International Journal of Sports Physiology and Performance, 2014, 9, 985-992 http://dx.doi.org/10.1123/ijspp.2013-0512 © 2014 Human Kinetics, Inc.
www.IJSPP-Journal.com ORIGINAL INVESTIGATION
Effect of Whole-Body Periodic Acceleration on Exercise-Induced Muscle Damage After Eccentric Exercise Daniel H. Serravite, Arlette Perry, Kevin A. Jacobs, Jose A. Adams, Kysha Harriell, and Joseph F. Signorile Purpose: To examine the effects of whole-body periodic acceleration (pGz) on exercise-induced-muscle-damage (EIMD) -related symptoms induced by unaccustomed eccentric arm exercise. Methods: Seventeen active young men (23.4 ± 4.6 y) made 6 visits to the research facility over a 2-wk period. On day 1, subjects performed a 1-repetition-maximum (1RM) elbowflexion test and were randomly assigned to the pGz (n = 8) or control group (n = 9). Criterion measurements were taken on day 2, before and immediately after performance of the eccentric-exercise protocol (10 sets, 10 repetitions using 120% 1RM) and after the recovery period. During subsequent sessions (24, 48, 72, and 96 h) these data were collected before pGz or passive recovery. Measurements included isometric strength (maximal voluntary contraction [MVC]), blood markers (creatine kinase, myoglobin, IL-6, TNF-α, TBARS, PGF2α, protein carbonyls, uric acid, and nitrites), soreness, pain, circumference, and range of motion (ROM). Results: Significantly higher MVC values were seen for pGz throughout the recovery period. Within-group differences were seen in myoglobin, IL-6, IL-10, protein carbonyls, soreness, pain, circumference, and ROM showing small negative responses and rapid recovery for the pGz condition. Conclusion: Our results demonstrate that pGz can be an effective tool for the reduction of EIMD and may contribute to the training-adaptation cycle by speeding up the recovery of the body due to its performance-loss-lessening effect. Keywords: muscle damage, inflammatory markers, nitric oxide, recovery methods, calcium homeostasis Exercise-induced muscle damage (EIMD) is commonly experienced after bouts of unaccustomed eccentric, high-intensity, or long-duration exercise. These exercise protocols can also result in a delayed perception of skeletal-muscle discomfort or pain termed delayed-onset muscle soreness (DOMS).1 DOMS usually involves soreness, decreased strength, localized swelling, stiffness, and reduced range of motion (ROM). The level of DOMS after exercise varies with the intensity, volume, and type of activity.2 The decrement in muscle performance can parallel soreness patterns or be independent of soreness. Eccentric exercises are the preferred procedure for evoking DOMS, since they produce more damage than concentric or isometric contractions and greater strength reductions. This is especially true in sedentary individuals or novice athletes performing unaccustomed high-speed eccentric exercises using small muscles.3 A number of mechanisms have been advanced to explain DOMS, leading to varied interventions being employed to counteract it with varying degrees of success. These include ice-water immersion, stretching, anti-inflammatory drugs, ultrasound, transcutaneous electric nerve stimulation, massage, compression garments, acupuncture, hyperbaric oxygen therapy, oral antioxidants, and exercise.1,4,5 Whole-body vibration has been shown to reduce calf and gluteal pain and decrease inflammation after downhill running,6 and when combined with stretching, it decreased pain levels 22% to 61% compared with stretching alone.7 These positive effects have Serravite is with the Dept of Teaching and Learning, Florida International University, Miami, FL. Perry, Jacobs, Harriell, and Signorile are with the Dept of Kinesiology and Sport Sciences, University of Miami, Coral Gables, FL. Adams is with the Div of Pulmonary Disease, Mt Sinai Medical Center, Miami Beach, FL. Address author correspondence to Joseph Signorile at [email protected].
been attributed to enhanced local blood flow or potentiation of pain inhibition through increased proprioceptive feedback. These studies, however, did not measure performance recovery. Whole-body periodic acceleration (pGz) is a novel intervention that produces low-frequency, low-intensity alternating horizontal movements. Unlike whole-body vibration, pGz does not rely on the transmission of vibratory stimuli applied at the feet through the tissues of the body. Rather, the entire body, which is in contact with the moving platform, is subjected to a uniform level of acceleration. This intervention can increase nitric oxide (NO) release from vascular endothelium into the circulation through increased pulsatile shear stress, as evidenced by the addition of small pulses superimposed on the natural pulse rate.8 Increased NO release with pGz has been demonstrated in perfused porcine aorta preparations8 and in anesthetized swine using a NO electrode technique.9 In healthy and diseased humans10,11 pGz increases NO release into the circulation, as demonstrated by a downward descent of the dicrotic notch of the pulse, a specific effect of NO-mediated vasodilation.12 Since endothelial-derived NO has anti-inflammatory, antioxidant, and antinociceptive properties,13 the purpose of this study was to determine whether pGz could hasten the recovery from DOMS after strenuous eccentric elbow-flexion exercise by young volunteers.
Materials and Methods Subjects Twenty active young men with recreational lifting experience, enrolled in the university’s exercise physiology program, volunteered for this study, and 17 completed it; 3 were unwilling to comply with the limited physical activity requirements. Subjects’ characteristics are presented in Table 1. A power analysis performed 985
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using a study that used creatine kinase (CK) as the dependent variable after massage yielded a sample of 10 subjects to achieve statistical significance (F5,10 = 3.32, P = .05).3 Volunteers provided written consent before participation. The investigation was approved by the university’s institutional review board and conformed to the Declaration of Helsinki for Medical Research Involving Human Subjects. Individuals who reported participation in competitive sports in the prior 12 months; cardiovascular, endocrine, or neuromuscular disorders; orthopedic problems that would limit or be aggravated by isoinertial or isometric arm curls; or other chronic medical conditions that might affect performance were excluded from participation. In addition, subjects taking anti-inflammatory agents, nutritional supplements, or medications that could affect neuromuscular performance, including L-Arginine and citrullinemalate supplements, could not participate. Subjects were required to avoid formal physical activity such as strength or endurance training for 48 hours before the study began and throughout its duration. All subjects were unaccustomed to the exercise protocol used during this study.
to continue their normal eating habits but to refrain from using dietary supplements. Subjects were also instructed to abstain from exercise for 48 hours before and throughout the study. Criterion measurements including pain, anthropometry, ROM, soreness, blood markers, and isometric strength were assessed during pretest and posttest and 24, 48, 72, and 96 hours after the exercise protocol. On day 1, participants completed a health status questionnaire to confirm eligibility. On acceptance, they completed the International Physical Activity Questionnaire. A maximum 1-repetitionmaximum (1RM) strength test, performed using the National Strength and Conditioning Association protocol,14 was used to determine subjects’ maximum load for a concentric elbow flexion using their dominant arm. The day concluded with familiarizing the participants with the lifting and pGz protocols. On day 2, participants were randomly assigned to the control or pGz group. Criterion measurements were made before the exercise protocol and after pGz or passive recovery. Days 3 through 5 began with criterion measurements, followed by the treatment. During day 6, only the criterion measurements were made, without treatment.
Design
Methodology
Figure 1 presents the study protocol. Participants were randomly assigned to a control or pGz condition. For 2 weeks before data collection and during the protocol period, subjects were instructed
Exercise Protocol. After the criterion measurements on day 2, the
Table 1 Subjects’ Physical Characteristics, Mean ± SD Variable
Control (n = 8)
Whole-body periodic acceleration (n = 9)
Age (y)
24.3 ± 6.5
22.6 ± 2.3
Height (cm)
175.8 ± 5.4
176.2 ± 7.2
Mass (kg)
80.7 ± 14.0
77.8 ± 9.2
Body-mass index
26.1 ± 4.1
25.1 ± 3.2
1-repetition maximum (kg)
12.9 ± 1.6
14.1 ± 2.2
Note: No significant differences were detected for any variable between groups.
participants performed 10 sets of 10 lengthening contractions on a seated preacher-curl bench (Model 202, Precor Inc, Woodinville, WA) using a dumbbell loaded at 120% 1RM.15–17 The dumbbell was lowered from 75° to 180° at 5 s/repetition controlled by matching the sound of a metronome. When a participant had difficulty controlling the velocity, minimal spotting was provided. After each eccentric movement, there was a 2-second pause while the researcher lifted the dumbbell to the starting position to prepare for the next repetition. The exercise protocol was followed by 30 minutes of passive recovery and a 45-minute pGz or control bout (lying on a bed) depending on group assignment. The day concluded with posttest measurements.
