Experimental Gerontology 58 (2014) 69–77

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Mechanical, hormonal, and hypertrophic adaptations to 10 weeks of eccentric and stretch-shortening cycle exercise training in old males Márk Váczi a,⁎, Szilvia A. Nagy b, Tamás Kőszegi c, Míra Ambrus a, Péter Bogner b, Gábor Perlaki b,d, Gergely Orsi b,d, Katalin Tóth e, Tibor Hortobágyi f,g a

Institute of Sport Sciences and Physical Education, University of Pécs, Ifjúság útja 6., 7624 Pécs, Hungary Diagnostic Center of Pécs, Rét utca 2., 7623 Pécs, Hungary Institute of Laboratory Medicine, University of Pécs, Szigeti út 2., 7624 Pécs, Hungary d MTA-PTE Clinical Neuroscience MR Research Group, Rét utca 2., 7623 Pécs, Hungary e Department of Radiography, Faculty of Health Sciences, University of Pécs, 7400 Kaposvár, Hungary f Center for Human Movement Sciences, University Medical Center Groningen, A. Deusinglaan 1, 9700 AD Groningen, The Netherlands g Faculty of Health and Life Sciences, Northumbria University, Newcastle-upon-Tyne, UK b c

a r t i c l e

i n f o

Article history: Received 9 December 2013 Received in revised form 13 July 2014 Accepted 23 July 2014 Available online 23 July 2014 Section Editor: Christiaan Leeuwenburgh Keywords: Aging Stretch-shortening cycle Elastic energy Hormone Hypertrophy Explosive strength

a b s t r a c t The growth promoting effects of eccentric (ECC) contractions are well documented but it is unknown if the rate of stretch per se plays a role in such muscular responses in healthy aging human skeletal muscle. We tested the hypothesis that exercise training of the quadriceps muscle with low rate ECC and high rate ECC contractions in the form of stretch-shortening cycles (SSCs) but at equal total mechanical work would produce rate-specific adaptations in healthy old males age 60–70. Both training programs produced similar improvements in maximal voluntary isometric (6%) and ECC torque (23%) and stretch-shortening cycle function (reduced contraction duration [24%] and enhanced elastic energy storage [12%]) (p b 0.05). The rate of torque development increased 30% only after SSC exercise (p b 0.05). Resting testosterone and cortisol levels were unchanged but after each program the acute exercise-induced cortisol levels were 12–15% lower (p b 0.05). Both programs increased quadriceps size 2.5% (p b 0.05). It is concluded that both ECC and SSC exercise training produces favorable adaptations in healthy old males' quadriceps muscle. Although the rate of muscle tension during the SSC vs. ECC contractions was about 4-fold greater, the total mechanical work seems to regulate the hypetrophic, hormonal, and most of the mechanical adaptations. However, SSC exercise was uniquely effective in improving a key deficiency of aging muscle, i.e., its ability to produce force rapidly. © 2014 Elsevier Inc. All rights reserved.

1. Introduction Sarcopenia is a gradual decline in muscle size and strength, resulting in mobility disability (Beijersbergen et al., 2013; Mitchell et al., 2012). There is some evidence that sarcopenic muscles exhibit preferential type II muscle fiber atrophy caused by age-related shifts in myosin heavy chain content and denervation (Hortobágyi et al., 1995; Lexell, Abbreviations: SSC, stretch-shortening cycle; ECC, eccentric; MRI, magnetic resonance imaging; MVC, maximal voluntary contraction; RTD, rate of torque development; Mecc, peak torque during eccentric contraction; Wssc, total mechanical work during the concentric phase of the stretch-shortening cycle contraction; Wcon, total mechanical work during pure concentric contraction; Tssc, total time to complete the stretch-shortening cycle contraction; ACSA, anatomical cross-sectional area; ICC, intraclass correlation coefficient; SEM, standard error of the measurement; MDC, minimal detectable change. ⁎ Corresponding author. E-mail addresses: [email protected] (M. Váczi), [email protected] (S.A. Nagy), [email protected] (T. Kőszegi), [email protected] (M. Ambrus), [email protected] (P. Bogner), [email protected] (G. Perlaki), [email protected] (G. Orsi), [email protected] (K. Tóth), [email protected] (T. Hortobágyi).

http://dx.doi.org/10.1016/j.exger.2014.07.013 0531-5565/© 2014 Elsevier Inc. All rights reserved.

1995; Nilwik et al., 2013). The conversion of young muscle to a slow phenotype sarcopenic muscle is associated with the slowing of voluntary movements because of the impaired ability to produce force rapidly (Faulkner et al., 2007). In addition, the sarcopenic plantarflexors have a reduced ability to store and reuse elastic energy measured during jumping, consisting of a stretch-shortening cycle (SSC) (Hoffrén et al., 2007; Wilson and Flanagan, 2008) and the velocity component seems to drive the reduction in power measured during SSC in old males (Edwén et al., 2014) and females (De Vito et al., 1998). There is a general consensus that the stretch element or eccentric (ECC) contraction of resistance exercise is an important stimulus in initiating hypertrophy and mechanical adaptations (LaStayo et al., 2003, 2014; Roig et al., 2008). A recent review recommends high-intensity resistance training with moderate velocity in the eccentric phase as an exercise modality for old adults (Granacher et al., 2011). Others demonstrated that interventions using an overload of ECC contractions are superior to exercise training using a standard load (Hortobágyi and DeVita, 2000). ECC contraction is extensively used to prevent atrophy and movement disability (LaStayo et al., 2014) and has been shown to

