THE EFFECTS OF SHORT-TERM EXERCISE TRAINING ON PEAK-TORQUE ARE TIME- AND FIBER-TYPE DEPENDENT DO´RA URECZKY,1,2 GABRIELLA VA´CZ,3 ANDREAS COSTA,1 BENCE KOPPER,1 ZSOMBOR LACZA,3 TIBOR HORTOBA´GYI,4 AND JO´ZSEF TIHANYI1 1
Department of Biomechanics, Kinesiology and Informatics, Faculty of Physical Education, and Sport Sciences, Semmelweis University, Budapest, Hungary; 2Department of Physical Education, Faculty of Pedagogy, Kaposva´r University, Kaposva´r, Hungary; 3Institute of Human Physiology and Clinical Experimental Research, Faculty of Medicine, Semmelweis University, Budapest, Hungary; and 4Center for Human Movement Sciences, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands ABSTRACT Ureczky, D, Va´cz, G, Costa, A, Kopper, B, Lacza, Z, Hortoba´gyi, T, and Tihanyi, J. The effects of short-term exercise training on peaktorque are time- and fiber-type dependent. J Strength Cond Res 28(8): 2204–2213, 2014—We examined the susceptibility of fast and slow twitch muscle fibers in the quadriceps muscle to eccentric exercise–induced muscle damage. Nine healthy men (age: 22.5 6 1.6 years) performed maximal eccentric quadriceps contractions at 1208$s21 over a 1208 of knee joint range of motion for 6 consecutive days. Biopsies were taken from the vastus lateralis muscle before repeated bouts of eccentric exercise on the third and seventh day. Immunohistochemical procedures were used to determine fiber composition and fibronectin activity. Creatine kinase (CK) and lactate dehydrogenase (LDH) were determined in serum. Average torque was calculated in each day for each subject. Relative to baseline, average torque decreased 37.4% till day 3 and increased 43.0% from the day 3 to day 6 (p , 0.001). Creatine kinase and LDH were 70.6 and 1.5 times higher on day 3 and 75.5 and 1.4 times higher on day 6. Fibronectin was found in fast fibers in subjects with high CK level on day 3 and 7 after exercise, but on day 7, fibronectin seemed in both slow and fast fibers except in muscles of 2 subjects with high fast fiber percentage. Peak torque and muscle fiber-type composition measured at baseline showed a strong positive association on day 3 (r = 0.76, p , 0.02) and strong negative association during recovery between day 3 and day 6 (r = 20.76, p , 0.02), and day 1 and day 6 (r = 0.84, p , 0.001). We conclude that the damage of fast fibers preceded the damage of slow fibers, and muscles with slow fiber dominance were more susceptible to repeated bouts of eccentric exercise Address correspondence to Dr. Jo´zsef Tihanyi, [email protected]. 28(8)/2204–2213 Journal of Strength and Conditioning Research Ó 2014 National Strength and Conditioning Association
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than fast fiber dominance muscles. The data suggest that the responses to repeated bouts of eccentric exercise are fibertype–dependent in the quadriceps muscle, which can be the basis for the design of individualized strength training protocols.
KEY WORDS eccentric exercise, knee extensors, muscle damage, fiber composition, fibronectin INTRODUCTION
E
ccentric compared with concentric exercise is associated with unique neural (11,23,25,26,46), biophysical (19,45), metabolic (12), cardiovascular (23,30), and clinical (10,13,33) characteristics and adaptations. Less understood is the muscle fiber-type– specific adaptations following bouts of eccentric exercise. Some initial studies suggested that the recruitment order during eccentric contraction deviates from the orderly recruitment of motor units (29,41,42). However, recent studies correct this view and identify the distinctive property of motor unit recruitment as a slower rate of discharge of action potentials by the motoneurons during eccentric compared with concentric contractions (11,16). Although it is well documented that high-force eccentric contractions produce myofibrillar disruption (8,26,28), biochemical, histochemical, and immunocytochemical studies report inconsistent findings concerning the muscle fiber-type specificity of the disruption. Several studies observed greater susceptibility to damage in type II muscle fibers, fibers comprising type IIa and IIx myosin-heavy chains, and satellite cells associated with type II fibers in human (4,15,16,31,36), animal (35,50), and other models (18) following bouts of eccentric exercise. However, there is also evidence for a preferential disruption in type I muscle fibers (1,20,38,50). Whether the magnitude of muscle damage is associated with muscle fiber-type composition is unclear. Using creatine kinase (CK) and lactate dehydrogenase (LDH) as indirect
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TABLE 1. Study design.*† Pre-ex Exercise DOMS Biopsy Blood test
3
D1
D2
D3
D4
D5
D6
6 3 15 3
6 3 15 3
6 3 15 3 3 3
6 3 15 3
6 3 15 3
6 3 15 3
3
D7 3 3 3
*DOMS = delayed onset muscle soreness. †On days 1, 2, 3, 4, 5, and 6, six sets of eccentric contraction of the knee extensors were performed with 15 repetitions in each.
Average peak torque was calculated for the first, third, and sixth sessions. Delayed onset muscle soreness was estimated on each intervention day. Pre-exercise (pre-ex) biopsy was taken 3 days before intervention. Blood was collected on days 1, 3, and 7.
markers of myofibrillar disruption, there was no relationship between muscle damage and muscle fiber-type composition in the knee extensors, but subjects whose vastus lateralis had a higher proportion of type II fibers did tend to report more muscle soreness (37). In addition, the association between torque loss and muscle fiber-type composition is unknown as are the effects of the number of eccentric bouts on this relationship. This latter factor is especially relevant because 1 eccentric bout of exercise causes myofibrillar disruption (2) and torque loss for up to 72 hours, but subsequent eccentric exercises produce rapid strength recovery and even strength gains coupled signs of less or no damage (5,9,23,24,48). Although CK and LDH have been often used as indirect markers of muscle damage (7,22), no significant relationship was reported between these markers and muscle fiber-type composition in the knee extensors (37). Moreover, the increased CK and LDH activity cannot indicate which type of fibers is subjected to damage.
Therefore, we also used fibronectin to quantify muscle damage more directly. Fibronectin is located in the endomysium and is normally absent in the sarcoplasm. However, after eccentric exercise, it appears in the sarcoplasm of the damaged muscle fibers and thus could serve as an indicator of myofibrillar disruption (17). Taken together, the purpose of this study was to determine the magnitude of torque loss, muscle fiber-type disruption, and the association between these 2 factors over the course of 6 days of maximal force eccentric exercise of the quadriceps muscle in healthy sedentary men.