Whole-Body Periodic Acceleration Protocol. The pGz motion platform and mattress were driven by a digitally controlled servomotor assembly (Exer-Rest, Non-Invasive Monitoring Systems, Inc, Miami, FL; Figure 2). The controller regulated
Figure 1 — Study design. Abbreviations: IPAQ, International Physical Activity Questionnaire; 1 RM, 1-repetition maximum; WBPA, whole-body periodic acceleration.
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Figure 2 — Subject during the whole-body periodic acceleration treatment using the Exer-Rest AT motion platform.
platform speed, travel distance, and treatment time. The participant lay supine on the mattress and was anchored via sandals to the footboard for stabilization purposes only, since the entire body and platform moved as a single unit. The platform moved in a 16-mm sinusoidal pattern at 140 times/min, applying approximately 0.22 g for the 45-minute pGz period.10,18 These settings have been shown to release NO into the circulation of healthy adults and patients with inflammatory diseases.19 Criterion Measurements . Each participant performed a
dominant-arm isometric maximal voluntary contraction with the elbow positioned at 90° (MVC90) and 150° (MVC150). Data were collected using a digital force gauge (Chatillon, DFS Series, Ametek, Largo, FL). The testing began with 2 warm-ups at 80% of perceived maximum and 1 MVC. The participant was then instructed to apply maximal force by pulling the force-gauge handle toward his body for 5 seconds. Strong verbal encouragement was provided. Three maximal contractions were performed with 2-minute recoveries between trials. Peak force was recorded for each trial, with the highest value considered the MVC. Approximately 20 mL of whole blood were collected from the antecubital vein via venipuncture pretest and immediately after the eccentric-exercise sequence and first day’s treatment (posttest) and at 24, 48, 72, and 96 hours. The 24-, 48-, 72-, and 96-hour samples were taken before the pGz or passive recoveries. Blood was collected into serum tubes and centrifuged for 15 minutes to obtain serum. Samples were stored at –80°C until analyzed for serum CK, myoglobin (MYO), IL-6, IL-10, TNF-α, TBARS, prostaglandin F2α (PGF2α), protein carbonyls, and uric acid using a microplate reader (Thermo Multiskan Spectrum, Vantaa, Finland) and for nitrites (only pretest and posttest) by tri-iodide-based reductive ozone chemiluminescence. Muscle soreness was evaluated using a 100-mm visual analog scale, where 0 mm indicated no pain at all and 100 mm indicated worst pain possible. Subjects were asked to draw a vertical line representing their current pain levels during 3 conditions: resting, after a palpation test, and during passive flexion and extension. With the subject seated and his exercised arm resting on a table, the investigator palpated the biceps brachii at and 3 cm above and below midbelly by applying firm pressure with the index and middle fingers. The participant then rated his soreness level as the researcher extended and flexed the subject’s relaxed elbow joint. The same investigator (K.H.) performed all soreness measurements.
Muscle pain was assessed using the Short-Form McGill Pain Questionnaire ,20 which contains 15 descriptors (11 sensory, 4 affective) rated on an intensity scale from 0 to 3 (0 = none, 1 = mild, 2 = moderate, and 3 = severe). Three pain scores were derived from the sum of the intensity values from words defined as sensory, affective, and total descriptors. Upper-arm circumference was assessed with the arm relaxed and hanging at the participant’s side according to the International Society of Advancement in Kynanthropometry21 using a constanttension tape. The measurement was taken midway between the superior and lateral border of the acromion process and the proximal and lateral border of the head of the radius. Passive elbow-joint ROM was evaluated via goniometer while the participant lay supine on an examination table. ROM was the difference between extended and flexed angles. The lateral epicondyle of the humerus, the proximal apex of the deltoid, and the styloid process of the radius were used as landmarks to measure elbow-joint angles. The participant’s arm was passively flexed and extended at a very low angular velocity.
Statistical Analysis Dependent variables (visual analog scale, pain, strength, ROM, circumference, CK, MYO, IL-6 and TNF-α, TBARS, PGF2α, protein carbonyls, uric acid) were compared using a series of 2 (pGz, control) × 6 (pretest, posttest, and 24, 48, 72, and 96 h after exercise) repeated-measures ANOVA. If significant main effects or interactions were found, least-significant-difference tests were used to determine the sources of these differences. In the case of nitrites, only pretest and posttest values were compared, as the latter were the only serum samples obtained posttest. One-way ANOVAs were used to analyze within-group differences. Analyses were performed using SPSS statistical software (version 17.0). Significance was set a priori at P < .05. Data presented in tables are means ± SD relative to preintervention values, while data in figures are means ± SE. Subjects who dropped out of the study were not included in the analyses unless 1 full trial was completed. If a subject did not remain inactive during the testing period his data were not included in the analysis. All instruments were calibrated before use. To increase intrarater and interrater reliability, every attempt was made to use the same examiner for each test, and a detailed examiner protocol with systematic instructions was provided and followed for each test. For isometric testing of the elbow flexors in our laboratory, an average ICC of .92 was calculated across testing sessions.
Results No significant differences were found between the pGz and controls for physical characteristics or for pretest criterion measures.
Muscle Strength Significant differences were seen between pGz and controls in MVC90 and MVC150 from posttest through 96 hours (P < .01). MVC90 values for pGz at 48, 72, and 96 hours were significantly higher than posttest (P = .01, P = .08, P = .02, respectively) and did not differ from the pretest value. For controls, MVC90 remained lower than pretest values across all 96 hours (P < .01). MVC150 for pGz was significantly higher than posttest (P = .03) and did not differ from the pretest value, while controls had significantly lower values than pretest from posttest through 96 hours (P < .01). The
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patterns of change in MVC90 and MVC150 for pGz and controls also differed across the 96-hour recovery; however, strength changes were consistent within groups (Figures 3 and 4). Both groups’ greatest strength decreases occurred immediately after exercise; however, pGz recovered to pretest levels by 48 hours postexercise, while controls’ values remained depressed throughout the 96-hour recovery.
Blood Measurements Creatine Kinase. As shown in Figure 5, control and pGz means for
CK were similar for pretest, posttest, 24 hours, and 48 hours. At 72 and 96 hours mean CK increased in controls but not in pGz. A mixed ANOVA was used to assess differences between groups across time points; however, the sphericity assumption was not met, χ2(14) = 84.24, P < .001. Therefore, we used the Huynh-Feldt correction to interpret the model in a manner that did not assume sphericity. For this correction, the observed power was .486, indicating that reaching significance at the .05 level would be difficult. Using the sphericity correction, a group × time interaction was detected that approached statistical significance (P = .074). This interaction explained 18.3% of the variance in CK. Although significance did not reach the a priori level of P = .05, the effect size (ηp2 = 0.183) and mean differences indicate that the effect is meaningful. Myoglobin. No significant differences between pGz and controls were seen in MYO concentration. Both pGz and controls peaked during the posttest and returned to pretest levels during the 4-day recovery (Figure 6). Nitrite Levels. Nitrite levels were measured pretest and posttest and showed no significant difference (Table 2).
Figure 3 — Maximal voluntary contraction (MVC) scores at 90° elbow angle for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. ‡Significant difference between groups (P < .01). *Significantly different from pretest (P = .01). **Significantly different from pretest (P = .05). †Significantly different from posttest (P = .01). ††Significantly different from posttest (P = .02). #Significantly different from posttest (P = .04). §Significantly different from 72 hours (P = .01). §§Significantly different from 72 hours (P = .04).
Figure 4 — Maximal voluntary contraction (MVC) scores at 150° elbow angle for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. ‡Significant difference between groups (P < .01). *Significantly different from pretest (P < .01). **Significantly different from pretest (P = .04). †Significantly different from posttest (P = .01). ††Significantly different from posttest (P = .02). §Significantly different from 24 hours (P = .02).
