Effectiveness of 448-kHz Capacitive Resistive Monopolar Radiofrequency Therapy After Eccentric Exercise-Induced Muscle Damage to Restore Muscle Strength and Contractile Parameters

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Boštjan Šimunič Science and Research Centre Koper, Institute for Kinesiology Research, Koper, Slovenia

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Monika Doles Science and Research Centre Koper, Institute for Kinesiology Research, Koper, Slovenia

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Robi Kelc Medical Faculty, Institute for Sports Medicine, University of Maribor, Maribor, Slovenia

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Andrej Švent Intact Ltd, Ljubljana, Slovenia

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Context: Exercise-induced muscle damage (EIMD) is prevalent especially in sports and rehabilitation. It causes loss in skeletal muscle function and soreness. As there are no firm preventive strategies, we aimed to evaluate the preventive efficacy of nonthermal 448-kHz capacitive resistive monopolar radiofrequency (CRMRF) therapy after eccentric bouts of EIMD response in knee flexors. Design: Twenty-nine healthy males (age: 25.2 [4.6] y) were randomized in control group (CG; n = 15) and experimental group (EG; n = 14) where EG followed 5 daily 448-kHz CRMRF therapies. All assessments were performed at baseline and post EIMD (EIMD + 1, EIMD + 2, EIMD + 5, and EIMD + 9 d). We measured tensiomyography of biceps femoris and semitendinosus to calculate contraction time, the maximal displacement and the radial velocity of contraction, unilateral isometric knee flexors maximal voluntary contraction torque, and rate of torque development in first 100 milliseconds. Results: Maximal voluntary contraction torque and rate of torque development in first 100 milliseconds decreased more in CG than in EG and recovered only in EG. Biceps femoris contraction time increased only in CG (without recovery), whereas in semitendinosus contraction time increased in EG (only at EIMD + 1) and in CG (without recovery). In both muscles, tensiomyographic maximal displacement decreased in EG (in EIMD + 1 and EIMD + 2) and in CG (without recovery). Furthermore, in both muscles, radial velocity of contraction decreased in EG (from EIMD + 1 until EIMD + 5) and in CG (without recovery). Conclusion: The study shows beneficial effect of CRMRF therapy after inducing EIMD in skeletal muscle strength and contractile parameters in knee flexors.

Resistance exercise has beneficial physiological effects and is highly recommended as a strategy to minimize loss in muscle mass and function across the lifespan, and to improve performance and quality of life.1 However, it has also been confirmed that unaccustomed exercise, especially high-load eccentric muscle contractions, is associated with temporary muscle damage, muscle pain, reductions in muscle force output, and transient muscle inflammation.2 This phenomenon is known as exercise-induced muscle damage (EIMD) and is characterized by symptoms that present both immediately and for up to 14 days after the initial exercise bout. The main consequence of EIMD for the individual is the loss of skeletal muscle function and soreness.

EIMD manifests as a temporary decrease in muscle function (eg, decrease in force production and rise in passive tension), increased muscle soreness, increased swelling of the involved muscles, and increased intramuscular proteins in blood.3 Most damage occurs when the exercise bout is both novel and eccentrically performed. Although eccentric contractions are potentially damaging, there are several benefits in conducting this muscle action in sports or late rehabilitation; they produce greater gains in hypertrophy1 and increases in eccentric contraction-specific strength4 than concentric contractions. Additionally, eccentric work demands lower metabolic cost than does concentric work.5,6 Specifically, eccentric muscle contractions enhance the performance also during the concentric phase of stretch-shortening cycles, which is important in disciplines like sprinting, jumping, throwing, and running.7 Muscles activated during lengthening movements can also function as shock absorbers, to decelerate during landing tasks or to precisely deal with high external loading in sports like alpine skiing.8 The few studies available on trained subjects reveal that eccentric training can further enhance maximal muscle strength and power. It can further optimize muscle length for maximal tension development at a greater degree of extension and has potential to improve muscle coordination during eccentric tasks.7 Furthermore, eccentric exercise has been shown to reduce hamstring injury rates by 60% to 70% in various sports and was implemented in athletic rehabilitation: tendinopathy, hamstring strains, and anterior cruciate ligament (ACL) reconstruction.9

EIMD is assessed indirectly using a variety of methods including blood markers, pain scales, measurement of range of motion and force/torque output, magnetic resonance imaging, or directly using muscle biopsies.10 Maximal or explosive voluntary contractions are best indicators that EIMD has occurred.11 EIMD assessment methods are following muscle damage pathways. Primary, metabolic, and mechanical pathways of muscle damage occur after eccentric exercise.12 Metabolic pathway of muscle damage is initiated by the ischemia or hypoxia during prolonged intensive exercise. The mechanical pathway of muscle damage relates to the mechanical overloading of the myofibers. Eccentric contractions are more powerful and require less energy per unit of torque, and lengthening of sarcomeres is non-uniform, which results in some myofilaments being stretched beyond the point of actin–myosin overlap and undergo mechanical damage—popping.13 Secondary, an increase of the intracellular Ca2+ leads to further myofibrillar damage.14 Tensiomyography (TMG), a skeletal muscle contractile properties assessment method, was used in 2 EIMD studies. The first study compared elbow flexors after eccentric contractions and reported lower TMG amplitude (maximal displacement) and longer contraction time for at least 6 days after eccentric overload.15 Those results were confirmed also by the second study16 with an addition that ischemic preconditioning before bout of eccentric contractions blunted EIMD response being confirmed also by TMG results: maximal displacement and contraction time did not change in preconditioning group. Thus, the sensitivity of TMG parameters for studying preventive and treatment interventions to ameliorate EIMD response was confirmed.

