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High-Intensity Running and Energy Restriction Reduce Postprandial Lipemia in Girls

THACKRAY, ALICE E.; BARRETT, LAURA A.; TOLFREY, KEITH

Medicine & Science in Sports & Exercise: March 2016 - Volume 48 - Issue 3 - p 402–411
doi: 10.1249/MSS.0000000000000788
BASIC SCIENCES
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Purpose This study examined the potency of combining acute high-intensity exercise and energy intake restriction on postprandial triacylglycerol concentrations ([TAG]) in healthy girls.

Methods Sixteen 11- to 13-yr-old girls (mean (SD) body mass, 45.1 (7.6) kg; peak oxygen uptake (V˙O2), 43 (6) mL·kg−1·min−1) completed three 2-d conditions in a counterbalanced crossover design separated by 14 d. On day 1, participants completed 10 × 1-min interval runs (HIIR) or 5 × 1-min interval runs combined with 0.82 (0.19) MJ energy intake restriction (HIIR-ER) or rested (CON). Exercise was completed at 100% maximal aerobic speed determined from an incremental peak V˙O2 test, with 1-min recovery between intervals. On day 2, capillary blood samples were taken in the fasted state and at predetermined intervals throughout the 6.5-h postprandial period. A standardized breakfast and lunch were consumed immediately and 4 h after the fasting sample, respectively.

Results Based on ratios of the geometric means (95% confidence intervals (CI) for ratios), fasting [TAG] was 16% and 8% lower than CON in HIIR (−24% to −7%; effect size (ES), 0.49; P = 0.002) and HIIR-ER (−17% to 1%; ES, 0.24; P = 0.09), respectively; HIIR was 8% lower than HIIR-ER (−17% to 1%; ES, 0.25; P = 0.08). The total area under the [TAG] versus time curve was 10% and 9% lower than CON in HIIR (−16% to −3%; ES, 0.30; P = 0.01) and HIIR-ER (−15% to −2%; ES, 0.28; P = 0.01), respectively; HIIR-ER and HIIR were similar (−1%; −8% to 6%; P = 0.80).

Conclusions Manipulations of HIIR and ER reduce postprandial [TAG] in girls. The magnitude of effect was marginally, although not meaningfully, greater after HIIR than that after HIIR-ER.

Paediatric Exercise Physiology Research Group, School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough, UNITED KINGDOM

Address for correspondence: Keith Tolfrey, Ph.D., Paediatric Exercise Physiology Research Group, School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough LE11 3TU, United Kingdom; E-mail: K.Tolfrey@lboro.ac.uk.

Submitted for publication July 2015.

Accepted for publication September 2015.

Elevated postprandial plasma triacylglycerol concentrations ([TAG]) are implicated in atherogenic development and progression (41) and are established as an independent predictor of cardiovascular disease incidence in women (2). Although the clinical manifestations of atherosclerotic disease are typically not apparent until adulthood, the process of atherosclerosis originates in childhood and progresses over the life span (26). Most waking hours are postprandial, resulting in extended periods of elevated postprandial [TAG]. Therefore, interventions that reduce postprandial [TAG] and delay precursors of atherosclerotic disease should be initiated early in life (26).

Studies with adults have shown consistently that acute aerobic exercise (30 min to 3 h in duration) performed the day before a standardized meal reduces postprandial [TAG] (25) and increases resting whole-body fat oxidation (9,38). Similar reductions in postprandial [TAG] have been reported after acute moderate- to vigorous-intensity exercise in young people (37). Several recent studies in adults highlight the potential efficacy of acute, intermittent high-intensity exercise to elicit reductions in postprandial [TAG] (e.g., (13,38)) in addition to improvements in insulin sensitivity and resting whole-body fat oxidation (38,40). Similarly, reductions in postprandial [TAG] have been demonstrated in healthy boys after acute high-intensity interval running (HIIR) (33) and repeated maximal cycle sprints (28). Approximately 80% of young people in England (19) and globally (17) fail to meet the current international guidelines of 60 min of daily moderate- to vigorous-intensity exercise for health promotion. Nevertheless, young people typically spend more of their active time engaged in high-intensity activities compared with adults (20). Considering lack of time and enjoyment are frequently highlighted as barriers to exercise participation in adolescent girls (5), the effect of different strategies that reduce the total exercise commitment and promote enjoyment on metabolic health markers should be investigated in girls. Therefore, the first aim of the present study was to examine the effect of a single session of HIIR on postprandial plasma [TAG] and resting whole-body fat oxidation in healthy girls.