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improve isometric, eccentric, and concentric strength (Knight and Marmon, 2008; Paddon-Jones et al., 2001; Porter and Vandervoort, 1997) but not explosive strength (Knight and Marmon, 2008; Porter and Vandervoort, 1997). In contrast with the review by Granacher et al. (2011), other papers suggested the implementation of bouts of SSCs, i.e., plyometric training, which would specifically target velocity improvements in elderly (Crawford and Jamnik, 2009; Faulkner et al., 2007; Malisoux et al., 2006). Despite these latter recommendations, there is a paucity of information on the effectiveness of training old adults with SSCs. One of only two studies showed that 8 weeks of plyometric training improved vertical jump height and chair-rise performance in sedentary women age 40–70 (Sáez Sáez de Villarreal et al., 2010). In contrast, 12 weeks of submaximal hopping failed to improve vertical jump performance in 73-year-old untrained males (Rantalainen et al., 2011). While both SSC and pure ECC training stimulus involves lengthening muscle actions, the nature of the eccentric contraction under each condition still differs. One distinguishing feature is the rapidity of the stretch, which has been suggested as a key factor in the stimulus for type II fiberspecific as well as whole muscle hypertrophy (Malisoux et al., 2006; Roig et al., 2008). In SSC, knee angular velocity can vary between 280 and 410°/s, implying high rate of ECC actions (Bobbert et al., 1987). Further, during SSC but not during cycles of isokinetic ECC–concentric contractions, there is a natural tendency to perform the eccentric– concentric transition without a time delay. A training stimulus consisting of such rapid transition selectively increased the stiffness of the type II muscle fibers (Malisoux et al., 2006), an important component of the ability to store and reuse elastic energy. In addition, the rapid eccentric–concentric transition in a SSC movement facilitates the ensuing muscle shortening, hence power generation. Several reviews emphasized the functional significance of exercises in which old adults execute the concentric movement phase rapidly (Fielding et al., 2002; Reid et al., 2008), a feature absent in interventions using pure ECC contractions. Hormonal adaptations to strength training represent an important element in the prevention of sarcopenia. Normally, resting testosterone levels increase and cortisol levels decrease after such interventions in old adults (Kraemer et al., 1999). However, there is a lack of data concerning the changes in these hormone levels following SSC or overloaded ECC exercise training. While bouts of concentric compared with eccentric exercise increased acute cortisol levels more (Gillies et al., 2006; Hollander et al., 2003) with similar testosterone responses in young adults (Durand et al., 2003; Kraemer et al., 2006), it is unknown if exercise with SSC compared with ECC contractions would produce contraction type-specific changes after chronic exercise training in old adults. Changes in testosterone and cortisol levels could be mechanistic markers of muscle anabolism/catabolism and overtraining in the aging muscle. Taken together, the purpose of the present study was to compare the effects of exercise training using SSC and ECC contractions on the mechanical function and size of the quadriceps muscle and hormonal adaptations in healthy old males. We used an experimental approach in which the total mechanical work was identical in the two training groups (Hortobágyi and DeVita, 2000; Moore et al., 2012; Raj et al., 2012). It was hypothesized that mechanical, hormonal, and muscular adaptations would differ in response to SSC vs. ECC exercise. 2. Materials and methods 2.1. Subjects Sixteen 60–70-year old males volunteered for the study in response to announcements posted at campus locations frequented by seniors (Table 1). Subjects were physically active and participated in recreational activities such as swimming, jogging, cycling, tennis, yoga, and horseback riding. None of the subjects were involved in resistance training at

Table 1 Group characteristics. Groups

Age (years)

Body mass (kg)

Height (cm)

Body fat (%)

Physical activity (h/week)

SSC (n = 8) ECC (n = 8)

64.4 ± 4.1 65.7 ± 5.3

77.5 ± 11.9 78.8 ± 7.6

181.6 ± 9.0 173.3 ± 5.9

17.9 ± 3.9 24.0 ± 3.0

3.6 ± 1.1 4.7 ± 1.1

Data are means (±SD). SSC, exercise training using stretch-shortening cycle. ECC, exercise training using eccentric contractions.

the time of the study. Subjects underwent a medical screening and filled in a training and health status questionnaire before the start of the study. Subjects were instructed to maintain their normal physical activity and not to engage in any new unusually intensive physical activity for the duration of the study. Exclusion criteria were abnormal ECG, resting blood pressure N 140 mm Hg, and any other cardiovascular, metabolic, or hormonal disease, recent knee or hip injury, or pain. As a medical precaution, resting blood pressure was measured before each training and testing session in each subject. After providing information about the study, each volunteer signed a written informed consent according to the Declaration of Helsinki. The University Ethics Committee approved the protocol. 2.2. Experimental procedure One week before the first test period subjects were familiarized with the training and test contractions performed on the dynamometer, and percentage of body fat and lean body mass were also measured with a foot-to-foot bioelectric impedance body composition analyzer (TANITA BC-420 MA, Tanita Corporation, Tokyo, Japan). After matching for age and maximal isometric quadriceps strength (described below), subjects were randomly assigned to one of two experimental groups (Table 1). Subjects exercised the quadriceps muscle with either SSC contractions (SSC group) or isokinetic ECC contractions (ECC group) for 10 weeks. There were two test periods, one before and one after the training program. In these periods we assessed, first, the mechanical properties of the quadriceps femoris muscle and then 48 h later, serum hormone levels were measured at rest as well as after an acute bout of eccentric– concentric exercise. The size of the quadriceps was measured at least one week before the beginning of the training program and within three days after the last training session, using magnetic resonance imaging (MRI). Exercise training consisted of unilateral knee extensions. Subjects trained both legs but exercised one leg at a time and only the right leg was tested for muscle mechanics and MRI. The warm up procedure was identical for every test and training session and included: 5 min of pedaling on a stationary cycle ergometer at a self-selected speed and stretching of the lower extremity muscles. 2.3. Mechanical muscle properties The Multicont II dynamometer (Mediagnost, Budapest and Mechatronic Ltd., Szeged, Hungary) was used to test the mechanical properties of the quadriceps femoris. Subjects were seated on the dynamometer's padded seat and performed maximal voluntary isometric contraction (MVC) at 70° of knee flexion (0° = full extension). Subjects were instructed to generate the highest possible torque as fast as possible. Peak torque during isometric MVC (MVC70) and rate of torque development (RTD) were determined offline from the torque–time curves. RTD was quantified as RTD (Nm/ms) = dM (Nm) / dt (ms), where M is the torque and t is the time. RTD was determined for the first 30, 50, and 100 ms intervals from the onset of the contraction (Aagaard et al., 2002). Maximal voluntary isometric torque was also measured at 30° knee angle to determine the trigger threshold for initiating the SSC test contraction (described below).