There is no firm evidence of any preventive treatments for EIMD, for example, oral supplementations, anti-inflammatory drugs, stretching, massage, electrical therapies, cryotherapy, or exercise. However, when electrical therapy has been combined with the use of radiofrequency (capacitive–resistive electric transfer—Tecar), it was used in physical rehabilitation and sports medicine to treat muscle, bone, ligament, and tendon lesions.17,18 Only one study used Tecar therapy after intense exercise and reported faster improvements in running biomechanical parameters with Tecar therapy than with passive rest.19 The mechanism of action of Tecar therapy relies on interaction of radiofrequency currents with the biological structures further resulting in endogenous temperature increase.17,18 The ensuing thermophysiological responses to heat can lead to therapeutic benefits,20 such as the blood flow stimulation, the processes of oxygen and nutrition substances delivery, and the processes of metabolic wastes removal.18,20 However, nonthermal Tecar therapy (448-kHz capacitive resistive monopolar radiofrequency therapy [CRMRF]) is currently used in physical rehabilitation and sports medicine to treat muscle, bone, ligament, and tendon lesions, and, unlike thermal therapies, does not induce side effects like edema and dermal or epidermal burns.21 The frequency of 448 kHz current promotes stem cell proliferation.21

Although there are promising results of thermal Tecar use in sport rehabilitation and recovery, there are no data on 448-kHz CRMRF therapy efficacy in the recovery after EIMD. Therefore, we hypothesized that the nonthermal 448-kHz CRMRF therapy will ameliorate EIMD response assessed by soreness, maximal voluntary strength measures, and TMG contractile properties in recreational athletes that underwent unaccustomed and high-load eccentric muscle contractions of knee flexors.

Methods

Participants

Twenty-nine healthy male participants were included in the study and randomly assigned in control group (CG) and experimental group (EG) (Table 1). Inclusion criteria are as follows: males, 18 ≤ age < 40 years, fat mass < 30%, and regularly active in different sport programs ≥5 years. Exclusion criteria are as follows: active national- or international-level athletes, contraindication for radiofrequency treatment, alcohol consumption in the period of the study, and skeletomuscular injuries of the lower limbs in the last year prior the study. All procedures were ethically approved by National Ethics Committee (No. 0120-84/2020/4), and all participants signed written consent after detailed explanation and prior any experimental procedures.

Table 1

Basic Anthropometric Data of Study Participants

Control groupExperimental groupP
n1514
Age, y25.2 (4.5)25.2 (4.7).993
Body height, m1.79 (0.06)1.81 (0.06).403
Body mass, kg77.6 (12.6)85.8 (16.8).147
Body mass index, kg/m224.1 (3.1)26.0 (4.1).160
Fat mass, %20.5 (4.7)23.6 (9.2).276
Bone mineral density, z score1.30 (0.11)1.37 (0.12).177

Research Design

In this randomized controlled trial, participants were randomly (by drawing tickets) assigned in 2 groups. CG (n = 15) had no therapeutical intervention after triggering EIMD. EG (n = 14) followed 448-kHz CRMRF therapies 5 times, immediately after triggering EIMD and following 4 days. All assessments were performed just before EIMD (baseline data collection [BDC]) and 1 day (EIMD + 1), 2 days (EIMD + 2), 5 days (EIMD + 5), and 9 days (EIMD + 9) after triggering EIMD.

Triggering EIMD

Triggering EIMD was performed immediately after BDC. EIMD was triggered in right knee flexors using isokinetic machine (KINEO, Globus Ltd). Participants stood on an elevated platform on the left leg, with the right leg of the ground and their arms fixed to arm holders. Hip was fixed by a frontal support, in 30° hip flexion. After assessing maximal isometric voluntary knee flexion (2 attempts at 30° and 2 attempts at 45° knee flexion), a 20% higher load was applied for eccentric contractions. Participants performed 5 sets of 10 eccentric contractions with the isokinetic velocity of 30°/s from 90° knee flexion to full knee extension. A 5-second break was allowed between the contractions within the set, and 1-minute rest was applied between sets.

A Nonthermal 448-kHz CRMRF Therapy

A nonthermal 448-kHz CRMRF therapy (INDIBA Activ CT9, Power 350 VA or 100 W, INDIBA Ltd) was performed in a right leg by a trained physiotherapist in a relaxed prone position 15 minutes after triggering EIMD and at EIMD + 1, EIMD + 2, EIMD + 3, and EIMD + 4. The protocol was proposed by producer’s expert team and consisted of treatment at the frequency of 448 kHz, in both capacitive and in resistive mode, for 20 minutes per session on participant’s targeted hamstring, divided to 10-minute capacitive mode and 10-minute resistive mode, in a nonthermal range of delivered energy (INDIBA Analog Scale: 1–2). Participants did not feel any thermal effects. INDIBA Activ Cream was used to reduce cutaneous resistance, to moisten the skin, and to minimize friction between the skin and the electrode. The probe was moved up and down along the hamstring line as well as in circular motion with slight pressure to assure good contact.

Assessments

Anthropometry was assessed at BDC by standard tools, scale, and stadiometer, and body mass index was calculated. Body fat and bone mineral density were measured by dual-energy X-ray absorptiometry (LUNAR Prodigy 511212MA, GE Healthcare Ltd) at BDC. Other assessments were performed at all time points: BDC, EIMD + 1, EIMD + 2, EIMD + 5, and EIMD + 9, in that order.

TMG was performed in biceps femoris and semitendinosus muscles in both legs; however, only results of the right leg are presented. It is important to mention that there were no significant changes found after EIMD or between groups in left leg. TMG measures mechanical response (a thickening of the muscle belly) during isometric contraction, elicited by 1-millisecond maximal electrical monophasic rectangular pulse.22 Electrical pulse was applied to the skin above the muscle belly using 2 self-adhesive 5-cm electrodes (PALS, Axelgaard), anode placed 5 cm distally and cathode placed 5 cm proximally from the measuring point. A measuring point was determined at a middle point of the muscle belly (in both muscles). From 2 saved responses, an average maximal displacement (in millimeters) was calculated as well as the average delay time (in milliseconds; from the pulse to 10% of maximal displacement) and contraction time (in milliseconds; from 10% to 90% of maximal displacement). The radial velocity of contraction was calculated as 0.8 × maximal displacement/contraction time.

Standardized warm-up consisted of 5-minute step test, changing pivot leg every minute. Afterward, a 5-minute series of stretching exercises were performed targeting only hamstring muscles.