METHODS Experimental Approach of the Problem
The eccentric exercise protocol consisted of 6 sets of 15 repetitions for 6 consecutive days (Table 1). Before exercise on days 1 and 3, and 24 hours after the last exercise session (day 7), venous blood was collected to measure CK and LDH concentration. The first muscle biopsy samples were taken 3 days before the intervention to avoid the effect of the exercise performed on the first day on the muscle biopsy samples. The second and third biopsies were taken on day 3 and day 7. The muscle biopsy procedure started 1 hour after the end of the exercise in all cases. Delayed onset muscle soreness (DOMS) was estimated on each day (D1–D7). Subjects
Nine healthy sedentary men participated in this experiment (age: 22.5 6 1.6, range: 20–24 years, mass: 82.2 6 8.0 kg, height: 180.0 6 5.1 cm) who, for at least up to 6 months before the study, were not involved in strenuous eccentric exercise. One subject was unable to continue the eccentric exercise intervention after the third day because of extreme soreness and pain. However, blood samples and biopsies were available from this subject. The university ethics committee approved the study protocol and each participant signed a written informed consent. Figure 1. Posture of the subject on the experimental setup during eccentric exercise. The picture shows the initial knee joint angle (108) and the range of motion (1208).
Eccentric Exercise Intervention
Subjects first warmed up by riding a bicycle ergometer for 10 minutes and static stretching of the leg muscles, VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Eccentric Exercise and Fiber Composition padded metal cuff placed around the shin just above the ankle (Figure 1). The transverse axis of the knee joint was aligned with the lever arm’s axis of rotation. To prevent the body from sliding on the bench, subjects grasped a handle mounted on each side of the dynamometer bench. When participants felt comfortable on the dynamometer, as a warm-up, they performed 15 eccentric contractions with the right leg each day before the training protocol without resisting against the rotating lever arm maximally. Subjects received careful instructions how to resist the lever arm rotation accessories. Eccentric quadriceps contraction started with the knee flexed 108 (nearly straight knee, just below horizontal). To initiate the rotation of the lever arm, subjects had to generate 20 Nm of torque Figure 2. Typical torque-time curves recorded during 15 repetitions of maximal effort eccentric contractions of and then the electric motor the quadriceps muscle at 1208$s21 over 1208 of range of motion. Peak torque was determined for each started to rotate and flex the contraction then averaged. A, B and C represent torque-time, angular velocit-time and angle-time curves, respectively. knee joint at 1208$s21. Figure 2 shows a typical recording of the torque-time curve recorded over the 1208 range of especially of knee extensors was performed for 5 minutes. motion. At the end of contraction, the lever arm reversed Subjects lay prone on the padded bench of a custom-built its rotation and passively returned the leg to the starting computer-controlled dynamometer (MultiCont II; Mechaposition at 608$s21. Then, the subject started the tronic Kft, Szeged, Hungary). The trunk, hip, and thighs were next contraction without any delay. During testing and stabilized with special accessories and straps. The right leg training, subjects received strong verbal encouragement was connected to the lever arm through an adjustable and to achieve maximal effort. On each day, subjects performed 6 sets of 10 repetitions with 2 minutes of rest between sets. Delayed Onset Muscle Soreness
Delayed onset muscle soreness was measured using a 10-cm perceived analog scale. The subjects were instructed that the left end of the scale represents no pain, whereas the right end represents extreme pain. Thereafter, all subjects were instructed to make a mark along the line according to their perceived pain on palpation of their quadriceps muscle. The first measurement was taken 8 hours after the first exercise session and thereafter, measurements were taken 24 hour after that point. Data Collection and Calculation of Torque Production Figure 3. Mean 6 SD of average peak torque calculated for session on day 1 (D1), day 3 (D3), and day 6 (D6). *Significant difference between D1 and D3, and D3 and D6.
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Peak torque from each torque—time curve was automatically selected by the customized software of the equipment and was inspected individually. The 15 peak torque values in each set were averaged, and the set averages were again
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goat anti-mouse). Nuclei were counterstained with Hoechst (Hoechst 33342; 1:1000). Visualization of the samples was performed with a Zeiss LSM510 META confocal fluorescent microscope. Two independent researchers evaluated fibronectin activity, and the number of damaged fibers was expressed as percent of the total number of fibers in the cross-section. The presence of fibronectin antibody signaling was the criterion to classify a fiber as damaged. Figure 4. Delayed onset muscle soreness peaked at day 3 and then gradually decreased such that at day 5 was significantly lower from day 3. Values are mean 6 SD. *Significant difference (p # 0.05) vs. pre-exercise level. #Significant difference (p # 0.05) vs. day 3. D1*: measurement was taken 8 hours after the first exercise session and thereafter, measurements were taken 24 hours after that point.
averaged for session on D1, D3, and D6 for each subject. Differences between D1, D3, and D6 were calculated and used for correlation analysis. Immunohistochemistry
Muscle biopsy samples weighing 40–60 mg were obtained with the single insertion and double-chop technique from the middle portion of the vastus lateralis using the percutaneous needle biopsy technique with suction to maximize muscle size sample 3 days before the start of the intervention on day 3 and day 7 (2,14). The samples were fixed in 7% buffered formaldehyde and embedded in paraffin. Immunohistochemical staining was performed using antibodies specific for fibronectin (polyclonal, rabbit antihuman, DakoCytomation, A 0245) and IGF-1 antigens and for differentiation of slow and fast fibers (Monoclonal antiMyosin, Skeletal, Fast; antibody produced in mouse, 1:400, Cat. number: M4276, Sigma, secondary antibody Alexa Fluor 488 goat anti-rabbit IgG, Alexa Fluor 546
Enzyme Activity
Bloodsamples of ;10 ml were drawn from an antecubital vein on days 1 and 3, and 24 hours after the last exercise session (day 7). The serum was separated and frozen at 2808 C for later analysis. Blood samples were analyzed with standard CK and LDH kits (Diagnosticum Zrt and Dialab Ltd, Budapest, Hungary), respectively, in a clinical chemistry analyzer (Hitachi 902).
Statistical Analyses
Mean and SD were calculated for each variables. We checked each variable for normality with the Shapiro-Wilk’s W test. Creatine kinase, LDH activities, and fiber composition were analyzed using Friedman analysis of variance (ANOVA) followed by Wilcoxon Matched Pairs post hoc test. Peak torque was analyzed with a repeated measures of ANOVA followed by Scheffe’s post hoc test. We computed Pearson’s product-moment correlations to determine the relationship between muscle fiber-type composition, DOMS indices, and peak torque measured on day 1, 3, and 6, and changes in peak torque. The level of significance was set at p # 0.05.
RESULTS Muscle Fiber Type Composition
TABLE 2. Mean and SD for CK and LDH concentration measured in the first, third, and sixth days.*
CK (IU$L21) LDH (IU$L21)
D1
D3
D6
165.4 665.8 283.0 658.6
11,684.6 629,425.9 417.9 6300.4
12,483.3a 617,249.8 400.4† 687.7
*CK = creatine kinase; LDH = lactate dehydrogenase. †Significant difference between D1 and D6 (p , 0.003).
The percent of ST fiber was 44.2 (611.2), 41.4 (611.8), and 42.5 (615.1) in the first, second, and third biopsy, respectively (p . 0.05). We used the baseline ST% in the correlation analyses. Maximal Voluntary Torque
Mp was 411.0 6 55.1 Nm on day 1, which reduced 39.0 6 13.9% reaching the lowest value (249.1 6 62.0 Nm) during VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Eccentric Exercise and Fiber Composition baseline and increased 2.9-fold on day 3 (p = 0.013) and was still elevated (p = 0.014) on day 6. Fibronectin Antibody Staining
Figure 5. Individual ST fiber percents and creatine kinase concentration (open bars) on day 3 (D3) and day 7 (D7). Black bars represent the averages in the categories of in FT (fibronectin was found in FT fibers), in ST and FT (fibronectin was found in both ST and FT fibers), and none (no fibronectin appeared either fiber types).
