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Time Course of Endothelial Adaptation After Acute and Chronic Exercise in Patients With Metabolic Syndrome

Tjønna, Arnt E; Rognmo, Øivind; Bye, Anja; Stølen, Tomas O; Wisløff, Ulrik

Journal of Strength and Conditioning Research: September 2011 - Volume 25 - Issue 9 - p 2552-2558
doi: 10.1519/JSC.0b013e3181fb4809
Original Research
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Tjønna, AE, Rognmo, Ø, Bye, A, Stølen, TO, and Wisløff, U. Time course of endothelial adaptation after acute and chronic exercise in patients with metabolic syndrome. J Strength Cond Res 25(9): 2552-2558, 2011—Clustering of cardiovascular risk factors may lead to endothelial dysfunction. Physical exercise is an important factor in prevention and treatment of endothelial dysfunction. We wanted to determine the time course of adaptation to a single bout of exercise at either high or moderate intensity upon endothelial function both before and after a 16-week fitness program in patients with metabolic syndrome. Twenty-eight patients with metabolic syndrome participated in the study and were randomized and stratified (according to age and sex) into an aerobic interval exercise training group (AIT, n = 11), a continuously moderate-intensity exercise training group (CME, n = 8) or to a control group (n = 9). Flow-mediated dilatation (FMD) was determined at baseline, immediately, 24, 48, and 72 hours after 1 bout of exercise and repeated after 16 weeks of exercise. In the untrained state, FMD improved from 5 to 11% (p = 0.003) immediately after a single bout of aerobic interval training (AIT), an effect lasting 72 hours postexercise. In comparison, continuous moderate exercise (CME) improved FMD immediately after a single bout of exercise from 5 to 8% (p = 0.02), an effect lasting 24 hours postexercise (group difference, p < 0.001). In the trained state, a single bout of AIT resulted in a 2% (p = 0.007) acute increase of FMD lasting 48 hours postexercise. The CME increased FMD by 3% (p < 0.01), an effect lasting 24 hours postexercise (group difference p = 0.0012). Blood glucose level decreased after 1 single bout of AIT in the untrained state (p < 0.05), and the effect lasted at least 72 hours postexercise (p < 0.01). Acute CME decreased blood glucose with normalization of the values 24 hours postexercise (p < 0.01). A single bout of exercise in the trained state reduced fasting blood glucose by 10% (p < 0.05) after both AIT and CME. Exercise training, especially high intensity, thus appears to be highly beneficial in reducing blood glucose and improving endothelial function.

Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway

A.E. Tjønna and Ø. Rognmo share first authorship.

Address correspondence to Arnt E. Tjønna, arnt.e.tjonna@ntnu.no.

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Introduction

Metabolic syndrome is a clustering of cardiovascular risk factors (9). The prevalence of metabolic syndrome is rapidly increasing and affects approximately one-quarter of the US population ≥20 years and is increasing with age (6). Accumulation of the risk factors associated with metabolic syndrome may result in endothelial dysfunction (2,12), an early indicator of the progress of atherosclerosis (5). Physical exercise is recognized as an important factor in the prevention and treatment of metabolic syndrome and in reversing an endothelial dysfunction (16,17,18,20,22,32).

Recently, we reported that 16 weeks of high-intensity exercise training was superior to moderate-intensity training in reversing endothelial dysfunction and risk factors related to the metabolic syndrome (32). However, the effect of acute exercise upon endothelial function in patients with metabolic syndrome is less known. Tyldum et al. (33) recently demonstrated that endothelial function assessed as flow-mediated dilatation (FMD) was substantially reduced after ingestion of a high fat meal (HFM) and that exercise 16-18 hours before HFM afforded an intensity-dependent protection against a transient endothelial dysfunction. Whether the link between vascular improvements and exercise intensity is apparent with a single bout of exercise in metabolic syndrome patients, where FMD is permanently impaired, is currently unknown. Also, it is not known whether an acute bout of exercise affects endothelial function in patients with metabolic syndrome who have already been through an extensive exercise-training regimen.