A small number of studies have compared manipulations in exercise and dietary intake on postprandial [TAG] to determine whether the exercise-evoked reduction in postprandial [TAG] is a consequence of the associated energy deficit or skeletal muscle contraction per se. Acute moderate-intensity exercise seems to be more efficacious in reducing postprandial [TAG] than isoenergetic, mild energy intake restriction in healthy 11- to 13-yr-old girls (34) and pre- and postmenopausal women (15,24). Although the combination of moderate-intensity exercise and energy intake restriction did not exceed the reduction seen for exercise alone in healthy premenopausal women, it did at least match it (24). To the author’s knowledge, however, no study has examined whether combining exercise with energy intake restriction to augment the total energy deficit reduces postprandial [TAG] in young people. Therefore, the second aim of the present study was to compare the effect of a smaller dose of HIIR combined with energy intake restriction (HIIR-ER) with the full HIIR protocol (undertaken previously in boys (33)) and a rest control condition on postprandial plasma [TAG] and whole-body fat oxidation in healthy, recreationally active girls.

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METHODS

Participants

Nineteen recreationally active girls recruited from local schools volunteered to participate in this study, with results presented for 16 girls (age, 12.1 (0.7) yr; body mass, 45.1 (7.6) kg; body mass index, 18.7 (2.1) kg·m−2; peak oxygen uptake (V˙O2), 43 (6) mL·kg−1·min−1) because one girl did not adhere to the required dietary replication and two girls dropped out for personal reasons unrelated to the study. The study procedures were approved by the university ethical advisory committee. A written assent from participants and a written informed consent from a parent or guardian were obtained before the study commenced. All participants indicated that they were in good general health, had no history of medical conditions that may compromise participation in the study, and were not taking any medications or dietary supplements known to influence lipid or CHO metabolism.

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Anthropometry and physical maturation

Stature was measured to the nearest 0.01 m using a fixed stadiometer (Holtain Ltd., Crosswell, United Kingdom), body mass was quantified to the nearest 0.1 kg using a digital scale (Seca 770; Seca Ltd., Hamburg, Germany), and body mass index was calculated as body mass (kg) divided by stature (m) squared. Skinfold thickness was measured at the triceps and subscapular to the nearest 0.2 mm using Harpenden calipers (Baty International, West Sussex, United Kingdom). All measurements were taken on the right hand side of the body by the same investigator, and the median of three measurements at each site was used to estimate the percentage of body fat (30).

Participants were asked to provide a self-assessment of their level of physical maturity using drawings depicting the five stages of breast and pubic hair development, ranging from 1, indicating prepubescence, to 5, indicating full sexual maturity (32). Participants identified the stage most closely resembling their current level of sexual development. The median (interquartile range) stage for breast development was 3 (2) (stage 1, n = 1; stage 2, n = 5; stage 3, n = 5; stage 4, n = 5) and for pubic hair development was 2 (3) (stage 1, n = 4; stage 2, n = 6; stage 3, n = 1; stage 4, n = 3; stage 5, n = 2).

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Preliminary exercise measurements

Participants were familiarized with walking and running on the treadmill (h/p/cosmos mercury med; h/p/cosmos, Nussdorf-Traunstein, Germany) before completing an incremental speed-based treadmill protocol to determine peak V˙O2 and maximal aerobic speed (MAS). The protocol started at 5.0 km·h−1 with 0.5 km·h−1 increments every 30 s until volitional exhaustion, with the treadmill gradient set at 1%. HR was recorded using short-range telemetry (PE 4000; Polar Electro, Kempele, Finland). RPE was recorded in the last 10 s of each 30-s stage, and expired air samples were monitored continuously using an online breath-by-breath gas analysis system (Metalyzer 3B; Cortex, Leipzig, Germany). The analyzer was calibrated according to the manufacturer’s instructions before the exercise protocol began. Attainment of maximal effort was confirmed on the basis of the presence of a plateau in V˙O2 (≤3% with an increase in treadmill speed). In the absence of a plateau in V˙O2, (10 (63%) participants), an exhaustive effort was confirmed on the basis of the following secondary criteria: a HRpeak ≥95% of age-predicted maximum (220 − chronological age), an RER ≥1.00, and clear subjective signs of fatigue. An average of the breath-by-breath V˙O2 data was taken every 10 s, and peak V˙O2 was defined as the highest 30-s rolling average; the treadmill speed corresponding to peak V˙O2 was recorded as MAS.

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Experimental design

Using a within-measures, incomplete counterbalanced, crossover design, participants completed the following three 2-d experimental conditions separated by a standardized period of 14 d: HIIR, HIIR and energy intake restriction (HIIR-ER), and rest control (CON). The study design is presented schematically in Figure 1.

FIGURE 1

FIGURE 1

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Day 1: intervention day

Participants reported to the laboratory at 1530 h and completed all measures by 1730 h. Body mass was quantified upon arrival to standardize the meals provided on day 2 (described in the next section). During HIIR and HIIR-ER, the girls completed a 5-min warm-up at 60% MAS followed immediately by the acute high-intensity running intervals. The high-intensity running comprised either 10 (HIIR) or 5 (HIIR-ER) × 1-min treadmill runs at 100% MAS, with 1-min active recovery between each interval. Participants dismounted the treadmill during the active recovery periods and were encouraged to pace around the laboratory to avoid venous pooling and feeling light headed. HR was monitored continuously, and the participants provided an RPE in the last 10 s of each running interval as described previously; affective valence was quantified at the end of each running interval using a validated feeling scale (FS) (18). Within 5 min of exercise completion, participants completed the modified physical activity enjoyment scale (PACES) (27), and total enjoyment was calculated by summing the 16 responses after eight items were reverse-scored. During CON, participants rested in the laboratory for the duration of the visit. Participants maintained and replicated their habitual dietary intake throughout the day in all three conditions but with a controlled reduction in habitual food energy intake at the evening meal in HIIR-ER by 0.82 (0.19) MJ (195 (46) kcal).

