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Are the Responses to Resistance Training Different Between the Preferred and Nonpreferred Limbs?

Baroni, Bruno M.; Franke, Rodrigo de A.; Rodrigues, Rodrigo; Geremia, Jeam M.; Schimidt, Helen L.; Carpes, Felipe P.; Vaz, Marco A.

Journal of Strength and Conditioning Research: March 2016 - Volume 30 - Issue 3 - p 733–738
doi: 10.1519/JSC.0000000000001148
Original Research
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Baroni, BM, Franke, RdA, Rodrigues, R, Geremia, JM, Schimidt, HL, Carpes, FP, and Vaz, MA. Are the responses to resistance training different between the preferred and nonpreferred limbs? J Strength Cond Res 30(3): 733–738, 2016—Humans preferentially recruit limbs to functionally perform a range of daily tasks, which may lead to performance asymmetries. Because initial training status plays an important role in the rate of progression during resistance training, could asymmetries between the preferred and nonpreferred limbs lead to different magnitudes of strengthening during a resistance training program? This issue motivated this study, in which 12 healthy and physically active men completed a 4-week control period followed by a 12-week isokinetic resistance training program, performed twice a week, including 3–5 sets of 10 maximal eccentric contractions for each limb. Every 4 weeks, knee extensor peak torques at concentric, isometric, and eccentric tests were measured using an isokinetic dynamometer and the sum of quadriceps muscle thickness was determined by ultrasound images. Before training, concentric peak torque was similar between limbs but isometric and eccentric peak torques were significantly smaller in the nonpreferred compared with the preferred limb (4.9 and 5.8%, respectively). Bilateral strength symmetry remained constant throughout the training period for concentric tests. For eccentric and isometric tests, symmetry was reached at the fourth and eighth training weeks, respectively. After 12 weeks, between-limb percent nonsignificant differences were −0.62% for isometric and −1.93% for eccentric tests. The sum of knee extensor muscle thickness had similar values before training and presented similar changes throughout the study for both the preferred and the nonpreferred limbs. In conclusion, the nonpreferred limb presents higher strength gain than the preferred limb at the initial phase of an isokinetic resistance training program, and this increased strength gain is not associated with muscle hypertrophy.

1Federal University of Rio Grande do Sul, Porto Alegre, Brazil;

2Federal University of Health Sciences of Porto Alegre, Porto Alegre, Brazil; and

3Federal University of Pampa, Uruguaiana, Brazil

Address correspondence to Bruno M. Baroni, bmbaroni@yahoo.com.br.

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Introduction

Resistance training has been extensively used to improve physical conditioning of healthy subjects and athletes, and the use of resistance exercises for injury prevention or rehabilitation purposes is also progressively increasing (24). This type of training is characterized by voluntary exercises performed against an external resistance and considered the most appropriate method to promote muscular strength gains (20). It is more commonly executed through movements, including both eccentric and concentric actions against free weights or gym machines. In addition, this type of training can be executed exclusively or with emphasis on one type of muscle action and using resistance from isokinetic dynamometers (16), elastic bands (9) or even water resistance (28).

It is well documented that strength increments in the first weeks of training are mainly attributed to neural adaptations (13), whereas morphological adaptations, especially those related to the increase in muscle mass, will contribute to strength gains more expressively after some weeks of training (32). This chronology of neural and morphological adaptations to the resistance training and their contributions to strength gains were demonstrated for training regimes encompassing conventional strength exercises (29) and exclusively eccentric (2), concentric (3), or isometric (21) exercises. Even those training protocols based on neuromuscular electrical stimulation seem to follow the same time course of neuromuscular adaptations (14).

Independent of the stimulus type used during the resistance training sessions, the initial conditioning status plays an important role for the rate of progression. The magnitude of strength gains after a given period of training differs considerably between untrained and trained individuals, as trained subjects show lower strength improvement rates (20). According to these evidences, because an untrained muscle has a larger window for strength gain compared with a trained muscle, it seems reasonable to assume that asymmetries between the preferred and nonpreferred limbs may lead to different adaptations to resistance training. Following this rationale, resistance training studies usually assess muscles' responses from a specific limb. However, this larger window for strength gains from the contralateral limb does not seem to have been investigated by previous studies.