M. Váczi et al. / Experimental Gerontology 58 (2014) 69–77

To increase the specificity of strength testing, in addition to MVC70, we also measured peak isokinetic eccentric torque at 30°·s−1. The contraction started at 30° and ended at 80° of knee flexion. To determine SSC function, subjects performed a quadriceps SSC protocol in which the dynamometer rapidly applied a preset amount of energy to stretch the quadriceps (Váczi et al., 2011). The eccentric phase of the contraction started at 30° of knee flexion and the subject had to exert force against the lever arm as fast and forcefully as possible. When the subject reached 60% of isometric MVC torque measured previously at 30° of knee flexion, the dynamometer's lever arm started to rotate in the direction of knee flexion. Subjects were instructed to resist the rotating lever arm maximally, stop it within the shortest range of motion (eccentric phase), and then extend the knee without a time delay and as fast as possible to 30°. The initial velocity of the lever arm was 300°·sˉ1 and the preset amount of stretch-load was half of the baseline MVC70. If, for example, MVC70 was 200 Nm for a subject, the stretch-load was set at 100 J for the SSC test contraction. Based on our previous observations such stretch-load to the quadriceps is optimal to produce a knee flexion similar to that in a vertical jump test (Váczi et al., 2011). The applied stretch-load represents the amount of work the dynamometer's lever arm performed on the shank to flex the knee joint. As the eccentric knee flexion progresses, the energy stored in the servomotor diminishes to zero (the lever arm stops) and some of the energy is stored in the quadriceps muscle. The instructions given to the subjects ensured that the transfer of energy that stretched the quadriceps muscle occurred in a short time and over a small range of motion so that the concentric contraction (i.e., knee extension) would start without delay. During the concentric phase, the dynamometer's motor was automatically turned off and provided resistance through friction and the inertia of the lever arm and lower leg. Torque and knee angle as function of time were recorded for each contraction and, similarly to Kyröläinen et al. (1998), we calculated the positive mechanical work (Wssc) during the SSC by integrating the torque–position curve between the boundaries of the range of motion:

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2.4. Magnetic resonance imaging Magnetic resonance measurements were performed using a 3 T Magnetom TIM Trio whole-body MRI scanner (Siemens AG, Erlangen, Germany) with a body matrix coil (centered over the quadriceps muscle) combined with the spine matrix coil (12-element design). The subjects were positioned feet-first supine and scanned from the head of femoral bone to lower extremity of femur. T1-weighted turbo spinecho (T1W) sequence was designed in the coronal section using the following parameters: TR = 890 ms; TE = 11 ms; slice thickness = 2 mm; distance factor = 0% (i.e. no gap); FOV = 398 × 500 mm2; matrix = 204 × 256; receiver bandwidth = 250 Hz/px; averages = 2; echo train length = 4 and interleaved slice order with 2 concatenations. The sequence was acquired without fat suppression. After 10 weeks of training, MRI measurements were repeated for each individual using the same protocol. Before and after training, muscle anatomical cross sectional area (ACSA) was measured on axial reformations of T1W images. Components of the quadriceps (vasti medialis, lateralis, intermedius, and rectus femoris) were delineated manually excluding bone, subcutaneous fat using regions of interest analysis. Regions of interest were outlined at 10% intervals from the points where the muscles were easily identified and their distances were measured proximally from the head of the femur and distally from the adductor tubercle (Fig. 1). The procedure was repeated after training using the defined distances to ensure the within subject measurement replication. To increase the reliability of the measurements, rigid body registration (6 degrees of freedom) was used to align MR images before and after training with the FSL Linear Image Registration Tool Version 4.1.9 (FMRIB Software Library, www.fmrib.ox.ac.uk/fsl/). The ACSAs were then derived from the muscle volumes and the mean ACSA was determined for each subject by averaging the outlined 11 sections from 0 to 100% (Hudelmaier et al., 2010). Values obtained for the four muscles

Zθn W ð JÞ ¼

MðθÞ  dθ θ1

where M = torque, dθ = angular displacement, and θ1 and θn represent the first and the last knee angle data points, respectively. Total time to complete the SSC contraction (Tssc) was also determined. To examine the ability to store and re-use elastic energy, after the SSC test, a pure concentric contraction was performed. For each subject this contraction started exactly at the knee angle where the dynamometer's lever was stopped during the SSC test (transition phase) and ended in the 30° position. Subjects fully relaxed their quadriceps and then performed maximal effort knee extension during which, similarly to the concentric phase of the SSC described above, the dynamometer's motor was turned off, and provided resistance through friction. For this contraction mechanical work (Wcon) was calculated as in the equation above. To investigate the ability to store and re-use elastic energy, positive SSC work and pure concentric work ratio (Wssc/Wcon) was determined. It is important to note that after the training period, the SSC test was repeated with the stretch parameters used at baseline (stretch-load, trigger threshold) in order to determine the changes in Tssc over the 10-week program. However, to correctly examine elastic energy utilization, a modified SSC test was also needed after the training program. This was done because subjects' isometric MVC torque increased over the 10-week training period and stretch loads and trigger thresholds for the SSC test were set according to the current MVCs. In the dynamometric test sessions, in addition to the general warm-up, subjects performed one warm-up trial for each contraction type with a submaximal effort. There were three maximal attempts for each test contraction, and the highest values were included in the data analysis.