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Standardization of dietary intake and physical activity

Participants weighed, recorded, and replicated their habitual dietary intake during the 48-h period (preintervention and intervention day) before day 2 of the first condition. The girls replicated this diet before the subsequent conditions but with a controlled reduction in energy intake on the intervention day of HIIR-ER. Participants completing HIIR-ER as the first condition were asked to record their usual dietary intake for two consecutive days at least 1 wk in advance, so that the prescribed energy intake restriction could be calculated and standardized. Two-day diet records were analyzed using a dietary analysis software (CompEat Pro version 5.8.0; Nutrition Systems, Banbury, United Kingdom).

Participants consumed a cereal snack bar at 1945 h on the intervention day to standardize the overnight fasting period, which provided 1.1 g of fat, 15.7 g of CHO, 1.0 g of protein, and 337 kJ of energy. Participants were allowed to drink plain water, but no other drinks or food, before arriving at the laboratory on day 2.

An ActiGraph GT1M accelerometer (ActiGraph, Pensacola, FL) was worn on the preintervention and intervention days of each condition, and participants were asked to minimize and replicate their physical activity during this period. The accelerometer was worn on the right hip during waking hours (removed for water-based activities). During data processing, 5-s epoch data were reintegrated to 60-s epochs, 60 min of consecutive zeros, allowing for 2 min of nonzero interruptions was used to remove nonwear, and a minimum of 9 h of valid wear time was required for a valid day. Physical activity was expressed as average counts per minute, and the following intensity cut points for 12-yr-old participants were applied (39): sedentary (<100 counts per minute), light (100–1262 counts per minute), moderate (1262–4136 counts per minute), and vigorous (>4136 counts per minute) activities.

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Day 2: postprandial day

After a 12-h overnight fast, participants arrived at the laboratory at approximately 0745 h and provided a fasting capillary blood sample after 10 min of seated rest. A standardized breakfast meal was consumed within 15 min, marking the start of the postprandial period (0800 h) (Fig. 1). Breakfast consisted of croissants, chocolate spread, whole milk, double cream, and milk shake powder. The meal quantity was prescribed relative to body mass and provided 1.5 g of fat (61.3% of the meal’s total energy), 1.8 g of CHO (32.3%), 0.4 g of protein (6.4%), and 94 kJ·kg−1 body mass. Subsequent capillary blood samples were taken at 0.5, 1, 3, 4.5, 5, and 6.5 h after the start of the breakfast, and participants consumed a standardized lunch, within 20 min, at 4 h (Fig. 1). Lunch consisted of white bread, butter, mild cheddar cheese, potato crisps, whole milk, and milk shake powder and provided 1.3 g of fat (53.5%), 1.9 g of CHO (35.5%), 0.6 g of protein (11.0%), and 92 kJ·kg−1 body mass. To ensure consistency across participants and experimental conditions, participants consumed either chocolate- or strawberry-flavored milk shake powder on all visits. Participants rested throughout the day and were able to read, watch DVD films, and play nonactive computer games. Participants consumed water ad libitum in the postprandial period of the first condition; the ingested volume was replicated in the subsequent conditions.

Resting expired air samples were collected in the semisupine position for 5 min after each blood sample into 100-L Douglas bags (Cranlea and Company, Birmingham, United Kingdom). Oxygen uptake and carbon dioxide production were analyzed using a paramagnetic oxygen analyzer and an infrared carbon dioxide analyzer (Servomex 1400; Servomex, East Sussex, United Kingdom), and the volume of expired air was quantified using a dry gas meter (Harvard Apparatus Ltd., Kent, United Kingdom). For each sample, V˙O2, expired carbon dioxide, and RER were determined, and energy expenditure (EE) and the oxidation of fat and CHO were estimated via indirect calorimetry (12), assuming that the urinary nitrogen excretion rate was negligible. The postprandial expired air data for one girl were spurious, so results are presented for 15 girls.