Figure 5 summarizes the results of sarcoplasmic fibronectin staining. There was only minor fibronectin staining in the sarcoplasm on day 3 except in 1 subject with the highest ST% who also had extremely high CK levels (89,700 IU L21). This subject was unable to continue the study. Figure 6 shows that in this subject, the FT fibers were damaged predominantly, with damage also present in ST fibers. Three subjects showed fibronectin in FT fibers on day 3. However, fibronectin staining was most pronounced in biopsy samples taken on day 7 (third biopsy) and was higher than that on day 3. In 2 subjects who had 32 and 36% FT fibers, the FT fibers did show sarcoplasmic fibronectin antibodies. In 4 subjects, fibronectin was present also in the ST fibers. Correlation Analyses
intervention (p , 0.001). Mp recovered by day 6 compared with day 3 (341.2 6 78.4 Nm) and the 15.6 6 21.1% increase was significant (p , 0.001). The difference between day 1 and day 6 was not significant (Figure 3). Delayed Onset Muscle Soreness
Delayed onset muscle soreness peaked at D3 and increase from D1 to D2, and from D2 to D3 was significant (p , 0.001). Then, DOMS decreased gradually reaching the lowest level in D6. The mean calculated in D5 and D6 was significantly lower than that in D3 (p , 0.001). In D6, DOMS was less than in D1, but the difference was not significant (Figure 4).
There was no significant correlation between ST% and peak torque measured on days 1, 3, and 6. Figure 7A shows that the magnitude of decline in peak torque from day 1 to day 3 correlated with ST% at baseline (r = 0.76, p , 0.02). Figure 7B shows that there also was an association between the recovery of peak torque between day 3 and day 6 and ST% at baseline (r = 20.76, p , 0.02). There also was an association between the changes in peak torque from day 1 to day 6 and ST% at baseline (r = 0.84, p , 0.001) (Figure 7C). There was no association between muscle fiber-type composition and changes in CK and LDH activity at any time point.
Enzyme Activity
DISCUSSION
Table 2 shows that CK concentration was in the range of normal values at baseline, but on days 3 and 6, it increased 70.6- and 75.5-fold over day 1 (both p , 0.001). The LDH concentration was in the range of the normal values at
Results of this study show a time-dependent variation in the association between muscle fiber-type composition and the level of torque after 6 days of high-force and largeamplitude eccentric exercise of the quadriceps muscle in
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Figure 6. The presence of fibronectin staining in muscle fibers, with green color indicating fibronectin antibodies inside the cells. Subject A with FT dominance. A1) Before eccentric training; A2) Day 3 of training, no fibronectin activity; A3) Day 6 of training day, some fibers exhibit fibronectin staining. Subject B with ST fibers dominance. B1) Before training; B2) Day 3 of training with FT fibers exhibiting greater presence of fibronectin staining; B3) Day 6, almost all fibers, including ST fibers exhibit fibronectin staining. Magnification 363.
sedentary healthy men. Although eccentric exercise produced significant DOMS, indirect markers of DOMS revealed no association with changes in torque or fiber-type composition. Based on cumulative evidence from previous studies, we specified large amplitude, medium speed, and moderate number of repetitions performed at maximal intensity as parameters for the eccentric protocol to maximize the exercise effects on the quadriceps muscle (40,47). As before, sedentary male subjects who were unaccustomed to eccentric exercise experienced significant (39%) torque loss on day 3 after bouts of eccentric exercise (3,8,15,26,37). The interpretation of the association between torque loss and muscle fiber composition is complex. The present results extend previous findings by observing that the large variation in torque loss (66.2–260.6 Nm) was associated with muscle fiber composition of the vastus lateralis on day 3: a higher proportion of ST fibers correlated with a greater decline in peak torque. An analysis of the fibronectin data however revealed that the exercise preferentially damaged FT fibers in muscles that are comprised predominantly ST fibers. Although initial studies suggested a deviation from the orderly recruitment of motor units during eccentric compared with concentric contractions in hand and foot muscles (29,41,42), recent reviews concluded that large vs. small motor units do discharge action potentials at a slower rate during eccentric
contractions but the recruitment occurs according the size principle (11,46). In view of new evidence, although the outdated view is still embraced (e.g., study by Cermak et al. (4)), it is unlikely that an altered motor unit recruitment is involved in the eccentric exercise–evoked effects on muscle. Biochemical, histochemical, and immunocytochemical studies observed greater susceptibility to damage in type II muscle fibers, fibers comprising type IIa and IIx myosinheavy chains, and satellite cells associated with type II fibers in human (4,15,16,31,36), animal (35,50), and primary cell cultures following bouts of eccentric exercise or passive mechanical stretch exerted on myotubes (18). However, there is also evidence for a preferential disruption in ST muscle fibers (1,20,38,50). In addition, there is evidence that eccentric exercise can stimulate satellite cells in FT muscle fibers without muscle damage (4), increase maximal voluntary force ;20% without any change in MHC composition (44), and eccentric exercise can also cause DOMS, large increases in CK, and ultrastructural damage in 68% of the total counted pixels in electron micrographs while voluntary torque is normal, pre-exercise levels (26). There is thus a large variation in the responses to bouts of eccentric exercise in the healthy quadriceps muscle. Still, the preponderance of evidence suggests that a single bout of eccentric exercise administered with parameters similar to those used VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Eccentric Exercise and Fiber Composition composition, the stretch lengthens the FT fibers further down the descending limb of their length-tension curve but additional studies concluded that the amount of damage was independent of fiber-type composition (43). Another prediction is that there are fiber-type–specific differences in structural proteins such as desmin and titin but eccentric exercise failed to affect these proteins in a fiber-type–specific manner (4). However, because the myofilament lattice is the site where the injury process is thought to originate (43), the possibility still exists that fiber-specific differences in the structure proteins are key in the mechanism of muscle damage. This is because eccentric exercise caused more damage in those chemically skinned human vastus lateralis muscle fibers, which had an abundance of MHC IIa/IIx but not MHC type I, suggesting that the damaged fibers have myofilament weakness (6). The methods of this study did not allow us to confirm this specific mechanism, but through fibronectin data, add confirmatory evidence for human FT vs. ST fibers being more susceptible to muscle damage after bouts of eccentric exercise and that fiber-type composition is associated with the magnitude of damage. We speculate that in individuals Figure 7. Relationship between muscle fiber-type composition (ST%) and the changes in peak torque (dMp in Nm). Panels A and B, respectively, show the association between loss of peak torque and recovery of peak torque with an ST dominant fiberand slow-twitch muscle fiber percent (ST%) measured at baseline. Panel C shows the association between type composition, the fewer recovery of peak torque by day 6 from day 2 (delta score) and ST% measured at baseline. number of FT fibers had to be repeatedly recruited during the initial exercise bouts, causing the FT fibers become damaged, leading to the torque loss. in this study can cause fiber-type–specific adaptations in The sporadic presence or an absence of fibronectin antihealthy humans. Although FT fibers may be susceptible to bodies in muscle fibers of FT-dominant muscles supports eccentric contractions, such susceptibility does not necessarthis contention. ily mean that there is a reversal of the orderly recruitment of The recovery of torque loss starts 2 or 3 days after the initial motor units from slow to fast. bout of eccentric exercise, and most often, it is accompanied Why FT fibers are susceptible to damage is unclear. One by a normalization of biochemical (e.g., CK and LDH hypothesis is that in muscles with extreme ST fiber
