Cardiovascular diseases (CVD) remain the leading cause of death in the United States (7), and epidemiological evidence has been used to identify several modifiable and nonmodifiable risk factors for the development of CVD (4,8). Individuals with a clustering of modifiable risk factors, known as metabolic syndrome (MetS), are particularly predisposed to an increased incidence of CVD and all-cause mortality (21). MetS encompasses abdominal obesity, low high-density lipoprotein cholesterol (HDL-C), elevated fasting triglycerides (TG), glucose intolerance or insulin resistance, and hypertension (13). In addition to the panoply of postabsorptive metabolic disturbances present in MetS, abnormal postprandial lipid metabolism is often displayed (20). This further amplifies the CVD risk associated with MetS because exaggerated postprandial lipemia (PPL) has been proposed as an independent risk factor for the development of CVD (19,34).
Lifestyle changes such as increases in exercise, which favorably alters many of the components of MetS, have been shown to be efficacious in reducing CVD risk (8). This ability to reduce CVD risk is also due, in part, to the effects of exercise on postprandial blood lipid metabolism. Single sessions of aerobic exercise have been shown to attenuate PPL observed after a high-fat meal (26). The key variable mediating this response appears to be the total energy expenditure (TEE) of the exercise session, as higher TEE typically results in larger PPL reductions (10). However, the vast majority of these investigations have used apparently healthy populations and single sessions of at least moderate-intensity exercise that resulted in relatively high TEE (26). The potential for exercise to attenuate PPL remains less clear when the TEE is approximately 500 kcal or less (18) or in populations at increased CVD risk, such as those with the MetS (26). Indeed, only two prior studies have examined exercise-induced alterations in PPL in men with the MetS (31,32). These studies suggest that an exercise TEE of slightly over 400 kcal may be the minimum caloric expenditure threshold required to attenuate PPL in this population. This level of caloric expenditure is consistent with weight loss and weight loss maintenance recommendations that are appropriate for the MetS population (16,17), emphasizing the importance of examining further issues pertaining to exercise prescription at similar caloric expenditures.
In addition to TEE, the exercise intensity and the pattern of caloric expenditure are also moderating factors that influence the postprandial lipemic response to a high-fat meal. Low- and moderate-intensity exercise resulted in similar PPL attenuations in physically active normotriglycerdemic males and females when the TEE was approximately 1000 kcal (29). This amount of exercise is well beyond the amounts of exercise that sedentary individuals at increased CVD risk are likely to participate in limiting the applicability of these findings to this population. To date, there has been no investigation examining the influence of exercise intensity on isocaloric exercise sessions in men with the MetS. Thus, further investigation into the issue of exercise intensity is warranted to determine whether low-intensity aerobic exercise is effective compared with moderate-intensity exercise for reducing PPL at lower TEE in this population.
The American College of Sports Medicine (ACSM) and the American Heart Association recommend that every US adult should accumulate a minimum of 30 min (or the equivalent of ≅200 kcal) of moderate-intensity physical activity on 5 d of the week (14,15). Yet, as with the issue of exercise intensity, this has yet to be investigated at lower caloric expenditures in those with MetS.
It is imperative to clarify these issues at the lower end of the caloric expenditure range in this population to guide effective exercise prescription to reduce CVD risk. Therefore, the purposes of this investigation were to compare the respective effects of single sessions of aerobic exercise requiring 500 kcal of caloric expenditure performed at low- versus moderate-intensity and in a continuous versus accumulated pattern on PPL in men with the MetS.
Fourteen males meeting the NCEP ATP III clinical identification criteria of the MetS (13) were studied. Participants were also physically inactive, defined as not meeting the US surgeon general's physical activity recommendations for at least 6 months before the study. All participants underwent screening for CVD using resting and maximal exercise electrocardiography. Individuals with known cardiovascular, pulmonary, or metabolic diseases or those taking prescription medications that alter lipid or carbohydrate metabolism were excluded from the study. Participants had the potential risks and benefits of participation fully explained to them and signed an institutionally approved informed consent document before completing any experimental procedures.
Height was determined to the nearest 0.25 inch with a stadiometer, and weight was measured to the nearest 0.25 lb using a calibrated balance scale. BMI was calculated from these measures as weight (kg)/height (m2) (30). WC was measured to the nearest 0.5 cm at the narrowest portion of the torso above the umbilicus and below the xyphoid process of the sternum (30). Body composition was assessed using Dual Energy X-Ray Absorptiometry (DEXA) (General Electric, Lunar Prodigy, Fairfield, CT).
Graded exercise testing.
