Exercise training enhances physical fitness (muscle strength and aerobic capacity) resulting in marked improvements in metabolic health and functional capacity (1 2–4 5 6,7
Although combined exercise training can induce robust changes in muscle strength and aerobic capacity over extended time periods (≥12 wk) (8 4
Six weeks of aerobic-based exercise training increases aerobic capacity (9–12 13,14 15–18
Another knowledge gap regarding muscle adaptation responses are the effects of short-term exercise training cessation (i.e., detraining) subsequent to divergent exercise training modalities. Detraining is the partial or complete loss of exercise training–induced adaptations due to a reduction or cessation in exercise frequency, intensity, or duration (19 20 21,22 23
In the current study, we tested the hypothesis that 6 wk of endurance, resistance, or high-intensity interval exercise training would induce divergent anabolic and metabolic skeletal muscle adaptive responses in middle-age men. Among the anabolic responses, we assessed vastus lateralis muscle fiber cross-sectional area (CSA) after exercise training and detraining. Here, we hypothesized that high-intensity interval training (HIIT), because of its closer resemblance in contractile intensity/activity with resistance exercise training, would induce a greater increase in muscle fiber CSA compared with endurance exercise training, although this increase would be less in magnitude compared with resistance exercise training.
METHODS
Participants and Ethics Approval
Thirty-nine men (age, 39 ± 3 yr; body mass, 94 ± 13 kg; body mass index (BMI), 29 ± 3 kg·m−2 ) who were not meeting current national physical activity guidelines (24 Fig. 1 ). All participants completed the Exercise & Sports Science Australia Adult Pre-exercise Screening Tool to identify individuals who may be at a risk of an adverse event while exercising, in which case clearance to participate was sought from a medical practitioner before participation. Exclusion criteria included the following: BMI <25 or >35 kg·m−2 , smoking, type 2 diabetes mellitus, regular use of nonsteroidal anti-inflammatory medication, scheduling conflicts prohibiting morning exercise session attendance, and previous injuries exacerbated by exercise. Written and informed consent was obtained from all participants included in the study. The study was approved by the Australian Catholic University Human Research Ethics Committee (No. 2017-104H), prospectively registered online (ACTRN12617000894392; 19/06/2017), and conducted in accordance with the most recent revisions of the Declaration of Helsinki. The study was undertaken at the exercise physiology laboratories at the Australian Catholic University’s St Patrick’s campus (Fitzroy, Victoria, Australia).
FIGURE 1: Participant recruitment flow.
Study Design and Overview
The study was conducted in a parallel groups design. Participants reported to the laboratory on 10 occasions for study measures and a further 18 occasions for supervised exercise training sessions (Fig. 2 ). Allocation to one of the three exercise training groups was based on enrolment date after completion of all preliminary testing (Pre) using randomized stratification (Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322 −1 ) range (resting energy expenditure (REE) × physical activity factor of 1.5) (25 −1 ·d−1 ) intake target. A study nutritionist monitored adherence to the study dietary prescription via face-to-face diet consultations every fortnight for the entire study, daily electronic dietary recordings, and weekly reminders. After 6 wk of exercise training, all measurements were repeated (Post). Thereafter, participants were instructed to refrain from exercise training and maintain their activities of daily living for 2.5 wk, after which all measurements were repeated for the final time (detraining; DT).
FIGURE 2: Study design. Overview of when measurements were taken throughout the study. Exercise training intensities were adjusted where necessary at week 4. All measurements were obtained under resting conditions except for the postexercise training muscle biopsy collected ~48 h after the final exercise training session (end of week 6). Postexercise training testing (Post) took place across study weeks 6 and 7 and postdetraining testing (DT) across study weeks 9 and 10.
Initially, participants reported to the laboratory in an overnight fasted state between 0630 and 0730 h where a dual-energy x-ray absorptiometry scan (GE Lunar iDXA Pro, enCORE software version 16; General Electric, Boston, MA) was conducted (26 −1 or 2-h plasma glucose ≥11.1 mmol·L−1 ). At this time, a 3-d diet recall was performed. The study diet requirements (described subsequently) were explained and participants were provided a standardized meal (45% carbohydrate, 25% protein, and 30% fat; 33% of total daily energy intake (~3700–4300 kJ) based on the Cunningham equation [27
Participants reported to the laboratory in an overnight fasted state (~10 h) between 0630 and 0730 h and underwent measures to estimate REE (Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322 vastus lateralis (~100–200 mg) was obtained, under local anesthesia (2–3 mL of 1% xylocaine) using a Bergström needle modified for manual suction. One to two pieces of the muscle tissue sample (~30–40 mg per piece) were mounted on a water-soluble compound (Tissue-Tek Optimal Cutting Temperature; Sakura Finetek, AJ Alphen aan den Rijn, the Netherlands), frozen in liquid nitrogen–cooled isopentane, and stored at −80°C until analysis. The remaining sample was also frozen in liquid nitrogen and stored at −80°C until analysis.
Approximately 48 h after a muscle biopsy, the left and right vastus lateralis were scanned by two-dimensional B-mode ultrasound (frequency, 12 MHz; depth, 8 cm; field of view, 14 × 47 mm; GE Healthcare Vivid-/, Wauwatosa, WI) to determine muscle thickness (MT) from ultrasound images taken along the longitudinal axis of the muscle belly (Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322 2peak ) and maximal aerobic power (MAP; Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322 2peak was used to determine exercise training intensities (W) for ENT and HIIT.