The aim of this study was to determine the time course of adaptation to a single bout of exercise at either high or moderate intensity upon FMD both before and after a 16-week fitness program in patients with metabolic syndrome. We hypothesized that aerobic interval training (AIT) would induce larger improvements on FMD compared to continuous moderate exercise (CME) after both acute and chronic exercises.

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Methods

Experimental Approach to the Problem

Patients were randomized and stratified (according to age and gender) into an aerobic interval exercise training group (AIT, n = 11), a continuously moderate-intensity exercise training group (CME, n = 8) or to a control group (n = 9) (flow chart). The randomization code was developed using a computer random number generator to select random permuted blocks. The unit of Applied Clinical Research at the university carried out all randomization procedures to secure complete blinded randomization. Both exercise groups performed endurance training, walking or running “uphill” on a treadmill 3 times per week for 16 weeks. The AIT warmed up for 10 minutes at ;70% of maximal heart rate (HRmax) before performing 4 3 4-minute intervals at 90-95% of HRmax, with a 3-minute active recovery at ;70% of HRmax between each interval, and a 5-minute cool-down period, giving a total of 40 minutes. To equalize training volume (i.e., spending the same amount of kcals each session) between the 2 groups, the CME group had to perform 47 minutes at ;70% of HRmax each exercise session (for calculation, see [31]). The control group followed the advice of their family doctor.

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Subjects

Twenty-eight patients with metabolic syndrome defined according to the World Health Organization definition (36) took part in the study. All subjects provided written, informed consent, and the regional committee for medical research ethics approved the study protocol. The subjects in this study are the same subjects used in a previous publication (33). All subjects were sedentary with,1 reported exercise session each week; this did not differ between groups. The main test period was during springtime, although we had to supply once during the following autumn. The research has been carried out according to the Declaration of Helsinki (2000).

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Endothelial Function

Endothelial function was determined at baseline, immediately, 24, 48,, and 72 hours after a single bout of exercise, and the same was done after 16 weeks of exercise.

Endothelial function was measured as FMD using high-resolution vascular ultrasound (14 MHz echo Doppler probe, Vivid 7 System, GE Vingmed Ultrasound, Horten, Norway) according to the current guidelines (3,29). All equipment was validated and calibrated by the person responsible for the test, before every test session. The measurements were made on the brachial artery approximately 4.5 cm above the antecubital fossa. All measurements were performed in the morning after an 8-hour fast. In addition, subjects were not allowed to use nicotine and coffee, or any other caffeine-containing beverages for 12 hours preceding testing. In consultation with a physician and participants, all unnecessary medication was not given at least 48 hours before starting the test session. After a 10 minutes of rest in the supine position in a quiet, air-conditioned room with a stable temperature of 22 ± 1°C, the internal diameter of the brachial artery was assessed. Thereafter, we inflated a pneumatic cuff (Hokanson SC10, Bellevue, WA, USA) on the upper arm to 250 mm Hg for 5 minutes and deflated it to create an ischemia-induced hyperemic elevated blood flow. Data were recorded 10 seconds after cuff release to measure peak blood flow, whereas artery diameter was recorded every 30 seconds for 5 minutes. The subjects then rested for 5 minutes until the baseline diameter was restored. To avoid confounding effects of arterial compliance and cyclic changes in arterial dimension, all measurements were obtained at the peak of the R-wave in the electrocardiogram. Diameters were measured from intima to intima using calipers with a 0.1-mm resolution. The mean of 3 diameter measurements and flow measurements was used in the calculation of FMD, glyceryl trinitrate (GTN), and flow responses. Maximal dilatation was in each case observed 1 minute after cuff release in all groups, and those data are therefore presented in the results. Shear rate was calculated as blood flow velocity (cm·s−1) divided by diameter (cm) according to Pyke and Tschakovsky (27), and all FMD data are corrected for shear rate. All ultrasound images were analyzed in random order, using EchoPACtm (GE Vingmed Ultrasound AS) by an investigator who was blinded to the group allocation of the subjects. The reproducibility and repeatability of the method have been established previously (13), and the coefficient of repeatability (14) of baseline brachial diameter measurements in our laboratory is 4%.