A sit and reach test was performed sitting on the floor with legs stretched out straight ahead. Shoes were removed. The soles of the feet were placed flat against the box. Both knees were locked and pressed flat to the floor. The participant reached forward with his fingers along the measuring line as far as possible and held that position for at least 2 seconds while the distance was recorded. The distance was recorded to the nearest centimeter. The level of the feet was 40 cm mark, whereas values higher than 40 cm represented fingers crossing toes. Two attempts were performed, and an average distance was recorded.

A visual analog pain score was assessed during the sit and reach test. During both maximal efforts, participants self-reported pain score in right hamstring muscles by 10-point visual analog score. An average value was further analyzed.

Maximal voluntary contraction (MVC) during knee flexion was measured unilaterally in isometric dynamometer with knee angle set at 30° flexion. Although both legs were assessed only results of the right leg are presented in this study. It is important to mention that there were no significant changes found after EIMD or between groups in left leg. Participants performed 2 warm-up knee flexions subjectively targeted at 50% and 75% MVC, being followed by three 5-second test knee flexions from where a maximal 1-second MVC torque was estimated. A 1-minute rest was applied between each trial. All participants were encouraged equally in all assessments. An effort with highest MVC torque was further analyzed.

Maximal rate of torque development in first 100 millisecond (RTD100) was measured unilaterally in isometric dynamometer with knee angle set at 30° flexion. Although both legs were assessed, only results of the right leg are presented in this study. It is important to mention that there were no significant changes found after EIMD or between groups in left leg. After MVC trials, participants performed three 3-second test knee flexions with a ready-steady-go instruction. A 1-minute rest was applied between each trial. All participants were encouraged equally in all assessments. An effort with highest RTD100 was further analyzed.

Statistics

All data are reported with mean and SD values. There were no violations of normality (visually checked with Q–Q plot and analytically with Shapiro–Wilk test) and homogeneity of variances (Levene test). Therefore, all statistical decisions were performed using a 2-factorial general linear model, with time (BDC, EIMD + 1, EIMD + 2, EIMD + 5, and EIMD + 9) as within and group (CG and EG) as between factors. If time × group interaction was significant at Ptime × group ≤ .05, a post hoc test was used to reveal differences at each time point. If there were differences at BDC, an analysis of covariance was used controlling for BDC differences. Furthermore, a series of paired t tests were used to distinguish return to BDC values at any time point in each group; however, a Bonferroni correction of P values (being initially set at ≤.05) was applied.

Results

All participants completed all study examinations, and there were no drop-out, serious injury, or permanent consequences from the study intervention or assessments.

MVC and RTD100 decreased with time (P < .001) and more in CG than in EG (Ptime × group = .043; η2 = .096 and Ptime × group = .040; η2 = .095, respectively). An interaction confirmed faster recovery in EG than in CG (Figure 1A and 1B); specifically, EG recovered to BDC values in EIMD + 9, but CG did not. There was no interaction found for sit and reach distance and pain score (Figure 1C and 1D). Pooled groups showed decrease in sit and reach distance with time, without recovery to BDC at EIMD + 9. The pain score of pooled groups increased only at EIMD + 2.

Figure 1
Figure 1

—MVC (A) torque, RTD100 (B), sit and reach distance (C), and VAS (D) for right hamstring pain during sit and reach test at BDC, 1 day, 2 days, 5 days, and 9 days after EIMD. Data for control and experimental groups. $Different from BDC for pooled groups (Ptime × group > .05) or for each group (Ptime × group ≤ .05). BDC indicates baseline data collection; EIMD, exercise-induced muscle damage; MVC, maximal voluntary contraction; RTD100, rate of torque development in first 100 milliseconds; VAS, visual analog scale.

Citation: Journal of Sport Rehabilitation 32, 6; 10.1123/jsr.2022-0162

Figure 2 presents TMG parameters change after EIMD in both groups. Interaction effect was found in all parameters, except in delay time; however, being close to significant in semitendinosus muscle. The delay time of both muscles increased with time (P < .001; biceps femoris η2 = .299; semitendinosus η2 = .308; Figure 2A and 2B) and did not recover to BDC values. An interaction confirms different changes of contraction time in both muscles with time in both groups (biceps femoris: Ptime × group = .032; η2 = .096 and semitendinosus: Ptime × group = .014; η2 = .127; Figure 2C and 2D). The biceps femoris contraction time increased with time only in CG (not in EG), without recovery, from EIMD + 1 to EIMD + 9 (P < .001; η2 = .375). The semitendinosus contraction time also increased with time (P < .001; η2 = .375)—specifically, in EG only at EIMD + 1 (P < .001; η2 = .342) and in CG without recovery to BDC values, from EIMD + 1 to EIMD + 9 (P < .001; η2 = .460). An interaction confirms different changes of maximal displacement in both muscles with time in both groups (biceps femoris: Ptime × group = .026; η2 = .110 and semitendinosus: Ptime × group = .030; η2 = .096; Figure 2E and 2F). The biceps femoris maximal displacement decreased with time, specifically, in EG from EIMD + 1 until EIMD + 2 (P < .001; η2 = .522), and in CG without recovery to BDC values, from EIMD + 1 to EIMD + 9 (P < .001; η2 = .575). The semitendinosus maximal displacement also decreased with time, specifically, in EG from EIMD + 1 until EIMD + 2 (P < .001; η2 = .458), and in CG without recovery to BDC values, from EIMD + 1 to EIMD + 9 (P < .001; η2 = .575). An interaction confirms different changes of radial contraction velocity in both muscles with time in both groups (biceps femoris: Ptime × group < .001; η2 = .232 and semitendinosus: Ptime × group < .001; η2 = .194; Figure 2G and 2H). The biceps femoris radial contraction velocity decreased with time, specifically, in EG from EIMD + 1 until EIMD + 5 (P < .001; η2 = .596), and in CG without recovery to BDC values, from EIMD + 1 to EIMD + 9 (P < .001; η2 = .658). The semitendinosus radial contraction velocity also decreased with time, specifically, in EG from EIMD + 1 until EIMD + 5 (P < .001; η2 = .596), and in CG without recovery to BDC values, from EIMD + 1 to EIMD + 9 (P < .001; η2 = .718).