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Journal of Strength and Conditioning Research activity) and neuromuscular function (e.g., electromyographic activity, excitation-contraction coupling) (1,5,9,26,39,48). We observed that peak torque has substantially recovered by day 6 but CK activity was ;76 times higher than baseline. These data agree with a previous study that also showed dissociation between a recovery to normal levels of force but ongoing disruption of the sarcolemma detected by electron microscopy (26). In this study, we found no association between the changes in peak torque, CK, LDH, and muscle fibertype composition, confirming previous data (37). Curiously, previous studies did not examine how and whether the changes in these variables during the course of recovery are associated with torque recovery and muscle fiber-type composition. We observed a strong association in torque recovery and muscle fiber-type composition measured at baseline so that the recovery was greater in subjects with a higher FT% (Figure 4B, C). This study thus adds to the published data on muscle damage and fiber-type composition by showing timevarying changes in the association of peak torque and fibertype composition at baseline because this association is strong positive on day 3 and strong negative during recovery between day 3 and day 6, and day 1 and day 6. We speculate that the faster recovery of voluntary torque in muscles with low ST% may be related to the restoration of excitationcontraction coupling and the early neural adaptation (24,26– 28,51). There are now several studies that examined the effects of single or multijoint eccentric exercise administered over a variety of time frame in sedentary, athletic, and clinical populations (2,30,34,48). For example, there is an emerging hypothesis that muscle weakness in old age is the result of an exaggerated susceptibility to contraction-induced injury and the subsequent inability to fully recover from these injuries and that some form of eccentric exercise is effective to combat this weakness (6,21,24,32,34). There is also anecdotal and experimental evidence that highly trained athletes incorporate in their conditioning program eccentrically biased exercises (49). In this regard, we note a consistent pattern across these studies that short-term eccentric training made up of bouts of eccentric exercise repeated over consecutive days does not exacerbate torque loss and muscle damage. Rather, such training creates positive adaptations in terms of maximal voluntary torque, muscle activation, and myofibrillar function (2001). In addition, it may be possible to individualize exercise training programs based on muscle fiber-type composition because different proportions of the number and intensity of eccentric to concentric contractions in the composition of the program could specifically target ST or FT fibers and the response to such a training program may also vary by the fiber-type composition at baseline. Accordingly, this study increased our understanding concerning the time-varying association between mechanical, physiological, and biochemical characteristics of muscles subjected to eccentric exercise. This study has limitations. The triplicate muscle biopsies inherently limit the sample size. The data are relevant only
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to healthy and highly fit young adults without relevance to clinical populations. A lack of quantification of fibronectin antibodies in sarcoplasm limited the scope of analysis and interpretation of the data. A second limitation is that we did not identify subtypes of type II muscle fibers that prevented us from detecting the more subtle adaptations to eccentric exercise. However, it seems subtypes of FT fibers react similarly to the unaccustomed eccentric exercise (37).
PRACTICAL APPLICATIONS The present data suggest that perhaps fibronectin could be used to monitor the fiber-type specificity of eccentric exercise training in athletes. For example, athletes with a predominantly high proportion of slow twitch muscle fibers in their quadriceps muscle could benefit from highintensity and eccentric contractions executed with largeamplitude lower extremity movements over 2 or 3 consecutive days followed by recovery days. In contrast, athletes with a predominantly high proportion of fast twitch fibers in their quadriceps muscle could preferentially benefit from eccentric exercise delivered over a longer period of time to engage most of the fast fibers. The data also point to the possibility that athletes with high fast twitch content in their quadriceps muscle could respond favorably to eccentric exercise using higher training loads (greater number of repetitions and sets). Most likely, such a program should be delivered over a fewer number days than the conventional high-intensity programs.
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17. Gulati, AK, Reddi, AH, and Zalewski, AA. Distribution of fibronectin in normal and regenerating skeletal muscle. Anat Rec 204: 175–183, 1982. 18. Hanke, N, Kubis, HP, Scheibe, RJ, Berthold-Losleben, M, Husing, O, Meissner, JD, and Gros, G. Passive mechanical forces upregulate the fast myosin heavy chain IId/x via integrin and p38 MAP kinase activation in a primary muscle cell culture. Am J Physiol Cell Physiol 298: C910–C920, 2010. 19. Herzog, W. Mechanisms of enhanced force production in lengthening (eccentric) muscle contractions. J Appl Physiol (1985) 2013. doi:10.1152/japplphysiol.00069.2013. 20. Hody, S, Lacrosse, Z, Leprince, P, Collodoro, M, Croisier, JL, and Rogister, B. Effects of eccentrically and concentrically biased training on mouse muscle phenotype. Med Sci Sports Exerc 45: 1460– 1468, 2013. 21. Hortobagyi, T. The positives of negatives. J Gerontol A Biol Sci Med Sci 58: M417–M418, 2003. 22. Hortobagyi, T and Denahan, T. Variability in creatine kinase: Methodological, exercise, and clinically related factors. Int J Sports Med 10: 69–80, 1989. 23. Hortobagyi, T and DeVita, P. Favorable neuromuscular and cardiovascular responses to 7 days of exercise with an eccentric overload in elderly women. J Gerontol A Biol Sci Med Sci 55: B401– B410, 2000. 24. Hortobagyi, T, DeVita, P, Money, J, and Barrier, J. Effects of standard and eccentric overload resistive exercise training in young women. Med Sci Sports Exerc 33: 1206–1212, 2001. 25. Hortobagyi, T, Hill, JP, Houmard, JA, Fraser, DD, Lambert, NJ, and Israel, RG. Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol (1985) 80: 765–772, 1996. 26. Hortobagyi, T, Houmard, J, Fraser, D, Dudek, R, Lambert, J, and Tracy, J. Normal forces and myofibrillar disruption after repeated eccentric exercise. J Appl Physiol (1985) 84: 492–498, 1998.