Fig. 1. T1W turbo-spin echo image of the right thigh and region of interest (ROI) locations from 0% to 100% (a) and the mirrored image of the “a” picture with representation of the regions of interest (b) for vastus medialis. The same procedure was performed for all muscles. L = lateral side, M = medial side. Bold dashed line is the mirror axis.

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were summed and considered as quadriceps ACSA. For intra-observer reliability analysis, two experienced observers analyzed all scans twice, with an interval of 12 months, and intra-observer differences between the separate occasions were calculated thereafter. Inter-observer reliability was measured between only the first readings of the observers. 2.5. Serum hormones Before and after the 10-week training program total testosterone and cortisol levels were measured before (resting), immediately (IP), and five minutes (5 min) after an acute resistance exercise bout, because previous research suggested that these hormone levels peak within this period (Kraemer et al., 1999). The exercise consisted of three sets of 10 bilateral eccentric–concentric full effort knee extensions on the dynamometer, with 90 s of rest between sets. The contractions were performed at 30°·s−1 between 30° and 80° of knee flexion. For every subject, blood draws and the acute exercise bout were performed between 7 and 8 a.m., a period when testosterone levels vary the least in both young and old males (Brambilla et al., 2009). Venous blood samples were obtained using Vacutainer (Becton Dickinson) plain tubes with gel. After complete coagulation, blood samples were centrifuged at 1500g for 10 min and sera were tested applying a fully automated competitive electrochemiluminescence immunoassay system (Modular E 170 analyzer, ROCHE). 2.6. Training program Table 2 shows the 10-week-long periodized training program. There were 2 to 3 training sessions per week, separated by at least 48 h of rest between sessions. Subjects performed 4 sets of 8 to 14 repetitions of unilateral knee extensions with both legs, with 2 min of rest between sets. The exercising legs were alternated across sets. The training contractions in SSC and ECC groups were similar to the SSC and ECC test contractions. A specific feature of the SSC training was that it consisted of contractions with small duration but high peak torque, while the ECC action lasted longer and had lower peak torques (Fig. 2). However, a unique element of the training program was that the average mechanical work for a session was still similar in the two groups. This was achieved by manipulating the stretch-load in the SSC group. For example, if a subject in the ECC group improved mechanical work production due to adaptation to the training, the stretch-load was adjusted to match subject-pair's mechanical work in the SSC group. This matching paradigm has been used previously (Hortobágyi and DeVita, 2000; Moore et al., 2012; Raj et al., 2012). In our protocol the average stretch-load ranged between 86 J and 120 J (Table 2). After each repetition, the software computed and displayed on the monitor the total work for each contraction. Therefore, the total work stimulus was similar in the two training groups but the nature of the stimulus was different. All exercise bouts were executed in the mornings between 9 and 12. 2.7. Statistical analyses Data are reported as mean and standard deviation. Training induced changes in mechanical and morphometric variables were analyzed using a two-way ANOVA (group × test period) with repeated measures.

Chronic and acute changes in cortisol were analyzed using a three-way ANOVA (group × test period × measurement time). At baseline group SSC vs. group ECC had significantly lower levels of testosterone and testosterone/cortisol ratio; therefore we used an ANCOVA with the baseline values as covariates to analyze the data. In the case of significant interaction the Bonferroni adjustment was used for post-hoc pairwise comparisons. For ACSA, the intra- and inter-observer reliability was assessed using the intraclass correlation coefficient (ICC) with a 2-way mixed model with absolute agreement for continuous variables. ICCs were also determined for the mechanical variables to evaluate test–retest reliability. According to Haley and Fragala-Pinkham (2006), we also calculated the standard error of the measurement (SEM) and the minimal detectable change (MDC) to determine the magnitude of change in a variable that would exceed the threshold of measurement error. An ICC ≥ 0.80 was considered to be acceptable. The statistical significance was set at p b 0.05. The statistical power ranged between 0.50 and 1.0.

3. Results There was no significant difference between groups in the selfreported weekly volume of physical activity (p = 0.374; Table 1). Table 3 shows the test–retest reliability and MDC data for the mechanical variables. Table 4 shows the changes in muscle mechanics. There was a significant test period main effect for MVC70, Mecc, Tssc, and Wssc/Wcon ratio (p b 0.05). There was a significant group by period interaction for RTD30 and RTD50 (p b 0.05), suggesting that the two groups responded differently to the training. Table 4 also shows the exact p values for the ANOVA, and the pairwise comparisons. Fig. 3 shows the hormone data. There was no group by period by time interaction in any of the hormonal variables, suggesting similar responses to the two training regimens. There was a significant time main effect in testosterone (p = 0.010), suggesting that the two exercise bouts (before and after 10 weeks training) uniformly increased testosterone 15% from pre to IP, and then decreased 10% from IP to 5 min post-exercise. The period by time interaction approached significance (p = 0.065). There was a time main effect for cortisol (p = 0.018), suggesting that the two exercise bouts uniformly increased cortisol 21% from pre to IP, and then further increased 6% to 5 min post-exercise. The period by time interaction (p = 0.020) and the post-hoc analyses suggest that in the second test period the acute response for the two groups combined was significantly smaller at 5 min post-exercise (p = 0.027), when compared to the corresponding time point in the first test period. There was a time main effect for testosterone/cortisol ratio (p = 0.002), suggesting that the two exercise bouts uniformly decreased the ratio 17% from pre to 5 min post-exercise. There was a period by time interaction (p = 0.032). The post-hoc analyses show that, compared with the first, in the second test period the ratio was significantly smaller at 5 min post-exercise (p = 0.034). The reliability analysis of ACSA showed significantly high intraobserver (observer 1: ICC 0.97; observer 2: ICC 0.99) and inter-observer (ICC 0.93) agreements. Table 4 shows the changes in quadriceps ACSA. There was a significant time main effect for quadriceps ACSA (p b 0.005) without a group by period interaction.