Figure 2
Figure 2

—Td (A and B), Tc (C and D), Dm (E and F), and Vc (G, and H) of BF (left column) and ST (right column), at BDC, 1 day, 2 days, 5 days, and 9 days after EIMD. Data for control and experimental groups. $Different from BDC for pooled groups (Ptime × group > .05) or for each group (Ptime × group ≤ .05). BDC indicates baseline data collection; BF, biceps femoris; Dm, maximal amplitude; EIMD, exercise-induced muscle damage; ST, semitendinosus; Td, tensiomyographic delay time; Tc, contraction time; Vc, contraction velocity.

Citation: Journal of Sport Rehabilitation 32, 6; 10.1123/jsr.2022-0162

Discussion

Our study confirms the efficacy of 5-day 448-kHz CRMRF nonthermal treatment on amelioration of EIMD in recreational athletes after unaccustomed high-load eccentric muscle contractions of knee flexors. This is the first study reporting effects of 448-kHz CRMRF nonthermal therapy on the muscle recovery on any exercise.

Muscle Soreness

Pooled participants reported increased soreness (during sit and reach test) in the hamstring muscles at EIMD + 2, confirming the presence of delayed muscle soreness. The average baseline soreness level was 4.5 out of 10 and when elevated 6.1 out of 10. The elevation in soreness was in agreement with similar study on the quadriceps.23 Although the mechanisms underlying soreness remain unclear, it is believed to be related to muscle structural damage followed by ion imbalance, inflammation, and pain triggered by muscle contraction, stretch, pressure, or mechanical stimuli that do not usually induce pain in an unexercised muscle.24

Maximal Voluntary Contractions

Although muscle maximal force (MVC) and explosive force (RTD100) were not ameliorated by CRMRF in first 5 days after EIMD, the EG achieved full recovery at EIMD + 9 while CG did not. The decrease in MVC and RTD100 were highest at EIMD + 2 being 43.2% and 38.2%, respectively. MVC decrease was in line with general findings of others in knee extensors, ranging from 15% to 50%, after eccentric exercise, which in general remained decreased for up to 4 days.25 However, there is a small number of studies for hamstrings, reporting power decrements (8%–14%) after plyometric exercises.26 Muscle force reduction is reported to be one of the best indicators that muscle damage has occurred following eccentric exercise.11 In general, maximal force declines immediately after eccentric exercise due to fatigue and muscle damage, whereas decline related to muscle damage reaches maximal values within the first 48 hours. Eccentric exercise may result in subcellular damage, including Z-line streaming, A-band widening, sarcomere disorganization, and cytoskeletal disruption, which are evident after exercise.11 Decreased MVC was reported for periods longer than 5.5 days,15,23 whereas the exact duration is unknown. To support this, studies reported unrecovered MVC also at the 26th day after eccentric exercise (declined by 19% in males and 7% in females)23; in 2 individuals, the full MVC recovery was reached at 61 and 89 days after eccentric exercise.23 Our data of CG confirmed unrecovered MVC at EIMD + 9 (declined by 25.9%), while EG fully recovered already at EIMD + 9.

Explosive Isometric Contractions

Compared with MVC, the effect of unaccustomed eccentric exercise on the ability to generate rapid power has received limited attention, especially in hamstring muscles.26 RTD100 decreased less than MVC (RTD100: 38.2% vs MVC: 43.2%), and that is in line with others reporting 21.8% lower quadriceps RFD100 after at least 24 hours post eccentric exercise25 and 18.4% lower hamstring RTD200 after 24 hours post plyometric exercises without full recovery at 5 days (decreased by 6.8%).26 It is very likely that common mechanisms were involved in the suppression of the maximal and explosive torque of the muscle. However, different neural strategies for the 2 tasks exist in the agonist and antagonist muscle activities25 within the first 24 hours after eccentric exercise. An increase in co-activation of the antagonists, because of fatigue, would limit the initial acceleration of the muscle contraction by counteracting the agonist muscle action, but no longer than 24 hours after eccentric exercise.25 Due to more severe exercise regime in our study (unaccustomed eccentric exercise) in comparison to plyometric exercise, we have reported higher RTD100 decline at EIMD + 2 than Sarabon et al26 in EIMD200 (38.2% vs 15.9%). Furthermore, our data in CG confirm lack of full recovery also at EIMD + 9 (decreased by 25.7%), whereas EG fully recovered already at EIMD + 9.

Tensiomyography

All TMG parameters of both muscles (except delay time) indicated ameliorated EIMD in EG when compared with CG. Nevertheless, delay time increased after EIMD without recovery to baseline values for at least at EIMD + 9, indicating higher latency between electrical stimuli and the beginning of the muscle contraction. In biceps femoris, there was no trend toward recovery, whereas in semitendinosus we found a trend toward reversibility of delay time values as well as a trend toward ameliorated changes in EG when compared with CG. Delay time was never reported before in EIMD studies but assimilates with evoked electromechanical delay. Delay time and evoked electromechanical delay are both indexes that are dependent on the excitation contraction coupling. The EIMD has been shown to negatively influence the excitation contraction coupling by reducing the Ca2+ release and by disturbing the Ca2+ dynamics (release and uptake) during this process.27 An additional factor that can influence electromechanical delay after EIMD can be the possible deterioration of muscle fiber conduction velocity and selective damage of the fast-twitch fiber.28 To support this theory, we have found prolonged TMG contraction time in both muscles as described below. EIMD decreases muscle force for several days mainly due to the reduction in the number of active sarcomeres. Considering the structural alterations, induced by EIMD, the force transmission around the disrupted sarcomeres could be impaired, due to disruption of force transmitters between myofibrils (eg, desmin) or muscle fibers (eg, extracellular matrix)24 leading to increased time to transmit the force from muscle to the bone.