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Analytical methods

After the hand was prewarmed for 5 min in water heated to 40°C, the fingertip was pierced (Unistik 3 Extra; Owen Mumford Ltd., Oxford, United Kingdom) and 600 μL of whole capillary blood was collected into potassium EDTA-coated Microvette CB 300 tubes (Sarstedt Ltd., Leicester, United Kingdom). The whole blood samples were centrifuged immediately at 12,800g for 15 min (Eppendorf 5415c; Hamburg, Germany), and the resulting plasma was stored at −80°C for up to 2 months before subsequent analyses. Plasma [TAG], glucose concentration ([glucose]) (HORIBA ABX Diagnostics, Montpellier, France), and nonesterified fatty acid concentrations ([NEFA]) (Randox Laboratories Ltd., County Antrim, United Kingdom) were analyzed by enzymatic colorimetric methods using a benchtop analyzer (Pentra 400; HORIBA ABX Diagnostics, Montpellier, France). The within-batch coefficient of variation for [TAG], [NEFA], and [glucose] were 1.6%, 1.5%, and 0.8%, respectively. Hemoglobin concentration and hematocrit were also quantified in duplicate in the fasting and final postprandial samples to estimate the acute change in plasma volume (10). Hemoglobin concentration was assessed using the cyanmethemoglobin method; 20-μL whole blood was added to 5-mL Drabkin solution, and the absorbance was quantified photometrically at a wavelength of 546 nm (Cecil CE1011; Cecil Instruments, Cambridge, United Kingdom). Hematocrit was quantified using a microhematocrit centrifuge and reader (Haematospin 1300 Microcentrifuge; Hawksley and Sons Ltd., Sussex, United Kingdom).

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Statistical analyses

Data were analyzed using the IBM SPSS Statistics Software for Windows version 21 (IBM Corporation, New York, NY). The trapezium rule was used to calculate the total area under the variable versus time curve for TAG (TAUC-TAG), NEFA (TAUC-NEFA), glucose (TAUC-glucose), and postprandial whole-body EE and substrate oxidation. The TAUC values for substrate oxidation were divided by the total duration of the postprandial period (6.5 h). The incremental area under the plasma concentration versus time curve for TAG (iAUC-TAG), NEFA (iAUC-NEFA), and glucose (iAUC-glucose) was calculated using the same method after adjusting for fasting concentrations. The iAUC-NEFA is negative because of the decrease in postprandial [NEFA] from the fasting concentration.

Normality of the data was checked using the Shapiro–Wilk test. Normally distributed data are presented as mean (SD). Data for free-living physical activity and sedentary time and concentrations of plasma TAG, NEFA, and glucose were not normally distributed and were natural log-transformed before analysis. These data are presented as geometric mean (95% confidence intervals (CI)), and analysis is based on the ratios of geometric means and 95% CI for ratios. Homogeneity of variances was confirmed by the Mauchly test of sphericity, and a Greenhouse–Geisser correction was applied to the degrees of freedom if the sphericity assumption was violated.

Linear mixed models repeated for condition and interval were used to examine differences between HIIR and HIIR-ER exercise responses for running intervals 1–5, and temporal changes between the first and final running intervals were modeled with running interval as the sole factor. Dietary intake, free-living physical activity and sedentary time, resting whole-body EE and substrate oxidation, fasting concentrations, and TAUC and iAUC responses were analyzed using separate linear mixed models, with condition analyzed as a repeated-measures factor in the model. Differences in postprandial [TAG], [NEFA], and [glucose] were examined using linear mixed models repeated for condition and time. Temporal changes in TAUC-TAG between experimental conditions were examined over subsections of the postprandial period (0–1 h, 1–4.5 h, and 4.5–6.5 h) using separate linear mixed models, with condition as the sole factor. All linear mixed models included a random effect for each participant and were adjusted appropriately for the period effect (29).

Bivariate correlations identifying possible determinants of the exercise-induced changes in TAUC-TAG were quantified using Pearson product-moment correlations. Statistical significance was accepted as P < 0.05, and absolute standardized effect sizes (ES) are included to supplement important findings. In the absence of a clinical anchor, an ES of 0.2 was considered the minimum important difference in all outcome measures, 0.5 as the moderate, and 0.8 as the large (6).

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RESULTS

Dietary intake

Energy and macronutrient intakes were similar on the preintervention day across the three conditions (P ≥ 0.14). Average daily energy intake was 7.0 (1.8) MJ, and dietary intake of protein, CHO, and fat were 59.8 (19.0) g, 231 (70) g, and 56.5 (14.7) g, respectively. Energy and macronutrient intakes during the intervention day are displayed in Table 1. Energy intake on the intervention day of HIIR-ER was lower compared with those in CON (ES, 0.60; P < 0.001) and HIIR (ES, 0.54; P < 0.001); HIIR was significantly, but not meaningfully, lower than CON (ES, 0.06; P = 0.05). Absolute protein, CHO, and fat intake were lower in HIIR-ER compared with those in CON and HIIR (ES, 0.35–0.63; P < 0.001) but were not different between HIIR and CON (P ≥ 0.09). The only statistical difference in the contribution of protein, CHO, and fat to total energy intake was a marginally lower contribution of CHO in HIIR than that in HIIR-ER (ES, 0.31; P = 0.02) and a marginally lower contribution of fat in HIIR-ER than those in CON (ES, 0.21; P = 0.03) and HIIR (ES, 0.23; P = 0.02).