Approximately 24–48 h after the V˙O2peak test, maximal upper and lower body muscle strength was assessed via a battery of one-repetition maximum (1RM) tests including bilateral leg press (45° incline), bilateral knee extension, and bench press. A series of sets (3–5, 2–8 repetitions) at increasing submaximal weights were lifted until the participant reported an RPE of ~16 using Borg’s CR6–20 scale. Each 1RM attempt was followed by 5 min of rest. The 1RM for each exercise was determined in isolation (i.e., exercises were not alternated). A maximum of five 1RM attempts were allowed per exercise. The 1RM achieved for each exercise was used to determine RET intensities (%1RM). After 1RM testing, participants met with the study nutritionist where daily energy (kJ) and protein (g·kg BW−1 ) intake targets were prescribed for the remainder of the study.
Approximately 48 h after the final exercise training session (i.e., the end of week 6), participants reported to the laboratory in an overnight fasted state (~10 h) for postexercise training testing (Post) in which a body composition scan and vastus lateralis muscle biopsy were performed as described previously. After ~48 h, two-dimensional ultrasound images of the left and right vastus lateralis were obtained followed by V˙O2peak testing. Subsequently (~24–48 h later), 1RM testing was performed. Completion of 1RM strength testing marked the commencement of the detraining period. Two and a half weeks later, postdetraining testing (DT) commenced where measurements were collected in the same order as per Post testing.
Exercise Training Protocols
All groups performed three morning exercise sessions per week for 6 wk. Progressive overload was applied to all exercise training protocols. The primary aim of the HIIT and ENT protocols was to increase aerobic capacity, whereas the overarching goal of the RET protocol was to increase skeletal muscle mass and strength. Participants in HIIT and ENT groups wore a heart rate monitor (Polar H2, Polar, Australia) during each exercise session, and RPE was obtained at regular intervals (i.e., at the conclusion of a work period) using Borg’s CR6–20 scale. At the beginning of week 4, participants in the HIIT and ENT groups performed a V˙O2peak test without breath analysis to reassess MAP. At the same time point, individuals in the RET group performed 1RM testing to reassess muscle strength. Based on results from week 4 exercise testing, training intensities were adjusted accordingly.
Endurance Exercise Training
A 3-min warm-up (100 W) preceded each training session on a stationary cycle ergometer. Total exercise session duration varied between 30 and 52 min, comprising 5- to 8-min work periods at 50%–75% peak power output with 1 min of active rest at 50 W. A 3-min cool-down at 50 W followed the final rest period. The duration and intensity of work periods increased throughout the exercise training program (Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322
High-Intensity Interval Training
A 3-min warm-up at (100 W) preceded each training session on a stationary cycle ergometer. Total exercise session duration varied between 13 and 23 min, comprising 30- to 60-s work periods at 90%–130% peak power output with 1 min of recovery at 50 W. The number of repetitions varied from 8 to 15 depending on the work period duration for that session. A 3-min cool-down at 50 W followed the final rest period. The duration and intensity of work periods increased throughout the exercise training program (Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322
Resistance Exercise Training
The RET protocol included upper and lower BW-bearing exercise using pulley machines and free weights. At the first session, all lower body exercise movements (45° incline bilateral leg press, bilateral knee extension, dumbbell stationary lunge, and dumbbell step ups) were introduced. At session 2, all upper body exercise movements were introduced (bench press, seated dumbbell overhead press, incline dumbbell chest press, latissimus dorsi pull-down, and pulley seated row). After the two familiarization sessions, training on Mondays and Fridays comprised predominantly lower body exercise movements, whereas Wednesday sessions predominantly comprised upper body exercise movements. A 3-min warm-up (50 W) on a cycle ergometer preceded each RET session. Two warm-up sets (9–12 reps) were performed for either the lower (Monday and Friday: leg press, 35% and 55% of 1RM) or upper body (Wednesday: bench press, 30% and 50% of 1RM) depending on the day of the week. Sets ranged from 3 to 4 and repetitions from 9 to 12 at 60%–80% 1RM. Three minutes of rest was standardized between sets for all exercise movements. Friday sessions from weeks 2 to 6 were performed to failure for all sets whereby the weight was increased at the next set (lower body exercise movements, 5–10 kg; upper body exercise movements, 2.5–5 kg) if the participant successfully completed more than 11 repetitions at the prescribed weight. A 3-min cool-down at 50 W on a cycle ergometer concluded each RET session (Document, Supplemental Digital Content 1, Appendix, https://links.lww.com/MSS/C322
Dietary Intervention and Analysis
For the both the exercise training and detraining periods, participants were prescribed a protein intake of ~1.4 (upper limit of 1.6) g·kg BW−1 ·d−1 deemed optimal for stimulating positive muscle protein turnover in exercising adults (28 −1 ), protein, carbohydrate, and fat (g·kg BW−1 for all macronutrients) for the duration of exercise training and detraining periods.