Increased contraction time, previously correlated to vastus lateralis myosin heavy chain I proportion,22 confirmed deterioration of muscle fiber conduction velocity and possible selective damage of the fast-twitch fiber reported previously.28 Specifically, they reported decreased electromyographic median frequency after eccentric exercise leading to EIMD. Investigations examining direct evidence of EIMD immediately postexercise have provided convincing data of myofibrillar disruption resulting from eccentric contractions,12 which appear to be focused within fast-twitch fibers. Indeed, there is some evidence that in eccentric actions there may be selective activation of high threshold fast-twitch motor units, whereas, in concentric actions, the low threshold slow units could be preferentially recruited,29 and animal studies confirmed that fast-twitch fibers may be selectively damaged after repeated lengthening of the muscle.30 However, the elongation of contraction time after EIMD was completely absent (biceps femoris: CG 37.1%) or ameliorated (semitendinosus: EG 9.4% vs CG 28.7%) in EG when compared with CG. The increased TMG contraction time was confirmed also previously in biceps brachii after eccentrically induced EIMD.15 Specifically, they reported 25.7% longer contraction time plateauing second day after induced EIMD with no indication of recovery by the end of the study (6 d), as was observed also in our study—no recovery in both muscles until the end of our study (9 d), too.

Decreased maximal displacement was found in both muscles. In CG, maximal displacement decreased the most at EIMD + 2 (biceps femoris: 49.6%; semitendinosus: 44.6%) without full recovery at EIMD + 9 (biceps femoris: 19.3%; semitendinosus: 24.8%). Decreased maximal displacement was found also in biceps brachii after eccentrically induced EIMD.15 Specifically, they reported 30.5% lower maximal displacement 1 day after EIMD with following linear recovery trend; however, without full recovery by the end of the study (being lower for 17.9% at 6 d following EIMD). maximal displacement, an indirect measure of passive muscle stiffness and tone31 where decreased maximal displacement should be interpreted as increased passive muscle tension, since higher maximal displacement was found after 35-day bed rest as well as after the first day of 35-day bed rest31 suggesting the maximal displacement is sensitive to early-atrophic changes. Indeed, decreased maximal displacement was reported previously after acute eccentric exercise triggering EIMD15 and after chronic plyometric exercise in young32 and old.33 Decreased maximal displacement reflects swelling response and/or increased intracellular water and increased passive muscle stiffness being regularly reported after EIMD. Passive stiffness rises because of damaged fibers developing an injury contracture, which occurs because of the damage to the sarcoreticular membranes, leading to an uncontrolled release of Ca2+ into the sarcoplasm and swelling (after 24–48 h).34 However, the decrease in maximal displacement was ameliorated in EG. In EG, the biceps femoris maximal displacement decreased only at EIMD + 2 (EG: 32.2% vs CG: 49.6%), while semitendinosus maximal displacement decreased at EIMD + 1 being highest in EIMD + 2 (EG: 28.0% vs CG: 44.6%). Furthermore, EG showed full recovery in both muscles already at EIMD + 5, while both muscles in CG do not recover even until EIMD-9.

A ratio between maximal displacement and contraction time yields radial contraction velocity. Decreased maximal displacement and increased contraction time result in decreased radial contraction velocity, being highest at EIMD + 2 for both muscles and both groups, specifically in CG (biceps femoris: 62.7%; semitendinosus: 56.0%) and much less in EG (biceps femoris: 39.1%; semitendinosus: 34.8%). Furthermore, radial contraction velocity in EG recovered at EIMD + 9 while it did not in CG.

Effect of Nonthermal CRMRF Therapy on Outcomes

We have found 5-day nonthermal 448-kHz CRMRF therapy as effective in almost all main outcomes of the study. In general, this therapy assures quicker recovery to BDC, after EIMD + 5 (MVC, RTD100, TMG radial contraction velocity) and after EIMD + 2 (TMG maximal displacement), or even prevents changes (TMG contraction time), while in some outcomes, it was not effective (sit and reach, pain, TMG delay time).

A 448-kHz CRMRF therapy is currently used in physical rehabilitation and sports medicine to treat muscle, bone, ligament, and tendon lesions, and unlike other thermal therapies, it does not induce side effects like edema and dermal or epidermal burns.21 EIMD is accompanied by a well-characterized inflammatory response, and clinical studies have shown that 448-kHz CRMRF therapy-elicited acceleration of injury recovery involves a general reduction of the extension of the damaged area, together with anti-inflammatory processes, analgesia, and recovery of muscle function,17,18 most likely through the mediation by stimulation of the proliferation of stem cells in the injured tissues.21

Conclusions

We have confirmed beneficial effects of nonthermal CRMRF therapy on the hamstring muscle recovery after EIMD using nonaccustomed eccentric exercise. After EIMD, hamstring flexibility decreased with increased muscle soreness sensation for as long as 5 and 2 days, respectively. A 448-kHz CRMRF therapy ameliorated MVC and RTD100 decrease after EIMD and assured recovery at ninth-day post EIMD when compared with no therapy group. Most interesting are TMG data, showing lower changes in muscle contractile properties after EIMD, with faster recovery afterward when compared with no therapy group.

Acknowledgments

The authors would like to thank Jan Čžan Stermšek for the laboratory work and all participants involved in the study. The study was financially supported by Slovenian Sport Foundation (grant no. RR-21-675) and Slovenian Research Agency ARRS (grant no. P5-0381).

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    • Search Google Scholar
    • Export Citation
  • 4.

    Hortobágyi T, Hill JP, Houmard JA, Fraser DD, Lambert NJ, Israel RG. Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol. 1996;80(3):765772. PubMed ID: 8964735 doi:10.1152/jappl.1996.80.3.765

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Lastayo PC, Reich TE, Urquhart M, Hoppeler H, Lindstedt SL. Chronic eccentric exercise: improvements in muscle strength can occur with little demand for oxygen. Am J Physiol Regul Integr Comp Physiol. 1999;276(2):R611R615. doi:10.1152/ajpregu.1999.276.2.R611

    • Search Google Scholar
    • Export Citation
  • 6.

    Hortobágyi T, Money J, Zheng D, Dudek R, Fraser D, Dohm L. Muscle adaptations to 7 days of exercise in young and older humans: eccentric overload versus standard resistive training. J Aging Phys Act. 2002;10(3):290305. doi:10.1123/japa.10.3.290

    • Search Google Scholar
    • Export Citation
  • 7.