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Blood Analyses

If not otherwise stated, all blood analyses were performed using standard local procedures at St. Olavs Hospital, Trondheim, Norway. Total nitrite (NO2) concentration was quantified using a commercially available assay for nitric oxide (NO) detection (R&D systems, Inc., Minneapolis, MN, USA).

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Statistical Analyses

The primary outcome variable was FMD, and prior experience suggests an SD of about 1.5-2 (32). No formal sample size calculation was done, but with 8 subjects in each group, a standardized within-group difference of 0.1 mm may be detected using a paired t-test with 80% power, at a significance level of 5% (20).

Comparison of continuous variables was done according to design (number of groups, paired or unpaired), using the linear model with correction for baseline value (analysis of covariance) (34). Wilcoxon's, Mann-Whitney's, or Kruskal-Wallis' nonparametric procedures were used if the assumption of normality and homogeneity of variance was in doubt. The potential for spurious significance because of multiple testing and a large number of variables relative to subjects is recognized, but because this was a pilot study, no correction for multiple comparisons was applied. Reported p values are 2 sided. Values ≤0.05 are considered as statistically significant. SPSS®16.0 (SPSS Inc. Chicago, IL, USA) was employed for all analyses.

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Results

Baseline Characteristics

At pretest, no differences in any physiological parameter between the groups (Table 1) were observed. Furthermore, no changes in the control group throughout the study were seen, and data are therefore not shown.

Table 1

Table 1

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Clinical Follow-Up

As previously described (32), despite no diet alterations during the 16-week intervention period (data not shown), AIT and CME patients exhibited a slight reduction of 3 and 4%, respectively, in body weight (both p < 0.05), and body mass index (both p < 0.05). Similarly, the waist width was reduced by 5 and 6 cm in AIT and CME, respectively (p < 0.05) (33).

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Endothelial Function

Untrained State

No differences in resting brachial artery diameter were observed between groups, and 16 weeks of exercise did not alter the resting diameter. The FMD increased from 5 to 11% (p = 0.003, Figure 1A) immediately after a single bout of AIT, and the effect lasted 72 hours. In comparison, CME improved FMD immediately after a single bout of exercise from 5 to 8% (p = 0.02, Figure 1B), but this effect lasted only for 24 hours (group difference, p < 0.001, Figure 1B). No change in FMD was observed in the control group at the corresponding time points (Figure 1C).

Figure 1

Figure 1

On average, a single bout of AIT, NO level significantly increased with 34.8% an effect lasting 72 hours postexercise (p < 0.01). The CME increased the NO level in the blood with 1.3%, which lasted 72 hours postexercise (not significant) group differences (p = 0.07) (Figure 2A, B).

Figure 2

Figure 2

Furthermore, blood glucose decreased after 1 single bout of AIT in untrained individuals (p < 0.05), and the effect lasted at least 72 hours postexercise (p < 0.01, Figure 3A). Acute CME decreased blood glucose with normalization of the values 24 hours postexercise (Figure 3B). Acute effect of high-density lipoprotein (HDL)-cholesterol levels did not change in either of the groups (data not shown).

Figure 3

Figure 3

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Trained State

Sixteen weeks of AIT and CME improved FMD by 9% (p < 0.001) and 5% (p < 0.001), respectively (group difference, p < 0.001) (32) . The acute effects of a single bout of exercise after 16 weeks of endurance training were less pronounced, although a single bout of AIT resulted in a 2% (p = 0.007, Figure 1D) acute increase of FMD lasting 48 hours postexercise. CME increased FMD by 3% (p < 0.01, Figure 1D), an effect that was absent 24 hours postexercise (group difference p = 0.0012). No changes in FMD were seen in the control group during the corresponding time points (Figure 1F).

The intervention period induced an increased availability of NO in AIT (36 ± 3%; p = 0.03) but not CME (p = 0.37; group difference, p < 0.05) (33). The effect of one single bout of exercise in the trained state with metabolic syndrome induced no changes in NO availability at any time points in either group (Figure 2C or D).