The preferred leg is usually defined as the preferential limb to perform a given motor task, which can be determined by kicking a ball or by questionnaires (for a review, see Ref. 8). The functional asymmetry between the lower limbs is observed in healthy subjects (22) and athletes involved in sports with both asymmetric and symmetric kinetic stimuli (8,26,27). Thus, could these functional asymmetries between the preferred and nonpreferred legs lead to different magnitudes of strengthening during a resistance training program? This issue motivated the development of the present study, in which we assessed muscle mass and strength of both limbs in healthy subjects engaged at a knee extensor isokinetic resistance training program.

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Methods

Experimental Approach to the Problem

A 4-month longitudinal trial was designed to verify the resistance training–induced changes in strength and muscle mass of healthy subjects. All volunteers experienced a 4-week control period without any kind of systematized physical exercise or changes in lifestyle. Then, they were engaged in a 12-week knee extensor resistance training program.

An appropriate design to verify the specific response of each limb (preferred and nonpreferred) to resistance training should encompass unilateral exercises. Also, subjects should not know how much load each limb was supporting to avoid possible attempts to match the performance of the 2 limbs. Therefore, we conducted our training protocol using an isokinetic dynamometer. Eccentric muscle contractions were chosen because of their potential to promote larger gains in muscle mass and strength compared with concentric contractions (30).

Evaluations were performed at 5 time points: 1 week before starting the control period (baseline); at the last week of the 4-week control period and, consequently, 1 week before starting the training period (pretraining); and at the weeks immediately after the fourth (post-4), eighth (post-8), and the 12th (post-12) weeks of training. Evaluation sessions comprised the assessment of quadriceps muscle morphology through acquisition of ultrasound images and knee extensor strength through maximal isometric, concentric, and eccentric torques determined using an isokinetic dynamometer.

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Subjects

Healthy and physically active male volunteers aged between 20 and 35 years were invited to participate in this study. All volunteers were undergraduate and graduate students, and they should be involved in a physical exercise routine (except resistance training) distributed at least in 3 different days of the week to be considered physically active. Exclusion criteria included (a) engagement in any kind of lower-limb systematized strength training program in the previous 6 months; (b) history of lower-limb musculoskeletal disorders that could be a contraindication for maximal tests or that could impair the performance during tests and training (e.g., patellar tendinitis, knee surgeries, ruptured but not operated knee ligaments, recent muscle strains, or joint sprains); (c) respiratory or cardiovascular diseases considered a risk or a limiting factor for maximal exercise; and (d) use of nutritional supplements or anabolic steroids (self-reported). Participants were informed about the study design and the possible risks and discomfort related to the procedures. Before starting the data collection, volunteers read and signed an informed consent term previously approved by the local University Ethics Committee on Human Research.

Twelve subjects (24.92 ± 4.29 years, 1.75 ± 0.06 m, 75.44 ± 7.45 kg) completed the full study schedule.

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Procedures

Training Program

The 12-week resistance training program was performed using an isokinetic dynamometer (Biodex System 3; Biodex Medical System, Shirley, NY, USA), following the protocol described elsewhere (2). Briefly, the training program was divided into 3 mesocycles, and the training session volume (number of sets per session × number of repetitions per set) was increased through an additional set in each mesocycle. Training sessions were performed twice a week with 72 hours of minimal interval between them. In the first week of training, participants performed only one training session because of the deleterious effects of eccentric exercise–induced muscle damage (1). They also performed only one training session at the fifth and ninth training weeks because of the exchange of mesocycles and consequent training volume increment. Each training session comprised a 5-minute warm-up cycloergometer exercise and 3–5 sets of 10 maximal eccentric isokinetic contractions with a 1-minute rest period between them. Participants were positioned in the dynamometer according to the manufacturer's recommendations for knee flexion/extension movements with the hip angle fixed at 85° and their trunk, hips, and thighs firmly strapped to the apparatus. When necessary, the position was adjusted to ensure a proper posture for the exercise sets. Each eccentric contraction started with knee flexed at 30° (considering 0° as full extension), and the dynamometer droved the segment to 90° of knee flexion (range of motion of 60°) at an angular velocity of 60°·s−1. Verbal encouragement was provided to the participants during each eccentric repetition. Visual feedback or data related to the torque production were not provided to ensure a maximal effort in each lower limb, independent of contralateral limb performance. The first lower limb to be trained was alternated between the trials to avoid any influence of the training order in the results.