37. Magal, M, Dumke, CL, Urbiztondo, ZG, Cavill, MJ, Triplett, NT, Quindry, JC, McBride, JM, and Epstein, Y. Relationship between serum creatine kinase activity following exercise-induced muscle damage and muscle fibre composition. J Sports Sci 28: 257–266, 2010. 38. Mair, J, Mayr, M, Muller, E, Koller, A, Haid, C, Artner-Dworzak, E, Calzolari, C, Larue, C, and Puschendorf, B. Rapid adaptation to eccentric exercise-induced muscle damage. Int J Sports Med 16: 352–356, 1995. 39. McHugh, MP, Tyler, TF, Greenberg, SC, and Gleim, GW. Differences in activation patterns between eccentric and concentric quadriceps contractions. J Sports Sci 20: 83–91, 2002. 40. Morgan, DL and Proske, U. Popping sarcomere hypothesis explains stretch-induced muscle damage. Clin Exp Pharmacol Physiol 31: 541– 545, 2004. 41. Nardone, A, Romano, C, and Schieppati, M. Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles. J Physiol 409: 451–471, 1989. 42. Nardone, A and Schieppati, M. Shift of activity from slow to fast muscle during voluntary lengthening contractions of the triceps surae muscles in humans. J Physiol 395: 363–381, 1988. 43. Proske, U and Morgan, DL. Muscle damage from eccentric exercise: Mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537: 333–345, 2001. 44. Raue, U, Terpstra, B, Williamson, DL, Gallagher, PM, and Trappe, SW. Effects of short-term concentric vs. eccentric resistance training on single muscle fiber MHC distribution in humans. Int J Sports Med 26: 339–343, 2005. 45. Roig, M, Macintyre, DL, Eng, JJ, Narici, MV, Maganaris, CN, and Reid, WD. Preservation of eccentric strength in older adults: Evidence, mechanisms and implications for training and rehabilitation. Exp Gerontol 45: 400–409, 2010. 46. Sekiguchi, H, Nakazawa, K, and Hortoba´gyi, T. Neural conrol of muscle lengthening: Task- and muscle-specificity. J Phys Fitness Sports Med 2: 191–201, 2013.
27. Howatson, G, Van, Someren, K, and Hortobagyi, T. Repeated bout effect after maximal eccentric exercise. Int J Sports Med 28: 557–563, 2007.
47. Talbot, JA and Morgan, DL. The effects of stretch parameters on eccentric exercise-induced damage to toad skeletal muscle. J Muscle Res Cell Motil 19: 237–245, 1998.
28. Howatson, G and van Someren, KA. Evidence of a contralateral repeated bout effect after maximal eccentric contractions. Eur J Appl Physiol 101: 207–214, 2007.
48. Vaczi, M, Costa, A, Racz, L, and Tihanyi, J. Effects of consecutive eccentric training at different range of motion on muscle damage and recovery. Acta Physiol Hung 96: 459–468, 2009.
29. Howell, JN, Fuglevand, AJ, Walsh, ML, and Bigland-Ritchie, B. Motor unit activity during isometric and concentric-eccentric contractions of the human first dorsal interosseus muscle. J Neurophysiol 74: 901–904, 1995.
49. Vaczi, M, Tihanyi, J, Hortobagyi, T, Racz, L, Csende, Z, Costa, A, and Pucsok, J. Mechanical, biochemical, and electromyographic responses to short-term eccentric-concentric knee extensor training in humans. J Strength Cond Res 25: 922–932, 2011.
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51. Warren, GL, Hermann, KM, Ingalls, CP, Masselli, MR, and Armstrong, RB. Decreased EMG median frequency during a second bout of eccentric contractions. Med Sci Sports Exerc 32: 820–829, 2000.
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Department of Biomechanics, Kinesiology and Informatics, Faculty of Physical Education, and Sport Sciences, Semmelweis University, Budapest, Hungary; 2Department of Physical Education, Faculty of Pedagogy, Kaposva´r University, Kaposva´r, Hungary; 3Institute of Human Physiology and Clinical Experimental Research, Faculty of Medicine, Semmelweis University, Budapest, Hungary; and 4Center for Human Movement Sciences, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands ABSTRACT Ureczky, D, Va´cz, G, Costa, A, Kopper, B, Lacza, Z, Hortoba´gyi, T, and Tihanyi, J. The effects of short-term exercise training on peaktorque are time- and fiber-type dependent. J Strength Cond Res 28(8): 2204–2213, 2014—We examined the susceptibility of fast and slow twitch muscle fibers in the quadriceps muscle to eccentric exercise–induced muscle damage. Nine healthy men (age: 22.5 6 1.6 years) performed maximal eccentric quadriceps contractions at 1208$s21 over a 1208 of knee joint range of motion for 6 consecutive days. Biopsies were taken from the vastus lateralis muscle before repeated bouts of eccentric exercise on the third and seventh day. Immunohistochemical procedures were used to determine fiber composition and fibronectin activity. Creatine kinase (CK) and lactate dehydrogenase (LDH) were determined in serum. Average torque was calculated in each day for each subject. Relative to baseline, average torque decreased 37.4% till day 3 and increased 43.0% from the day 3 to day 6 (p , 0.001). Creatine kinase and LDH were 70.6 and 1.5 times higher on day 3 and 75.5 and 1.4 times higher on day 6. Fibronectin was found in fast fibers in subjects with high CK level on day 3 and 7 after exercise, but on day 7, fibronectin seemed in both slow and fast fibers except in muscles of 2 subjects with high fast fiber percentage. Peak torque and muscle fiber-type composition measured at baseline showed a strong positive association on day 3 (r = 0.76, p , 0.02) and strong negative association during recovery between day 3 and day 6 (r = 20.76, p , 0.02), and day 1 and day 6 (r = 0.84, p , 0.001). We conclude that the damage of fast fibers preceded the damage of slow fibers, and muscles with slow fiber dominance were more susceptible to repeated bouts of eccentric exercise Address correspondence to Dr. Jo´zsef Tihanyi, [email protected]. 28(8)/2204–2213 Journal of Strength and Conditioning Research Ó 2014 National Strength and Conditioning Association
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than fast fiber dominance muscles. The data suggest that the responses to repeated bouts of eccentric exercise are fibertype–dependent in the quadriceps muscle, which can be the basis for the design of individualized strength training protocols.
KEY WORDS eccentric exercise, knee extensors, muscle damage, fiber composition, fibronectin INTRODUCTION
E
ccentric compared with concentric exercise is associated with unique neural (11,23,25,26,46), biophysical (19,45), metabolic (12), cardiovascular (23,30), and clinical (10,13,33) characteristics and adaptations. Less understood is the muscle fiber-type– specific adaptations following bouts of eccentric exercise. Some initial studies suggested that the recruitment order during eccentric contraction deviates from the orderly recruitment of motor units (29,41,42). However, recent studies correct this view and identify the distinctive property of motor unit recruitment as a slower rate of discharge of action potentials by the motoneurons during eccentric compared with concentric contractions (11,16). Although it is well documented that high-force eccentric contractions produce myofibrillar disruption (8,26,28), biochemical, histochemical, and immunocytochemical studies report inconsistent findings concerning the muscle fiber-type specificity of the disruption. Several studies observed greater susceptibility to damage in type II muscle fibers, fibers comprising type IIa and IIx myosin-heavy chains, and satellite cells associated with type II fibers in human (4,15,16,31,36), animal (35,50), and other models (18) following bouts of eccentric exercise. However, there is also evidence for a preferential disruption in type I muscle fibers (1,20,38,50). Whether the magnitude of muscle damage is associated with muscle fiber-type composition is unclear. Using creatine kinase (CK) and lactate dehydrogenase (LDH) as indirect
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TABLE 1. Study design.*† Pre-ex Exercise DOMS Biopsy Blood test
3
D1
D2
D3
D4
D5
D6
6 3 15 3
6 3 15 3
6 3 15 3 3 3
6 3 15 3
6 3 15 3
6 3 15 3
3
D7 3 3 3
*DOMS = delayed onset muscle soreness. †On days 1, 2, 3, 4, 5, and 6, six sets of eccentric contraction of the knee extensors were performed with 15 repetitions in each.