Table 2 Parameters of the 10-week periodized eccentric and stretch-shortening cycle exercise training programs. The table shows the stretch-load, in J, for the group exercising with the stretchshortening cycle (SSC group). The stretch-load is the amount of energy used for stretching the quadriceps in every single SSC contraction in the SSC group during each week of training. The stretch-load in the SSC group was manipulated from week to week according to the actual total work in the ECC group, making it possible to equate total mechanical work in the two groups. Week

1

2

3

4

5

6

7

8

9

10

Sessions/week Set × repetition/session Stretch-load/contraction (J)

2 4×8 86 ± 26

3 4 × 12 92 ± 22

3 4 × 12 92 ± 22

2 4×8 112 ± 19

3 4 × 13 114 ± 18

3 4 × 13 112 ± 13

2 4 × 10 116 ± 13

3 4 × 14 119 ± 10

3 4 × 14 119 ± 10

2 4 × 10 120 ± 10

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Fig. 2. Representative torque–time curves of a stretch-shortening cycle and an eccentric exercise training contraction performed by one subject in the SSC group and his subject-pair matched for total mechanical work in the ECC group. Total mechanical work, an index used to match pairs of subjects, was calculated between the time points of stretch initiation and the end of the contraction.

4. Discussion To the best of our knowledge, this is the first study that compared the effects of SSC and ECC exercise training on muscle mechanics, muscle size, and hormonal responses in healthy old males. In general, our data provide evidence that the aging male muscle adapts well to slow and rapid stretches with the latter form preferentially improving explosive muscle strength. A unique aspect of the present study was that subjects in SSC and ECC groups were matched on initial level of isometric MVC torque and also on the amount of mechanical work they performed during the training, a design used before (Hortobágyi and DeVita, 2000; Moore et al., 2012; Raj et al., 2012). However, we were still able to vary the nature of the mechanical stimulus: the rate of tension development was about 4-fold greater and the eccentric loading duration was 7-fold shorter in SSC compared with those in ECC. The hypothesis was that rapidity of loading is a key element in triggering favorable adaptations of explosive force in the aging muscle, akin to the idea proposed by proponents of power training that high contraction velocity at medium loads

Table 3 Test–retest reliability results of for the mechanical variables and quadriceps crosssectional area. Intraclass correlation coefficients (ICC) and the 95% confidence intervals (IC) are presented. Standard error of the measurement (SEM) and the minimal detectable change (MDC) expressed in absolute values are also shown to demonstrate the threshold of measurement error. Variables

ICC

CI

SEM

MDC

MVC70 RTD30 RTD50 RTD100 Mecc Tssc Wssc/Wcon ACSA

0.98 0.82 0.87 0.91 0.95 0.96 0.91 0.98

0.96–0.99 0.75–0.90 0.79–0.91 0.80–0.95 0.85–0.98 0.92–0.99 0.84–0.97 0.96–0.99

6.9 0.16 0.15 0.08 11.2 17.3 0.03 135.2

16.1 Nm 0.39 Nm·ms−1 0.35 Nm·ms−1 0.18 Nm·ms−1 26.2 Nm 40.3 ms 0.07 315.6 mm2

MVC70 = maximal isometric voluntary torque measured at 70° of knee flexion. RTD = rate of torque development measured in the 30, 50, and 100 ms interval (subscripts) from the onset of the isometric contraction. Mecc = peak torque during the eccentric contraction. Tssc = total time to complete the SSC test contraction. Wssc = positive work in the SSC test contraction. Wcon = work during the pure concentric contraction. ACSA = anatomical cross-sectional area of the quadriceps.

also results in positive adaptations (Fielding et al., 2002; Reid et al., 2008). While previous studies focused on using ECC exercise training of aging human muscles (Hortobágyi and DeVita, 2000; Knight and Marmon, 2008; LaStayo et al., 2014; Paddon-Jones et al., 2001; Porter and Vandervoort, 1997), the way how SSC training affects mechanical output of healthy aged muscle is less studied and poorly understood. Young practitioners have been using short-term SSC interventions (plyometric training) for over 50 years to improve athletic performance and such SSC training stimulus has been shown to increase explosive and maximum strength, as well as elastic energy storage and reutilization (Markovic and Mikulic, 2010). Similarly to ECC, the SSC contraction contains an ECC muscle action, however, in a way that the stretch rate is high and the eccentric–concentric transition is quick. Although the nature of the training stimulus was thus different between our experimental groups, in spite of the principles of training specificity, we found similar isometric (6%) and eccentric (23%) strength gains. Although the SSC interventions are designed to improve power, a favorable transfer effect to the ability to generate maximal isometric force is often reported in young adults. In a previous study changes in maximal force following SSC training were measured indirectly in old adults using the chair-rise test (Sáez Sáez de Villarreal et al., 2010). The small improvement in isometric MVC torque is not unusual after using either SSC or ECC exercise contractions: there was 7% gain in young males' quadriceps muscle using the SSC stimulus (Váczi et al., 2013) and there was 2% gain in elderly males using the pure ECC stimulus (Mueller et al., 2009). The large, 23% increase in ECC MVC torque in the present study shows contraction-specific effects because both interventions incorporated eccentric muscle action with a strong activation of the quadriceps muscle. Pure ECC stimulus has been demonstrated to increase old adults' ECC MVC torque through reduced neural inhibition in exercise interventions as short as one week (Hortobágyi and DeVita, 2000). Although there are no data in old adults, the SSC training was superior to traditional weight training to induce eccentric strength gains in young males, probably because of the greater tension achieved during the lengthening phase of SSC (Wilson et al., 1996). The SSC is a key factor in muscle economy, which becomes impaired with age (Hortobágyi et al., 1995). Hoffrén et al. (2007) demonstrated impaired tendinous tissue elasticity utilization due to increased muscle activation in the braking phase, and reduced activation in the overcoming