TABLE 1

TABLE 1

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Free-living physical activity and sedentary time

On the preintervention day, no differences were seen in physical activity levels or sedentary time across the conditions (P ≥ 0.27). Physical activity levels and sedentary time on the intervention day are displayed in Table 2. No significant differences were seen across the conditions for daily wear time (P = 0.30), sedentary time (P = 0.47), or time spent in light-intensity activities (P = 0.15). Average counts per minute were higher than CON by 128 counts per minute in HIIR (ES, 1.49; P < 0.001) and by 54 counts per minute in HIIR-ER (ES, 0.69; P = 0.01); HIIR was 74 counts per minute higher than HIIR-ER (ES, 0.80; P = 0.005). Time spent in moderate-intensity activities was higher in HIIR by 18 min and 15 min compared with those in CON (ES, 1.06; P = 0.001) and HIIR-ER (ES, 0.85; P = 0.01), respectively; CON and HIIR-ER were similar (3 min; P = 0.43). Time spent in vigorous-intensity activities was higher than CON by 12 min in HIIR (ES, 1.59; P < 0.001) and by 7 min in HIIR-ER (ES, 1.21; P < 0.001); HIIR and HIIR-ER were similar (P = 0.10). No differences were observed in free-living physical activity or sedentary time when accounting for the time spent resting or exercising in the laboratory on the intervention day (P ≥ 0.13).

TABLE 2

TABLE 2

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Responses to HIIR

The interval running session was performed at an average MAS of 11.5 (1.1) km·h−1 and was well tolerated by participants in HIIR and HIIR-ER. Linear mixed models revealed no differences between HIIR-ER and HIIR over running intervals 1–5 for HR, RPE, or FS response (P ≥ 0.11). During HIIR, there was a progressive increase from interval 1 to interval 10 for RPE (10 (3) to 18 (2), respectively; 95% CI, 6–10; ES, 2.82; P < 0.001) and end-interval HR (185 (12) to 202 (7) bpm, respectively; 95% CI, 12–21 bpm; ES, 1.36; P < 0.001), corresponding to 91% (4) and 99% (2) of HRpeak, respectively (95% CI, 6%–10%; ES, 1.99; P < 0.001). The FS response declined from interval 1 to interval 10 (3 (2) to −2 (3), respectively; 95% CI, −6 to −3; ES, 2.99; P < 0.001). During HIIR-ER, there was a progressive increase from interval 1 to interval 5 for RPE (10 (3) to 15 (3), respectively; 95% CI, 3–6; ES, 1.50; P < 0.001) and end-interval HR (184 (12) to 196 (9) bpm, respectively; 95% CI, 8–16 bpm; ES, 0.99; P < 0.001), corresponding to 90% (4) and 96% (2) of HRpeak, respectively (95% CI, 4%–8%; ES, 1.51; P < 0.001), and a decline in the FS response (3 (2) to −1 (2), respectively; 95% CI, −5 to −2; ES, 1.57; P < 0.001). The summed PACES score was similar between HIIR-ER and HIIR (57 (9) vs 56 (10), respectively; 95% CI, −6 to 3; P = 0.55).

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Resting whole-body EE and substrate oxidation

Total resting EE over the 6.5-h postprandial period was similar across the conditions (HIIR, 2.3 (0.3) MJ; HIIR-ER, 2.2 (0.3) MJ; CON, 2.3 (0.3) MJ; P = 0.42). The relative contribution of fat oxidation to total resting EE tended to be greater than CON (44% (17)) in HIIR (53% (17); 95% CI, −1% to 20%; ES, 0.50; P = 0.09), but HIIR-ER (51% (13)) was not significantly different from CON (95% CI, −4% to 18%; ES, 0.39; P = 0.18) or HIIR (95% CI, −13% to 9%; P = 0.69). Reciprocally, the relative contribution of CHO oxidation to total resting EE tended to be lower compared with CON (56% (17)) in HIIR (47% (17); 95% CI, −20% to 1%; ES, 0.50; P = 0.09), but HIIR-ER (49% (13)) was not significantly different from CON (95% CI, −18% to 4%; ES, 0.39; P = 0.18) or HIIR (95% CI, −9% to 13%; P = 0.69).

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Plasma volume changes and fasting [TAG], [NEFA], and [glucose]

Average changes in plasma volume between the fasting and 6.5-h postprandial samples were not different across the three conditions (HIIR, −0.3%; HIIR-ER, 0.4%; CON, −0.4%; P = 0.77). Therefore, the raw plasma [TAG], [NEFA], and [glucose] were used in all statistical analyses without adjustment. The fasting plasma [TAG], [NEFA], and [glucose] for each condition are displayed in Table 3. Linear mixed models revealed differences across the conditions in fasting plasma [TAG] (P = 0.01) and [NEFA] (P = 0.04) but not [glucose] (P = 0.41). Specifically, fasting plasma [TAG] was 16% and 8% lower than CON in HIIR (ES, 0.49; P = 0.002) and HIIR-ER (ES, 0.24; P = 0.09), respectively; HIIR was 8% lower than HIIR-ER (ES, 0.25; P = 0.08). Fasting plasma [NEFA] was 22% and 20% lower than CON in HIIR (ES, 0.65; P = 0.02) and HIIR-ER (ES, 0.58; P = 0.04), respectively; HIIR-ER and HIIR were not significantly different (−3%; P = 0.78).