Biochemical and Histochemical Analyses
Immunohistochemistry
A cryostat (Leica CM1850; Leica Biosystems, Victoria, Australia) was used to obtain serial muscle cross sections (7 μm), which were fixed to specimen slides (SuperFrost Plus; ThermoFisher Scientific, Victoria, Australia), dried at room temperature for 30–60 min, and stored at −80°C until analysis. Slides were fixed in 2% formaldehyde (4% formaldehyde solution; Merck & Co, Darmstadt, Germany) for 10 min and washed in phosphate-buffered solution (PBS) for 5 min. The PBS was removed and washed in PBS with Tween (PBST) for 5 min. The PBST was removed, and the muscle sections were blocked in a solution containing 2% bovine serum albumin in PBS, 5% fetal bovine serum, 0.2% Triton X-100, 0.1% sodium azide, and 5% goat serum for 90 min. The blocking solution was removed, and sections were incubated in a primary antibody against laminin (rabbit–antihuman, 1:250 (i.e., one-part antibody in 249 parts 1% bovine serum albumin), ab11575; Abcam, Cambridge, United Kingdom, RRID:AB_298179) overnight at 4°C. The following morning, the primary antibody was removed, and slides were washed in PBST (3 × 5 min) and incubated in secondary antibody (goat–antirabbit, 1:500, Alexa Fluor 488; Life Technologies, Carlsbad, CA, RRID:AB_2633280) for 120 min at room temperature. Sections were then washed in PBST (3 × 5 min), fixed in 2% PFA for 5 min, washed again in PBST (2 × 5 min), blocked with 10% GS in PBS for 90 min, and then incubated in a primary antibody against myosin heavy-chain slow (MHCI; mouse–antihuman, 1:2, isoform A4.951; DHSB, Iowa City, IA, RRID:AB_528385) overnight at 4°C. The following morning, sections were washed three times in PBST (3 × 5 min), incubated in secondary antibody (goat–antimouse, 1:500, Alexa Fluor 488; Life Technologies, RRID:AB_2633275) for 120 min at room temperature, and washed again in PBST (3 × 5 min) before being air-dried in the dark for 2 min. One drop of fluorescent mounting medium (ProLong™ Diamond Antifade Mountant; Life Technologies) was then applied to each section, and slides were stored at −20°C until imaging.
A microscope with a high-resolution fluorescent camera attached was used to view slides. All images were captured through the 20× objective using associated software (EVOS FL Auto 2 cell imaging system; Invitrogen, Carlsbad, CA). In this study, 58 ± 8 and 78 ± 16 type I and II muscle fibers, respectively, were counted at each biopsy/participant/time point for CSA. Slides were blinded for both group and time before one study researcher (M.C.) performing all analysis using cell counting software (Fiji, ImageJ Version 2; National Institute of Health, RRID:SCR_002285). The CV between two blinded measurements, completed before the commencement of muscle fiber CSA analysis, was 2.7%. Fibers on the periphery of sections were excluded from the analysis. Areas of sections that were affected by freeze fracture artifact or contained longitudinally oriented fibers were excluded from the analysis. If <50 fibers in total were counted at a time point, all muscle fiber CSA data for that participant at that time point were excluded from the analysis. In this study, 31 participants (ENT, n = 11; HIIT, n = 10; RET, n = 10) were included for muscle fiber CSA analysis.
Blood analyses
Frozen plasma aliquots were thawed on ice, and plasma glucose concentrations were determined in duplicate using a biochemistry analyzer (YSI 2900; YSI Life Sciences, Yellow Springs, OH), with a CV of 0.6%. Plasma insulin concentrations were determined in duplicate using an enzyme-linked immunosorbent assay (80-INSHU-E01.1; Abnova Corporation, Tapei, Taiwan), with a CV of 3.2%. Updated homeostatic model assessment of insulin resistance (HOMA2-IR) was calculated using an online calculator by the Diabetes Trials Unit, University of Oxford (http://www.dtu.ox.ac.uk/homacalculator/index.php
Statistical Analysis
Because no previous studies have compared muscle fiber CSA responses between three different types of single-mode exercise training in human skeletal muscle, sample size was determined a priori (G*Power, Version 3.1) using previous literature assessing muscle fiber CSA changes in response to endurance or resistance exercise training (29 d ) = 1.3, α = 0.05, and power = 0.80. Statistical analyses were performed using SPSS software (version 25; IBM, Armonk, NY). Data normality was assessed before statistical analysis by assessing skewness, kurtosis, and results from Shaprio–Wilk tests. Linear mixed-effect models (LME), with subject for random intercept, were used to determine main effects of fixed factors: time (Pre, Post, DT), group (ENT, HIIT, RET), and interaction (time–group ) from which residuals were plotted on a histogram to inspect data distribution. For muscle biopsy data, fiber type (i.e., type I and II) was included as a third fixed factor in the LME where muscle fiber CSA was the dependent variable.
Where significant main effects were observed (i.e., time, group, or fiber type), post hoc comparisons with Bonferroni correction were used to locate differences. When significant interaction effects were observed, post hoc comparison with Bonferroni corrections was used to determine within- and/or between-group differences. Where significant group–time interactions were detected, one-way ANOVA tests of group were subsequently performed to compare the change scores (i.e., the difference between pre and post) to identify significant between-group interactions. Significance was accepted at P < 0.05. All data in text and tables are presented as mean ± SD. All data in figures are presented as mean and individual participant responses. Estimated mean differences with 95% confidence intervals from the LME are presented in the Supplementary Table 1 (Table, Supplemental Digital Content 2, Estimated mean differences and 95% confidence intervals, https://links.lww.com/MSS/C323
RESULTS
Participant characteristics and dietary intake
At baseline, there were no significant differences in age, BMI (Table 1 ), habitual energy, or macronutrient intake between groups (Table 1 ). A significant main effect of time (P < 0.001) was observed for protein intake relative to body mass. Post hoc comparisons showed that protein intake relative to body mass increased significantly during exercise training in all groups (P < 0.001) and remained unchanged during the period of detraining. A significant main effect of time (P = 0.007) was observed for carbohydrate intake relative to body mass. After detraining, carbohydrate intake relative to body mass decreased significantly compared with baseline in all groups (P = 0.005).
