Exercise improves fitness level and controls weight. However, exhaustive training, particularly exercise training at high intensity, can induce temporary damage to muscle with a change in the sarcomeres and components of the excitation-contraction coupling system (10,12,35). Namely, exercise-induced muscle damage (EIMD) can occur by sudden active stretching of the muscle-tendon unit through unaccustomed or overtraining exercise. Muscle damage is frequently observed in athletes, weight lifters, recreational athletes, and ordinary persons who do not exercise regularly (22). Such muscle damage is characterized by pain, disturbed proprioception, decreases in strength and power, inflammation, and delayed onset muscle soreness (20,32). Many studies have reported therapeutic interventions such as electrical stimulation, cryotherapy, massage, and drugs to alleviate muscle damage (9,20,36). These treatments relieve symptoms, prevent sustained impairment, and help in the healing process (28).
Therapeutic massage is frequently used as a treatment to recover from muscle fatigue or damage. Massage increases local blood and lymph flow, decreases edema production, reduces muscular tone, and enhances mood (11,36). Many studies have investigated the recovery signs and symptoms of muscle and joint function following massage after muscle damage. It has been suggested that massage decreases the stress hormone cortisol and increases levels of serotonin and dopamine (13). Mechanical pressure on the muscle by massage has been associated with nervous system activity. These neural changes are believed to affect muscular tensions, and the potential for spasm and pain (25).
It is important to relieve the muscle function symptoms in athletes. Muscle and proprioception play important roles in functional joint stability. Dynamic tasks require accurate proprioceptive information and adequate muscular strength (30). Proprioception is the sense of joint and limb position derived partially from neural inputs arising from mechanoreceptors in the joints, muscles, tendons, and associated tissue. Afferent information from articular and muscle receptors (muscle spindle) determines muscle coordination, stiffness, and control. Awareness of the orientation of the body in space and direction, extent, and rate of movement in the limbs is essential to position and coordinate movement (2,17). Therefore, damage into muscle and proprioception affects normal coordinated movement. However, despite the important role of muscle and proprioception, the effect of therapeutic massage on muscular strength and proprioception remains unclear. In this study, we investigated whether therapeutic massage affects recovery of muscle function, particularly muscular strength and proprioception after EIMD.
Experimental Approach to the Problem
The participants were randomly divided to either the massage-treated after EIMD experimental group (n = 11) or EIMD control group (n = 10). The participant's characteristics are summarized in Table 1. The experimental group received 15-minute massage on the gastrocnemius; an experienced physical therapist provided 15-minute massage consisting of light stroking, milking, friction, and skin rolling. The control group received an attached transcutaneous electrical nerve stimulation pad without electrical stimuli on the gastrocnemius for 15 minutes; however, subjects in the control group were treated with electrical therapy for pain relief from physical therapist after all experimental procedures. We applied massage to the gastrocnemius of dominant foot. The dominant foot was selected as the foot used to kick a ball 3 m.
Twenty-one healthy subjects (age > 19 years) voluntarily participated in this study. We received informed consent from all subjects after explaining their rights and the experimental process. The inclusion criteria were as follows: (a) subjects who did not regularly conduct strengthening exercises on lower extremities and (b) those without a recent musculoskeletal injury. The exclusion criteria were (a) subjects with orthopedic disease or who had surgery on a lower extremity within 6 months and (b) those with hypersensitivity, cardiopulmonary disease, inflammatory disease, or an open lower leg wound.
Exercise-Induced Muscle Damage
Subjects performed exercise by going up and down a 5-story building 20 times. The subjects rested for 5 minutes, and then we measured lactate with a portable Lactate Pro analyzer (LT-1710; Arkray, Inc., Kyoto, Japan) by extracting blood form the tip of the right index finger. We compared blood lactate both pre- and postexercise to confirm muscle fatigue.
Surface electromyography was used to track muscle activity directly. We measured resting and isometric contractions on the gastrocnemius using sEMG. To induce isometric contraction on the gastrocnemius, subjects pushed a wall without the ankle movement for 5 seconds in the prone position. Disposable surface electrodes (Ag/AgCl) were placed on the proposed site to allow noninvasive collection of sEMG signals on the gastrocnemius of the dominant foot. The electrodes were placed on the medial gastrocnemius (2 cm medial to the midline of the calf) and the lateral gastrocnemius (2 cm lateral to the midline of the calf) in the direction of the muscle fibers. The skin was prepared before electrode attachment to reduce skin impedance. The sEMG signals were collected using the Delsys Tringo Wireless system (Delsys, Inc., Boston, MA, USA). The sEMG signals were digitized at a sampling frequency of 2,000 Hz, smooth full-wave rectified, and band-pass filtered (20–450 Hz) to remove low-frequency motion artifacts and high-frequency noise. We used average root mean square for muscle activity and then adopted maximum voluntary isometric contraction to normalize the EMG amplitude. The sEMG data were then analyzed by EMGworks 4.0.7 software (Delsys, Inc.). Subjects performed the test 3 times and the average values were used.