Fasting glucose after 16 weeks of endurance training was reduced after AIT (p < 0.05), whereas CME experienced an slightly increase (32). Additionally, we saw that a single bout of exercise in the trained state reduced fasting blood glucose by ∼10% (p < 0.05) after both AIT and CME, and the effect lasted up to 72 hours postexercise. The HDL cholesterol increased by ∼25% after 16 weeks of AIT (p < 0.05) but remained unaltered in the other groups (32). No effect of either acute AIT or CME induced changes in HDL in the trained and untrained states. Furthermore, in the untrained state, we saw a slight increase in total antioxidant status after acute exercise in both AIT and CME (both +3%) lasting 72 hours postexercise, although not significant (data not shown). But in the trained state, no change occurred.

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Blood Pressure

Untrained State

A single bout of AIT in untrained individuals acutely reduced systolic blood pressure (SBP) with −7 mm Hg, an effect lasting for 72 hours (p < 0.05, data not shown), whereas CME in untrained individuals induced no significant response. Furthermore, diastolic blood pressure (DBP) decreased significantly after AIT and the effect sustained 72 hours postexercise (p < 0.05), whereas no significant changes occurred in the CME group.

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Trained State

Both AIT and CME decreased SBP and DBP after 16 weeks of endurance training with ∼10 mm Hg (both groups, p < 0.05) and DBP with ∼6 mm Hg (AIT, p < 0.05; CME, p < 0.24), respectively (33). A single bout of AIT in trained individuals reduced SBP (from 135 to 119 mm Hg, p < 0.01) and DBP (from 89 to 80 mm Hg, p < 0.01) pressure acutely after exercise, but the effect was gone 24 hours postexercise. No changes were seen after CME.

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Discussion

The major findings in this study were that endothelial function improves dramatically after 1 single bout of exercise, and that the response is different between untrained vs. trained individuals.

It is well established from previous studies that systematic exercise training improves endothelial function (11,31,32), whereas the acute effects of exercise are less studied. Previous studies in individuals with reduced endothelial function because of age or cardiovascular risk factors indicate that acute effects of exercise improve the endothelial function (1,15,24,26,33), but conflicting results exist (14). To our knowledge, only 2 previous studies have examined the effect of different exercise intensities upon FMD (14,33), and data from these 2 studies are also conflicting. Although Tyldum et al. (33) demonstrate greater improvements in FMD after an AIT session compared to CME and controls, Harris et al. demonstrate that exercise intensity did not influence the FMD response (14). The reason for these discrepancies is currently not known but may be because of the different intensities of exercise training applied in the 2 studies and need to be addressed in future studies.

Endothelial dysfunction is characterized by a reduction in the bioavailability of vasodilators, in particular NO, prostacyclin, etc., which lead to impaired vessel responsiveness. Several studies (11,32) have reported an increase in NO bioavailability after a training intervention, but few, if any, have reported anything about time course of adaptation after a single bout of exercise in trained or untrained individuals. Our results show that AIT significantly increases NO bioavailability acutely after a single bout of exercise in the untrained state, an effect lasting 72 hours postexercise, whereas CME had a small but not significant response acutely after exercise in the untrained state. This could be one of the main reasons why AIT induces larger improvements in endothelial function acutely after 1 single bout of exercise compared to CME.

Hyperglycemia is one of the major factors in the development of endothelial dysfunction in patients with metabolic syndrome (23), but the relationship between endothelial vasodilator dysfunction and inflammatory markers and their changes in response to glucose loading is not fully understood yet. Although the formation of advanced glycation end products is an important biochemical abnormality accompanying inflammation, the mechanism underlying this phenomenon is likely to be multifacorial, involving the pathway of diacylglycerol-protein kinase C, which activates superoxide-producing enzymes (nicotinamide adenine dinicleotide phosphate, leading to uncoupling of endothelial nitric oxide synthase (eNOS), which inhibits the activity and expression of NO (10). Our results indicate that 1 session of AIT in untrained individuals decreases the fasting levels of glucose, with an effect lasting for 72 hours postexercise, which may explain the increased levels of NO and improved FMD after exercise. Fasting glucose, NO, and FMD did not improve to a similar level after CME in untrained individuals.