IL-6, IL-10, and TNF-a. There were no significant differences
between groups for cytokines (Table 2). When normalized to pretest values, however, IL-6 and IL-10 showed significant increases for pGz, posttest and at 48 hours, respectively (P < .05); however, controls showed no increase in normalized IL-6 and IL-10 at any time point. TBARS, PGF2a, Protein Carbonyls, and Uric Acid. For normalized values of TBARS, PGF2α, protein carbonyls, and uric acid, no significant differences were found between groups; however, controls showed increased protein carbonyls at 48 hours (P < .05; Table 2).
Figure 5 — Concentration of creatine phosphokinase normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE.
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Discussion
Muscle Soreness, McGill Pain Questionnaire, Circumference, and ROM. Ratings of muscle soreness, McGill pain scores,
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changes in upper-arm circumference, and ROM are shown in Figures 7 through 10. No significant differences were seen between groups for any variable.
Figure 6 — Concentration of myoglobin normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .02). †Significantly different from posttest (P < .01).
The purpose of this study was to examine the effectiveness of pGz as a recovery method to lessen the effects of EIMD after a bout of unaccustomed eccentric elbow-flexion exercise. The major finding was that pGz during recovery enhanced muscle performance and diminished the negative effects of EIMD in active young men. To our knowledge, this is the first study to show a more rapid strength recovery using a therapeutic intervention compared with passive recovery. In contrast, other interventions such as cryotherapy, active recovery, stretching, electrical stimulation, massage, nonsteroidal anti-inflammatory drugs, hyperbaric oxygen therapy, and acupuncture1,4,5,22 fail to produce positive impacts on strength during recovery from eccentric exercise. However, contrast water therapy (CWT) did enhance strength recovery at 24, 48, and 72 hours when compared with passive recovery.2,23 Differences existed in the damage protocol, muscle groups, and performance measures between the CWT investigation and the current study. Compared with the CWT protocol, a greater decrease in performance was seen immediately after the first treatment in controls and pGz, indicating a disparity in damage0protocol effectiveness. Although one CWT damage protocol used a similar intensity (120% 1RM),23 the other used a higher intensity (140% of 1RM).2 Less work was performed during the bilateral leg press used in the CWT studies than the unilateral arm curl used in our study. In addition, the improved strength recovery with CWT took 24 hours, while pGz produced improvements immediately after exposure that lasted throughout
Table 2 Blood Markers, Mean ± SD Marker
Group
Pretest
Posttest
24 h
48 h
72 h
96 h
IL-6
Control
1.14 ± 0.55
1.82 ± 1.14
1.14 ± 0.54
0.91 ± 0.30
1.53 ± 0.66†
0.73 ± 0.19
pGz
0.60 ± 0.35
1.06 ± 0.83*
1.34 ± 1.62
1.25 ± 1.03
1.01 ± 1.24
0.98 ± 0.76
Control
3.80 ± 1.40
3.85 ± 1.59
4.11 ± 2.44
4.69 ± 3.51
3.88 ± 2.01
3.88 ± 1.50
pGz
3.48 ± 1.12
3.44 ± 0.94
3.42 ± 1.12
3.88 ± 1.46§
4.74 ± 3.86
4.43 ± 3.13
Control
0.00 ± 0.00
0.02 ± 0.04
0.00 ± 0.00
0.03 ± 0.07
0.00 ± 0.00
0.00 ± 0.00
pGz
0.00 ± 0.00
0.15 ± 0.29
0.09 ± 0.26
0.25 ± 0.51
0.00 ± 0.00
0.44 ± 1.24
Control
0.02 ± 0.01
0.02 ± 0.00
pGz
0.02 ± 0.01
0.04 ± 0.07
Control
31.74 ± 29.41
27.09 ± 29.02
30.45 ± 24.75
24.50 ± 24.90
30.89 ± 39.0
26.54 ± 27.64
pGz
30.26 ± 16.53
30.87 ± 17.70
36.15 ± 18.25
30.35 ± 24.78
25.95 ± 16.66
25.48 ± 16.01
Control
41.02 ± 31.00
54.45 ± 45.50
39.34 ± 19.70
30.67 ± 13.94
41.75 ± 29.53
30.38 ± 8.85
pGz
28.65 ± 14.74
22.21 ± 16.89
26.15 ± 15.43
26.57 ± 9.44
25.89 ± 16.79
35.27 ± 24.53
Control
1.53 ± 0.34
1.72 ± 0.67
1.54 ± 0.42
1.80 ± 0.52††
1.56 ± 0.32
1.61 ± 0.36
pGz
1.53 ± 0.34
1.72 ± 0.67
1.54 ± 0.42
1.80 ± 0.52
1.56 ± 0.32
1.61 ± 0.36
Control
8.92 ± 1.68
9.35 ± 2.48
9.22 ± 1.79
9.25 ± 1.61
9.39 ± 2.12
9.97 ± 2.45
pGz
9.53 ± 1.24
9.24 ± 1.44
9.31 ± 1.54
9.63 ± 1.60
9.31 ± 1.53
9.29 ± 1.37
IL-10
TNF-α
Nitrite
TBARS
PGF2α
Carbonyls
Uric acid
Abbreviations: pGz, whole-body periodic acceleration. Control n = 7, pGz n = 9. †Significantly different from 96 h (P = .03). *Significantly different from pretest (P = .02). §Significantly different from pretest (P = .04). ††Significantly different from pretest (P < .01).
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990 Serravite et al
Figure 7 — Muscle soreness using the visual analog scale for the wholebody periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P < .01). §Significantly different from 72 hours (P = .05). †Significantly different from 96 hours (P = .01). ††Significantly different from 96 hours (P = .03). #Significantly different from 96 hours (P = .03).
Figure 8 — Pain questionnaire score for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .01). **Significantly different from pretest (P < .02). §Significantly different from 72 hours (P = .02). †Significantly different from 96 hours (P = .01). ††Significantly different from 96 hours (P = .03).
the 96-hour evaluation period. As a caveat, our posttest measurements were taken after subjects performed the recovery intervention, which does not guarantee equal levels of muscle damage for pGz and controls. The mechanisms that may have contributed to improved strength during recovery when applying pGz are unclear. If reduced structural damage is responsible for improved force production with pGz, the impact of NO on calcium homeostasis and oxidative stress should be considered. Lopez et al24 recently found that in mice, pGz accelerated recovery of intramuscular Ca2+ levels after increases seen after an acute bout of downhill running. However,
Figure 9 — Circumference of the upper arm normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .01). **Significantly different from pretest (P = .03). †Significantly different from posttest (P < .05).
Figure 10 — Range of motion of the elbow joint normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .01). **Significantly different from pretest (P = .02). #Significantly different from pretest (P = .04). †Significantly different from posttest (P = .05). §Significantly different from 96 hours (P = .02).