Subjects lay prone on an examining table for the ultrasound study of the gastrocnemius. The lower limbs of the subjects were extended with their feet resting over the edge of the table. We collected ultrasound images while the subjects pushed a wall without the ankle movement in the starting position. Each midpoint of the medial and lateral gastrocnemius was clearly marked on the skin with a surgical pen to confirm proper placement of the probe for repeated scans. A gel pad (Aquasonic 100; Parker Laboratories, Inc., NJ, USA) was used to avoid compression or deformation of the muscle. We used a real-time computerized ultrasound scanner (Sonoace X8; Samsung Medison, Seoul, South Korea) with a 7.5-MHz linear array transducer 4 cm long and 1 cm thick to evaluate pennation angle (θ) on the gastrocnemius. θ is angle of the fiber insertions into the superficial and deep aponeuroses. It was measured on the ultrasound scan using a scaled ruler and a protractor. We analyzed θs and θd. The θs was defined as the angle between muscle fibers and superficial aponeurosis, and the θd was expressed as the angle between muscle fibers and deep aponeurosis.
We measured the knee and ankle proprioception for passive-to-active angle reproduction. The knee and ankle joint angles were measured using an electronic dual inclinometer (Dualer IQ; JTECH Medical, Salt Lake City, UT, USA). We attached an electronic dual inclinometer to check the knee joint position sense (JPS) on the head of the fibula in line with the lateral malleolus and measured the ankle JPS on the sole of the foot using a very small medical strap. The subjects wore shorts with bare feet to eliminate cutaneous receptor input and were examined in the prone position to eliminate visual compensation. External auditory stimuli were limited to standardized commands by the examiner. For each trial, proprioceptive acuity was taken as the difference between the targeted angle and the reproduced angle in the ankle and knee joints, respectively. The test was completed in 3 trials, and we used the average value. To avoid any learning effect, the order of target angles was randomly applied for each subject.
The results are presented as the mean ± SD. We used the independent t-test to assess differences between groups and the paired t-test for differences between pretest and posttest within each group. All statistical analyses were conducted with IBM SPSS (version 20.0; IBM/SPSS, Inc., NY, USA). The differences were considered significant at p ≤ 0.05.
Lactate in Pre- and Post-EIMD Induction
Lactate increased significantly from 1.97 ± 0.82 to 9.14 ± 6.02 mmol·L−1 in the control group and from 1.99 ± 1.11 to 9.70 ± 5.56 mmol·L−1 in the experimental group (p ≤ 0.05). However, no significant difference was observed between the groups. These results show that EIMD was induced in both groups (Figure 1).
Change in Muscle Activation After Massage Treatment
The difference in the medial gastrocnemius muscle was 2.00 ± 1.47% in the control group and 2.93 ± 1.68% in the experimental group in the relaxed condition. The difference in the lateral gastrocnemius muscle was 2.02 ± 3.45% in the control group and 1.95 ± 1.60% in the experimental group. In the contracted condition, the difference in the medial gastrocnemius muscle was 39.59 ± 9.39% in the control group and 52.73 ± 20.25% in the experimental group (p ≤ 0.05). The difference in the lateral gastrocnemius muscle was 11.78 ± 8.78% in the control group and 10.63 ± 4.39% in the experimental group (Figure 2). These results demonstrate that massage on the gastrocnemius after EIMD increased activation of medial gastrocnemius under the contracted condition.
Change in Pennation Angle
The θs angle in the medial gastrocnemius muscle was 16.87 ± 5.13° in the control group and 19.87 ± 4.15° in the experimental group (p ≤ 0.05). The θd angle was 23.52 ± 6.21° in the control group and 24.35 ± 4.92° in the experimental group. The θs angle in the lateral gastrocnemius muscle was 9.80 ± 3.25° in the control group and 12.71 ± 2.79° in the experimental group (p ≤ 0.05). The θd angle was 19.19 ± 6.39° in the control group and 20.84 ± 3.46° in the experimental group (Figure 3). These results show that massage treatment on the gastrocnemius after EIMD changed the superficial layer in the gastrocnemius.