The HDL cholesterol promotes the production of the atheroprotective signaling molecule NO by upregulating eNOS expression, which is important in the pathways regulating endothelial function (21). Previous studies have reported increased expression of HDL cholesterol after a single bout of exercise although these changes occur from 24 hours and last 48 hours postexercise (4,8). Surprisingly, in our study, we did not see any change in HDL cholesterol in either of the training groups acutely after 1 single bout of exercise, in the untrained state.

Hypertension is a factor underlying metabolic syndrome, and we know that there is a positive relationship between cardiovascular disease risk and blood pressure (BP). The elevated risk occurs already at a BP of 115/75 mm Hg and doubles for each 20/10-mm Hg increase (25). Although there is an agreement that dynamic aerobic exercise training reduces resting BP in individuals with normal BP and in those with hypertension, it seems like the reduction is more pronounced in hypertensive than in normotensive subjects (25,32). Our study demonstrates that when comparing CME and AIT in untrained individuals with metabolic syndrome, the SBP decreases immediately after 1 bout of AIT with an effect lasting for 72 hours postexercise, whereas CME only had a significant decrease 48 hours postexercise. These findings are in line with those of previous reports, indicating that the peak exercise hypotension is greater and lasts longer after more intense exercise (7,28). Looking at DBP after 1 single bout of exercise, CME only had a minor decrease ∼3 mm Hg (not significant) lasting 72 hours postexercise, whereas AIT decreased DBP with ∼6 mm Hg (p < 0.05) an effect lasting 72 hours postexercise.

Sixteen weeks of exercise training improved baseline FMD in both AIT and CME (32), and the effect of a single bout of exercise after 16 weeks of training was less pronounced compared with in the untrained individuals. This indicates that more fit individuals do not respond to an acute bout of exercise on FMD in the same way as unfit individuals (13,30). Even though the baseline FMD improved before the exercise bout in these individuals, we saw an acute FMD elevation of 2.1% (Figure 1C) in the AIT group that lasted for 48 hours. The CME group showed no FMD response to acute exercise in the trained state (Figure 1D). These results are in line with the findings of Haram et al. (13), who reported improved endothelium-dependent dilatation in chronically trained rats 12-24 hours after a single bout of exercise, with an effect lasting 1 week. The 16 weeks of training induced a significant NO increase after AIT, whereas no change occurred after CME (32). Given the small increase in FMD, we did not see a significant increase in NO after a single bout of exercise in trained individuals. This may also be because of unchanged results in fasting glucose. As mentioned in untrained individuals, there was a clear link between fasting glucose, NO, and FMD. But in trained individuals, we did not see this clear relationship, which may indicate that there are other unknown factors relating to the increased FMD after AIT. This needs to be further investigated.

The BP variables in the trained state showed that AIT had significant decreases acutely after 1 bout of exercise, but the effect was gone 24 hours postexercise, whereas CME induced no change. These data are in line with previous findings indicating that endurance training in normotensive subjects is not as pronounced as in hypertensive patients (25).

This study demonstrates that high-intensity exercise training is superior to moderate-intensity training in improving FMD in both untrained and trained individuals with metabolic syndrome. Exercise training, especially high intensity, thus appears to be highly beneficial in improving FMD. These findings may have important implications for exercise training in rehabilitation programs. Although multicenter prospective studies using exercise with high relative intensity to treat patients with the metabolic syndrome are needed to advance our conclusions, we propose that high-intensity exercise training programs may yield more favorable results than those with low-to-moderate intensities.

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Practical Applications

This study demonstrates that 1 single bout of AIT and CME induces a positive effect upon endothelial function in patients with metabolic syndrome, although with a larger and longer lasting effect after AIT.

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      Keywords:

      aerobic interval training; continuous moderate exercise; flow-mediated dilatation; endothelial dysfunction

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