TABLE 3

TABLE 3

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Plasma [TAG], [NEFA], and [glucose] in the postprandial period

Plasma TAG responses over the postprandial period for HIIR, HIIR-ER, and CON are shown in Figure 2. Linear mixed models revealed differences in postprandial plasma [TAG] over time and across conditions (main effect condition, P < 0.001; main effect time, P < 0.001; condition–time interaction, P = 0.71). Mean postprandial plasma [TAG] was 11% and 8% lower than CON in HIIR (−14% to −7%; ES, 0.27; P < 0.001) and HIIR-ER (−12% to −4%; ES, 0.21; P < 0.001), respectively; HIIR-ER and HIIR were similar (−3%; −7% to 2%; P = 0.24). The TAUC-TAG was 10% and 9% lower than CON in HIIR (ES, 0.30; P = 0.01) and HIIR-ER (ES, 0.28; P = 0.01), respectively; HIIR-ER and HIIR were similar (−1%; P = 0.80) (Table 3). Specifically, TAUC-TAG was lower after HIIR than CON between 0 and 1 h by 16% (−22% to −9%; ES, 0.53; P < 0.001) and between 1 and 4.5 h by 11% (−17% to −4%; ES, 0.31; P = 0.003); HIIR-ER was lower than CON between 0 and 1 h by 11% (−17% to −4%; ES, 0.37; P = 0.003) and between 1 and 4.5 h by 10% (−16% to −4%; ES, 0.30; P = 0.005). No differences in TAUC-TAG over subsections of the total postprandial period were seen between HIIR-ER and HIIR (P ≥ 0.16). No differences were seen in iAUC-TAG across the conditions (P = 0.53) (Table 3).

FIGURE 2

FIGURE 2

Individual changes (Δ) in TAUC-TAG for HIIR and HIIR-ER relative to CON are shown in Figure 3. The reductions in TAUC-TAG after HIIR and HIIR-ER were greater than changes in CON for ten (63%) and eleven (69%) girls, respectively. Meaningful positive correlations were identified between the intervention-induced change in fasting plasma [TAG] and the change in TAUC-TAG relative to CON for HIIR (r = 0.52; P = 0.04) and HIIR-ER (r = 0.59; P = 0.02). The measured physical and physiological characteristics, dietary intake (Table 1), free-living physical activity and sedentary time (Table 2), exercise responses, resting whole-body EE and substrate oxidation, and fasting [NEFA] or [glucose] (Table 3) did not account for any of the interindividual variability in ΔTAUC-TAG for HIIR or HIIR-ER. The Pearson product-moment correlation for the individual changes in TAUC-TAG between HIIR and HIIR-ER was small (r = 0.31; P = 0.25).

FIGURE 3

FIGURE 3

No differences were observed in postprandial plasma [NEFA] across the conditions over time (main effect condition, P = 0.58; main effect time, P < 0.001; condition–time interaction, P = 0.57). No meaningful differences were evident for TAUC-NEFA across the conditions (P = 0.45) (Table 3). The iAUC-NEFA was 56% and 55% higher than CON in HIIR (ES, 0.67; P = 0.01) and HIIR-ER (ES, 0.65; P = 0.01), respectively; HIIR-ER and HIIR were not different (1%; P = 0.95) (Table 3).

Linear mixed models revealed a trend for differences in postprandial plasma [glucose] between conditions and over time (main effect condition, P = 0.06; main effect time, P < 0.001; condition–time interaction, P = 0.77). The TAUC-glucose was 4% higher in HIIR compared with CON (ES, 0.58; P = 0.01), but HIIR-ER was not significantly different from HIIR (−1%; P = 0.27) or CON (2%; P = 0.08) (Table 3). The only significant difference in iAUC-glucose was a greater response in HIIR compared with that in HIIR-ER (39%; ES, 1.43; P = 0.04) (Table 3).

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DISCUSSION

The primary finding from the present study is that acute manipulations of low-volume HIIR and ER completed the day before standardized meals reduced postprandial plasma [TAG] and increased whole-body fat oxidation in healthy, 11- to 13-yr-old girls. The magnitude of this effect was marginally, although not meaningfully, greater after HIIR than that after HIIR-ER. The exercise and diet interventions were well tolerated by all participants and therefore may have practical metabolic health benefits in similar cohorts.

The exercise- and dietary restriction-induced reductions in fasting plasma [TAG] support the majority of previous exercise postprandial studies in young people (e.g., (3,28,34,35)). Although the lower fasting plasma [TAG] in HIIR and HIIR-ER are likely to influence the subsequent postprandial TAG response (7), substantial intraindividual variation is evident in childhood fasting [TAG] (36), and fasting [TAG] is less predictive of cardiovascular disease risk than postprandial [TAG] in women (2).