Participants also performed a graded exercise test motor-driven treadmill using the Bruce Protocol (3). Oxygen consumption was measured using breath-by-breath analysis and was averaged over 30-s intervals with an automated metabolic testing system (Ultima Exercise Stress Testing System; Medical Graphics, Minneapolis, MN). The highest observed oxygen uptake was considered the peak oxygen consumption (V(dot)dot;O2peak) or maximal oxygen consumption (V(dot)dot;O2max) if a minimum of two of the following criteria were met: 1) maximal heart rate within ± 10 beats·min−1 of age predicted maximum; 2) respiratory exchange ratio (R) ≥ 1.15; and 3) rating of perceived exertion on the Borg scale ≥18. These results were used to individualize experimental exercise sessions.
Hemoglobin concentrations and hematocrit values from whole blood samples were used to estimate plasma volume shifts resulting from the exercise sessions and the high-fat test meals (6). Serum concentrations of TG were determined using an enzymatic reagent (Raichem, San Diego, CA). Concentrations of glucose were determined using a glucose oxidase and a modified Trinder color reaction (Raichem). Insulin concentrations were determined with a human insulin-specific radioimmunoassay kit (LINCO Research, St. Charles, MO). Homeostasis model assessment (HOMA) scores were calculated by multiplying fasting glucose concentration (mg·dL−1) by fasting insulin concentration (μU·mL−1) and by dividing the result by 22.5 (23). The ratio of glucose to insulin was also calculated for baseline blood samples to evaluate insulin resistance. The intra- and interassay coefficients of variation for all assays were <2% and <3%, respectively.
Although these participants were not habitually physically active, they were asked to discontinue outside physical activity other than activities of daily living for at least 3 d before each condition. Additionally, participants were instructed to replicate their baseline diet and abstain from caffeine use during this period. Participants first completed a nonexercise control condition, followed by three aerobic exercise conditions completed in a randomized order. At least 1 wk, but no more than 2 wk, separated subsequent conditions.
Nonexercise control condition.
For the nonexercise control condition, participants reported to the laboratory between 6 and 9 a.m. after a 10- to 12-h fast for blood collection followed immediately by the high-fat test meal. Participants were asked to consume the test meal within 10 min. Subsequent blood sampling occurred at 2-h intervals for 6 h after meal consumption. During the 6-h period, participants rested quietly and were only allowed to consume water ad libitum.
For all three exercise conditions, on the morning of day 1, participants had a fasting blood collection and returned to the laboratory later in the day for their exercise session(s). Participants walked on a treadmill until approximately 500 kcal were expended in each of the following exercise conditions: 1) a continuous session performed at 60-70% of V(dot)dot;O2peak (Mod-1), 2) a continuous session performed at 35-45% of V(dot)dot;O2peak (Low-1), and 3) two accumulated sessions performed at 60-70% of V(dot)dot;O2peak (Mod-2). Both sessions in the accumulated exercise condition resulted in an approximate caloric expenditure of 250 kcal and were separated by 3 to 5 h. Furthermore, the last accumulated exercise session ended at approximately the same time of day as the exercise sessions in the other conditions. Participants returned to the laboratory in the fasted state 12-14 h after the completion of exercise for each condition for a fasting blood collection, high-fat test meal, and subsequent blood sampling as described above for the nonexercise control condition. Please see Figure 1.
Participants performed a standardized 3-min warm-up on the treadmill at 2 mph and 2% grade, then speed and grade were adjusted to elicit the appropriate intensity for each condition. The intensity for each of the exercise sessions were calculated based on each participant's V(dot)dot;O2peak from the graded exercise test. Heart rate and respiratory gas analysis values were checked at 15-min intervals throughout all exercise sessions to verify intensity and estimate energy expenditure. If necessary, treadmill speed and grade were adjusted throughout the exercise sessions to maintain the appropriate intensity. Caloric expenditure was estimated by multiplying a standard caloric equivalent of 5 kcal·L−1 of oxygen consumed by the corresponding absolute V(dot)dot;O2. Exercise duration was determined by dividing 500 kcal by the estimated rate of caloric expenditure.
High-fat test meal.
The high-fat test meal used in all four experimental conditions was prepared by blending 65 g of vanilla ice cream and 270 mL of heavy whipping cream into a 16-oz. shake. This meal consisted of approximately 1000 kcal, 100 g of fat, 17 g of carbohydrate, and 3 g of protein (33). Participants were given a 10-min period to consume the meal.
Blood sampling procedures.
An intravenous catheter (Becton Dickinson Infusion Therapy Systems, Sandy, UT) was inserted into an antecubital vein, and blood samples were collected into two red top, nonadditive 10-mL serum vacutainer tubes (Becton Dickinson Vacutainer, Franklin Lakes, NJ). Catheter patency was maintained by a 2-mL injection of sodium heparin lock flush (Abbott Laboratories, North Chicago, IL) after each blood sampling time point.