TABLE 1 -
Baseline participant characteristics and macronutrient intake (Pre) and changes after 6 wk of exercise training (Post) and 2.5 wk of detraining (DT) in middle-age men.
ENT
HIIT
RET
Main Effects (P )
Pre
Post
DT
Pre
Post
DT
Pre
Post
DT
Time
Group
Time–Group Interaction
Participant characteristics
Age, yr
38.6 ± 2.3
40.4 ± 3.2
39.6 ± 3.5
Height, cm
181.2 ± 9.5
179.2 ± 6.1
182.4 ± 6.1
Body mass, kg
95.9 ± 15.8
95.9 ± 16.6
95.8 ± 16.4
92.1 ± 11.3
93.1 ± 12.2
93.2 ± 12
93.9 ± 10.4
95.7 ± 11.0
94.4 ± 11.6
0.028
0.835
0.162
BMI, kg·m−2
29.0 ± 2.6
29.0 ± 3.0
29.0 ± 3.1
28.6 ± 3.0
28.8 ± 3.3
28.8 ± 3.4
28.1 ± 2.2
28.6 ± 2.3
28.5 ± 2.8
0.042
0.888
0.334
Body composition
ALM, kg
8.0 ± 1.3
8.0 ± 1.4
8.0 ± 1.3
7.9 ± 1.0
8.0 ± 1.0
8.0 ± 1.0
8.1 ± 1.0
8.4 ± 1.0
a
8.3 ± 1.0
0.040
0.784
0.042
Trunk LM, kg
27.7 ± 2.8
28.0 ± 3.0
27.9 ± 2.8
27.3 ± 2.9
27.4 ± 2.7
27.2 ± 2.5
27.6 ± 3.5
28.1 ± 3.5
27.6 ± 3.3
0.117
0.879
0.609
Body fat, %
31.8 ± 6.1
31.4 ± 6.1
31.3 ± 6.4
30.8 ± 3.7
30.4 ± 3.7
30.6 ± 3.7
31.8 ± 3.9
30.9 ± 4.1
31.0 ± 4.1
0.016
0.922
0.074
MT, cm
2.6 ± 0.3
2.6 ± 0.4
2.6 ± 0.3
2.5 ± 0.3
2.8 ± 0.3
a
2.7 ± 0.3
a
2.5 ± 0.3
2.8 ± 0.3
a
2.5 ± 0.3
b
<0.001
0.769
<0.001
Energy, kJ·d−1
9707 ± 1649
1000 ± 1047
9532 ± 1555
10,680 ± 2658
10,388 ± 1118
11,052 ± 1555
10,004 ± 1834
10,352 ± 1338
9916 ± 1546
0.281
0.520
0.840
Protein, g·kg BW−1
1.3 ± 0.3
1.5 ± 0.2
1.4 ± 0.3
1.2 ± 0.3
1.5 ± 0.2
1.4 ± 0.3
1.1 ± 0.4
1.4 ± 0.2
1.4 ± 0.2
<0.001
0.733
0.130
CHO, g·kg BW−1
2.4 ± 0.5
2.3 ± 0.5
2.2 ± 0.6
2.9 ± 1.0
2.6 ± 0.4
2.4 ± 0.6
2.6 ± 0.8
2.6 ± 0.8
2.3 ± 0.7
0.007
0.354
0.671
Fat, g·kg BW−1
1.0 ± 0.2
1.0 ± 0.2
1.0 ± 0.2
1.1 ± 0.3
1.1 ± 0.1
1.0 ± 0.2
1.0 ± 0.2
1.0 ± 0.2
1.0 ± 0.2
0.778
0.639
0.960
Values are mean ± SD. RET at DT: n = 10 due to one dropout before final measurements. Values are mean ± SD.
a P < 0.05 versus Pre within group.
b P < 0.05 versus Post within group.
BMI, body mass index; BW, Body weight; CHO, carbohydrate; ENT, endurance exercise training; HIIT, high-intensity interval training; RET, resistance exercise training; y, years.
Body composition
At baseline, there were no significant differences in body mass, total lean mass (LM), appendicular (ALM), leg lean mass (LLM), or body fat percentage between groups (Table 1 , Fig. 3 ). A significant time–group interaction effect (P = 0.023) was observed for LM. In response to exercise training, LM increased significantly for both RET (+2.0 ± 1.0 kg, P < 0.001) and HIIT (+1.0 ± 1.2 kg, P = 0.011), but not for ENT. The LM increase from pre to post was greater with RET compared with ENT only (+1.2 ± 1.8 kg, P = 0.041). After detraining, LM remained unchanged compared with postexercise training for both RET and HIIT. After detraining, LM remained significantly elevated compared with baseline for both RET (+1.0 ± 1.2 kg, P = 0.020) and HIIT (+1.0 ± 1.3 kg, P = 0.010), but not for ENT.