the contributions of this mechanism to the improved performance in our study remain in question, since no significant differences in serum nitrite levels were seen between pGz and controls. Several factors may have affected our measurement of nitrite levels, including subjects’ nutritional status and oxidative-stress levels.25 The attenuated CK response for pGz toward the end of the recovery period, along with improved strength recovery, may indicate reduced levels of muscle damage with pGz; however, CK is not a direct measure of the degree of muscle damage due to the large variability in its response in similarly exercised individuals.26 While some recovery studies have shown CK peaking within the first 24 hours after exercise, others confirmed that the highest CK
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concentration occurs 4 to 5 days after exercise.27 In addition, patterns of change in CK have differed with differing recovery methods. MYO is also used to measure muscle damage. Although we found no significant between-groups differences in MYO, its earlier peak compared with CK agrees with previous studies.23 In addition, the increased MYO levels at 72 and 96 hours postexercise reflect the results reported by Howatson et al,28 using ice massage. The differences in the time course of the appearance of MYO and CK can be explained by MYO’s smaller size and more direct delivery route into the blood.29 Unlike MYO, CK, due to its larger molecular size, is delivered into the bloodstream via the lymphatic system, delaying its appearance after acute muscle damage. Our current findings, showing significant within-group increases in IL-6 by the pGz group during the posttest assessment, have not been previously reported; however, the peaking of IL-6 immediately after exercise and its return to near pretest values within 24 hours have been reported previously after an acute exercise bout.30 Although IL-6 is expected to increase with exercise, the lack of response in our controls is not without precedent.31 Increased IL-6 can be considered a positive response, since it is proposed to stimulate anti-inflammatory cytokine production and may indirectly inhibit proinflammatory cytokines.32 The anti-inflammatory environment induced by IL-6 may have contributed to IL-10 increases with pGz, since IL-6, independent of TNF-α, can enhance IL-1ra and IL-10 levels.33 Moreover, IL-6 increases satellite-cell proliferation and muscle regeneration.34 The lack of significant differences in systemic TNF-α in our study reflects findings of other researchers who examined inflammatory markers after acute exercise and IL-6 infusion,32 reflecting the fact that TNF-α is more important later in muscle recovery. Previous studies that examined acute muscle-damaging exercise in humans have reported that eccentric contractions induce greater oxidative stress than concentric contraction.35 Although oxidativestress indices such as TBARS, protein carbonyls and uric acid may be elevated several days after eccentric exercise, we only found significant increases in protein carbonyls, which are markers of protein oxidation, for controls 72 hours after our eccentric-exercise bout. Although no significant differences in soreness, pain, circumference, or ROM were seen between groups, the shorter durations of soreness and pain responses, lack of significant circumference increases, and rapid recovery of ROM for pGz over controls demonstrate an enhanced recovery pattern in this group. The positive impact of pGz on pain is not without precedent; in a comparable study with fibromyalgia patients, 45 minutes of pGz produced significant reductions in pain within 1 to 3 treatments.11 A limitation of this study was our failure to quantify the effects of the damage protocol immediately after its administration or to measure leukocytes during the recovery period. However, the quantification of cytokines provided a reliable indicator of inflammation. In addition, the quantification of glutathione could further help explain changes in some criterion measurement, since subjects with low total plasma glutathione levels display lower plasma CK and MYO responses and faster recovery from eccentric exercise than subjects with higher levels.26 Moreover, failure to control hydration levels during recovery may have affected lymph flow and therefore affected CK levels after exercise.36 Finally, controlling diet during the recovery period may have also provided a more stable testing environment, although the impacts of nutrition on DOMS and inflammation are equivocal.37 The use of pGz after high-intensity eccentric exercise improved strength recovery and positively affected EIMD symptoms. These
benefits may be the result of enhanced NO release; however, our results using nitrite levels as a marker of NO release cannot support this contention. Future research should investigate the effects of pGz in skeletal muscle through quantification of inflammatory and oxidative-stress markers, as well as ultrastructural damage using electron microscopy. In addition, the impact of pGz on EIMDmediated disruptions in excitation–contraction coupling should be investigated in humans. Finally, using pGz for preconditioning to reduce levels of DOMS and improve muscle performance should be investigated.
Practical Applications Exercise induces positive adaptations ranging from improved health to enhanced performance when appropriate stress and recovery patterns are applied. Although several methods are available to help the body recover after unaccustomed exercise resulting in EIMD, no single method can be identified as the gold standard. pGz may improve the training-adaptation cycle by speeding up the body’s recovery as it reduces performance losses generally experienced with EIMD.
Conclusions By accelerating the recovery of neuromuscular performance, pGz may benefit recreational athletes who seldom employ adequate recovery periods after exercising or high-performance athletes who need to increase their training load to achieve maximum performance. Acknowledgments The authors would like to thank Tom E. Abdenour, head trainer for the Golden State Warriors Basketball Team of the National Basketball Association, for the suggestion to undertake this investigation. We would also like to thank the students who helped with the data collection. A special thanks to Dr Randall Penfield and Corrine Huggins of the Dunspaugh-Dalton Community & Educational Well-Being Research Center at the University of Miami School of Education for their help with the statistical analyses and Cameron Dezfulian and Laura Quirola for their extensive help with data collection and interpretation.
References 1. Gulick DT, Kimura IF, Sitler M, Paolone A, Kelly JD. Various treatment techniques on signs and symptoms of delayed onset muscle soreness. J Athl Train. 1996;31(2):145–152. PubMed 2. Vaile JM, Gill ND, Blazevich AJ. The effect of contrast water therapy on symptoms of delayed onset muscle soreness. J Strength Cond Res. 2007;21(3):697–702. PubMed 3. Chapman D, Newton M, Sacco P, Nosaka K. Greater muscle damage induced by fast versus slow velocity eccentric exercise. Int J Sports Med. 2006;27(8):591–598. PubMed doi:10.1055/s-2005-865920 4. Hübscher M, Vogt L, Bernhorster M, Rosenhagen A, Banzer W. Effects of acupuncture on symptoms and muscle function in delayed-onset muscle soreness. J Altern Complement Med. 2008;14(8):1011–1016. PubMed doi:10.1089/acm.2008.0173 5. Mekjavic IB, Exner JA, Tesch PA, Eiken O. Hyperbaric oxygen therapy does not affect recovery from delayed onset muscle soreness. Med Sci Sports Exerc. 2000;32(3):558–563. PubMed doi:10.1097/00005768200003000-00002
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992 Serravite et al 6. Broadbent S, Rousseau JJ, Thorp RM, Choate SL, Jackson FS, Rowlands DS. Vibration therapy reduces plasma IL-6 and muscle soreness after downhill running. Br J Sports Med. 2010;44(12):888–894. PubMed doi:10.1136/bjsm.2008.052100 7. Rhea MR, Bunker D, Marin PJ, Lunt K. Effect of iTonic wholebody vibration on delayed-onset muscle soreness among untrained individuals. J Strength Cond Res. 2009;23(6):1677–1682. PubMed doi:10.1519/JSC.0b013e3181b3f6cd 8. Adams JA, Moore JE, Jr, Moreno MR, Coelho J, Bassuk J, Wu D. Effects of periodic body acceleration on the in vivo vasoactive response to N-omega-nitro-L-arginine and the in vitro nitric oxide production. Ann Biomed Eng. 2003;31(11):1337–1346. PubMed doi:10.1114/1.1623486 9. Adams JA, Bassuk J, Wu D, Grana M, Kurlansky P, Sackner MA. Periodic acceleration: effects on vasoactive, fibrinolytic, and coagulation factors. J Appl Physiol. 2005;98(3):1083–1090. PubMed doi:10.1152/ japplphysiol.00662.2004 10. Sackner MA, Gummels E, Adams JA. Nitric oxide is released into circulation with whole-body, periodic acceleration. Chest. 2005;127(1):30–39. PubMed doi:10.1378/chest.127.1.30 11. Sackner MA, Gummels EM, Adams JA. Say NO to fibromyalgia and chronic fatigue syndrome: an alternative and complementary therapy to aerobic exercise. Med Hypotheses. 2004;63(1):118–123. PubMed doi:10.1016/j.mehy.2004.01.025 12. Nier BA, Harrington LS, Carrier MJ, Weinberg PD. Evidence for a specific influence of the nitrergic pathway on the peripheral pulse waveform in rabbits. Exp Physiol. 2008;93(4):503–512. PubMed doi:10.1113/expphysiol.2007.041129 13. Abraham WM, Ahmed A, Serebriakov I, et al. Whole-body periodic acceleration modifies experimental asthma in sheep. Am J Respir Crit Care Med. 2006;174(7):743–752. PubMed doi:10.1164/rccm.200601048OC 14. National Strength & Conditioning Association. Baechle TR, Earle RW, eds. Essentials of Strength Training and Conditioning. 3rd ed. Champaign, IL: Human Kinetics; 2008. 15. Wojcik JR, Walber-Rankin J, Smith LL, Gwazdauskas FC. Comparison of carbohydrate and milk-based beverages on muscle damage and glycogen following exercise. Int J Sport Nutr Exerc Metab. 2001;11(4):406–419. PubMed 16. Jackman SR, Witard OC, Jeukendrup AE, Tipton KD. Branched-chain amino acid ingestion can ameliorate soreness from eccentric exercise. Med Sci Sports Exerc. 2010;42(5):962–970. PubMed doi:10.1249/ MSS.0b013e3181c1b798 17. Burd NA, Dickinson JM, Lemoine JK, et al. Effect of a cyclooxygenase-2 inhibitor on postexercise muscle protein synthesis in humans. Am J Physiol Endocrinol Metab. 2010;298(2):E354–E361. PubMed doi:10.1152/ajpendo.00423.2009 18. Fukuda S, Shimada K, Kawasaki T, et al. “Passive exercise” using whole body periodic acceleration: effects on coronary microcirculation. Am Heart J. 2010;159(4):620–626. PubMed doi:10.1016/j. ahj.2009.12.034 19. Sackner MA, Gummels E, Adams JA. Effect of moderate-intensity exercise, whole-body periodic acceleration, and passive cycling on nitric oxide release into circulation. Chest. 2005;128(4):2794–2803. PubMed doi:10.1378/chest.128.4.2794 20. Melzack R. The Short-Form McGill Pain Questionnaire. Pain. 1987;30(2):191–197. PubMed doi:10.1016/0304-3959(87)91074-8 21. Stewart A, Marfell-Jones M, Olds T, de Ridder H. International Standards for Anthropometric Assessment. Lower Hutt, New Zealand: International Society for the Advancement of Kinanthropometry; 2011.