Hemoglobin and hematocrit were determined immediately after each blood sample using a minute portion of the whole blood sample; the remainder of the sample was allowed to clot and centrifuged at 1500g for 10 min for isolation of serum. Serum was aliquoted into 2-mL ultracentrifuge tubes and stored at −70°C for subsequent analysis.
Participants completed 3-d dietary records following all screening procedures and then subsequent records for 3 d before each condition. Participants were instructed not to alter their current dietary habits for the duration of the study. Dietary records were analyzed for total caloric intake and macronutrient content including protein, carbohydrate, fat, and polyunsaturated to saturated fat ratio by a registered dietician with a commercially available software package (NutritionCalc Plus; ESHA Research, Inc., Portland, OR).
Mean temporal responses at each blood sampling time point over the 6-h postprandial period were determined for TG and insulin concentrations. Also, area under the curve (AUC) scores were calculated for TG and insulin as follows (24):
where n2, n4, and n6 are representative of postprandial concentrations and nB is representative of baseline concentrations. Two-way (4 (condition) × 4 (time)) ANOVA with repeated measures on condition and time were used to compare mean postprandial TG and insulin responses in each condition. A one-way ANOVA with repeated measures on condition was used to determine significant differences in AUC and TG and insulin concentrations. Duncan's New Multiple Range Test was used to further explore significant findings determined by ANOVA. The a priori significance level for all analyses was P < 0.05. Data analysis was completed with the Statistical Analysis System (SAS for Windows, version 9.1; SAS Institute, Cary, NC).
Participant baseline physiological characteristics and blood variables are presented in Tables 1 and 2, respectively. Plasma volume was not significantly altered in any of the four conditions; thus, all analyses were completed using concentrations unadjusted for plasma volume shifts. There were no significant differences in preexercise versus 12-h postexercise fasting blood variables among any of the three exercise conditions (Table 3); therefore, postexercise TG and insulin concentrations were used as the baseline measures for AUC calculations. The one-way ANOVA with repeated measures on condition revealed a significant difference among conditions (P < 0.05). Further analysis revealed that the TG AUC was significantly diminished by 27% the day after a low-intensity exercise was undertaken (P = 0.02). Similarly, a single session of moderate-intensity exercise reduced the TG AUC the following day by 20%, albeit nonsignificant. In contrast, two sessions of accumulated moderate-intensity exercise did not produce a significant attenuation in TG AUC. See Figure 2 for TG AUC responses.
A significant condition × time interaction was found for postprandial TG (P < 0.05). Upon further analysis, it was determined that single sessions of low- and moderate-intensity exercise reduced TG concentrations at the 4-h postprandial time point by 22% and 21% compared with control, respectively. However, two sessions of moderate-intensity exercise resulted in a nonsignificant 9% reduction compared with the control condition at this same time point (Fig. 3). TG concentrations were not significantly altered from control at baseline or at 2 and 6 h after the test meal by any of the exercise conditions. Additionally, the average time to reach peak TG concentration (4.1 ± 0.1 h) was not significantly different among any of the conditions (P = 0.19).
Neither insulin AUC scores nor the temporal response was significantly different among any of the exercise conditions compared with the control condition (P = 0.55). Insulin concentrations collapsed across conditions rose significantly by 32% 2 h after the consumption of the test meal (P = 0.0002). Insulin concentrations subsequently decreased at 4 h and were ultimately 24% lower than baseline at the end of the 6-h postprandial period, although this difference was not statistically significant (Fig. 4).
All participants were able to complete each of the three exercise conditions without any adverse events. For the low-intensity exercise condition, participants walked between 79 and 120 min. By design, the single session and the accumulated sessions of moderate-intensity exercise were performed at a higher range of intensities than the low-intensity session and therefore required less time to achieve the target caloric expenditure (45-84 min). There were no significant differences in exercise intensity (P = 0.50) or total exercise time (P = 0.46) between the two moderate-intensity exercise conditions.
Participants reported back to the laboratory for the test meal 13 ± 0.2 h after the completion of each exercise condition. There was no statistically significant difference in the number of hours between the end of exercise and the test meal among the three exercise conditions (P = 0.31). Exercise intervention data are presented in Table 4.
All participants completed the protocol within 6 wk of commencement. Body weight did not significantly differ over the course of the study protocol (P = 0.59). Additionally, analysis of dietary records indicated no significant differences in total caloric intake or major macronutrient content among any of the study conditions (Table 5).
This is this first study to directly compare the effects of low-intensity exercise on PPL to an isocaloric session of moderate-intensity exercise in men with MetS. Our data uniquely show that 500 kcal of low-intensity exercise was sufficient to attenuate PPL in men with the MetS in a similar manner to the reduction produced by a single session of moderate-intensity exercise. In contrast, performing two sessions of moderate-intensity exercise of the same total caloric expenditure did not significantly ameliorate PPL. These findings suggest that although single sessions of both low-intensity and moderate-intensity exercise may be effective strategies to reduce this CVD risk factor, accumulating moderate-intensity exercise throughout the day may not be effective in this population.
