Influence of Maturation Status on Eccentric Exercise-Induced Muscle Damage and the Repeated Bout Effect in Females

Ming-Ju Lin, Kazunori Nosaka, Chih-Chiao Ho, Hsin-Lian Chen, Kuo-Wei Tseng, Sébastien Ratel, Trevor Chung-Ching Chen, Ming-Ju Lin, Kazunori Nosaka, Chih-Chiao Ho, Hsin-Lian Chen, Kuo-Wei Tseng, Sébastien Ratel, Trevor Chung-Ching Chen

Abstract

This study compared changes in indirect muscle damage markers, proprioception and arterial stiffness after elbow flexor eccentric exercise between pre-pubescent (9-10 y), pubescent (14-15 y), and post-pubescent (20-24 y) healthy, untrained females (n = 13/group). The maturation of the participants was confirmed by the hand bone age. All participants performed two bouts of 30 sub-maximal eccentric contractions (EC1, EC2) using a dumbbell set at 60% of pre-exercise maximal voluntary isometric elbow flexion strength at 90°. Changes in maximal voluntary concentric contraction (MVC) torque, muscle soreness (SOR), plasma creatine kinase activity, proprioception (position sense, joint reaction angle) and arterial stiffness (carotid-femoral pulse-wave velocity: cfPWV) before to 5 days after EC1 and EC2 were compared among groups by a mixed-design two-way ANOVA. Pre-exercise MVC torque and cfPWV were smaller (P < 0.05) for the pre-pubescent (MVC: 10.0 ± 0.9 Nm, cfPWV: 903 ± 60 cm/s) and the pubescent (14.3 ± 1.1 Nm, 967 ± 61 cm/s) than the post-pubescent (19.1 ± 1.4 Nm, 1,103 ± 73 cm/s). Changes in all variables after EC1 were smaller (P < 0.05) for the pre-pubescent (e.g., MVC at 1 d post-exercise: -10 ± 6%, peak SOR: 5 ± 2 mm) than the pubescent (-15 ± 9%, 12 ± 6 mm) and the post-pubescent (-25 ± 7%, 19 ± 13 mm). After EC2, changes in all variables were smaller (P < 0.05) than those after EC1 for all groups (e.g., MVC at 1 d post-exercise, pre-pubescent: -4 ± 6%, pubescent: -9 ± 4%, post-pubescent: -14 ± 5%; peak SOR: 3 ± 2, 7 ± 3, 11 ± 6 mm), but the magnitude of the repeated bout effect was not different (P > 0.05) among the groups. These results show that the extents of muscle damage, and proprioception and arterial stiffness changes after eccentric exercise are greater at later stages of maturation, but the repeated bout effect is not affected by maturation.

Keywords: delayed onset muscle soreness; lengthening contractions; maturation; muscle strength; proprioception.