22. Martin V, Millet GY, Lattier G, Perrod L. Effects of recovery modes after knee extensor muscles eccentric contractions. Med Sci Sports Exerc. 2004;36(11):1907–1915. PubMed doi:10.1249/01. MSS.0000145526.43208.08 23. Vaile J, Halson S, Gill N, Dawson B. Effect of hydrotherapy on the signs and symptoms of delayed onset muscle soreness. Eur J Appl Physiol. 2008;102(4):447–455. PubMed doi:10.1007/s00421-0070605-6 24. Lopez JR, Mosquera J, Mijares A, Allen PD. Eccentric exercise elicits elevation of resting calcium in skeletal muscle: periodic acceleration enhanced the recovery. Biophys J. 2012;102(3):510a–511a. doi:10.1016/j.bpj.2011.11.2796 25. Dreissigacker U, Wendt M, Wittke T, Tsikas D, Maassen N. Positive correlation between plasma nitrite and performance during highintensive exercise but not oxidative stress in healthy men. Nitric Oxide. 2010;23(2):128–135. PubMed doi:10.1016/j.niox.2010.05.003 26. Lee J, Clarkson PM. Plasma creatine kinase activity and glutathione after eccentric exercise. Med Sci Sports Exerc. 2003;35(6):930–936. PubMed doi:10.1249/01.MSS.0000069553.47739.36 27. Smith LL, Keating MN, Holbert D, et al. The effects of athletic massage on delayed onset muscle soreness, creatine kinase, and neutrophil count: a preliminary report. J Orthop Sports Phys Ther. 1994;19(2):93–99. PubMed doi:10.2519/jospt.1994.19.2.93 28. Howatson G, Gaze D, van Someren KA. The efficacy of ice massage in the treatment of exercise-induced muscle damage. Scand J Med Sci Sports. 2005;15(6):416–422. PubMed doi:10.1111/j.16000838.2005.00437.x 29. Sayers SP, Clarkson PM. Short-term immobilization after eccentric exercise, part II: creatine kinase and myoglobin. Med Sci Sports Exerc. 2003;35(5):762–768. PubMed doi:10.1249/01. MSS.0000064933.43824.ED 30. Ispirlidis I, Fatouros IG, Jamurtas AZ, et al. Time-course of changes in inflammatory and performance responses following a soccer game. Clin J Sport Med. 2008;18(5):423–431. PubMed doi:10.1097/ JSM.0b013e3181818e0b 31. Hirose L, Nosaka K, Newton M, et al. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc Immunol Rev. 2004;10:75–90. PubMed 32. Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J. 2003;17(8):884–886. PubMed 33. Steensberg A, Keller C, Hillig T, et al. Nitric oxide production is a proximal signaling event controlling exercise-induced mRNA expression in human skeletal muscle. FASEB J. 2007;21(11):2683–2694. PubMed doi:10.1096/fj.06-7477com 34. Filippin LI, Moreira AJ, Marroni NP, Xavier RM. Nitric oxide and repair of skeletal muscle injury. Nitric Oxide. 2009;21(3-4):157–163. PubMed doi:10.1016/j.niox.2009.08.002 35. Kon M, Tanabe K, Lee H, Kimura F, Akimoto T, Kono I. Eccentric muscle contractions induce greater oxidative stress than concentric contractions in skeletal muscle. Appl Physiol Nutr Metab. 2007;32(2):273–281. PubMed doi:10.1139/H06-115 36. Sayers SP, Peters BT, Knight CA, Urso ML, Parkington J, Clarkson PM. Short-term immobilization after eccentric exercise, part I: contractile properties. Med Sci Sports Exerc. 2003;35(5):753–761. PubMed doi:10.1249/01.MSS.0000064932.55998.CC 37. Miles MP, Pearson SD, Andring JM, Kidd JR, Volpe SL. Effect of carbohydrate intake during recovery from eccentric exercise on interleukin-6 and muscle-damage markers. Int J Sport Nutr Exerc Metab. 2007;17(6):507–520. PubMed
www.IJSPP-Journal.com ORIGINAL INVESTIGATION
Effect of Whole-Body Periodic Acceleration on Exercise-Induced Muscle Damage After Eccentric Exercise Daniel H. Serravite, Arlette Perry, Kevin A. Jacobs, Jose A. Adams, Kysha Harriell, and Joseph F. Signorile Purpose: To examine the effects of whole-body periodic acceleration (pGz) on exercise-induced-muscle-damage (EIMD) -related symptoms induced by unaccustomed eccentric arm exercise. Methods: Seventeen active young men (23.4 ± 4.6 y) made 6 visits to the research facility over a 2-wk period. On day 1, subjects performed a 1-repetition-maximum (1RM) elbowflexion test and were randomly assigned to the pGz (n = 8) or control group (n = 9). Criterion measurements were taken on day 2, before and immediately after performance of the eccentric-exercise protocol (10 sets, 10 repetitions using 120% 1RM) and after the recovery period. During subsequent sessions (24, 48, 72, and 96 h) these data were collected before pGz or passive recovery. Measurements included isometric strength (maximal voluntary contraction [MVC]), blood markers (creatine kinase, myoglobin, IL-6, TNF-α, TBARS, PGF2α, protein carbonyls, uric acid, and nitrites), soreness, pain, circumference, and range of motion (ROM). Results: Significantly higher MVC values were seen for pGz throughout the recovery period. Within-group differences were seen in myoglobin, IL-6, IL-10, protein carbonyls, soreness, pain, circumference, and ROM showing small negative responses and rapid recovery for the pGz condition. Conclusion: Our results demonstrate that pGz can be an effective tool for the reduction of EIMD and may contribute to the training-adaptation cycle by speeding up the recovery of the body due to its performance-loss-lessening effect. Keywords: muscle damage, inflammatory markers, nitric oxide, recovery methods, calcium homeostasis Exercise-induced muscle damage (EIMD) is commonly experienced after bouts of unaccustomed eccentric, high-intensity, or long-duration exercise. These exercise protocols can also result in a delayed perception of skeletal-muscle discomfort or pain termed delayed-onset muscle soreness (DOMS).1 DOMS usually involves soreness, decreased strength, localized swelling, stiffness, and reduced range of motion (ROM). The level of DOMS after exercise varies with the intensity, volume, and type of activity.2 The decrement in muscle performance can parallel soreness patterns or be independent of soreness. Eccentric exercises are the preferred procedure for evoking DOMS, since they produce more damage than concentric or isometric contractions and greater strength reductions. This is especially true in sedentary individuals or novice athletes performing unaccustomed high-speed eccentric exercises using small muscles.3 A number of mechanisms have been advanced to explain DOMS, leading to varied interventions being employed to counteract it with varying degrees of success. These include ice-water immersion, stretching, anti-inflammatory drugs, ultrasound, transcutaneous electric nerve stimulation, massage, compression garments, acupuncture, hyperbaric oxygen therapy, oral antioxidants, and exercise.1,4,5 Whole-body vibration has been shown to reduce calf and gluteal pain and decrease inflammation after downhill running,6 and when combined with stretching, it decreased pain levels 22% to 61% compared with stretching alone.7 These positive effects have Serravite is with the Dept of Teaching and Learning, Florida International University, Miami, FL. Perry, Jacobs, Harriell, and Signorile are with the Dept of Kinesiology and Sport Sciences, University of Miami, Coral Gables, FL. Adams is with the Div of Pulmonary Disease, Mt Sinai Medical Center, Miami Beach, FL. Address author correspondence to Joseph Signorile at [email protected].
been attributed to enhanced local blood flow or potentiation of pain inhibition through increased proprioceptive feedback. These studies, however, did not measure performance recovery. Whole-body periodic acceleration (pGz) is a novel intervention that produces low-frequency, low-intensity alternating horizontal movements. Unlike whole-body vibration, pGz does not rely on the transmission of vibratory stimuli applied at the feet through the tissues of the body. Rather, the entire body, which is in contact with the moving platform, is subjected to a uniform level of acceleration. This intervention can increase nitric oxide (NO) release from vascular endothelium into the circulation through increased pulsatile shear stress, as evidenced by the addition of small pulses superimposed on the natural pulse rate.8 Increased NO release with pGz has been demonstrated in perfused porcine aorta preparations8 and in anesthetized swine using a NO electrode technique.9 In healthy and diseased humans10,11 pGz increases NO release into the circulation, as demonstrated by a downward descent of the dicrotic notch of the pulse, a specific effect of NO-mediated vasodilation.12 Since endothelial-derived NO has anti-inflammatory, antioxidant, and antinociceptive properties,13 the purpose of this study was to determine whether pGz could hasten the recovery from DOMS after strenuous eccentric elbow-flexion exercise by young volunteers.