Several studies with adults have reported reductions in postprandial [TAG] after a single session of intermittent high-intensity exercise (e.g., (13,38)); however, this finding is not universal (1,31). The contrasting results in these studies may reflect the variety of high-intensity exercise protocols adopted, which, coupled with differences in participant characteristics, exercise timing, meal content, and blood sampling, is likely to promote heterogeneity in the individual responses (1,31). Nevertheless, we have demonstrated previously that a single session of HIIR promotes moderate reductions in postprandial plasma [TAG] in 11- to 12-yr-old boys (33). The current study extends this novel finding to 11- to 13-yr-old girls and supports the commonly reported reductions in postprandial [TAG] after acute moderate- to vigorous-intensity exercise in boys and girls (37) and repeated maximal cycle sprints in boys (28).

An additional novel feature of the current study was the inclusion of a condition combining a lower volume of HIIR with a small reduction in energy intake (0.82 (0.19) MJ, 195 (46) kcal), which reduced postprandial plasma [TAG] to a similar extent as the full HIIR protocol (approximately 10%) (Table 3; Fig. 2). Acute energy intake restriction alone has been shown to elicit a small reduction in postprandial [TAG] previously in healthy girls (−10%; ES, 0.32) (34) and pre-menopausal women (−12%) (24). Although an exercise-induced energy deficit seems to be a more potent stimulus to reduce postprandial [TAG] than an isoenergetic diet-induced energy deficit in girls (34) and women (15,24), the combination of light walking and energy intake restriction did match the reduction seen for exercise alone in sedentary, premenopausal women (24). The similar reduction in postprandial plasma [TAG] after HIIR and HIIR-ER is promising and highlights the potential for metabolic health benefits after time-efficient exercise combined with manageable dietary restriction in girls. A combination of low-volume, high-intensity exercise and mild dietary energy intake restriction may represent a practical and attractive alternative in girls who struggle to accumulate sufficient physical activity for health. It contributes to providing girls with a variety of lifestyle options that can reduce postprandial plasma [TAG] and may have important long-term metabolic health implications if employed regularly, but further work is required to support this in young people. One limitation of the present study is that the girls recruited were healthy and recreationally active. Therefore, further research is needed in overweight/obese girls who may require appropriate exercise and dietary interventions for weight management and improvements in the lipid profile.

The mechanisms underpinning the acute exercise- and diet-induced reductions in postprandial plasma [TAG] in young people were not measured directly in the present study because of the invasive nature of the methods required to do this accurately. In adults, two primary pathways have been proposed, involving the increased clearance of circulating TAG facilitated by enhanced lipoprotein lipase (LPL) activity (16) and/or the secretion of fewer, TAG-richer VLDL that have a higher affinity for LPL (23). A recent stable isotope enrichment study in obese women suggested that the TAG-lowering effect of acute exercise is mediated by a reduced abundance of endogenous fatty acids in plasma TAG and not the enhanced clearance of dietary fat (9). The notion that endogenous, and not exogenous, TAG metabolism exerts a stronger influence on the postprandial TAG response is indirectly supported by the current study evidenced by the small differences in iAUC-TAG between the conditions and the meaningful relationship seen between the intervention-induced changes in fasting plasma [TAG] and TAUC-TAG for HIIR (r = 0.52; P = 0.04) and HIIR-ER (r = 0.59; P = 0.02).

Although whole-body fat oxidation was not statistically significant between the three conditions, a thorough appraisal of the mean differences and absolute standardized ES revealed that HIIR was 8% higher than CON (ES, 0.50) and HIIR-ER was 7% higher than CON (ES, 0.39). Therefore, combinations of HIIR and ER seem to elevate resting whole-body fat oxidation the following day, which represents a novel finding in young people and supports exercise postprandial studies in adults employing acute high-intensity exercise protocols (38,40). The postexercise shift in whole-body substrate use toward fat oxidation has been linked to several regulatory mechanisms promoting the resynthesis of depleted skeletal muscle and/or hepatic glycogen stores (21). Circulating plasma fatty acids and TAG-rich lipoproteins are potential lipid sources used for oxidation, which is in agreement with the lower postprandial plasma [TAG] after HIIR and HIIR-ER, likely mediated by enhanced LPL activity (16,21). However, the similar postprandial NEFA response between the three experimental conditions suggests that plasma fatty acids did not contribute to the greater whole-body fat oxidation in HIIR and HIIR-ER. Nevertheless, it is possible that differences in plasma [NEFA] were evident before the commencement of the postprandial period, considering that large increases in plasma-free fatty acids have been shown in the early postexercise recovery period (21). The lack of association between whole-body fat oxidation and indices of lipemia in the current study is in contrast with previous findings in adults (38), suggesting that exercise- and diet-induced changes in postprandial plasma [TAG] and whole-body fat oxidation may occur independently in girls. Nevertheless, elevated postprandial [TAG] is associated independently with cardiovascular disease risk in women (2) and low resting fat oxidation with an increased risk of weight gain (11) and type 2 diabetes mellitus (4), highlighting the potential efficacy of acute high-intensity exercise and dietary restriction to improve metabolic health outcomes early in life.