Figures

Figure 1
Figure 1
Normalized changes in maximal voluntary concentric contraction torque of the elbow flexors (MVC-EF, A), absolute changes in range of motion of the elbow joint (ROM, B), and normalized changes in muscle passive stiffness (MPS, C) from baseline (pre) to immediately (post) and 1–5 days after the first (EC1) and second (EC2) eccentric exercise bouts for the pre-pubescent, pubescent and post-pubescent groups. A significant (P < 0.05) interaction (group × time) effect based on a pairwise comparison between two groups by a mixed design two-way ANOVA is shown by * in the figure. P, F, and eta-squared (η2) values shown by a mixed design two-way ANOVA for the comparison between two groups are shown below. Pre-pubescent vs. Pubescent. EC1: MVC-EF F(5, 60) = 5.91, P < 0.001, η2 = 0.313. ROM F(5, 60) = 3.30, P = 0.006, η2 = 0.203. MPS F(5, 60) = 2.27, P = 0.045, η2 = 0.149. EC2: MVC-EF F(5, 60) = 7.93, P < 0.001, η2 = 0.379. ROM F(5, 60) = 2.75, P = 0.018, η2 = 0.174. MPS F(5, 60) = 8.72, P < 0.001, η2 = 0.402. Pre-pubescent vs. Post-pubescent. EC1: MVC-EF F(5, 60) = 36.75, P < 0.001, η2 = 0.739. ROM F(5, 60) = 12.28, P < 0.001, η2 = 0.486. MPS F(5, 60) = 17.22, P < 0.001, η2 = 0.570. EC2: MVC-EF F(5, 60) = 17.04, P < 0.001, η2 = 0.567. ROM F(5, 60) = 6.56, P < 0.001, η2 = 0.335. MPS F(5, 60) = 15.03, P < 0.001, η2 = 0.536. Pubescent vs. Post-pubescent; EC1: MVC-EF F(5, 60) = 13.61, P < 0.001, η2 = 0.511. ROM F(5, 60) = 2.91, P = 0.013, η2 = 0.183. MPS F(5, 60) = 4.46, P = 0.001, η2 = 0.255. EC2: MVC-EF F(5, 60) = 4.78, P < 0.001, η2 = 0.269. ROM F(5, 60) = 3.07, P = 0.010, η2 = 0.191. MPS F(5, 60) = 5.42, P < 0.001, η2 = 0.294. P, F and eta-squared (η2) values of a pairwise comparison between bouts for each group by a mixed design two-way ANOVA are shown below. Pre-pubescent: MVC-EF F(5, 60) = 3.29, P = 0.006, η2 = 0.202. ROM F(5, 60) = 5.80, P < 0.001, η2 = 0.308. MPS F(5, 60) = 5.19, P < 0.001, η2 = 0.285. Pubescent: MVC-EF F(5, 60) = 3.60, P = 0.003, η2 = 0.21. ROM F(5, 60) = 12.18, P < 0.001, η2 = 0.484. MPS F(5, 60) = 3.19, P = 0.008, η2 = 0.197. Post-pubescent: MVC-EF F(5, 60) = 8.72, P < 0.001, η2 = 0.401. ROM F(5, 60) = 6.65, P < 0.001, η2 = 0.338. MPS F(5, 60) = 2.93, P = 0.012, η2 = 0.184.
Figure 2
Figure 2
Changes in muscle soreness (A), and changes in plasma creatine kinase activity (CK, B) and myoglobin concentration (Mb, C) before, and 1–5 days or 2 and 4 days following the first (EC1) and second (EC2) eccentric exercise bout for the pre-pubescent, pubescent and post-pubescent groups. A significant (P < 0.05) interaction (group × time) effect based on a pairwise comparison between two groups by a mixed design two-way ANOVA is shown by * in the figure. P, F, and eta-squared (η2) values shown by a mixed design two-way ANOVA for the comparison between two groups are shown below. Pre-pubescent vs. Pubescent; EC1: muscle soreness F4, 48 = 6.04, P < 0.001, η2 = 0.317. CK F(2, 24) = 4.99, P = 0.015, η2 = 0.277. Mb F(2, 24) = 5.63, P = 0.009, η2 = 0.302. Pre-pubescent vs. Pubescent; EC2: muscle soreness F(4, 48) = 16.92, P < 0.001, η2 = 0.565. CK F(2, 24) = 2.49, P = 0.103, η2 = 0.160. Mb F(2, 24) = 1.31, P = 0.288, η2 = 0.091. Pre-pubescent vs. Post-pubescent; EC1: muscle soreness F(4, 48) = 4.57, P = 0.001, η2 = 0.260. CK F(2, 24) = 9.74, P = 0.001, η2 = 0.428. Mb F(2, 24) = 5.19, P = 0.013, η2 = 0.285. Pre-pubescent vs. Post-pubescent; EC2: muscle soreness F(4, 48) = 12.01, P < 0.001, η2 = 0.480. CK F(2, 24) = 2.79, P = 0.080, η2 = 0.177. Mb F(2, 24) = 2.24, P = 0.126, η2 = 0.147. Pubescent vs. Post-pubescent; EC1: muscle soreness F(4, 48) = 2.94, P = 0.019, η2 = 0.184. CK F(2, 24) = 8.76, P = 0.001, η2 = 0.403. Mb F(2, 24) = 4.67, P = 0.019, η2 = 0.264. Pubescent vs. Post-pubescent; EC2: muscle soreness F(4, 48) = 2.39, P = 0.047, η2 = 0.155. CK F(2, 24) = 0.88, P = 0.429, η2 = 0.063. Mb F(2, 24) = 0.68, P = 0.515, η2 = 0.050. P, F and eta-squared (η2) values of a pairwise comparison between bouts for each group by a mixed design two-way ANOVA are shown below. Pre-pubescent; EC1 vs. EC2: muscle soreness F(4, 48) = 8.33, P < 0.001, η2 = 0.410. CK F(2, 24) = 2.25, P = 0.126, η2 = 0.147. Mb F(2, 24) = 2.00, P = 0.156, η2 = 0.133. Pubescent; EC1 vs. EC2: muscle soreness F(4, 48) = 13.20, P < 0.001, η2 = 0.504. CK F(2, 24) = 10.00, P = 0.001, η2 = 0.435. Mb F(2, 24) = 5.77, P = 0.008, η2 = 0.307. Post-pubescent; EC1 vs. EC2: muscle soreness F(4, 48) = 7.30, P < 0.001, η2 = 0.360. CK F(2, 24) = 11.33, P < 0.001, η2 = 0.466. Mb F(2, 24) = 5.19, P = 0.003, η2 = 0.285.