Average peak torque was calculated for the first, third, and sixth sessions. Delayed onset muscle soreness was estimated on each intervention day. Pre-exercise (pre-ex) biopsy was taken 3 days before intervention. Blood was collected on days 1, 3, and 7.
markers of myofibrillar disruption, there was no relationship between muscle damage and muscle fiber-type composition in the knee extensors, but subjects whose vastus lateralis had a higher proportion of type II fibers did tend to report more muscle soreness (37). In addition, the association between torque loss and muscle fiber-type composition is unknown as are the effects of the number of eccentric bouts on this relationship. This latter factor is especially relevant because 1 eccentric bout of exercise causes myofibrillar disruption (2) and torque loss for up to 72 hours, but subsequent eccentric exercises produce rapid strength recovery and even strength gains coupled signs of less or no damage (5,9,23,24,48). Although CK and LDH have been often used as indirect markers of muscle damage (7,22), no significant relationship was reported between these markers and muscle fiber-type composition in the knee extensors (37). Moreover, the increased CK and LDH activity cannot indicate which type of fibers is subjected to damage.
Therefore, we also used fibronectin to quantify muscle damage more directly. Fibronectin is located in the endomysium and is normally absent in the sarcoplasm. However, after eccentric exercise, it appears in the sarcoplasm of the damaged muscle fibers and thus could serve as an indicator of myofibrillar disruption (17). Taken together, the purpose of this study was to determine the magnitude of torque loss, muscle fiber-type disruption, and the association between these 2 factors over the course of 6 days of maximal force eccentric exercise of the quadriceps muscle in healthy sedentary men.
METHODS Experimental Approach of the Problem
The eccentric exercise protocol consisted of 6 sets of 15 repetitions for 6 consecutive days (Table 1). Before exercise on days 1 and 3, and 24 hours after the last exercise session (day 7), venous blood was collected to measure CK and LDH concentration. The first muscle biopsy samples were taken 3 days before the intervention to avoid the effect of the exercise performed on the first day on the muscle biopsy samples. The second and third biopsies were taken on day 3 and day 7. The muscle biopsy procedure started 1 hour after the end of the exercise in all cases. Delayed onset muscle soreness (DOMS) was estimated on each day (D1–D7). Subjects
Nine healthy sedentary men participated in this experiment (age: 22.5 6 1.6, range: 20–24 years, mass: 82.2 6 8.0 kg, height: 180.0 6 5.1 cm) who, for at least up to 6 months before the study, were not involved in strenuous eccentric exercise. One subject was unable to continue the eccentric exercise intervention after the third day because of extreme soreness and pain. However, blood samples and biopsies were available from this subject. The university ethics committee approved the study protocol and each participant signed a written informed consent. Figure 1. Posture of the subject on the experimental setup during eccentric exercise. The picture shows the initial knee joint angle (108) and the range of motion (1208).
Eccentric Exercise Intervention
Subjects first warmed up by riding a bicycle ergometer for 10 minutes and static stretching of the leg muscles, VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Eccentric Exercise and Fiber Composition padded metal cuff placed around the shin just above the ankle (Figure 1). The transverse axis of the knee joint was aligned with the lever arm’s axis of rotation. To prevent the body from sliding on the bench, subjects grasped a handle mounted on each side of the dynamometer bench. When participants felt comfortable on the dynamometer, as a warm-up, they performed 15 eccentric contractions with the right leg each day before the training protocol without resisting against the rotating lever arm maximally. Subjects received careful instructions how to resist the lever arm rotation accessories. Eccentric quadriceps contraction started with the knee flexed 108 (nearly straight knee, just below horizontal). To initiate the rotation of the lever arm, subjects had to generate 20 Nm of torque Figure 2. Typical torque-time curves recorded during 15 repetitions of maximal effort eccentric contractions of and then the electric motor the quadriceps muscle at 1208$s21 over 1208 of range of motion. Peak torque was determined for each started to rotate and flex the contraction then averaged. A, B and C represent torque-time, angular velocit-time and angle-time curves, respectively. knee joint at 1208$s21. Figure 2 shows a typical recording of the torque-time curve recorded over the 1208 range of especially of knee extensors was performed for 5 minutes. motion. At the end of contraction, the lever arm reversed Subjects lay prone on the padded bench of a custom-built its rotation and passively returned the leg to the starting computer-controlled dynamometer (MultiCont II; Mechaposition at 608$s21. Then, the subject started the tronic Kft, Szeged, Hungary). The trunk, hip, and thighs were next contraction without any delay. During testing and stabilized with special accessories and straps. The right leg training, subjects received strong verbal encouragement was connected to the lever arm through an adjustable and to achieve maximal effort. On each day, subjects performed 6 sets of 10 repetitions with 2 minutes of rest between sets. Delayed Onset Muscle Soreness
Delayed onset muscle soreness was measured using a 10-cm perceived analog scale. The subjects were instructed that the left end of the scale represents no pain, whereas the right end represents extreme pain. Thereafter, all subjects were instructed to make a mark along the line according to their perceived pain on palpation of their quadriceps muscle. The first measurement was taken 8 hours after the first exercise session and thereafter, measurements were taken 24 hour after that point. Data Collection and Calculation of Torque Production Figure 3. Mean 6 SD of average peak torque calculated for session on day 1 (D1), day 3 (D3), and day 6 (D6). *Significant difference between D1 and D3, and D3 and D6.
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Peak torque from each torque—time curve was automatically selected by the customized software of the equipment and was inspected individually. The 15 peak torque values in each set were averaged, and the set averages were again
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goat anti-mouse). Nuclei were counterstained with Hoechst (Hoechst 33342; 1:1000). Visualization of the samples was performed with a Zeiss LSM510 META confocal fluorescent microscope. Two independent researchers evaluated fibronectin activity, and the number of damaged fibers was expressed as percent of the total number of fibers in the cross-section. The presence of fibronectin antibody signaling was the criterion to classify a fiber as damaged. Figure 4. Delayed onset muscle soreness peaked at day 3 and then gradually decreased such that at day 5 was significantly lower from day 3. Values are mean 6 SD. *Significant difference (p # 0.05) vs. pre-exercise level. #Significant difference (p # 0.05) vs. day 3. D1*: measurement was taken 8 hours after the first exercise session and thereafter, measurements were taken 24 hours after that point.