    Vogt M, Hoppeler HH. Eccentric exercise: mechanisms and effects when used as training regime or training adjunct. J Appl Physiol. 2014;116(11):14461454. PubMed ID: 24505103 doi:10.1152/japplphysiol.00146.2013

    • Search Google Scholar
    • Export Citation
  • 8.

    Berg HE, Eiken O, Tesch PA. Involvement of eccentric muscle actions in giant slalom racing. Med Sci Sports Exerc. 1995;27(12):16661670. PubMed ID: 8614323 doi:10.1249/00005768-199512000-00013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Lorenz D, Reiman M. The role and implementation of eccentric training in athletic rehabilitation: tendinopathy, hamstring strains, and ACL reconstruction. Int J Sports Phys Ther. 2011;6(1):2744. PubMed ID: 21655455

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Markus I, Constantini K, Hoffman JR, Bartolomei S, Gepner Y. Exercise-induced muscle damage: mechanism, assessment and nutritional factors to accelerate recovery. Eur J Appl Physiol. 2021;121(4):969992. PubMed ID: 33420603 doi:10.1007/s00421-020-04566-4

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Butterfield TA. Eccentric exercise in vivo. Exerc Sport Sci Rev. 2010;38(2):5160. PubMed ID: 20335736 doi:10.1097/JES.0b013e3181d496eb

  • 12.

    Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med. 1991;12(3):184207. PubMed ID: 1784873 doi:10.2165/00007256-199112030-00004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Morgan DL, Proske U. Popping sarcomere hypothesis explains stretch-induced muscle damage. Clin Exp Pharmacol Physiol. 2004;31(8):541545. PubMed ID: 15298548 doi:10.1111/j.1440-1681.2004.04029.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Gissel H, Clausen T. Excitation-induced Ca 2+ influx and skeletal muscle cell damage. Acta Physiol Scand. 2001;171(3):327334. PubMed ID: 11412145 doi:10.1046/j.1365-201x.2001.00835.x

    • Search Google Scholar
    • Export Citation
  • 15.

    Hunter AM, Galloway SD, Smith IJ, et al. Assessment of eccentric exercise-induced muscle damage of the elbow flexors by tensiomyography. J Electromyogr Kinesiol. 2012;22(3):334341. PubMed ID: 22336641 doi:10.1016/j.jelekin.2012.01.009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Franz A, Behringer M, Harmsen JF, et al. Ischemic preconditioning blunts muscle damage responses induced by eccentric exercise. Med Sci Sports Exerc. 2018;50(1):109115. PubMed ID: 28832392 doi:10.1249/MSS.0000000000001406

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Takahashi K, Suyama T, Takakura Y, Hirabayashi S, Tsuzuki N, Li ZS. Clinical effects of capacitive electric transfer hyperthermia therapy for cervico-omo-brachial pain. J Phys Ther Sci. 2000;12(1):4348. doi:10.1589/jpts.12.43

    • Search Google Scholar
    • Export Citation
  • 18.

    Takahashi K, Suyama T, Onodera M, Hirabayashi S, Tsuzuki N, Zhong-Shi L. Clinical effects of capacitive electric transfer hyperthermia therapy for lumbago. J Phys Ther Sci. 1999;11(1):4551. doi:10.1589/jpts.11.45

    • Search Google Scholar
    • Export Citation
  • 19.

    Duñabeitia I, Arrieta H, Torres-Unda J, et al. Effects of a capacitive-resistive electric transfer therapy on physiological and biomechanical parameters in recreational runners: a randomized controlled crossover trial. Phys Ther Sport. 2018;32:227234. PubMed ID: 29870922 doi:10.1016/j.ptsp.2018.05.020

    • Search Google Scholar
    • Export Citation
  • 20.

    Kumaran B, Watson T. Skin thermophysiological effects of 448 kHz capacitive resistive monopolar radiofrequency in healthy adults: a randomised crossover study and comparison with pulsed shortwave therapy. Electromagn Biol Med. 2018;37(1):112. PubMed ID: 29308927 doi:10.1080/15368378.2017.1422260

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Hernández-Bule ML, Paíno CL, Trillo , Úbeda A. Electric stimulation at 448 kHz promotes proliferation of human mesenchymal stem cells. Cell Physiol Biochem. 2014;34(5):17411755. PubMed ID: 25427571 doi:10.1159/000366375

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Šimunič B, Degens H, Rittweger J. Noninvasive estimation of myosin heavy chain composition in human skeletal muscle. Med Sci Sports Exerc. 2011;43(9):16191625. PubMed ID: 21552151 doi:10.1249/MSS.0b013e31821522d0

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Sayers SP, Clarkson PM. Force recovery after eccentric exercise in males and females. Eur J Appl Physiol. 2001;84(1–2):122126. PubMed ID: 11394240 doi:10.1007/s004210000346

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol. 2001;537(2):333345. doi:10.1111/j.1469-7793.2001.00333.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Vila-Chã C, Hassanlouei H, Farina D, Falla D. Eccentric exercise and delayed onset muscle soreness of the quadriceps induce adjustments in agonist–antagonist activity, which are dependent on the motor task. Exp Brain Res. 2012;216(3):385395. PubMed ID: 22094715 doi:10.1007/s00221-011-2942-2

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Sarabon N, Panjan A, Rosker J, Fonda B. Functional and neuromuscular changes in the hamstrings after drop jumps and leg curls. J Sports Sci Med. 2013;12(3):431438. PubMed ID: 24149148

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Morgan DL, Allen DG. Early events in stretch-induced muscle damage. J Appl Physiol. 1999;87(6):20072015. PubMed ID: 10601142 doi:10.1152/jappl.1999.87.6.2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Linnamo V, Bottas R, Komi PV. Force and EMG power spectrum during and after eccentric and concentric fatigue. J Electromyogr Kinesiol. 2000;10(5):293300. PubMed ID: 11018439 doi:10.1016/S1050-6411(00)00021-3

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Nardone A, Romanò C, Schieppati M. Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles. J Physiol. 1989;409(1):451471. doi:10.1113/jphysiol.1989.sp017507

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Lieber RL, Friden J. Selective damage of fast glycolytic muscle fibres with eccentric contraction of the rabbit tibialis anterior. Acta Physiol Scand. 1988;133(4):587588. PubMed ID: 3227940 doi:10.1111/j.1748-1716.1988.tb08446.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Šimunič B, Koren K, Rittweger J, et al. Tensiomyography detects early hallmarks of bed-rest-induced atrophy before changes in muscle architecture. J Appl Physiol. 2019;26(4):815822. doi:10.1152/japplphysiol.00880.2018

    • Search Google Scholar
    • Export Citation
  • 32.