Although the clinical significance of our findings cannot be established, the majority (93%) of the postprandial TAG samples were below the 2.3 mmol·L−1 threshold considered a desirable concentration in young people (22). On the basis of the physical activity data, nine (56%) girls in the present study were achieving the current international physical activity recommendations, although it should be noted that this is not a valid measure of habitual physical activity because the girls were asked to minimize and replicate their physical activity levels over a short measurement period. Most girls in England and globally (approximately 80%) fall short of the current physical activity guidelines for health (17,19), and time and enjoyment are frequently reported as barriers to exercise participation in adolescent girls (5). Therefore, the potential for HIIR and HIIR-ER, with a total exercise time commitment of 24 and 14 min, respectively (including warm-up and active recovery between intervals), to reduce postprandial plasma [TAG] and increase resting whole-body fat oxidation in girls is encouraging. The girls spent a greater amount of time engaged in vigorous-intensity activities in HIIR and HIIR-ER and a greater amount of time in moderate-intensity activities in HIIR on the intervention day as a result of the prescribed exercise intervention. There were no differences between conditions after accounting for the time spent resting or exercising in the laboratory, suggesting that the implemented between-condition control of free-living physical activity and sedentary time was effective. The high-intensity nature of the exercise adopted in the present study may better reflect the activity patterns of young people who spend a greater proportion of time engaged in high-intensity activities than adults (20). Furthermore, it has been demonstrated that children associate moderate-intensity exercise interspersed with short high-intensity efforts with greater perceived enjoyment than completing continuous moderate-intensity exercise alone (8). In the present study, the similarly high PACES score between HIIR and HIIR-ER suggests that interval running performed at a high intensity may be an attractive exercise model in girls independent of whether five or ten 1-min intervals are completed.

Previous high-intensity exercise postprandial studies highlight the substantial heterogeneity evident in postprandial TAG responses in young people (33) and adults (1,31). We have shown previously in boys that exercising at a higher relative exercise intensity during HIIR is associated with a greater reduction in postprandial plasma [TAG] (33); however, this relation was not apparent in the current study with girls and the other measured variables in the study could not explain any of the heterogeneity present. A study with adults reported that exercise-induced changes in 3-OHB, a marker of hepatic fatty acid oxidation, were a strong predictor of the moderate-intensity exercise-induced reduction in fasting and postprandial [TAG] (14). Although this marker may explain some of the heterogeneity in the present study, we measured postprandial 3-OHB concentrations but the assay was unable to detect concentrations of 3-OHB in most fasting and postprandial samples; therefore, further investigation is required in young people.

The higher postprandial plasma [glucose] after HIIR compared with CON supports a recent study in girls adopting a moderate-intensity exercise protocol (34); however, most of the previous exercise postprandial studies in young people report no difference in postprandial [glucose] after acute exercise (e.g., (3,28)). The reason for this discrepant finding is not known; however, it is unlikely that the higher postprandial [glucose] in HIIR is implicated in the TAG-lowering effect of HIIR, considering that glucose has not been linked to the potential mechanistic pathways discussed previously. Nevertheless, all participants in the present study demonstrated a healthy postprandial glucose profile independent of the experimental condition and the time of glucose measurement, suggesting the girls exhibited good glycemic control.

The present study is limited, as the exercise protocol comprised running; therefore, the findings may not apply to other exercise modalities such as cycling and game-based activities. Despite this limitation, the exercise protocol adopted in the present study is attainable for young people in a natural setting.

In conclusion, acute manipulations of low-volume HIIR and ER completed the day before standardized meals reduced postprandial plasma [TAG] and increased resting whole-body fat oxidation in healthy, 11- to 13-yr-old girls. The magnitude of this effect was marginally, although not meaningfully, greater after HIIR than that after HIIR-ER. Low-volume HIIR performed alone or in combination with a mild reduction in habitual energy intake may represent time-efficient and enjoyable strategies to improve metabolic health in girls, but further work is required to examine this chronically and in overweight/obese girls for whom HIIR-ER may be an efficacious intervention.

We thank Woodbrook Vale School and Rawlins Academy in Loughborough for their support and understanding throughout this research. We also thank the participants and their parents for their commitment throughout the study.

This study was supported partly by the NASPEM Marco Cabrera Student Research Grant and by funding available internally through Loughborough University. The research was supported by the National Institute for Health Research Diet, Lifestyle, and Physical Activity Biomedical Research Unit based at the university hospitals of the University of Leicester and the Loughborough University.

The authors declare that they have no conflict of interest. The views expressed are those of the authors and not necessarily those of the National Health Service, the National Institute for Health Research, or the Department of Health.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

CARDIOVASCULAR DISEASE RISK; ENERGY DEFICIT; EXERCISE INTENSITY; TRIACYLGLYCEROL; YOUNG PEOPLE

© 2016 American College of Sports Medicine