitate comparison of CVR over time and between studies.

This study had several limitations. We included only healthy, normal-weight adolescents who were not physically trained. Furthermore, although we included youth from a variety of racial/ethnic backgrounds, our sample was predominantly white. Thus, the results may not generalize to youth with preexisting cardiovascular diseases, overweight youth, minority youth, or physically trained youth. A treadmill protocol was used for exercise, but adolescents were seated during psychological stress testing. It would be advantageous to compare CVR during psychological stress to exercise in a seated position, such as bicycling, because posture can affect BP.27,28 Importantly, we did not investigate any mechanisms that might account for the relationships of SBP reactivity with CIMT.

In conclusion, SBP reactivity during submaximal exercise and psychological stress were highly correlated with each other and showed similar associations with CIMT in healthy adolescents. Further work is needed to identify the precise mechanisms whereby SBP reactivity is associated with subclinical CVD in youth and to determine how cardiovascular responses during submaximal exercise generalize to real-world cardiovascular responses. Given that exercise testing can be standardized for comparison across studies, submaximal exercise tests may be a valuable tool to assess CVR in youth.

DISCLOSURE

The authors declared no conflict of interest.

ACKNOWLEDGMENTS

We thank Vivian Boyd and Debbie Saltino for their technical assistance in completing the ultrasound measurements. We thank the Mark Diamond Research Fund for their financial support which helped to reimburse participants.

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