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Assessment of Muscle Mass

Participants were evaluated in supine position, after 10 minutes of rest, using a B-mode ultrasound system (Aloka SSD-4000; Aloka Inc., Tokyo, Japan), along with a linear array transducer (60 mm, 7.5 MHz) of the same manufacturer. Participants were requested to refrain from any vigorous physical activity in the 48 hours before the assessment. All ultrasound images were obtained with the transducer positioned longitudinally to the muscle fibers by the same experienced investigator. The midway point between the greater trochanter and the lateral femur condyle was used as a reference point for assessment of rectus femoris (RF), vastus intermedius (VI), and vastus lateralis (VL) muscle thickness, whereas vastus medialis (VM) measurements were made at 25–30% of this distance according to the subject's characteristics. Great care was taken to determine the specific site from where the images were collected, and maps on overhead transparency films were made using anatomical reference points and markings on the skin to ensure that the same specific site was measured on each occasion. Three ultrasound images were taken, and the thickness of each knee extensor muscle was further analyzed through Image-J software (National Institutes of Health, USA). The distance between the deep and the superficial aponeuroses was measured at 5 different points in each longitudinal ultrasound image, and a mean value was used as the mean thickness of that ultrasound image. Mean values were obtained from 3 ultrasound images and taken as the muscle thickness for each muscle. Finally, muscle thickness from the 4 knee extensor muscles (RF, VI, VL, and VM) was summed, and this value was considered as representative of quadriceps femoris muscle mass.

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Assessment of Muscle Strength

Peak torque was considered a measure of strength in our study. Isometric, concentric, and eccentric knee extensor peak torques were measured using the same dynamometry apparatus used for resistance training. A general warm-up exercise on a cycloergometer (5 minutes) was followed by a specific warm-up protocol comprising 10 knee extension/flexion repetitions controlled at 90°·s−1 at submaximal effort level. Subjects were instructed to execute all tests in a standardized way, aiming at the highest effort possible. Researchers provided verbal encouragement during each test. Isometric torque assessment comprised 3 maximal knee extensor contractions at 60° of knee flexion. Each isometric test lasted 5 seconds, and a 2-minute interval was observed between the consecutive contractions. Peak torque values from each contraction were obtained, and an additional test was performed if a torque variation higher than 10% was observed. Concentric torque evaluation encompassed 3 consecutive maximal knee extensor concentric contractions at 60°·s−1 and a range of motion between 90 and 10° of knee flexion. Eccentric torque was measured through 3 consecutive maximal knee extensor eccentric contractions at 60°·s−1 and a range of motion between 30 and 90° of knee flexion. Concentric and eccentric tests were repeated 2 times with a 2-minute rest period between the attempts. The highest peak torque values obtained in each type of contraction were considered for data analysis.

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Statistical Analyses

An intraclass correlation coefficient was applied to verify the test-retest reliability between baseline and pretraining evaluations for isometric, concentric, and eccentric peak torques and the sum of muscle thickness in each lower limb. All measurements were compared between preferred and nonpreferred limbs at each time point of the study (baseline, pretraining, post-4, post-8, and post-12) using paired t-tests. The mean difference between the 2 groups was presented in SD units, reported as Cohen's d, simply referred to as effect size (ES) throughout the Results. Significance level was set at 0.05 for all analyses. Data are presented in Figures 1–4 as mean ± SE.

Figure 1

Figure 1

Figure 2

Figure 2

Figure 3

Figure 3

Figure 4

Figure 4

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Results

High test-retest reliability scores were observed between baseline and pretraining evaluations for all tests: at the preferred limb, isometric peak torque (r = 0.981), concentric peak torque (r = 0.958), eccentric peak torque (r = 0.949), and sum of muscle thickness (r = 0.893); and at the nonpreferred limb, isometric peak torque (r = 0.966), concentric peak torque (r = 0.932), eccentric peak torque (r = 0.934), and sum of muscle thickness (r = 0.940).

Before starting the resistance training program, volunteers presented similar values between preferred and nonpreferred limbs for concentric peak torque (Figure 1; p = 0.301, ES = 0.23). However, the preferred limb showed superiority in terms of isometric peak torque (Figure 2; p = 0.041, ES = 0.36) and eccentric peak torque (Figure 3; p = 0.021, ES = 0.45). At pretraining evaluation, mean isometric and eccentric peak torque values of the nonpreferred limb were 4.9 and 5.8% smaller compared with the preferred limb, respectively.