Figure 3
Figure 3
Absolute changes in angle of position sense (PS, A) and joint reaction angle (JRA, B) from the baseline (Pre, 0), immediately after exercise (0) and 1–5 days following the first (EC1) and second (EC2) eccentric exercise bout for the pre-pubescent, pubescent and post-pubescent groups. A significant (P < 0.05) interaction (group × time) effect based on a pairwise comparison between two groups by a mixed design two-way ANOVA is shown by * in the figure. P, F, and eta-squared (η2) values shown by a mixed design two-way ANOVA for the comparison between two groups are shown below. Pre-pubescent vs. Pubescent; EC1: PS F(5, 60) = 6.69, P < 0.001, η2 = 0.340. JRA F(5, 60) = 3.08, P = 0.009, η2 = 0.191. Pre-pubescent vs. Pubescent; EC2: PS F(5, 60) = 6.71, P < 0.001, η2 = 0.341. JRA F(5, 60) = 0.54, P = 0.776, η2 = 0.040. Pre-pubescent vs. Post-pubescent; EC1: PS F(5, 60) = 14.03, P < 0.001, η2 = 0.519. JRA F(5, 60) = 11.96, P < 0.001, η2 = 0.479. Pre-pubescent vs. Post-pubescent; EC2: PS F(5, 60) = 20.30, P < 0.001, η2 = 0.610. JRA F(5, 60) = 3.41, P = 0.005, η2 = 0.208. Pubescent vs. Post-pubescent; EC1: PS F(5, 60) = 2.65, P = 0.031, η2 = 0.169. JRA F(5, 60) = 6.98, P < 0.001, η2 = 0.349. Pubescent vs. Post-pubescent; EC2: PS F(5, 60) = 2.86, P = 0.014, η2 = 0.180. JRA F(5, 60) = 4.66, P < 0.001, η2 = 0.264. P, F and eta-squared (ηp2) values of a pairwise comparison between bouts for each group by a mixed design two-way ANOVA are shown below. Pre-pubescent; EC1 vs. EC2: PS F(5, 60) = 5.29, P < 0.001, η2 = 0.274. JRA F(5, 60) = 0.97, P = 0.448, η2 = 0.070. Pubescent; EC1 vs. EC2: PS F(5, 60) = 4.06, P < 0.001, η2 = 0.238. JRA F(5, 60) = 2.78, P = 0.017, η2 = 0.176. Post-pubescent; EC1 vs. EC2: PS F(5, 60) = 5.70, P < 0.001, η2 = 0.305. JRA F(5, 60) = 8.89, P < 0.001, η2 = 0.406.
Figure 4
Figure 4
Normalized changes in carotid-femoral pulse-wave velocity (cfPWV) from baseline (Pre: 100%) immediately (post) and 1–5 days after the first (EC1) and second (EC2) eccentric exercise bouts for the pre-pubescent, pubescent and post-pubescent groups. *: significant (P < 0.05) interaction (group × time) effect based on a pairwise comparison between groups. A significant (P < 0.05) interaction (group × time) effect based on a pairwise comparison between two groups by a mixed design two-way ANOVA is shown by * in the figure. P, F, and eta-squared (η2) values shown by a mixed design two-way ANOVA for the comparison between two groups are shown below. Pre-pubescent vs. Pubescent; EC1: F(5, 60) = 8.65, P < 0.001, η2 = 0.419. Pre-pubescent vs. Pubescent; EC2: F(5, 60) = 1.40, P = 0.237, η2 = 0.105. Pre-pubescent vs. Post-pubescent; EC1: F(5, 60) = 41.71, P < 0.001, η2 = 0.777. Pre-pubescent vs. Post-pubescent; EC2: F(5, 60) = 7.81, P < 0.001, η2 = 0.394. Pubescent vs. Post-pubescent; EC1: F(5, 60) = 7.73, P < 0.001, η2 = 0.392. Pubescent vs. Post-pubescent; EC2: F(5, 60) = 13.68, P < 0.001, η2 = 0.533. P, F and eta-squared (η2) values of a pairwise comparison between bouts for each group by a mixed design two-way ANOVA are shown below. Pre-pubescent; EC1 vs. EC2: F(5, 60) = 3.18, P = 0.013, η2 = 0.209. Pubescent; EC1 vs. EC2: F(5, 60) = 40.01, P < 0.001, η2 = 0.769. Post-pubescent; EC1 vs. EC2: F(5, 60) = 19.24, P < 0.001, η2 = 0.616.
Figure 5
Figure 5
Comparison in protective index [(EC1–EC2)/EC1 × 100%] amongst the pre-pubescent, pubescent and post-pubescent groups for maximal voluntary concentric contraction torque of the elbow flexors (MVC), range of motion (ROM), muscle passive stiffness (MPS), plasma creatine kinase activity (CK), plasma myoglobin concentration (Mb) and muscle soreness (SOR), angle of position sense (PS), joint reaction angle (JRA), and carotid-femoral pulse-wave velocity (cfPWV). For the calculation of the index, the values at 1 day post-exercise were used for MVC and ROM, and highest post-exercise values were used for MPS, SOR, CK, Mb, and cfPWV, and lowest post-exercise values were used for PS and JRA. At the bottom of the figure, effect size (Cohen's d) for the difference in each variable between EC1 and EC2 for each group is shown. *Significantly (P < 0.05) different from the post-pubescent group.

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Source: PubMed

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