Change in Position Sense at the Ankle and Knee Joints
The difference before massage treatment was 6.06 ± 5.13° in the control group and 5.94 ± 4.82° in the experimental group in the ankle joint, and 7.56 ± 4.07° in the control group and 7.18 ± 2.25° in the experimental group in the knee joint. The difference after massage treatment was 5.11 ± 2.19° in the control group and 3.90 ± 1.45° in the experimental group in the ankle joint (p ≤ 0.05), and 6.83 ± 2.81° in the control group and 6.40 ± 3.17° in the experimental group in the knee joint (Figure 4). These results show that massage treatment on the gastrocnemius after EIMD increased proprioceptive acuity in the ankle joint. However, the changes in the knee joint were not significant.
Exercise-induced muscle damage may be the result of damage in the contractile components of muscle with subsequent release of certain biomarkers such as lactate, ammonia, and oxypurines. The concentration of the biomarker produced depends on the degree of fatigue or muscle damage (10,14). Of these, blood lactate concentration is a valuable tool in determining the intensity of exercise and is commonly accepted as a performance index (3). Elevated lactate has been reported during exercise with EIMD and has similarly been attributed to a shift to more glycolytic energy production (5,8). It has been suggested that damage to type II fibers would necessitate a greater recruitment of these fibers during exercise with EIMD to maintain the required force production (18). In this study, pre- and postexercise in all groups showed difference in lactate. We determined that our repeated exercise was sufficient to induce EIMD.
Muscular strength is an important factor to determine exercise capacity. However, muscle damage caused by repetitive intense activity does not maintain power in conditions requiring muscle contraction. Muscle fatigue reduces motor control ability (25). In the present results, we found that therapeutic massage on the gastrocnemius after EIMD affected muscular strength of the gastrocnemius. Jakeman et al. (21) showed that massage reduces the decline in muscle strength, consistent with our findings. However, Zainuddin et al. (36) reported no significant protective effect of massage against loss in muscle strength. They explained that massage is apparently not effective enough to increase blood flow to regenerate damaged tissue. However, a massage treatment should last at least 10 minutes per body part to be effective (29). The timing and duration of massage, massage type, and exercise damaging protocols seem to play an important part in determining effectiveness (6,21). Therefore, a difference in the duration and type of massage can show conflicting results on muscle activity. We suggest that our massage application to the gastrocnemius after EIMD was effective to restore muscular strength.
Muscular architecture is the most important factor for muscle function (4). It can identify condition of muscle fiber organization by checking parameters such as θ, fascicle length, and muscle thickness (26). Of these, increased θ indicates a condition to pack more contractile material along the tendon aponeurosis and shows an increase in sarcomeres in parallel (16,22). Matta et al. (27) reported that strength training program increases muscular thickness and θ on muscles of upper arm. They explained that the capacity to produce strength in skeletal muscles is affected by its architecture, in particular with respect to the number of muscle fibers in parallel (22,27). We found that massage application after EIMD increased θ in the superficial but not in the deep layer of the gastrocnemius. The timing and method of massage used in this experiment may have affected muscle fiber regeneration of the superficial layer of the gastrocnemius, and this change may have led to increase muscular strength in the superficial layer of gastrocnemius.
Proprioception is a specialized sensory modality that encompasses the sensations of joint motion and joint position. Joint position sense is necessary for normal muscle coordination and timing and plays an important role in joint stability (19,23). Although impairment of the gastrocnemius by repetitive exercise in this study attenuated JPS in the ankle and knee joints, respectively, massage of the gastrocnemius helped recover JPS in the ankle joint. Muscle damage or fatigue may result in insensitive JPS, such that can be connected to joint instability. Exercise-induced muscle damage is harmful to extrafusal fibers, and this damage affects muscle receptors particularly the intrafusal fibers of the muscle spindle and can extend a decrease in the JPS. The decrease of JPS in athletes can cause a decline in performance or a sports injury (35). Interestingly, we found that recovery of JPS appeared at the ankle joint and not at the knee joint. We measured proprioceptive acuity of the ankle joint in the knee flexion position. Activation of the gastrocnemius at pronounced knee flexion position decreases because of the force-length relationship. Reduced muscle activation can influence the accuracy of proprioception (1,34).