FIGURE 3: Baseline (Pre) total (A), appendicular (B), and leg (C) lean mass and changes after 6 wk of exercise training (Post) and 2.5 wk of detraining (DT) in middle-age men. Data are presented as mean and individual responses. ENT, endurance exercise training; HIIT, high-intensity interval training; RET, resistance exercise training. a P < 0.05 versus Pre within group; b P < 0.05 versus Post within group; *Main effect of time (P < 0.05) versus Pre. RET at DT: n = 10.
A significant time–group interaction effect (P = 0.033) was observed for ALM. In response to exercise training, ALM increased significantly for both RET (+1.3 ± 1.2 kg, P < 0.001) and HIIT (+0.8 ± 0.8 kg, P = 0.004), but not for ENT. After detraining, ALM remained unchanged compared with postexercise training for both RET and HIIT. After detraining, ALM remained significantly elevated compared with baseline for RET (+1.0 ± 1.0 kg, P = 0.001) and HIIT (+1.0 ± 0.8 kg, P = 0.001), but not for ENT.
A significant main effect of time (P < 0.001) was observed for LLM, with an increase in LLM in response to exercise training in all groups (P < 0.001), which was maintained after detraining.
A significant main effect of time (P = 0.016) was observed for body fat percentage. Post hoc comparisons showed a significant decrease for body fat percentage after exercise training (P = 0.014), which was maintained after detraining.
1RM muscle strength
There were no significant differences at baseline for 1RM leg press, leg extension, or bench press muscle strength between groups (Fig. 4 ). A significant time–group interaction effect (P < 0.001) was observed for 1RM leg press muscle strength (Fig. 4 A). In response to exercise training, 1RM leg press muscle strength increased significantly in all groups (RET: +70 ± 31 kg, P < 0.001; HIIT: +27 ± 19 kg, P < 0.001; ENT: +16 ± 16 kg, P = 0.026). The pre–post 1RM leg press muscle strength increase was greater with RET compared with both ENT (+51 ± 38 kg, P < 0.001) and HIIT (+41 ± 40 kg, P = 0.001). After detraining, 1RM leg press muscle strength increased significantly compared with postexercise training for ENT (+16 ± 18 kg, P = 0.008), but remained unchanged for both RET and HIIT. As such, 1RM leg press between posttraining and detraining was higher with ENT compared with both RET (+22 ± 24 kg, P = 0.003) and HIIT (+17 ± 25 kg, P = 0.033). Compared with baseline, 1RM leg press muscle strength remained significantly elevated after detraining (all, P < 0.001).
FIGURE 4: Baseline (Pre) leg press 1RM (A), leg extension 1RM (B), bench press 1RM (C), sum of all 1RMs (D), and changes after 6 wk of exercise training (Post) and 2.5 wk of detraining (DT) in middle-age men. Data are presented as mean and individual responses. ENT, endurance exercise training; HIIT, high-intensity interval training; RET, resistance exercise training; 1RM, one-repetition maximum. a P < 0.05 versus Pre within group; b P < 0.05 versus Post within group. ENT, bench press: n = 11; HIIT, leg press at Post: n = 11; RET at DT: n = 10.
A significant time–group interaction effect (P = 0.022) was observed for 1RM leg extension muscle strength (Fig. 4 B). In response to exercise training, 1RM leg extension muscle strength increased significantly for both RET (+23 ± 11 kg, P < 0.001) and HIIT (+11 ± 11 kg, P = 0.005), whereas there was a trend for and increase for ENT (+8 ± 12 kg, P = 0.064). The increase in 1RM leg extension muscle strength between rest and posttraining with RET was only higher than ENT (+14 ± 19 kg, P = 0.024). After detraining, 1RM leg extension muscle strength remained unchanged in all groups compared with postexercise training. After detraining, 1RM leg extension muscle strength remained significantly elevated compared with baseline (all, P < 0.05).
A significant time–group interaction effect (P = 0.001) was observed for 1RM bench press muscle strength (Fig. 4 C). In response to exercise training, 1RM bench press muscle strength increased significantly for both RET (+10 ± 4 kg, P < 0.001) and HIIT (+5 ± 6 kg, P = 0.034), but not for ENT, with this increase greater between RET and ENT (+7 ± 8 kg, P = 0.005). After detraining, 1RM bench press muscle strength remained unchanged compared with postexercise training for both RET and HIIT. After detraining, 1RM bench press muscle strength remained significantly elevated compared with baseline for RET (+15 ± 13 kg, P < 0.001), but not for HIIT or ENT.
A significant time–group interaction effect (P = 0.001) was observed for the sum of all 1RMs (Fig. 4 D). In response to exercise training, the sum of all 1RMs increased significantly in all groups (RET: +90 ± 38 kg, P < 0.001; HIIT: +41 ± 23 kg, P = 0.001; ENT: +23 ± 21 kg, P = 0.002). The increase in the sum of 1RMs was greater with RET compared with both ENT (+71 ± 42 kg, P < 0.001) and HIIT (+53 ± 43 kg, P < 0.001). After detraining, the sum of all 1RMs remained unchanged compared with postexercise training in all groups. After detraining, the sum of all 1RMs remained significantly elevated compared with baseline (all, P < 0.05).