averaged for session on D1, D3, and D6 for each subject. Differences between D1, D3, and D6 were calculated and used for correlation analysis. Immunohistochemistry
Muscle biopsy samples weighing 40–60 mg were obtained with the single insertion and double-chop technique from the middle portion of the vastus lateralis using the percutaneous needle biopsy technique with suction to maximize muscle size sample 3 days before the start of the intervention on day 3 and day 7 (2,14). The samples were fixed in 7% buffered formaldehyde and embedded in paraffin. Immunohistochemical staining was performed using antibodies specific for fibronectin (polyclonal, rabbit antihuman, DakoCytomation, A 0245) and IGF-1 antigens and for differentiation of slow and fast fibers (Monoclonal antiMyosin, Skeletal, Fast; antibody produced in mouse, 1:400, Cat. number: M4276, Sigma, secondary antibody Alexa Fluor 488 goat anti-rabbit IgG, Alexa Fluor 546
Enzyme Activity
Bloodsamples of ;10 ml were drawn from an antecubital vein on days 1 and 3, and 24 hours after the last exercise session (day 7). The serum was separated and frozen at 2808 C for later analysis. Blood samples were analyzed with standard CK and LDH kits (Diagnosticum Zrt and Dialab Ltd, Budapest, Hungary), respectively, in a clinical chemistry analyzer (Hitachi 902).
Statistical Analyses
Mean and SD were calculated for each variables. We checked each variable for normality with the Shapiro-Wilk’s W test. Creatine kinase, LDH activities, and fiber composition were analyzed using Friedman analysis of variance (ANOVA) followed by Wilcoxon Matched Pairs post hoc test. Peak torque was analyzed with a repeated measures of ANOVA followed by Scheffe’s post hoc test. We computed Pearson’s product-moment correlations to determine the relationship between muscle fiber-type composition, DOMS indices, and peak torque measured on day 1, 3, and 6, and changes in peak torque. The level of significance was set at p # 0.05.
RESULTS Muscle Fiber Type Composition
TABLE 2. Mean and SD for CK and LDH concentration measured in the first, third, and sixth days.*
CK (IU$L21) LDH (IU$L21)
D1
D3
D6
165.4 665.8 283.0 658.6
11,684.6 629,425.9 417.9 6300.4
12,483.3a 617,249.8 400.4† 687.7
*CK = creatine kinase; LDH = lactate dehydrogenase. †Significant difference between D1 and D6 (p , 0.003).
The percent of ST fiber was 44.2 (611.2), 41.4 (611.8), and 42.5 (615.1) in the first, second, and third biopsy, respectively (p . 0.05). We used the baseline ST% in the correlation analyses. Maximal Voluntary Torque
Mp was 411.0 6 55.1 Nm on day 1, which reduced 39.0 6 13.9% reaching the lowest value (249.1 6 62.0 Nm) during VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Eccentric Exercise and Fiber Composition baseline and increased 2.9-fold on day 3 (p = 0.013) and was still elevated (p = 0.014) on day 6. Fibronectin Antibody Staining
Figure 5. Individual ST fiber percents and creatine kinase concentration (open bars) on day 3 (D3) and day 7 (D7). Black bars represent the averages in the categories of in FT (fibronectin was found in FT fibers), in ST and FT (fibronectin was found in both ST and FT fibers), and none (no fibronectin appeared either fiber types).
Figure 5 summarizes the results of sarcoplasmic fibronectin staining. There was only minor fibronectin staining in the sarcoplasm on day 3 except in 1 subject with the highest ST% who also had extremely high CK levels (89,700 IU L21). This subject was unable to continue the study. Figure 6 shows that in this subject, the FT fibers were damaged predominantly, with damage also present in ST fibers. Three subjects showed fibronectin in FT fibers on day 3. However, fibronectin staining was most pronounced in biopsy samples taken on day 7 (third biopsy) and was higher than that on day 3. In 2 subjects who had 32 and 36% FT fibers, the FT fibers did show sarcoplasmic fibronectin antibodies. In 4 subjects, fibronectin was present also in the ST fibers. Correlation Analyses
intervention (p , 0.001). Mp recovered by day 6 compared with day 3 (341.2 6 78.4 Nm) and the 15.6 6 21.1% increase was significant (p , 0.001). The difference between day 1 and day 6 was not significant (Figure 3). Delayed Onset Muscle Soreness
Delayed onset muscle soreness peaked at D3 and increase from D1 to D2, and from D2 to D3 was significant (p , 0.001). Then, DOMS decreased gradually reaching the lowest level in D6. The mean calculated in D5 and D6 was significantly lower than that in D3 (p , 0.001). In D6, DOMS was less than in D1, but the difference was not significant (Figure 4).
There was no significant correlation between ST% and peak torque measured on days 1, 3, and 6. Figure 7A shows that the magnitude of decline in peak torque from day 1 to day 3 correlated with ST% at baseline (r = 0.76, p , 0.02). Figure 7B shows that there also was an association between the recovery of peak torque between day 3 and day 6 and ST% at baseline (r = 20.76, p , 0.02). There also was an association between the changes in peak torque from day 1 to day 6 and ST% at baseline (r = 0.84, p , 0.001) (Figure 7C). There was no association between muscle fiber-type composition and changes in CK and LDH activity at any time point.
Enzyme Activity
DISCUSSION
Table 2 shows that CK concentration was in the range of normal values at baseline, but on days 3 and 6, it increased 70.6- and 75.5-fold over day 1 (both p , 0.001). The LDH concentration was in the range of the normal values at
Results of this study show a time-dependent variation in the association between muscle fiber-type composition and the level of torque after 6 days of high-force and largeamplitude eccentric exercise of the quadriceps muscle in
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Figure 6. The presence of fibronectin staining in muscle fibers, with green color indicating fibronectin antibodies inside the cells. Subject A with FT dominance. A1) Before eccentric training; A2) Day 3 of training, no fibronectin activity; A3) Day 6 of training day, some fibers exhibit fibronectin staining. Subject B with ST fibers dominance. B1) Before training; B2) Day 3 of training with FT fibers exhibiting greater presence of fibronectin staining; B3) Day 6, almost all fibers, including ST fibers exhibit fibronectin staining. Magnification 363.