Bilateral symmetry remained constant throughout the training program for concentric peak torque (Figure 1). Between-limb symmetry in eccentric peak torque was reached at the fourth training week (p = 0.534, ES = 0.08) and remained unchanged until the end of the training program (Figure 3). Similar isometric peak torque values were found after 8 training weeks (p = 0.253, ES = 0.12) and also did not change until the final evaluation (Figure 2). After 12 training weeks, the percent differences between the preferred and the nonpreferred limbs were 0.73% (ES = −0.03) for concentric, −0.62% (ES = 0.09) for isometric, and −1.93% (ES = 0.21) for eccentric peak torques, respectively.

The sum of knee extensor muscle thickness presented similar values at the 5 time points of this study (Figure 4). Throughout the study, percent differences between preferred and nonpreferred muscle mass ranged between 0.61 and 1.27%.

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Discussion

Our main findings suggest that (a) knee extensor muscle strength deficits at the nonpreferred limb of healthy subjects are dependent on muscle contraction type; (b) these strength asymmetries are not related to differences in quadriceps muscle mass; and (c) an isokinetic resistance training program, performed at maximal intensity by each lower limb, resulted in symmetric knee extensor strength in a short period of training (4–8 weeks).

Although there is no consensus in the literature, strength imbalances between the preferred and nonpreferred limbs smaller than 10% have been considered “normal” (18). Despite some contrary results (19), strength asymmetries seem to impair functional (23) and sports performance (17). Lower-limb asymmetries have also been related to increased injury risks in sports practice (12), and systematic isokinetic evaluations have a remarkable place for injury prevention in elite athletes (25). In addition, knee extensor strength deficits in previously injured limbs predict functional performance at the time of sport return (31) and may help clinical decision making to optimize sports participation after surgery/immobilization/rehabilitation.

Our initial expectation about the nonpreferred limb having smaller peak torque values compared with the preferred limb was partially confirmed because participants of this study presented significant deficits at the nonpreferred limb in isometric and eccentric tests, but not in the concentric test. Assuming that the subjects were not engaged in any kind of systematic exercise with asymmetric kinetic patterns, the torque asymmetries may result from the preferential recruitment of the preferred lower limb for a range of mobilization task during daily life that is able to affect maximal strength capacity. In addition, these findings further support the notion that lower-limb strength asymmetry is dependent on the contraction type (11,22). Therefore, because daily and sports activities are not restricted to one type of muscle action, it is advisable that isokinetic evaluations contemplate concentric and eccentric tests to get a reliable comparison between preferred and nonpreferred (or injured and uninjured) limbs.

Similar between-limb knee extensor muscle thickness before training suggested factors beyond muscle mass as responsible for the bilateral strength asymmetry. Differences in activation of motor units are a possible explanation, although there is evidence refuting between-limb asymmetries in knee extensor activation during concentric maximal tests (15). Another hypothesis is related to possible between-limb differences in muscle quality, i.e., the amount of noncontractile tissue (connective and adipose tissues) infiltrated in the muscle belly, which determines the force developed by unit of muscle area (7). A third possibility is the contribution of elastic elements (such as tendon, intramuscular connective tissue, and titin) during strength tests (5) because between-limb differences in mechanical and morphological properties of tendons were recently demonstrated (4). However, we did not assess tendon properties, muscle quality, or muscle activation; thus, we cannot determine the mechanism(s) responsible for strength deficits observed in the nonpreferred leg.

The primary aim of this study was to compare knee extensor responses of preferred and nonpreferred limbs subjected to an isokinetic resistance training program. Because the preferred limb probably has higher level of demands in healthy and physically active subjects and consequently this limb would have a superior training level compared with the contralateral, we hypothesized that the nonpreferred leg would have a larger window for strength gains through more expressive neural and/or morphological adaptations if compared with the preferred limb. The results obtained for isometric and eccentric tests support our hypothesis, and the similar between-limb muscle thickness changes suggested that the muscular hypertrophy was not related to increased strength gain in the nonpreferred limb.