Materials and Methods Subjects Twenty active young men with recreational lifting experience, enrolled in the university’s exercise physiology program, volunteered for this study, and 17 completed it; 3 were unwilling to comply with the limited physical activity requirements. Subjects’ characteristics are presented in Table 1. A power analysis performed 985
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986 Serravite et al
using a study that used creatine kinase (CK) as the dependent variable after massage yielded a sample of 10 subjects to achieve statistical significance (F5,10 = 3.32, P = .05).3 Volunteers provided written consent before participation. The investigation was approved by the university’s institutional review board and conformed to the Declaration of Helsinki for Medical Research Involving Human Subjects. Individuals who reported participation in competitive sports in the prior 12 months; cardiovascular, endocrine, or neuromuscular disorders; orthopedic problems that would limit or be aggravated by isoinertial or isometric arm curls; or other chronic medical conditions that might affect performance were excluded from participation. In addition, subjects taking anti-inflammatory agents, nutritional supplements, or medications that could affect neuromuscular performance, including L-Arginine and citrullinemalate supplements, could not participate. Subjects were required to avoid formal physical activity such as strength or endurance training for 48 hours before the study began and throughout its duration. All subjects were unaccustomed to the exercise protocol used during this study.
to continue their normal eating habits but to refrain from using dietary supplements. Subjects were also instructed to abstain from exercise for 48 hours before and throughout the study. Criterion measurements including pain, anthropometry, ROM, soreness, blood markers, and isometric strength were assessed during pretest and posttest and 24, 48, 72, and 96 hours after the exercise protocol. On day 1, participants completed a health status questionnaire to confirm eligibility. On acceptance, they completed the International Physical Activity Questionnaire. A maximum 1-repetitionmaximum (1RM) strength test, performed using the National Strength and Conditioning Association protocol,14 was used to determine subjects’ maximum load for a concentric elbow flexion using their dominant arm. The day concluded with familiarizing the participants with the lifting and pGz protocols. On day 2, participants were randomly assigned to the control or pGz group. Criterion measurements were made before the exercise protocol and after pGz or passive recovery. Days 3 through 5 began with criterion measurements, followed by the treatment. During day 6, only the criterion measurements were made, without treatment.
Design
Methodology
Figure 1 presents the study protocol. Participants were randomly assigned to a control or pGz condition. For 2 weeks before data collection and during the protocol period, subjects were instructed
Exercise Protocol. After the criterion measurements on day 2, the
Table 1 Subjects’ Physical Characteristics, Mean ± SD Variable
Control (n = 8)
Whole-body periodic acceleration (n = 9)
Age (y)
24.3 ± 6.5
22.6 ± 2.3
Height (cm)
175.8 ± 5.4
176.2 ± 7.2
Mass (kg)
80.7 ± 14.0
77.8 ± 9.2
Body-mass index
26.1 ± 4.1
25.1 ± 3.2
1-repetition maximum (kg)
12.9 ± 1.6
14.1 ± 2.2
Note: No significant differences were detected for any variable between groups.
participants performed 10 sets of 10 lengthening contractions on a seated preacher-curl bench (Model 202, Precor Inc, Woodinville, WA) using a dumbbell loaded at 120% 1RM.15–17 The dumbbell was lowered from 75° to 180° at 5 s/repetition controlled by matching the sound of a metronome. When a participant had difficulty controlling the velocity, minimal spotting was provided. After each eccentric movement, there was a 2-second pause while the researcher lifted the dumbbell to the starting position to prepare for the next repetition. The exercise protocol was followed by 30 minutes of passive recovery and a 45-minute pGz or control bout (lying on a bed) depending on group assignment. The day concluded with posttest measurements.
Whole-Body Periodic Acceleration Protocol. The pGz motion platform and mattress were driven by a digitally controlled servomotor assembly (Exer-Rest, Non-Invasive Monitoring Systems, Inc, Miami, FL; Figure 2). The controller regulated
Figure 1 — Study design. Abbreviations: IPAQ, International Physical Activity Questionnaire; 1 RM, 1-repetition maximum; WBPA, whole-body periodic acceleration.
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Figure 2 — Subject during the whole-body periodic acceleration treatment using the Exer-Rest AT motion platform.
platform speed, travel distance, and treatment time. The participant lay supine on the mattress and was anchored via sandals to the footboard for stabilization purposes only, since the entire body and platform moved as a single unit. The platform moved in a 16-mm sinusoidal pattern at 140 times/min, applying approximately 0.22 g for the 45-minute pGz period.10,18 These settings have been shown to release NO into the circulation of healthy adults and patients with inflammatory diseases.19 Criterion Measurements . Each participant performed a
dominant-arm isometric maximal voluntary contraction with the elbow positioned at 90° (MVC90) and 150° (MVC150). Data were collected using a digital force gauge (Chatillon, DFS Series, Ametek, Largo, FL). The testing began with 2 warm-ups at 80% of perceived maximum and 1 MVC. The participant was then instructed to apply maximal force by pulling the force-gauge handle toward his body for 5 seconds. Strong verbal encouragement was provided. Three maximal contractions were performed with 2-minute recoveries between trials. Peak force was recorded for each trial, with the highest value considered the MVC. Approximately 20 mL of whole blood were collected from the antecubital vein via venipuncture pretest and immediately after the eccentric-exercise sequence and first day’s treatment (posttest) and at 24, 48, 72, and 96 hours. The 24-, 48-, 72-, and 96-hour samples were taken before the pGz or passive recoveries. Blood was collected into serum tubes and centrifuged for 15 minutes to obtain serum. Samples were stored at –80°C until analyzed for serum CK, myoglobin (MYO), IL-6, IL-10, TNF-α, TBARS, prostaglandin F2α (PGF2α), protein carbonyls, and uric acid using a microplate reader (Thermo Multiskan Spectrum, Vantaa, Finland) and for nitrites (only pretest and posttest) by tri-iodide-based reductive ozone chemiluminescence. Muscle soreness was evaluated using a 100-mm visual analog scale, where 0 mm indicated no pain at all and 100 mm indicated worst pain possible. Subjects were asked to draw a vertical line representing their current pain levels during 3 conditions: resting, after a palpation test, and during passive flexion and extension. With the subject seated and his exercised arm resting on a table, the investigator palpated the biceps brachii at and 3 cm above and below midbelly by applying firm pressure with the index and middle fingers. The participant then rated his soreness level as the researcher extended and flexed the subject’s relaxed elbow joint. The same investigator (K.H.) performed all soreness measurements.
Muscle pain was assessed using the Short-Form McGill Pain Questionnaire ,20 which contains 15 descriptors (11 sensory, 4 affective) rated on an intensity scale from 0 to 3 (0 = none, 1 = mild, 2 = moderate, and 3 = severe). Three pain scores were derived from the sum of the intensity values from words defined as sensory, affective, and total descriptors. Upper-arm circumference was assessed with the arm relaxed and hanging at the participant’s side according to the International Society of Advancement in Kynanthropometry21 using a constanttension tape. The measurement was taken midway between the superior and lateral border of the acromion process and the proximal and lateral border of the head of the radius. Passive elbow-joint ROM was evaluated via goniometer while the participant lay supine on an examination table. ROM was the difference between extended and flexed angles. The lateral epicondyle of the humerus, the proximal apex of the deltoid, and the styloid process of the radius were used as landmarks to measure elbow-joint angles. The participant’s arm was passively flexed and extended at a very low angular velocity.