In this study, we found that the massage was effective to restore muscular strength and JPS after EIMD. The mechanical action of massage may promote a return to more normal muscle fiber alignment. The promotion of muscle fiber alignment afforded by massage facilitates recovery of muscle function, overcomes fatigue, and enhances performance (7,21). Mechanical pressure on the muscle is thought to increase or decrease neural excitability. These neural changes are believed to affect muscular tension, and the potential for spasms or pain (24). Massage is widely used as a therapeutic modality for recovery from muscle fatigue and injury. However, the effectiveness of massage remains controversial. Robertson et al. (33) reported that massage after fatiguing exercise has no clear beneficial effects. Zainuddin et al. (36) showed that massage is effective for alleviating delayed onset muscle soreness, and reducing swelling, but it has no effects on muscle function. Frey Law et al. (15) suggested that massage is capable of reducing myalgia symptoms. These controversial results are attributable to critical components of massage such as the therapist's intention, depth of pressure, speed of stroke, duration, and targeted muscle (21,31,33,36).
Our study also had limitations of study in that how much of exercise needed to muscle damage because it did not express numerically. Furthermore, although skilled physical therapist standardized massage methods, it is hard to maintain a constant pressure to experimental participants. Further studies will be needed to confirm effects of massage in various participants such as elders, patients with neuromuscular disease, or vestibular dysfunction.
The purpose of this study was to identify effects of massage application on gastrocnemius after EIMD. Massage treatment increased EMG activity in medial gastrocnemius and resulted in change of structure properties in superficial layer than deep layer of gastrocnemius. In addition, massage application after EIMD decreased the difference between the targeted angle and the reproduced angle in the ankle joint and not in the knee joint. In conclusion, these findings demonstrate that massage for EIMD can improve proprioceptive accuracy and muscle strength because of changes in the superficial layer of the gastrocnemius. Based on the present result, it suggests that massage can be used as a beneficial tool after EIMD.
1. Arampatzis A, Karamanidis K, Stafilidis S, Morey-Klapsing G, DeMonte G, Brüggemann GP. Effect of different ankle- and knee-joint positions on gastrocnemius
medialis fascicle length and EMG activity during isometric plantar flexion. J Biomech 39: 1891–1902, 2006.
2. Barrack RL, Lund PJ, Skinner HB. Knee joint proprioception revisited. J Sport Rehabil 3: 18–42, 1994.
3. Beneke R, Leithauser RM, Ochentel O. Blood lactate diagnostics in exercise
testing and training. Int J Sports Physiol Perform 6: 8–24, 2011.
4. Brancaccio P, Somma F, Provenzano F, Rastrelli L. Changes in muscular pennation angle after crenotherapy. Muscles Ligaments Tendons J 3: 112–115, 2013.
5. Braun WA, Dutto DJ. The effects of a single bout of downhill running and ensuing delayed onset of muscle soreness on running economy performed 48 h later. Eur J Appl Physiol 90: 29–34, 2003.
6. Butterfield TA, Zhao Y, Agarwal S, Haq F, Best TM. Cyclic compressive loading facilitates recovery after eccentric exercise
. Med Sci Sports Exerc 40: 1289–1296, 2008.
7. Cè E, Limonta E, Maggioni MA, Rampichini S, Veicsteinas A, Esposito F. Stretching and deep and superficial massage do not influence blood lactate levels after heavy-intensity cycle exercise
. J Sports Sci 31: 856–866, 2013.
8. Chen TC, Nosaka K, Tu JH. Changes in running economy following downhill running. J Sports Sci 25: 55–63, 2007.
9. Curtis D, Fallows S, Morris M, McMakin C. The efficacy of frequency specific microcurrent therapy on delayed onset muscle soreness. J Bodyw Mov Ther 14: 272–279, 2010.
10. Deschenes MR, Brewer RE, Bush JA, McCoy RW, Volek JS, Kraemer WJ. Neuromuscular disturbance outlasts other symptoms of exercise
-induced muscle damage. J Neurol Sci 174: 92–99, 2000.
11. Ernst E. Does post-exercise
massage treatment reduce delayed onset muscle soreness? A systematic review. Br J Sports Med 32: 212–214, 1998.
12. Eston R, Byrne C, Twist C. Muscle function after exercise
-induced muscle damage: Considerations for athletic performance in children and adults. J Exerc Sci Fit 1: 85–96, 2003.
13. Field T, Hernandez-Reif M, Diego M, Schanberg S, Kuhn C. Cortisol decreases and serotonin and dopamine increase following massage therapy. Int J Neurosci 115: 1397–1413, 2005.
14. Finsterer J. Biomarkers of peripheral muscle fatigue during exercise
. BMC Musculoskelet Disord 13: 218, 2012.