V˙O2peak and MAP
At baseline, there were no significant differences in V˙O2peak or MAP between groups (Fig. 5 ). A significant time–group interaction effect (P = 0.001) was observed for V˙O2peak (Fig. 5 A). In response to exercise training, V˙O2peak increased significantly for both HIIT (+0.4 ± 0.2 L·min−1 , 14% ± 7%, P < 0.001) and ENT (+0.3 ± 0.3 L·min−1 , 11% ± 11%, P < 0.001), but not for RET. Indeed, the increase in V˙O2peak posttraining was higher with HIIT compared with RET (+0.3 ± 0.3 L·min−1 , P = 0.003). After detraining, V˙O2peak decreased significantly compared with postexercise training for HIIT (−0.2 ± 0.1 L·min−1 , −6% ± 4%, P = 0.005), and there was a trend for a decreased V˙O2peak for ENT (−0.1 ± 0.2 L·min−1 , −4% ± 5%, P = 0.055). After detraining, V˙O2peak remained elevated compared with baseline for both HIIT (+0.2 ± 0.2 L·min−1 , 8% ± 6%, P = 0.001) and ENT (+0.2 ± 0.2 L·min−1 , 6% ± 7%, P = 0.009), but not for RET. As such, V˙O2peak was higher between baseline and detraining after HIIT compared with RET (+0.2 ± 0.4 L·min−1 , P = 0.043).
FIGURE 5: Baseline (Pre) V˙O2peak (A), MAP (B), and changes after 6 wk of exercise training (Post) and 2.5 wk of detraining (DT) in middle-age men. Data are presented as mean and individual responses. ENT, endurance exercise training; HIIT, high-intensity interval training; RET, resistance exercise training; W, watt. a P < 0.05 versus Pre within group; b P < 0.05 versus Post within group. HIIT at DT: n = 11; RET at DT: n = 10.
A significant time–group interaction effect (P < 0.001) was observed for MAP (Fig. 5 B). In response to exercise training, MAP increased significantly for both HIIT (+30 ± 9 W, P < 0.001) and ENT (+26 ± 14 W, P < 0.001), but not for RET. The change in MAP between rest and posttraining was higher with ENT compared with RET (+16 ± 20 W, P = 0.007) as well as with HIIT compared with RET (+20 ± 20 W, P = 0.001). After detraining, MAP decreased significantly for HIIT (−17 ± 11 W, P = 0.001) compared with postexercise training but remained unchanged for ENT. The decrease in MAP with HIIT from postexercise to detraining was significantly greater compared with ENT (−13 ± 15 W, P = 0.004) and RET (−13 ± 16 W, P = 0.007). After detraining, MAP remained significantly elevated compared with baseline for both HIIT (+13 ± 14 W, P < 0.001) and ENT (+23 ± 13 W, P < 0.001), but not for RET. MAP was significantly higher from baseline to detraining between HIIT and RET only (+17 ± 21 W, P = 0.009).
Muscle fiber characteristics
At baseline, there were no significant differences in type I or II muscle fiber CSA between groups (Table 2 ). There was no significant time–group–fiber type interaction effect for muscle fiber CSA. A significant main effect of time was observed for type I and II muscle fiber CSA in all groups (all, P = 0.007). In response to exercise training, type I and type II muscle fiber CSA increased significantly (P = 0.006) in all groups. After detraining, type I and II muscle fiber CSA remained unchanged compared with postexercise training in all groups.
TABLE 2 -
Baseline
vastus lateralis muscle fiber characteristics (Pre) and changes after 6 wk of exercise training (Post) and 2.5 wk of detraining (DT) in middle-age men.
ENT
HIIT
RET
Main Effects (P )
Pre
Post
DT
Pre
Post
DT
Pre
Post
DT
Time
Group
Time–Group Interaction
Type I CSA, μm2
3672 ± 776
4245 ± 1309
4268 ± 1336
3672 ± 698
4611 ± 1364
3616 ± 555
4412 ± 1329
4345 ± 962
3837 ± 872
0.007
0.760
0.313
Type II CSA, μm2
4269 ± 943
4949 ± 2060
4804 ± 1548
3423 ± 719
3960 ± 774
3690 ± 961
3479 ± 865
4222 ± 867
3552 ± 456
0.007
0.760
0.313
Type I %
46 ± 12
41 ± 10
49 ± 14
40 ± 18
39 ± 21
48 ± 18
36 ± 10
44 ± 10
40 ± 8
0.034
0.923
0.383
Type II %
54 ± 12
59 ± 10
51 ± 14
60 ± 18
61 ± 21
52 ± 18
64 ± 10
56 ± 10
60 ± 8
0.034
0.923
0.383
Values are mean ± SD. Fiber type % is ENT: n = 11; HIIT: n = 10; RET: n = 10.
CSA, muscle fiber cross-sectional area; ENT, endurance exercise training; HIIT, high-intensity interval training; RET, resistance exercise training.
At baseline, there were no significant differences in the proportion of type I or type II fibers between groups (Table 3 ). A significant main effect of time was observed for both type I and II fiber type percentages (both, P < 0.05); however, no significant differences between time points could be detected in all groups.
TABLE 3 -
Baseline (Pre) REE and oral glucose tolerance measurements and changes after 6 wk of exercise training (Post) and 2.5 wk of detraining (DT) in middle-age men.