Low-intensity exercise significantly reduced the TG AUC by 27%. In comparison, an equal caloric expenditure of moderate-intensity exercise performed in a single-session also attenuated TG AUC by 20%. Although this reduction was not significantly different than that of low-intensity exercise, it was also not significantly different than that of the control condition. Further emphasizing the similarity of the responses, low- and moderate-intensity exercise performed in a single session significantly reduced TG concentrations 4 h after the test meal to a strikingly similar extent (22% and 21%, respectively). Thus, low- and moderate-intensity exercises are capable of producing similar effects on PPL at relatively low levels of caloric expenditure in MetS. Tsetsonis and Hardman (29) reported that both low- and moderate-intensity exercise yielding caloric expenditures of over 1000 kcal attenuated TG AUC by approximately 20% and reduced TG concentrations 4 h after the test meal by approximately 43%. The current findings are consistent with this and extend this observation to a lower caloric threshold and to men with MetS. The implication of these findings is that low-intensity exercise reduces PPL, and thus CVD risk, in males with MetS as effectively, if not more so, than moderate-intensity exercise of an equal energy expenditure performed in a single session. This is an important finding in terms of exercise prescription, as low-intensity exercise has been shown to promote exercise adherence (5).
Low-intensity exercise successfully attenuated PPL in our cohort, as evidenced by the reductions in both TG AUC and TG concentrations at the 4-h time point. These findings are similar to those of Zhang et al. (32), who reported that TG AUC was attenuated by 30% in men with MetS after an exercise energy expenditure of 425 kcal at 40% of V(dot)dot;O2max. Thus, our findings substantiate that this amount of total caloric expenditure is sufficient to favorably alter PPL in men with MetS. In contrast, similar caloric expenditures performed at low intensities have not yielded significant reductions in TG AUC or the temporal TG response in healthy populations (25,28). To date, the lowest amount of low-intensity exercise shown to reduce TG AUC in a healthy population is approximately 625 kcal (1). Thus, lower amounts of low-intensity exercise may be sufficient to attenuate PPL in men with MetS than are required to achieve this effect in apparently healthy populations.
Although we found that 500 kcal of exercise was sufficient to reduce PPL when performed in a single session, there were no significant alterations in the TG AUC scores or temporal TG response after the accumulated exercise condition. Our findings indicate that public health recommendations advising accumulation of moderate-intensity exercise throughout the day may not be sufficient to attenuate PPL in men with MetS at this level of caloric expenditure. This is not consistent with a previous study using accumulated exercise in a similar manner. Gill et al. (12) demonstrated that TG AUC was 18% lower after three sessions of moderate-intensity exercise accumulated throughout the day and that this was equally effective compared with a single session. Thus, participants with MetS appear to respond differently to this form of exercise stimulus. Alternatively, differences in study design may offer an explanation for our contrasting findings. The participants in Gill's study expended approximately 1125 kcal over three exercise sessions spaced apart by 4 h. Therefore, it is possible that accumulated exercise may only reduce PPL at higher caloric expenditures and/or if the exercise is distributed over more than two sessions.
Our finding that the temporal insulin response as well as the insulin AUC was not significantly altered by any of the exercise conditions provides evidence that PPL may be reduced without changes in postprandial insulin concentrations in men with MetS. Although decreases in insulin concentration during the postprandial period after exercise have been proposed to have a role in the attenuation of PPL, this does not appear to be obligatory for this response. Indeed, Gill et al. (11) reported that when postprandial reductions in insulin and TG coincide, they are not related to one another in apparently healthy individuals.
This study did not directly assess the mechanisms by which exercise attenuates PPL. However, based on available evidence from the composite body of work on PPL and exercise, it is likely that the reductions in PPL seen in this study are a result of two complementary mechanisms. First, exercise may reduce hepatic VLDL-TG secretion (9,22). Second, increases in skeletal muscle lipoprotein lipase activity after a single session of exercise may mediate increases in TG clearance (2,27).
In conclusion, this is the first study to demonstrate that 500 kcal of low-intensity exercise reduces PPL in men with MetS as effectively as moderate-intensity exercise. Although this effect can be achieved through a single session of low- or moderate-intensity exercise, accumulating moderate-intensity exercise does not appear to be an effective strategy for creating this response. The practical importance of these findings is that even at lower caloric expenditures, low-intensity exercise appears to be as effective as moderate-intensity exercise in reducing PPL in men with MetS. These results provide useful information for prescribing exercise to reduce this CVD risk in this population.
The results of the present study do not constitute endorsement by ACSM.
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