sedentary healthy men. Although eccentric exercise produced significant DOMS, indirect markers of DOMS revealed no association with changes in torque or fiber-type composition. Based on cumulative evidence from previous studies, we specified large amplitude, medium speed, and moderate number of repetitions performed at maximal intensity as parameters for the eccentric protocol to maximize the exercise effects on the quadriceps muscle (40,47). As before, sedentary male subjects who were unaccustomed to eccentric exercise experienced significant (39%) torque loss on day 3 after bouts of eccentric exercise (3,8,15,26,37). The interpretation of the association between torque loss and muscle fiber composition is complex. The present results extend previous findings by observing that the large variation in torque loss (66.2–260.6 Nm) was associated with muscle fiber composition of the vastus lateralis on day 3: a higher proportion of ST fibers correlated with a greater decline in peak torque. An analysis of the fibronectin data however revealed that the exercise preferentially damaged FT fibers in muscles that are comprised predominantly ST fibers. Although initial studies suggested a deviation from the orderly recruitment of motor units during eccentric compared with concentric contractions in hand and foot muscles (29,41,42), recent reviews concluded that large vs. small motor units do discharge action potentials at a slower rate during eccentric
contractions but the recruitment occurs according the size principle (11,46). In view of new evidence, although the outdated view is still embraced (e.g., study by Cermak et al. (4)), it is unlikely that an altered motor unit recruitment is involved in the eccentric exercise–evoked effects on muscle. Biochemical, histochemical, and immunocytochemical studies observed greater susceptibility to damage in type II muscle fibers, fibers comprising type IIa and IIx myosinheavy chains, and satellite cells associated with type II fibers in human (4,15,16,31,36), animal (35,50), and primary cell cultures following bouts of eccentric exercise or passive mechanical stretch exerted on myotubes (18). However, there is also evidence for a preferential disruption in ST muscle fibers (1,20,38,50). In addition, there is evidence that eccentric exercise can stimulate satellite cells in FT muscle fibers without muscle damage (4), increase maximal voluntary force ;20% without any change in MHC composition (44), and eccentric exercise can also cause DOMS, large increases in CK, and ultrastructural damage in 68% of the total counted pixels in electron micrographs while voluntary torque is normal, pre-exercise levels (26). There is thus a large variation in the responses to bouts of eccentric exercise in the healthy quadriceps muscle. Still, the preponderance of evidence suggests that a single bout of eccentric exercise administered with parameters similar to those used VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Eccentric Exercise and Fiber Composition composition, the stretch lengthens the FT fibers further down the descending limb of their length-tension curve but additional studies concluded that the amount of damage was independent of fiber-type composition (43). Another prediction is that there are fiber-type–specific differences in structural proteins such as desmin and titin but eccentric exercise failed to affect these proteins in a fiber-type–specific manner (4). However, because the myofilament lattice is the site where the injury process is thought to originate (43), the possibility still exists that fiber-specific differences in the structure proteins are key in the mechanism of muscle damage. This is because eccentric exercise caused more damage in those chemically skinned human vastus lateralis muscle fibers, which had an abundance of MHC IIa/IIx but not MHC type I, suggesting that the damaged fibers have myofilament weakness (6). The methods of this study did not allow us to confirm this specific mechanism, but through fibronectin data, add confirmatory evidence for human FT vs. ST fibers being more susceptible to muscle damage after bouts of eccentric exercise and that fiber-type composition is associated with the magnitude of damage. We speculate that in individuals Figure 7. Relationship between muscle fiber-type composition (ST%) and the changes in peak torque (dMp in Nm). Panels A and B, respectively, show the association between loss of peak torque and recovery of peak torque with an ST dominant fiberand slow-twitch muscle fiber percent (ST%) measured at baseline. Panel C shows the association between type composition, the fewer recovery of peak torque by day 6 from day 2 (delta score) and ST% measured at baseline. number of FT fibers had to be repeatedly recruited during the initial exercise bouts, causing the FT fibers become damaged, leading to the torque loss. in this study can cause fiber-type–specific adaptations in The sporadic presence or an absence of fibronectin antihealthy humans. Although FT fibers may be susceptible to bodies in muscle fibers of FT-dominant muscles supports eccentric contractions, such susceptibility does not necessarthis contention. ily mean that there is a reversal of the orderly recruitment of The recovery of torque loss starts 2 or 3 days after the initial motor units from slow to fast. bout of eccentric exercise, and most often, it is accompanied Why FT fibers are susceptible to damage is unclear. One by a normalization of biochemical (e.g., CK and LDH hypothesis is that in muscles with extreme ST fiber
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Journal of Strength and Conditioning Research activity) and neuromuscular function (e.g., electromyographic activity, excitation-contraction coupling) (1,5,9,26,39,48). We observed that peak torque has substantially recovered by day 6 but CK activity was ;76 times higher than baseline. These data agree with a previous study that also showed dissociation between a recovery to normal levels of force but ongoing disruption of the sarcolemma detected by electron microscopy (26). In this study, we found no association between the changes in peak torque, CK, LDH, and muscle fibertype composition, confirming previous data (37). Curiously, previous studies did not examine how and whether the changes in these variables during the course of recovery are associated with torque recovery and muscle fiber-type composition. We observed a strong association in torque recovery and muscle fiber-type composition measured at baseline so that the recovery was greater in subjects with a higher FT% (Figure 4B, C). This study thus adds to the published data on muscle damage and fiber-type composition by showing timevarying changes in the association of peak torque and fibertype composition at baseline because this association is strong positive on day 3 and strong negative during recovery between day 3 and day 6, and day 1 and day 6. We speculate that the faster recovery of voluntary torque in muscles with low ST% may be related to the restoration of excitationcontraction coupling and the early neural adaptation (24,26– 28,51). There are now several studies that examined the effects of single or multijoint eccentric exercise administered over a variety of time frame in sedentary, athletic, and clinical populations (2,30,34,48). For example, there is an emerging hypothesis that muscle weakness in old age is the result of an exaggerated susceptibility to contraction-induced injury and the subsequent inability to fully recover from these injuries and that some form of eccentric exercise is effective to combat this weakness (6,21,24,32,34). There is also anecdotal and experimental evidence that highly trained athletes incorporate in their conditioning program eccentrically biased exercises (49). In this regard, we note a consistent pattern across these studies that short-term eccentric training made up of bouts of eccentric exercise repeated over consecutive days does not exacerbate torque loss and muscle damage. Rather, such training creates positive adaptations in terms of maximal voluntary torque, muscle activation, and myofibrillar function (2001). In addition, it may be possible to individualize exercise training programs based on muscle fiber-type composition because different proportions of the number and intensity of eccentric to concentric contractions in the composition of the program could specifically target ST or FT fibers and the response to such a training program may also vary by the fiber-type composition at baseline. Accordingly, this study increased our understanding concerning the time-varying association between mechanical, physiological, and biochemical characteristics of muscles subjected to eccentric exercise. This study has limitations. The triplicate muscle biopsies inherently limit the sample size. The data are relevant only
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to healthy and highly fit young adults without relevance to clinical populations. A lack of quantification of fibronectin antibodies in sarcoplasm limited the scope of analysis and interpretation of the data. A second limitation is that we did not identify subtypes of type II muscle fibers that prevented us from detecting the more subtle adaptations to eccentric exercise. However, it seems subtypes of FT fibers react similarly to the unaccustomed eccentric exercise (37).
PRACTICAL APPLICATIONS The present data suggest that perhaps fibronectin could be used to monitor the fiber-type specificity of eccentric exercise training in athletes. For example, athletes with a predominantly high proportion of slow twitch muscle fibers in their quadriceps muscle could benefit from highintensity and eccentric contractions executed with largeamplitude lower extremity movements over 2 or 3 consecutive days followed by recovery days. In contrast, athletes with a predominantly high proportion of fast twitch fibers in their quadriceps muscle could preferentially benefit from eccentric exercise delivered over a longer period of time to engage most of the fast fibers. The data also point to the possibility that athletes with high fast twitch content in their quadriceps muscle could respond favorably to eccentric exercise using higher training loads (greater number of repetitions and sets). Most likely, such a program should be delivered over a fewer number days than the conventional high-intensity programs.
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