ENT
HIIT
RET
Main Effects (P )
Pre
Post
DT
Pre
Post
DT
Pre
Post
DT
Time Group
Group
Time –Group Interaction
Resting metabolic rate test
REE, kcal
1974 ± 210
1968 ± 210
1926 ± 198
1955 ± 210
1941 ± 210
1922 ± 204
2056 ± 210
2014 ± 210
2028 ± 190
0.349
0.486
0.924
Oral glucose tolerance test
Fasting plasma glucose (mmol·L−1 )
5.4 ± 0.5
5.2 ± 0.5
5.5 ± 0.8
5.1 ± 0.3
5.0 ± 0.3
5.1 ± 0.3
5.2 ± 0.9
5.5 ± 0.5
a
5.1 ± 0.9
b
0.848
0.501
0.001
AUC total glucose, mmol·h−1 ·L−1
893 ± 193
824 ± 131
899 ± 179
726 ± 99
721 ± 108
731 ± 154
874 ± 165
798 ± 139
773 ± 146
0.085
0.273
0.113
Fasting plasma insulin, mIU·L−1
7.4 ± 5.9
6.0 ± 5.1
6.7 ± 5.4
5.3 ± 2.7
5.5 ± 2.8
4.5 ± 2.4
9.8 ± 7.7
8.1 ± 6.6
7.9 ± 4.7
0.035
0.349
0.246
AUC total insulin, mmol·h−1 ·L−1
6098 ± 3810
6096 ± 6496
7136 ± 6297
4563 ± 2063
3955 ± 1883
4194 ± 2118
9277 ± 5751
7271 ± 4196
7239 ± 4819
0.129
0.097
0.061
HOMA2-IR
1.0 ± 0.7
0.8 ± 0.7
0.9 ± 0.7
0.7 ± 0.3
0.7 ± 0.4
0.6 ± 0.3
1.2 ± 1.0
1.1 ± 0.9
1.1 ± 0.6
0.133
0.207
0.559
Values are mean ± SD. RET at DT: n = 10.
AUC, area under the curve; ENT, endurance exercise training; HIIT, high-intensity interval training; HOMA2-IR, homeostatic model assessment of insulin resistance; RET, resistance exercise training.
a P < 0.05 versus Pre within group.
b P < 0.05 versus Post within group.
Muscle thickness
At baseline, there were no significant differences in MT between groups (Table 1 ). A significant time–group interaction effect (P < 0.001) was observed for MT (Table 1 ). In response to exercise training, MT increased significantly for both RET (+0.3 ± 0.2 cm, P < 0.001) and HIIT (+0.3 ± 0.2 cm, P < 0.001), but not for ENT. As such, changes in MT between baseline and posttraining were greater between RET and ENT (+0.3 ± 0.2 cm, P < 0.001) and between HIIT and ENT (+0.3 ± 0.2 cm, P < 0.001). After detraining, MT decreased significantly compared with postexercise training for RET (−0.3 ± 0.1 cm, P < 0.001), but remained unchanged for HIIT. Changes between posttraining and detraining were greater with RET compared with ENT (+0.3 ± 0.2 cm, P = 0.000) as well as with HIIT compared RET (+0.2 ± 0.2 cm, P = 0.015). After detraining, MT remained significantly elevated compared with baseline for HIIT (+0.2 ± 0.2 cm, P < 0.001), but returned to preexercise training levels for RET.
REE and OGTT
At baseline, there were no significant differences in REE between groups (Table 3 ). REE did not change after exercise training or detraining in all groups.
At baseline, there were no differences between groups for any measurements derived from the OGTT (Table 3 ). A significant time–group interaction effect (P = 0.001) was observed for fasting plasma glucose. In response to exercise training, fasting plasma glucose increased significantly for RET (+0.4 ± 0.6 mmol·L−1 , P = 0.001), but not HIIT or ENT. After detraining, fasting plasma glucose decreased significantly compared with postexercise training for RET (−0.4 ± 0.5 mmol·L−1 , P = 0.002) that was also greater compared with ENT (+0.5 ± 0.7 mmol·L−1 , P = 0.049). Total glucose area under the curve did not change after exercise training or detraining in all groups.
A significant main effect of time (P = 0.035) was observed for fasting plasma insulin. Post hoc comparisons showed a significant decrease for fasting plasma insulin after detraining (P = 0.038) compared with baseline. A trend for a time–group interaction effect was observed for total insulin area under the curve (P = 0.061). HOMA2-IR did not change after exercise training or detraining in all groups.
Physical activity
At baseline, there were no significant differences in physical activity measurements between groups (Table, Supplemental Digital Content 3, Physical activity, https://links.lww.com/MSS/C324 P = 0.067). A significant main effect of time was observed for the percentage of the day spent moving (P = 0.011) and standing (P = 0.023). Post hoc comparisons showed a reduction in the percentage of the day spent moving (P = 0.011) and standing (P = 0.020) during detraining compared with week 4 of exercise training.
A significant main effect of time was observed for percentage of the day spent sitting (P = 0.011). Post hoc comparisons showed an increase in the percentage of the day spent sitting during detraining compared with week 4 of exercise training (P = 0.011).
A significant time–group interaction effect (P < 0.001) was observed for the percentage of the day spent cycling. At week 4 of exercise training, the percentage of the day spent cycling increased significantly compared with baseline for ENT (+1% ± 1%, P < 0.001), but not for HIIT or RET. At week 4 of exercise training, the percentage of the day spent cycling was significantly greater for ENT compared with HIIT (+1% ± 1%, P = 0.010) and RET (+2% ± 1%, P < 0.001). The difference at week 4 in the percentage of the day spent cycling was greater with ENT compared with RET (+1% ± 2%, P = 0.003).