A previous study from our group (2) used a similar isokinetic eccentric training regime and found significant increases of knee extensor activation after 4 training weeks for eccentric tests and after 8 training weeks for isometric tests. These time points agree with the time points when subjects from the present study reached strength balance between legs in eccentric and isometric muscle actions, respectively. Hence, it supports the idea that higher strength gains in the nonpreferred leg may be attributed to the increased neural adaptations of this lower limb. However, eccentric training is also able to improve muscle quality (6) and tendon properties (10); so, we cannot exclude the possibility that these adaptations might have contributed to the strength increments observed in our study.

Finally, reduction of strength asymmetry between lower limbs after an isokinetic training program is a novelty of our study. Future studies should address the mechanism behind the specific adaptation of preferred and nonpreferred limbs. In addition, the impact of other resistance training regimes (e.g., free weights, gym machines, elastic bands) with unilateral and bilateral exercises and responses from other muscle groups with clinical significance (such as the hamstrings) should be investigated, especially considering that our training was performed in an isokinetic dynamometer, which does not resemble real-life training situations. Finding effective programs to counteract bilateral asymmetry may be an important step to decrease injury risk and to improve athletes' performance.

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Practical Applications

Our findings support that the nonpreferred lower limb presented strength deficits compared with the preferred limb, and this asymmetry is not attributed to the amount of muscle mass. Therefore, health professionals should have greater concerns on the muscle functional status than the limb circumference or other measures of muscle mass. Unilateral tests in different types of exercises (or muscle actions) are useful to identify bilateral asymmetries. Once the functional deficit is diagnosed, symmetry patterns may be restored with relatively short periods (4–8 weeks) of unilateral training programs using the specific exercise where the strength deficit was identified. In addition, subjects with bilateral strength asymmetries should focus on unilateral exercises to avoid potential compensations of the preferred leg in bilateral exercises.

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Acknowledgments

The authors would like to thank Coordenacão de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil) for financial support.