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Table 4 Effects of the 10-week stretch-shortening cycle (SSC) and eccentric (ECC) quadriceps training on muscle mechanics and quadriceps size. Mean values (±SD) for the individual groups, and percentage of changes for the two groups combined (test period main effect) are presented. Asterisk represents significant difference between “before” and “after”, revealed by the posthoc test. For the ANOVA results asterisk represents significant main effect or interaction. Variables

SSC group

ECC group

Before MVC70 RTD30 RTD50 RTD100 Mecc Tssc Wssc/Wcon ACSA

(Nm) (Nm·ms−1) (Nm·ms−1) (Nm·ms−1) (Nm) (ms) (mm2)

218 1.28 1.44 1.14 264 534 1.01 5139

After ±53 ±0.38 ±0.39 ±0.32 ±52 ±79 ±0.10 ±879

230 1.67 1.86 1.13 309 382 1.16 5245

Before ±63 ±1.05* ±1.00* ±0.40 ±72 ±20 ±0.17 ±866

After

216 1.22 1.36 1.03 235 571 0.95 5762

±47 ±0.52 ±0.45 ±0.22 ±39 ±131 ±0.10 ±977

229 1.10 1.34 1.04 306 460 1.04 5938

±62 ±0.87 ±0.94 ±0.43 ±60 ±100 ±0.18 ±985

Test period main effect and % change

Interaction

5.7% 10.4% 14.2% 0.0% 23.2% −23.8% 12.2% 2.5%

p p p p p p p p

p p p p p p p p

= = = = = = = =

0.017* 0.238 0.310 0.421 0.000* 0.000* 0.007* 0.004*

= = = = = = = =

0.438 0.045* 0.041* 0.369 0.248 0.198 0.239 0.421

MVC70 = maximal isometric voluntary torque measured at 70° of knee flexion. RTD = rate of torque development measured in the 30, 50, and 100 ms interval (subscripts) from the onset of the isometric contraction. Mecc = peak torque during the eccentric contraction. Tssc = total time to complete the SSC test contraction. Wssc = positive work in the SSC test contraction. Wcon = work during the pure concentric contraction. ACSA = anatomical cross-sectional area of the quadriceps.

phase of the SSC. During SSC, it is important to have a rapid eccentric– concentric transition because slow transitions can compromise the reuse of elastic energy (Wilson and Flanagan, 2008). Because SSC and

Fig. 3. Acute resistance exercise-induced hormonal responses before and after 10 weeks of stretch-shortening cycle (SSC) or eccentric (ECC) exercise training measured at pre-, immediately post (IP), and 5 min after the acute exercise bout. * Significantly different from the corresponding time point measured before the 10 weeks training (p b 0.05). Vertical bars denote + or −SD.

ECC training stimuli both involve a stretch element, one rapidly and the other slowly, one prediction is that the contraction-speed related differences between the two treatments would differentially affect eccentric–concentric transition time and the ability to store and reuse elastic energy, variables tested for the first time in the present study. Against such predictions, the two interventions produced similar effects when assessed so that the pre- and post-training stretch-loads were set identical: the period main effect revealed 24% faster transition time. For the examination of elastic energy storage and reuse we applied the classic indirect in vivo method (Turner et al., 2003), adapted to a single joint dynamometric SSC model and calculated the work in the concentric phase with and without a stretch. These data demonstrate that, with respect to the negative work, the positive work done by the previously stretched quadriceps increased 12%, independent of the intervention type, suggesting similar improvements in the ability to use elastic energy after the interventions. Improvements in elastic energy storage and its re-use are SSC training-specific adaptations, although such data are limited to young subjects. When Sáez Sáez de Villarreal et al. (2010) examined the effects of plyometric training on jump performance in old adults, subjects increased jump height by greater elastic energy reutilization but the exact mechanisms were unexplored. Such adaptations are often explained with either neural (Bonacci et al., 2009) (more refined motor unit recruitment pattern during stretch) or structural (Malisoux et al., 2006) (increased tendon or fiber stiffness) changes, common influencing factors of muscle economy during cyclic movements (Turner et al., 2003). A unique finding was the group by test period interaction in contractile RTD, demonstrating that the SSC but not ECC stimulus improved explosive strength. The ineffectiveness of ECC exercise training in this regard agrees with previous data (Knight and Marmon, 2008; Porter and Vandervoort, 1997). RTD reflects the neuromuscular system's capacity to recruit muscle fibers rapidly, which determines the ability to move one's limbs rapidly in response to unexpected perturbations often associated with falls. We hypothesized that the rate of stretch, rapid vs. slow, that distinguishes SSC and ECC training stimuli, would induce different RTD gains. During the isometric MVC test, we measured RTD in the 30–100 ms interval, a sensitive window to assess adaptations in type II muscle fiber after SSC training. We observed 30% increase in RTD in the early phase (30–50 ms) of isometric contraction, implying that perhaps adaptations occurred in the fastest motor units following SSC training. In contrast with our results, Maganaris et al. (2004) reported 27% increase in RTD for the 100 ms window in old adults' quadriceps muscle, however this study used a longer (14-week-long) resistance training program than the 10 weeks in the present study. Those authors