DISCUSSION
We show that short-term HIIT can induce widespread changes in whole-body physical fitness and skeletal muscle adaptation as demonstrated by increases in peak aerobic capacity, LM, MT, and muscle strength. Although the exercise training–induced gains in LM with RET and HIIT were maintained after short-term detraining, improvements in aerobic capacity after HIIT and ENT did not persist.
Exercise Training Responses
Muscle strength and aerobic capacity
Physical fitness before surgery is an independent predictor of postoperative morbidity and mortality (6 4 30 30 30 −1 ·d−1 ) to help augment anabolic adaptations to exercise training. Finally, all our training sessions were supervised in the laboratory to monitor first-hand training technique and ensure appropriate training intensity. Collectively, increases in muscle strength with short-term aerobic-based exercise training may be dependent on incorporating supervised training programs that provide appropriate training intensity/progressive overload and with supportive nutritional measures. However, an important limitation to this inference is that our study only recruited men. Whether women could similarly increase muscle strength with short-term HIIT, particularly in light of substantial differences in hormonal milieu between sexes in middle-age adulthood, remains an area of further investigation. In addition, we cannot discount the potential of a “learned effect” that may explain our current strength results. Thus, future studies that incorporate appropriate strength testing familiarization sessions preceding short-term HIIT and END training are warranted. We also found that aerobic capacity increased with HIIT and ENT (+14% and +11%, respectively), but not after RET, in agreement with previous reports in middle-age adults (9,31–34 30
LM, MT, and muscle fiber size
In many populations, reduced functional capacity and skeletal muscle mass is a predictor of unfavorable postoperative outcomes (15,16,35 7 36 36 −1 ·d−1 ) recommended to promote and maintain muscle growth while exercise training (28 −1 ·d−1 ) we cannot evaluate the contribution of increased protein intake to observed gains in LM.
Six weeks of RET and HIIT but not ENT increased vastus lateralis MT (+11% and 10%, respectively). We have previously reported that 12 wk of RET and ENT increased vastus lateralis MT (+14% and 10%, respectively) in young recreationally active men consuming a high-protein diet (2 g·kg BW−1 ·d−1 ) (37 37 vastus lateralis that may have affected MT measurements. Taken together, these findings suggest that higher-intensity intermittent exercise (aerobic- or resistance-based) may be an important consideration where exercise training–induced increases in muscle mass/thickness are required in a relatively short period of time (i.e., 6 wk) in middle-age men. To the best of our knowledge, this is the first study to report changes in muscle fiber size after ENT, HIIT, and RET in middle-age adults. de Souza and coworkers (38 39 29
The current findings demonstrate that short-term HIIT can concurrently increase aerobic capacity and LM, an outcome that would typically be achieved using combined exercise training. As HIIT is a time-efficient intervention and may be perceived as more enjoyable to undertake compared with ENT (40
REE and glucose homeostasis
Fat-free mass, including metabolically active tissue such as skeletal muscle, is a large determinant of REE (41 42 43,44
Detraining Responses
Muscle strength & aerobic capacity
Short periods (~2 wk) of reduced physical activity induce skeletal muscle deconditioning (45,46 47
Spence and coworkers (48 48 2peak concomitant with loss of capillarization and mitochondrial enzyme activities have been reported after 2–4 wk of detraining proceeding short-term aerobic exercise training (49,50 51 48
LM, MT, and muscle fiber size
We found exercise training–induced increases in surrogates of whole-body and regional muscle mass after RET and HIIT were maintained after a short period of exercise training cessation similar in duration to the early postoperative period faced by patients who have undergone surgery. As such, short-term single-mode higher-intensity exercise training before periods of forced inactivity may provide benefits to physical function, combatting the catabolic effects of reduced physical activity typically observed after inactivity and/or surgery (52,53
Although the middle-age men in the current study are likely to have been more physically active during the detraining period than many postoperative patients, early ambulation is often encouraged where possible after surgery (2
CONCLUSIONS
Six weeks of RET and HIIT but not ENT increased markers of skeletal muscle mass including LM and vastus lateralis MT. The magnitude in LM increase with HIIT was less than RET and must be interpreted with caution, given that this increase was similar to the CV of the densitometer. Although all exercise training modalities increased muscle fiber size and lower body maximal strength, only HIIT and ENT increased aerobic capacity. After short-term detraining, lower body muscle strength gains were maintained, and LM gains persisted with RET and HIIT. In contrast, exercise training–induced increases in aerobic capacity with HIIT and ENT were not retained after detraining.
The authors gratefully thank the participants for completing the protocol; Dr. Andrew Garnham, Mr. John Waters, and Mr. Matthew Rawnsley for their technical assistance with data collection; Dr. Collene Steward and Mr. Guilherme Telles for their technical assistance with laboratory analysis; and Dr. Lex Verdijk and Professor Luc Van Loon for their assistance with data interpretation. The authors also acknowledge the following companies for generously supporting the study by supplying foods and supplements consumed by participants at no charge: Swisse Wellness Pty Ltd, Australia, and Bulk Nutrients, Pty Ltd, Australia for whey protein powder, and Chobani LLC, Australia, and Jalna Dairy Foods Pty Ltd, Australia for high-protein yoghurt. This project was funded by the Australian Catholic University Research Fund (2016000340) awarded to Donny Camera. The authors declare that the results of the present study do not constitute endorsement by American College of Sports Medicine. Also, the results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The authors declare no conflict of interest.
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