15. Frey Law LA, Evans S, Knudtson J, Nus S, Scholl K, Sluka KA. Massage reduces pain perception and hyperalgesia in experimental muscle pain: A randomized controlled trial. J Pain 9: 714–721, 2008.
16. Gans C. Fiber architecture and muscle function. Exerc Sport Sci Rev 10: 160–207, 1982.
17. Garsden LR, Bullock-Saxton JE. Joint reposition sense in subjects with unilateral osteoarthritis of the knee. Clin Rehabil 13: 148–155, 1999.
18. Gleeson M, Blannin AK, Walsh NP, Field CN, Pritchard JC. Effect of exercise
-induced muscle damage on the blood lactate response to incremental exercise
in humans. Eur J Appl Physiol Occup Physiol 77: 292–295, 1998.
19. Grigg P. Peripheral neural mechanisms in proprioception. J Sport Rehabil 3: 2–17, 1993.
20. Guilhem G, Hug F, Couturier A, Regnault S, Bournat L, Filliard JR, Dorel S. Effects of air-pulsed cryotherapy on neuromuscular recovery subsequent to exercise
-induced muscle damage. Am J Sports Med 41: 1942–1951, 2013.
21. Jakeman JR, Byrne C, Eston RG. Efficacy of lower limb compression and combined treatment of manual massage and lower limb compression on symptoms of exercise
-induced muscle damage in women. J Strength Cond Res 24: 3157–3165, 2010.
22. Kawakami Y, Abe T, Fukunaga T. Muscle-fiber pennation angle are greater in hypertrophied than in normal muscles. J Appl Physiol 74: 2740–2744, 1993.
23. Lee HM, Liau JJ, Cheng CK, Tan CM, Shih JT. Evaluation of shoulder proprioception following muscle fatigue. Clin Biomech 18: 843–847, 2003.
24. Lee HM, Wu SK, You JY. Quantitative application of transverse friction massage and its neurological effects on flexor carpi radialis. Man Ther 14: 501–507, 2009.
25. Lee WK, Oh SJ, Choi BK, Park HK. Effect of position sense in used taping and icing on muscle fatigue occurred on knee joint. J Korean Acad Clin Electrophysiol 5: 95–105, 2007.
26. Malas FÜ, Ozçakar L, Kaymak B, Ulaşli A, Güner S, Kara M, Akinci A. Effects of different strength training on muscle architecture: Clinical and ultrasonographic evaluation in knee osteoarthritis. PM R 5: 655–662, 2013.
27. Matta T, Simão R, de Salles BF, Spineti J, Oliveira LF. Strength training's chronic effects on muscle architecture parameters of different arm sites. J Strength Cond Res 25: 1711–1717, 2011.
28. Miller J, MacDermid JC. Interventions for relieving the symptoms of exercise
-induced muscle damage: A review. Clin J Sport Med 23: 327–328, 2013.
29. Moraska A. Sports massage. A comprehensive review. J Sports Med Phys Fitness 45: 370–380, 2005.
30. Nagai T, Sell TC, House AJ, Abt JP, Lephart SM. Knee proprioception and strength and landing kinematics during a single-leg stop-jump task. J Athl Train 48: 31–38, 2013.
31. Nelson N. Delayed onset muscle soreness: Is massage effective? J Bodyw Mov Ther 17: 475–482, 2013.
32. Proske U, Morgan DL. Muscle damage from eccentric exercise
: Mechanism, mechanical signs, adaptation and clinical application. J Physiol 537: 333–345, 2001.
33. Robertson A, Watt JM, Galloway SD. Effects of leg massage on recovery from high intensity cycling exercise
. Br J Sports Med 38: 173–176, 2004.
34. Sanchez-Ramirez DC, van der Leeden M, Knol DL, van der Esch M, Roorda LD, Verschueren S, van Dieën J, Lems WF, Dekker J. Association of postural control with muscle strength, proprioception, self-reported knee instability and activity limitations in patients with knee osteoarthritis. J Rehabil Med 45: 192–197, 2013.
35. Torres R, Ribeiro F, Alberto Duarte J, Cabri JM. Evidence of the physiotherapeutic interventions used currently after exercise
-induced muscle damage: Systematic review and meta-analysis. Phys Ther Sport 13: 101–114, 2012.
36. Zainuddin Z, Newton M, Sacco P, Nosaka K. Effects of massage on delayed-onset muscle soreness, swelling, and recovery of muscle function. J Athl Train 40: 174–180, 2005.