Statistical Analysis Dependent variables (visual analog scale, pain, strength, ROM, circumference, CK, MYO, IL-6 and TNF-α, TBARS, PGF2α, protein carbonyls, uric acid) were compared using a series of 2 (pGz, control) × 6 (pretest, posttest, and 24, 48, 72, and 96 h after exercise) repeated-measures ANOVA. If significant main effects or interactions were found, least-significant-difference tests were used to determine the sources of these differences. In the case of nitrites, only pretest and posttest values were compared, as the latter were the only serum samples obtained posttest. One-way ANOVAs were used to analyze within-group differences. Analyses were performed using SPSS statistical software (version 17.0). Significance was set a priori at P < .05. Data presented in tables are means ± SD relative to preintervention values, while data in figures are means ± SE. Subjects who dropped out of the study were not included in the analyses unless 1 full trial was completed. If a subject did not remain inactive during the testing period his data were not included in the analysis. All instruments were calibrated before use. To increase intrarater and interrater reliability, every attempt was made to use the same examiner for each test, and a detailed examiner protocol with systematic instructions was provided and followed for each test. For isometric testing of the elbow flexors in our laboratory, an average ICC of .92 was calculated across testing sessions.
Results No significant differences were found between the pGz and controls for physical characteristics or for pretest criterion measures.
Muscle Strength Significant differences were seen between pGz and controls in MVC90 and MVC150 from posttest through 96 hours (P < .01). MVC90 values for pGz at 48, 72, and 96 hours were significantly higher than posttest (P = .01, P = .08, P = .02, respectively) and did not differ from the pretest value. For controls, MVC90 remained lower than pretest values across all 96 hours (P < .01). MVC150 for pGz was significantly higher than posttest (P = .03) and did not differ from the pretest value, while controls had significantly lower values than pretest from posttest through 96 hours (P < .01). The
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patterns of change in MVC90 and MVC150 for pGz and controls also differed across the 96-hour recovery; however, strength changes were consistent within groups (Figures 3 and 4). Both groups’ greatest strength decreases occurred immediately after exercise; however, pGz recovered to pretest levels by 48 hours postexercise, while controls’ values remained depressed throughout the 96-hour recovery.
Blood Measurements Creatine Kinase. As shown in Figure 5, control and pGz means for
CK were similar for pretest, posttest, 24 hours, and 48 hours. At 72 and 96 hours mean CK increased in controls but not in pGz. A mixed ANOVA was used to assess differences between groups across time points; however, the sphericity assumption was not met, χ2(14) = 84.24, P < .001. Therefore, we used the Huynh-Feldt correction to interpret the model in a manner that did not assume sphericity. For this correction, the observed power was .486, indicating that reaching significance at the .05 level would be difficult. Using the sphericity correction, a group × time interaction was detected that approached statistical significance (P = .074). This interaction explained 18.3% of the variance in CK. Although significance did not reach the a priori level of P = .05, the effect size (ηp2 = 0.183) and mean differences indicate that the effect is meaningful. Myoglobin. No significant differences between pGz and controls were seen in MYO concentration. Both pGz and controls peaked during the posttest and returned to pretest levels during the 4-day recovery (Figure 6). Nitrite Levels. Nitrite levels were measured pretest and posttest and showed no significant difference (Table 2).
Figure 3 — Maximal voluntary contraction (MVC) scores at 90° elbow angle for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. ‡Significant difference between groups (P < .01). *Significantly different from pretest (P = .01). **Significantly different from pretest (P = .05). †Significantly different from posttest (P = .01). ††Significantly different from posttest (P = .02). #Significantly different from posttest (P = .04). §Significantly different from 72 hours (P = .01). §§Significantly different from 72 hours (P = .04).
Figure 4 — Maximal voluntary contraction (MVC) scores at 150° elbow angle for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. ‡Significant difference between groups (P < .01). *Significantly different from pretest (P < .01). **Significantly different from pretest (P = .04). †Significantly different from posttest (P = .01). ††Significantly different from posttest (P = .02). §Significantly different from 24 hours (P = .02).
IL-6, IL-10, and TNF-a. There were no significant differences
between groups for cytokines (Table 2). When normalized to pretest values, however, IL-6 and IL-10 showed significant increases for pGz, posttest and at 48 hours, respectively (P < .05); however, controls showed no increase in normalized IL-6 and IL-10 at any time point. TBARS, PGF2a, Protein Carbonyls, and Uric Acid. For normalized values of TBARS, PGF2α, protein carbonyls, and uric acid, no significant differences were found between groups; however, controls showed increased protein carbonyls at 48 hours (P < .05; Table 2).
Figure 5 — Concentration of creatine phosphokinase normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE.
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Discussion
Muscle Soreness, McGill Pain Questionnaire, Circumference, and ROM. Ratings of muscle soreness, McGill pain scores,
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changes in upper-arm circumference, and ROM are shown in Figures 7 through 10. No significant differences were seen between groups for any variable.
Figure 6 — Concentration of myoglobin normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .02). †Significantly different from posttest (P < .01).
The purpose of this study was to examine the effectiveness of pGz as a recovery method to lessen the effects of EIMD after a bout of unaccustomed eccentric elbow-flexion exercise. The major finding was that pGz during recovery enhanced muscle performance and diminished the negative effects of EIMD in active young men. To our knowledge, this is the first study to show a more rapid strength recovery using a therapeutic intervention compared with passive recovery. In contrast, other interventions such as cryotherapy, active recovery, stretching, electrical stimulation, massage, nonsteroidal anti-inflammatory drugs, hyperbaric oxygen therapy, and acupuncture1,4,5,22 fail to produce positive impacts on strength during recovery from eccentric exercise. However, contrast water therapy (CWT) did enhance strength recovery at 24, 48, and 72 hours when compared with passive recovery.2,23 Differences existed in the damage protocol, muscle groups, and performance measures between the CWT investigation and the current study. Compared with the CWT protocol, a greater decrease in performance was seen immediately after the first treatment in controls and pGz, indicating a disparity in damage0protocol effectiveness. Although one CWT damage protocol used a similar intensity (120% 1RM),23 the other used a higher intensity (140% of 1RM).2 Less work was performed during the bilateral leg press used in the CWT studies than the unilateral arm curl used in our study. In addition, the improved strength recovery with CWT took 24 hours, while pGz produced improvements immediately after exposure that lasted throughout
Table 2 Blood Markers, Mean ± SD Marker
Group
Pretest
Posttest
24 h
48 h
72 h
96 h
IL-6
Control
1.14 ± 0.55
1.82 ± 1.14
1.14 ± 0.54
0.91 ± 0.30
1.53 ± 0.66†
0.73 ± 0.19
pGz
0.60 ± 0.35
1.06 ± 0.83*
1.34 ± 1.62
1.25 ± 1.03
1.01 ± 1.24
0.98 ± 0.76
Control
3.80 ± 1.40
3.85 ± 1.59
4.11 ± 2.44
4.69 ± 3.51
3.88 ± 2.01
3.88 ± 1.50
pGz
3.48 ± 1.12
3.44 ± 0.94
3.42 ± 1.12
3.88 ± 1.46§
4.74 ± 3.86
4.43 ± 3.13
Control
0.00 ± 0.00
0.02 ± 0.04
0.00 ± 0.00
0.03 ± 0.07
0.00 ± 0.00
0.00 ± 0.00
pGz
0.00 ± 0.00
0.15 ± 0.29
0.09 ± 0.26
0.25 ± 0.51
0.00 ± 0.00
0.44 ± 1.24
Control
0.02 ± 0.01
0.02 ± 0.00
pGz
0.02 ± 0.01
0.04 ± 0.07
Control
31.74 ± 29.41
27.09 ± 29.02
30.45 ± 24.75
24.50 ± 24.90
30.89 ± 39.0
26.54 ± 27.64
pGz
30.26 ± 16.53
30.87 ± 17.70
36.15 ± 18.25
30.35 ± 24.78
25.95 ± 16.66
25.48 ± 16.01
Control
41.02 ± 31.00
54.45 ± 45.50
39.34 ± 19.70
30.67 ± 13.94
41.75 ± 29.53
30.38 ± 8.85
pGz
28.65 ± 14.74
22.21 ± 16.89
26.15 ± 15.43
26.57 ± 9.44
25.89 ± 16.79
35.27 ± 24.53
Control
1.53 ± 0.34
1.72 ± 0.67
1.54 ± 0.42
1.80 ± 0.52††
1.56 ± 0.32
1.61 ± 0.36
pGz
1.53 ± 0.34
1.72 ± 0.67
1.54 ± 0.42
1.80 ± 0.52
1.56 ± 0.32
1.61 ± 0.36
Control
8.92 ± 1.68
9.35 ± 2.48
9.22 ± 1.79
9.25 ± 1.61
9.39 ± 2.12
9.97 ± 2.45
pGz
9.53 ± 1.24
9.24 ± 1.44
9.31 ± 1.54
9.63 ± 1.60
9.31 ± 1.53
9.29 ± 1.37
IL-10
TNF-α
Nitrite
TBARS
PGF2α
Carbonyls
Uric acid
Abbreviations: pGz, whole-body periodic acceleration. Control n = 7, pGz n = 9. †Significantly different from 96 h (P = .03). *Significantly different from pretest (P = .02). §Significantly different from pretest (P = .04). ††Significantly different from pretest (P < .01).