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References

1. Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 12: 184–207, 1991.
2. Baroni BM, Rodrigues R, Franke RA, Geremia JM, Rassier DE, Vaz MA. Time course of neuromuscular adaptations to knee extensor eccentric training. Int J Sports Med 34: 904–911, 2013.
3. Blazevich AJ, Cannavan D, Coleman DR, Horne S. Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol (1985) 103: 1565–1575, 2007.
4. Bohm S, Mersmann F, Marzilger R, Schroll A, Arampatzis A. Asymmetry of achilles tendon mechanical and morphological properties between both legs. Scand J Med Sci Sports 25: e124–e 132, 2015.
5. Bojsen-Moller J, Magnusson SP, Rasmussen LR, Kjaer M, Aagaard P. Muscle performance during maximal isometric and dynamic contractions is influenced by the stiffness of the tendinous structures. J Appl Physiol (1985) 99: 986–994, 2005.
6. Cadore EL, Gonzalez-Izal M, Pallares JG, Rodriguez-Falces J, Hakkinen K, Kraemer WJ, Pinto RS, Izquierdo M. Muscle conduction velocity, strength, neural activity, and morphological changes after eccentric and concentric training. Scand J Med Sci Sports 24: e343–e352, 2014.
7. Cadore EL, Izquierdo M, Conceicao M, Radaelli R, Pinto RS, Baroni BM, Vaz MA, Alberton CL, Pinto SS, Cunha G, Bottaro M, Kruel LF. Echo intensity is associated with skeletal muscle power and cardiovascular performance in elderly men. Exp Gerontol 47: 473–478, 2012.
8. Carpes FP, Mota CB, Faria IE. On the bilateral asymmetry during running and cycling—A review considering leg preference. Phys Ther Sport 11: 136–142, 2010.
9. Colado JC, Triplett NT. Effects of a short-term resistance program using elastic bands versus weight machines for sedentary middle-aged women. J Strength Cond Res 22: 1441–1448, 2008.
10. Duclay J, Martin A, Duclay A, Cometti G, Pousson M. Behavior of fascicles and the myotendinous junction of human medial gastrocnemius following eccentric strength training. Muscle Nerve 39: 819–827, 2009.
11. Fousekis K, Tsepis E, Vagenas G. Lower limb strength in professional soccer players: Profile, asymmetry, and training age. J Sports Sci Med 9: 364–373, 2010.
12. Fousekis K, Tsepis E, Vagenas G. Multivariate isokinetic strength asymmetries of the knee and ankle in professional soccer players. J Sports Med Phys Fitness 50: 465–474, 2010.
13. Gabriel DA, Kamen G, Frost G. Neural adaptations to resistive exercise: Mechanisms and recommendations for training practices. Sports Med 36: 133–149, 2006.
14. Gondin J, Guette M, Ballay Y, Martin A. Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 37: 1291–1299, 2005.
15. Guette M, Gondin J, Martin A. Time-of-day effect on the torque and neuromuscular properties of dominant and non-dominant quadriceps femoris. Chronobiol Int 22: 541–558, 2005.
16. Guilhem G, Cornu C, Maffiuletti NA, Guevel A. Neuromuscular adaptations to isoload versus isokinetic eccentric resistance training. Med Sci Sports Exerc 45: 326–335, 2013.
17. Hart NH, Nimphius S, Spiteri T, Newton RU. Leg strength and lean mass symmetry influences kicking performance in Australian football. J Sports Sci Med 13: 157–165, 2014.
18. Kannus P. Isokinetic evaluation of muscular performance: Implications for muscle testing and rehabilitation. Int J Sports Med 15(Suppl 1): S11–S18, 1994.
19. Kobayashi Y, Kubo J, Matsubayashi T, Matsuo A, Kobayashi K, Ishii N. Relationship between bilateral differences in single-leg jumps and asymmetry in isokinetic knee strength. J Appl Biomech 29: 61–67, 2013.
20. Kraemer WJ, Adams K, Cafarelli E, Dudley GA, Dooly C, Feigenbaum MS, Fleck SJ, Franklin B, Fry AC, Hoffman JR, Newton RU, Potteiger J, Stone MH, Ratamess NA, Triplett-McBride T; American College of Sports Medicine. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc 34: 364–380, 2002.
21. Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H. Time course of changes in muscle and tendon properties during strength training and detraining. J Strength Cond Res 24: 322–331, 2010.
22. Lanshammar K, Ribom EL. Differences in muscle strength in dominant and non-dominant leg in females aged 20-39 years—a population-based study. Phys Ther Sport 12: 76–79, 2011.
23. Laroche DP, Cook SB, Mackala K. Strength asymmetry increases gait asymmetry and variability in older women. Med Sci Sports Exerc 44: 2172–2181, 2012.
24. Lorenz DS, Reiman MP, Walker JC. Periodization: Current review and suggested implementation for athletic rehabilitation. Sports Health 2: 509–518, 2010.
25. McCall A, Carling C, Davison M, Nedelec M, Le Gall F, Berthoin S, Dupont G. Injury risk factors, screening tests and preventative strategies: A systematic review of the evidence that underpins the perceptions and practices of 44 football (soccer) teams from various premier leagues. Br J Sports Med 49: 583–589, 2015.
26. Menzel HJ, Chagas MH, Szmuchrowski LA, Araujo SR, de Andrade AG, de Jesus-Moraleida FR. Analysis of lower limb asymmetries by isokinetic and vertical jump tests in soccer players. J Strength Cond Res 27: 1370–1377, 2013.
27. Pappas E, Carpes FP. Lower extremity kinematic asymmetry in male and female athletes performing jump-landing tasks. J Sci Med Sport 15: 87–92, 2012.
28. Pinto SS, Cadore EL, Alberton CL, Zaffari P, Bagatini NC, Baroni BM, Radaelli R, Lanferdini FJ, Colado JC, Pinto RS, Vaz MA, Bottaro M, Kruel LF. Effects of intra-session exercise sequence during water-based concurrent training. Int J Sports Med 35: 41–48, 2014.
29. Radaelli R, Botton CE, Wilhelm EN, Bottaro M, Brown LE, Lacerda F, Gaya A, Moraes K, Peruzzolo A, Pinto RS. Time course of low- and high-volume strength training on neuromuscular adaptations and muscle quality in older women. Age (Dordr) 36: 881–892, 2014.
30. Roig M, O'Brien K, Kirk G, Murray R, McKinnon P, Shadgan B, Reid WD. The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: A systematic review with meta-analysis. Br J Sports Med 43: 556–568, 2009.
31. Schmitt LC, Paterno MV, Ford KR, Myer GD, Hewett TE. Strength asymmetry and landing mechanics at return to sport after anterior cruciate ligament reconstruction. Med Sci Sports Exerc 47: 1426–1434, 2015.
32. Wernbom M, Augustsson J, Thomee R. The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Med 37: 225–264, 2007.
Keywords:

strength training; eccentric training; limb preference; bilateral asymmetry; knee

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