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suggested that the increase in RTD was related to an increase in patella tendon stiffness that aided the muscle-to-bone force transmission. Furthermore, the RTD improvements were greater in the earlier (30 ms) vs. later (100 ms) phase of the contraction when very low-fit (hospitalized) elderly exercise-trained the quadriceps for 12 weeks (Suetta et al., 2004). The adaptations in RTD, in addition to the changes in tendon properties, are often attributed to muscle hypertrophy (Suetta et al., 2004), altered neural activation (Aagaard et al., 2002; Suetta et al., 2004), and/or fiber type transformation (Harridge, 1996). Evidence exists that faster (210°/s) vs. slower (20°/s) lengthening contractions can induce greater hypertrophy in type II vs. type I fibers (Shepstone et al., 2005). We speculate that the present SSC stimulus (comprising an initial stretch of 300°/s) caused adaptation similar to that described by Shepstone et al. (2005). Our aim to examine the anabolic changes after ECC and SSC exercise was motivated by data suggesting that the stretch stimulus can play a key role in muscle cell growth (Vandenburgh et al., 1990). In young humans, intensive SSC exercise (Bosco et al., 1996) and even mechanical vibration, consisting of a high number of rapid SSCs, can induce an acute rise in testosterone (Bosco et al., 2000) and such rapid changes can sum to chronic adaptations (Kraemer et al., 1996). In addition, SSC performance was associated with resting testosterone levels in young adults (Bosco et al., 1996). Others suggested the importance of the magnitude of mechanical tension in the muscle during exercise (Buresh et al., 2009). Because SSC comprises both rapid stretch and high tension, it is reasonable to predict that SSC vs. ECC exercise training would be associated with greater anabolic response. Against our expectations, however, we found neither changes in resting levels of testosterone and cortisol nor changes in the acutely induced testosterone response after 10 weeks of either SSC or ECC exercise. These data confirm a series of previous studies that reported no changes in anabolic hormone levels measured at rest after various forms of strength training in elderly despite 15% increase in maximum strength (Häkkinen et al., 2000; Kraemer et al., 1999). While resting cortisol levels in Kraemer's study decreased after 10 weeks, we found no changes in cortisol levels after either training protocol. We speculate that a training protocol that uses a single muscle exercise provides not large enough stimulus to elicit chronic changes, which could be a limitation of studies using similar (single muscle training) models. Studies that examined exercise training-specific regulation of testosterone found no evidence for contraction-specific responses after acute bouts of eccentric and concentric exercise in young males (Durand et al., 2003; Kraemer et al., 2006). Our data extends these findings in young adults to healthy old adults using SSC and ECC contractions. Although the resting values did not change after training, the acute exercise-induced cortisol and testosterone/cortisol ratio responses were 14% lower, and 15% higher, respectively, following 10 weeks of exercise training, suggesting important hormonal adaptations to both ECC and SSC exercise training. Similarly, Kraemer et al. (1999) found greater testosterone/cortisol ratio response after strength training. The ratio is an indicator of overtraining and our data show that the subjects' acute catabolic sensitivity decreased after 10 weeks of training, suggesting that greater training volume could be tolerated without overtraining. We note that our hormone data should be interpreted with caution because the analysis was somewhat underpowered (0.50–0.75), therefore we cannot exclude the possibility that overtraining did occur in some of our subjects. Together, it remains unclear why basal hormonal measures of anabolism and catabolism are resistant to adaptations. It is important to note that although all of our subjects exercised in the mornings between 9 and 12, the exact time of exercise within this period still varied between subjects because only one subject could exercise at a time on the dynamometer. Therefore diurnal variations in the hormone levels affecting the protein turnover (synthesis and degradation) might have influenced strength and muscular adaptations (see review by Hayes et al., 2010). In addition, maximal eccentric and concentric torque also exhibits a circadian pattern, peaking in the

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afternoon (Miles et al., 2008; Sedliak et al., 2008). Therefore, it is possible that the exercise-training stimulus was optimal with respect to the hormonal measures (morning) but not for maximizing the strength response (for which the training should have been delivered in the afternoon). To slow aging-induced atrophy is a primary goal of geriatric rehabilitation. The magnitude of load is an important contributor to muscle hypertrophy (Schoenfeld, 2010). Indeed, exercise training with an overload ECC contraction is superior to exercise training using isometric or concentric-only contractions probably because the muscle is under a greater mechanical tension. Contraction velocity may also play a role in muscle hypertrophy because high-velocity lengthening contractions tend to hypertrophy type II muscle fibers (Shepstone et al., 2005) more than type I fibers, while contractions at moderate speed (longer duration under the mechanical stress) act through the mechanisms of ischemia and hypoxia, a metabolic path to hypertrophy (Tanimoto et al., 2008). However, ECC vs. concentric contraction is known to have lower metabolic demand (Overend et al., 2000). The similar training adaptations to SSC and ECC seem to suggest that total work is the stimulus for hypertrophy. Not even 4-fold faster and 7-fold longer stretch stimulus seemed to have an effect on muscle size. The uniform hypertrophy quantified by MRI (2.5%) after SSC vs. ECC exercise is not totally surprising because each stimulus has one element of the hypertrophy pathway operating under either rapid tension (SSC) or the long exposure (ECC) (Fig. 2). When the stretch was initiated in our SSC training protocol, we observed rapid rise in torque (short-range stiffness) (Váczi et al., 2011) and this represents one element of the stimulus that causes hypertrophy. Malisoux et al. (2006) suggested that, in addition to improving contraction velocity, SSC training is a potential method to prevent muscle wasting. Surprisingly, using biopsy samples, in young individuals those authors demonstrated unusually large, 23%, hypertrophy of the vastus lateralis muscle fibers after an 8-week-long intensive jump training. Moderate velocity eccentric contractions induced smaller quadriceps hypertrophy in young males after five weeks of training (Norrbrand et al., 2008). When old subjects trained for 16 weeks with moderate velocity eccentric biased contractions, there was 5% increase in the fiber size of the vastus lateralis (Raj et al., 2012). Healthy aging human muscle may have a similar or somewhat diminished hypertrophic ability to respond to strength training (Lambert and Evans, 2002) and the duration of the interventions and the methodology used to quantify hypertrophy (i.e. MRI vs. ultrasound; ACSA vs. muscle volume) can both affect the magnitude of hypertrophic response. The 2.5% change in quadriceps ACSA measured with MRI (using 11 slices) suggests small hypertrophic response in our cohort of fit elderly, however it remains unknown whether longer exercise duration would produce greater and/or training-specific adaptation. There are several limitations in the present study. One limitation is a lack of measures of activities of daily living or ADLs. Therefore it was not possible to determine if the adaptations to the two training protocols would have improved function in ADLs requiring muscle strength and speed. A second limitation is the absence of measures that could have detected changes in elements of the nervous system. Future experiments will have to include a young control group to determine if SSC and ECC exercise produces age-specific adaptations. We also examined only healthy and active old males and the SSC training protocol is feasible in frail old adults and also in women. Finally, the hormonal data analysis was underpowered, and we have no biopsy data to complement the MRI measurements with data at the muscle cell level or determine if there were any changes in receptors involved in testosterone and cortisol signaling. We note that changes in most of the muscle strength measurements reached or exceeded the MDC, a threshold that indicates true changes beyond changes due to measurement errors. MDC is an important index for clinicians and researchers to interpret the effectiveness of therapeutic or exercise interventions. However, we found somewhat lower changes in MVC and ACSA (6% and 2.5%, respectively) compared