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990 Serravite et al
Figure 7 — Muscle soreness using the visual analog scale for the wholebody periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P < .01). §Significantly different from 72 hours (P = .05). †Significantly different from 96 hours (P = .01). ††Significantly different from 96 hours (P = .03). #Significantly different from 96 hours (P = .03).
Figure 8 — Pain questionnaire score for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .01). **Significantly different from pretest (P < .02). §Significantly different from 72 hours (P = .02). †Significantly different from 96 hours (P = .01). ††Significantly different from 96 hours (P = .03).
the 96-hour evaluation period. As a caveat, our posttest measurements were taken after subjects performed the recovery intervention, which does not guarantee equal levels of muscle damage for pGz and controls. The mechanisms that may have contributed to improved strength during recovery when applying pGz are unclear. If reduced structural damage is responsible for improved force production with pGz, the impact of NO on calcium homeostasis and oxidative stress should be considered. Lopez et al24 recently found that in mice, pGz accelerated recovery of intramuscular Ca2+ levels after increases seen after an acute bout of downhill running. However,
Figure 9 — Circumference of the upper arm normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .01). **Significantly different from pretest (P = .03). †Significantly different from posttest (P < .05).
Figure 10 — Range of motion of the elbow joint normalized to pretest values for the whole-body periodic acceleration (black circles) and control (white circles) groups, mean ± 95% CI SE. *Significantly different from pretest (P = .01). **Significantly different from pretest (P = .02). #Significantly different from pretest (P = .04). †Significantly different from posttest (P = .05). §Significantly different from 96 hours (P = .02).
the contributions of this mechanism to the improved performance in our study remain in question, since no significant differences in serum nitrite levels were seen between pGz and controls. Several factors may have affected our measurement of nitrite levels, including subjects’ nutritional status and oxidative-stress levels.25 The attenuated CK response for pGz toward the end of the recovery period, along with improved strength recovery, may indicate reduced levels of muscle damage with pGz; however, CK is not a direct measure of the degree of muscle damage due to the large variability in its response in similarly exercised individuals.26 While some recovery studies have shown CK peaking within the first 24 hours after exercise, others confirmed that the highest CK
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pGz and DOMS 991
concentration occurs 4 to 5 days after exercise.27 In addition, patterns of change in CK have differed with differing recovery methods. MYO is also used to measure muscle damage. Although we found no significant between-groups differences in MYO, its earlier peak compared with CK agrees with previous studies.23 In addition, the increased MYO levels at 72 and 96 hours postexercise reflect the results reported by Howatson et al,28 using ice massage. The differences in the time course of the appearance of MYO and CK can be explained by MYO’s smaller size and more direct delivery route into the blood.29 Unlike MYO, CK, due to its larger molecular size, is delivered into the bloodstream via the lymphatic system, delaying its appearance after acute muscle damage. Our current findings, showing significant within-group increases in IL-6 by the pGz group during the posttest assessment, have not been previously reported; however, the peaking of IL-6 immediately after exercise and its return to near pretest values within 24 hours have been reported previously after an acute exercise bout.30 Although IL-6 is expected to increase with exercise, the lack of response in our controls is not without precedent.31 Increased IL-6 can be considered a positive response, since it is proposed to stimulate anti-inflammatory cytokine production and may indirectly inhibit proinflammatory cytokines.32 The anti-inflammatory environment induced by IL-6 may have contributed to IL-10 increases with pGz, since IL-6, independent of TNF-α, can enhance IL-1ra and IL-10 levels.33 Moreover, IL-6 increases satellite-cell proliferation and muscle regeneration.34 The lack of significant differences in systemic TNF-α in our study reflects findings of other researchers who examined inflammatory markers after acute exercise and IL-6 infusion,32 reflecting the fact that TNF-α is more important later in muscle recovery. Previous studies that examined acute muscle-damaging exercise in humans have reported that eccentric contractions induce greater oxidative stress than concentric contraction.35 Although oxidativestress indices such as TBARS, protein carbonyls and uric acid may be elevated several days after eccentric exercise, we only found significant increases in protein carbonyls, which are markers of protein oxidation, for controls 72 hours after our eccentric-exercise bout. Although no significant differences in soreness, pain, circumference, or ROM were seen between groups, the shorter durations of soreness and pain responses, lack of significant circumference increases, and rapid recovery of ROM for pGz over controls demonstrate an enhanced recovery pattern in this group. The positive impact of pGz on pain is not without precedent; in a comparable study with fibromyalgia patients, 45 minutes of pGz produced significant reductions in pain within 1 to 3 treatments.11 A limitation of this study was our failure to quantify the effects of the damage protocol immediately after its administration or to measure leukocytes during the recovery period. However, the quantification of cytokines provided a reliable indicator of inflammation. In addition, the quantification of glutathione could further help explain changes in some criterion measurement, since subjects with low total plasma glutathione levels display lower plasma CK and MYO responses and faster recovery from eccentric exercise than subjects with higher levels.26 Moreover, failure to control hydration levels during recovery may have affected lymph flow and therefore affected CK levels after exercise.36 Finally, controlling diet during the recovery period may have also provided a more stable testing environment, although the impacts of nutrition on DOMS and inflammation are equivocal.37 The use of pGz after high-intensity eccentric exercise improved strength recovery and positively affected EIMD symptoms. These
benefits may be the result of enhanced NO release; however, our results using nitrite levels as a marker of NO release cannot support this contention. Future research should investigate the effects of pGz in skeletal muscle through quantification of inflammatory and oxidative-stress markers, as well as ultrastructural damage using electron microscopy. In addition, the impact of pGz on EIMDmediated disruptions in excitation–contraction coupling should be investigated in humans. Finally, using pGz for preconditioning to reduce levels of DOMS and improve muscle performance should be investigated.
Practical Applications Exercise induces positive adaptations ranging from improved health to enhanced performance when appropriate stress and recovery patterns are applied. Although several methods are available to help the body recover after unaccustomed exercise resulting in EIMD, no single method can be identified as the gold standard. pGz may improve the training-adaptation cycle by speeding up the body’s recovery as it reduces performance losses generally experienced with EIMD.
Conclusions By accelerating the recovery of neuromuscular performance, pGz may benefit recreational athletes who seldom employ adequate recovery periods after exercising or high-performance athletes who need to increase their training load to achieve maximum performance. Acknowledgments The authors would like to thank Tom E. Abdenour, head trainer for the Golden State Warriors Basketball Team of the National Basketball Association, for the suggestion to undertake this investigation. We would also like to thank the students who helped with the data collection. A special thanks to Dr Randall Penfield and Corrine Huggins of the Dunspaugh-Dalton Community & Educational Well-Being Research Center at the University of Miami School of Education for their help with the statistical analyses and Cameron Dezfulian and Laura Quirola for their extensive help with data collection and interpretation.
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