    Zubac D, Šimunič B. Skeletal muscle contraction time and tone decrease after 8 weeks of plyometric training. J Strength Cond Res. 2017;31(6):16101619. PubMed ID: 28538312 doi:10.1519/JSC.0000000000001626

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Zubac D, Paravlić A, Koren K, Felicita U, Šimunič B. Plyometric exercise improves jumping performance and skeletal muscle contractile properties in seniors. J Musculoskelet Neuronal Interact. 2019;19(1):38.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Whitehead NP, Weerakkody NS, Gregory JE, Morgan DL, Proske U. Changes in passive tension of muscle in humans and animals after eccentric exercise. J Physiol. 2001;533(2):593604. doi:10.1111/j.1469-7793.2001.0593a.x

    • PubMed
    • Search Google Scholar
    • Export Citation

Nonthermal 5-day 448-kHz CRMRF therapy:

ameliorated muscle deterioration after EIMD;

yielded lower deterioration of muscle function with faster recovery;

yielded lower changes in muscle contractile properties with faster recovery.

  • Collapse
  • Expand
  • Figure 1

    —MVC (A) torque, RTD100 (B), sit and reach distance (C), and VAS (D) for right hamstring pain during sit and reach test at BDC, 1 day, 2 days, 5 days, and 9 days after EIMD. Data for control and experimental groups. $Different from BDC for pooled groups (Ptime × group > .05) or for each group (Ptime × group ≤ .05). BDC indicates baseline data collection; EIMD, exercise-induced muscle damage; MVC, maximal voluntary contraction; RTD100, rate of torque development in first 100 milliseconds; VAS, visual analog scale.

  • Figure 2

    —Td (A and B), Tc (C and D), Dm (E and F), and Vc (G, and H) of BF (left column) and ST (right column), at BDC, 1 day, 2 days, 5 days, and 9 days after EIMD. Data for control and experimental groups. $Different from BDC for pooled groups (Ptime × group > .05) or for each group (Ptime × group ≤ .05). BDC indicates baseline data collection; BF, biceps femoris; Dm, maximal amplitude; EIMD, exercise-induced muscle damage; ST, semitendinosus; Td, tensiomyographic delay time; Tc, contraction time; Vc, contraction velocity.

  • 1.

    Franchi MV, Reeves ND, Narici MV. Skeletal muscle remodeling in response to eccentric vs. concentric loading: morphological, molecular, and metabolic adaptations. Front Physiol. 2017;8:447. doi:10.3389/fphys.2017.00447

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  • 2.

    Owens DJ, Twist C, Cobley JN, Howatson G, Close GL. Exercise-induced muscle damage: what is it, what causes it and what are the nutritional solutions? Eur J Sport Sci. 2019;19(1):7185. PubMed ID: 30110239 doi:10.1080/17461391.2018.1505957

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Howatson G, van Someren KA. The prevention and treatment of exercise-induced muscle damage. Sports Med. 2008;38(6):483503. PubMed ID: 18489195 doi:10.2165/00007256-200838060-00004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Hortobágyi T, Hill JP, Houmard JA, Fraser DD, Lambert NJ, Israel RG. Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol. 1996;80(3):765772. PubMed ID: 8964735 doi:10.1152/jappl.1996.80.3.765

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Lastayo PC, Reich TE, Urquhart M, Hoppeler H, Lindstedt SL. Chronic eccentric exercise: improvements in muscle strength can occur with little demand for oxygen. Am J Physiol Regul Integr Comp Physiol. 1999;276(2):R611R615. doi:10.1152/ajpregu.1999.276.2.R611

    • Search Google Scholar
    • Export Citation
  • 6.

    Hortobágyi T, Money J, Zheng D, Dudek R, Fraser D, Dohm L. Muscle adaptations to 7 days of exercise in young and older humans: eccentric overload versus standard resistive training. J Aging Phys Act. 2002;10(3):290305. doi:10.1123/japa.10.3.290

    • Search Google Scholar
    • Export Citation
  • 7.

    Vogt M, Hoppeler HH. Eccentric exercise: mechanisms and effects when used as training regime or training adjunct. J Appl Physiol. 2014;116(11):14461454. PubMed ID: 24505103 doi:10.1152/japplphysiol.00146.2013

    • Search Google Scholar
    • Export Citation
  • 8.

    Berg HE, Eiken O, Tesch PA. Involvement of eccentric muscle actions in giant slalom racing. Med Sci Sports Exerc. 1995;27(12):16661670. PubMed ID: 8614323 doi:10.1249/00005768-199512000-00013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Lorenz D, Reiman M. The role and implementation of eccentric training in athletic rehabilitation: tendinopathy, hamstring strains, and ACL reconstruction. Int J Sports Phys Ther. 2011;6(1):2744. PubMed ID: 21655455

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Markus I, Constantini K, Hoffman JR, Bartolomei S, Gepner Y. Exercise-induced muscle damage: mechanism, assessment and nutritional factors to accelerate recovery. Eur J Appl Physiol. 2021;121(4):969992. PubMed ID: 33420603 doi:10.1007/s00421-020-04566-4

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Butterfield TA. Eccentric exercise in vivo. Exerc Sport Sci Rev. 2010;38(2):5160. PubMed ID: 20335736 doi:10.1097/JES.0b013e3181d496eb

  • 12.

    Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med. 1991;12(3):184207. PubMed ID: 1784873 doi:10.2165/00007256-199112030-00004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Morgan DL, Proske U. Popping sarcomere hypothesis explains stretch-induced muscle damage. Clin Exp Pharmacol Physiol. 2004;31(8):541545. PubMed ID: 15298548 doi:10.1111/j.1440-1681.2004.04029.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Gissel H, Clausen T. Excitation-induced Ca 2+ influx and skeletal muscle cell damage. Acta Physiol Scand. 2001;171(3):327334. PubMed ID: 11412145 doi:10.1046/j.1365-201x.2001.00835.x

    • Search Google Scholar
    • Export Citation
  • 15.

    Hunter AM, Galloway SD, Smith IJ, et al. Assessment of eccentric exercise-induced muscle damage of the elbow flexors by tensiomyography. J Electromyogr Kinesiol. 2012;22(3):334341. PubMed ID: 22336641 doi:10.1016/j.jelekin.2012.01.009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Franz A, Behringer M, Harmsen JF, et al. Ischemic preconditioning blunts muscle damage responses induced by eccentric exercise. Med Sci Sports Exerc. 2018;50(1):109115. PubMed ID: 28832392 doi:10.1249/MSS.0000000000001406

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Takahashi K, Suyama T, Takakura Y, Hirabayashi S, Tsuzuki N, Li ZS. Clinical effects of capacitive electric transfer hyperthermia therapy for cervico-omo-brachial pain. J Phys Ther Sci. 2000;12(1):4348. doi:10.1589/jpts.12.43

    • Search Google Scholar
    • Export Citation
  • 18.

    Takahashi K, Suyama T, Onodera M, Hirabayashi S, Tsuzuki N, Zhong-Shi L. Clinical effects of capacitive electric transfer hyperthermia therapy for lumbago. J Phys Ther Sci. 1999;11(1):4551. doi:10.1589/jpts.11.45

    • Search Google Scholar
    • Export Citation
  • 19.

    Duñabeitia I, Arrieta H, Torres-Unda J, et al. Effects of a capacitive-resistive electric transfer therapy on physiological and biomechanical parameters in recreational runners: a randomized controlled crossover trial. Phys Ther Sport. 2018;32:227234. PubMed ID: 29870922 doi:10.1016/j.ptsp.2018.05.020

    • Search Google Scholar
    • Export Citation
  • 20.

    Kumaran B, Watson T. Skin thermophysiological effects of 448 kHz capacitive resistive monopolar radiofrequency in healthy adults: a randomised crossover study and comparison with pulsed shortwave therapy. Electromagn Biol Med. 2018;37(1):112. PubMed ID: 29308927 doi:10.1080/15368378.2017.1422260

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Hernández-Bule ML, Paíno CL, Trillo , Úbeda A. Electric stimulation at 448 kHz promotes proliferation of human mesenchymal stem cells. Cell Physiol Biochem. 2014;34(5):17411755. PubMed ID: 25427571 doi:10.1159/000366375

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Šimunič B, Degens H, Rittweger J. Noninvasive estimation of myosin heavy chain composition in human skeletal muscle. Med Sci Sports Exerc. 2011;43(9):16191625. PubMed ID: 21552151 doi:10.1249/MSS.0b013e31821522d0

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Sayers SP, Clarkson PM. Force recovery after eccentric exercise in males and females. Eur J Appl Physiol. 2001;84(1–2):122126. PubMed ID: 11394240 doi:10.1007/s004210000346

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol. 2001;537(2):333345. doi:10.1111/j.1469-7793.2001.00333.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Vila-Chã C, Hassanlouei H, Farina D, Falla D. Eccentric exercise and delayed onset muscle soreness of the quadriceps induce adjustments in agonist–antagonist activity, which are dependent on the motor task. Exp Brain Res. 2012;216(3):385395. PubMed ID: 22094715 doi:10.1007/s00221-011-2942-2

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Sarabon N, Panjan A, Rosker J, Fonda B. Functional and neuromuscular changes in the hamstrings after drop jumps and leg curls. J Sports Sci Med. 2013;12(3):431438. PubMed ID: 24149148

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Morgan DL, Allen DG. Early events in stretch-induced muscle damage. J Appl Physiol. 1999;87(6):20072015. PubMed ID: 10601142 doi:10.1152/jappl.1999.87.6.2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Linnamo V, Bottas R, Komi PV. Force and EMG power spectrum during and after eccentric and concentric fatigue. J Electromyogr Kinesiol. 2000;10(5):293300. PubMed ID: 11018439 doi:10.1016/S1050-6411(00)00021-3

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Nardone A, Romanò C, Schieppati M. Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles. J Physiol. 1989;409(1):451471. doi:10.1113/jphysiol.1989.sp017507

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Lieber RL, Friden J. Selective damage of fast glycolytic muscle fibres with eccentric contraction of the rabbit tibialis anterior. Acta Physiol Scand. 1988;133(4):587588. PubMed ID: 3227940 doi:10.1111/j.1748-1716.1988.tb08446.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Šimunič B, Koren K, Rittweger J, et al. Tensiomyography detects early hallmarks of bed-rest-induced atrophy before changes in muscle architecture. J Appl Physiol. 2019;26(4):815822. doi:10.1152/japplphysiol.00880.2018

    • Search Google Scholar
    • Export Citation
  • 32.

    Zubac D, Šimunič B. Skeletal muscle contraction time and tone decrease after 8 weeks of plyometric training. J Strength Cond Res. 2017;31(6):16101619. PubMed ID: 28538312 doi:10.1519/JSC.0000000000001626

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Zubac D, Paravlić A, Koren K, Felicita U, Šimunič B. Plyometric exercise improves jumping performance and skeletal muscle contractile properties in seniors. J Musculoskelet Neuronal Interact. 2019;19(1):38.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Whitehead NP, Weerakkody NS, Gregory JE, Morgan DL, Proske U. Changes in passive tension of muscle in humans and animals after eccentric exercise. J Physiol. 2001;533(2):593604. doi:10.1111/j.1469-7793.2001.0593a.x

    • PubMed
    • Search Google Scholar
    • Export Citation
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