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with their MDC (8% and 5%, respectively). All in all, our data showed statistically significant improvements but analysis of the same data using MDC warrants caution and calls for a replication of the study using larger sample sizes and more homogenous groups to arrive at a more accurate estimate of the functionally significant effects. In conclusion, this is the first study that compared SSC and ECC exercise training in healthy old males. Even though the two forms of training stimuli were very different (SSC contraction stretched the muscle 4-times faster than ECC and ECC kept the muscle under tension 7-times longer than SSC), the total mechanical load was similar and thus represents a key factor that improves muscle strength and size and produces favorable hormonal responses. The only training-specific adaptation in favor of SSC was the 30% greater improvement in explosive strength. This is an important finding, considering the need to identify interventions that target a key deficiency in the aging muscle, i.e., impaired ability to produce force rapidly. Conflict of interest The authors report that there is no conflict of interest. Acknowledgments The authors wish to thank the employees of the Institute of Laboratory Medicine, University of Pécs, Hungary, and the subjects for their contribution to this research. Special thanks to István Csethe, former instructor of the Institute of Sport Sciences and Physical Education, University of Pécs, Hungary, for his assistance in organizing the experiment. The study was supported in part by a grant from the Hungarian Sport Science Society (MSTT-74/2011). References Aagaard, P., Simonsen, E.B., Andersen, J.L., Magnusson, P., Dyhre-Poulsen, P., 2002. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J. Appl. Physiol. 93, 1318–1326. Beijersbergen, C.M., Granacher, U., Vandervoort, A.A., Devita, P., Hortobagyi, T., 2013. The biomechanical mechanism of how strength and power training improves walking speed in old adults remains unknown. Ageing Res. Rev. 12, 618–627. Bobbert, M.F.,Huijing, P.A.,van Ingen Schenau, G.J., 1987. Drop jumping. I. The influence of jumping technique on the biomechanics of jumping. Med. Sci. Sports Exerc. 19, 332–338. Bonacci, J., Chapman, A., Blanch, P., Vicenzino, B., 2009. Neuromuscular adaptations to training, injury and passive interventions: implications for running economy. Sports Med. 39, 903–921. Bosco, C.,Tihanyi, J., Rivalta, L.,Parlato, G.,Tranquilli, C.,Pulverenti, G.,Foti, C.,Viru, M.,Viru, A., 1996. Hormonal responses to strenuous jumping effort. Jpn. J. Physiol. 46, 93–98. Bosco, C., Iacovelli, M., Tsarpela, O., Cardinale, M., Bonifazi, M., Tihanyi, J., Viru, M., De Lorenzo, A., Viru, A., 2000. Hormonal responses to whole-body vibration in men. Eur. J. Appl. Physiol. 81, 449–454. Brambilla, D.J.,Matsumoto, A.M.,Araujo, A.B.,McKinlay, J.B., 2009. The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in men. J. Clin. Endocrinol. Metab. 94, 907–913. Buresh, R.,Berg, K.,French, J., 2009. The effect of resistive exercise rest interval on hormonal response, strength, and hypertrophy with training. J. Strength Cond. Res. 23, 62–71. Crawford, M.,Jamnik, V.R., 2009. Plyometric training for health-related fitness. Health Fitness J. Can. 2, 13–16. De Vito, G., Bernardi, M., Forte, R., Pulejo, C., Macaluso, A., Figura, F., 1998. Determinants of maximal instantaneous muscle power in women aged 50–75 years. Eur. J. Appl. Physiol. Occup. Physiol. 78, 59–64. Durand, R.J., Castracane, V.D., Hollander, D.B., Tryniecki, J.L., Bamman, M.M., O'Neal, S., Hebert, E.P., Kraemer, R.R., 2003. Hormonal responses from concentric and eccentric muscle contractions. Med. Sci. Sports Exerc. 35, 937–943. Edwén, C.E.,Thorlund, J.B.,Magnusson, S.P.,Slinde, F.,Svantesson, U.,Hulthén, L.,Aagaard, P., 2014. Stretch-shortening cycle muscle power in women and men aged 18–81 years: influence of age and gender. Scand. J. Med. Sci. Sports 24, 714–726. Faulkner, J.A.,Larkin, L.M.,Claflin, D.R.,Brooks, S.V., 2007. Age-related changes in the structure and function of skeletal muscles. Clin. Exp. Pharmacol. Physiol. 34, 1091–1096. Fielding, R.A., LeBrasseur, N.K., Cuoco, A., Bean, J., Mizer, K., Fiatarone Singh, M.A., 2002. High-velocity resistance training increases skeletal muscle peak power in older women. J. Am. Geriatr. Soc. 50, 655–662. Gillies, E.M., Putman, C.T., Bell, G.J., 2006. The effect of varying the time of concentric and eccentric muscle actions during resistance training on skeletal muscle adaptations in women. Eur. J. Appl. Physiol. 97, 443–453.

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