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Addition of Synchronous Whole-Body Vibration to Body Mass Resistive Exercise Causes Little or No Effects on Muscle Damage and Inflammation

Hazell, Tom J.; Olver, T. Dylan; Hamilton, Craig D.; Lemon, Peter W.R.

Journal of Strength and Conditioning Research: January 2014 - Volume 28 - Issue 1 - p 53–60
doi: 10.1519/JSC.0b013e318296484f
Original Research
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Hazell, TJ, Olver, TD, Hamilton, CD, and Lemon, PWR. Addition of synchronous whole-body vibration to body mass resistive exercise causes little or no effects on muscle damage and inflammation. J Strength Cond Res 28(1): 53–60, 2014—The purpose of this study was to determine if a moderate intensity whole-body vibration (WBV) body mass resistive exercise session causes additional muscle damage, soreness, and inflammation compared with the same exercise session without vibration (NoV). Ten recreationally active male university students completed 2 separate 24-hour study periods incorporating an exercise session with WBV or NoV. Muscle torque was measured (at 0, 60, and 240°·s−1 angular velocities), soreness (10-point scale) in the upper (UE [triceps]) and lower (LE [quadriceps]) extremities, and muscle inflammation markers (interleukin [IL]-1β, IL-6, IL-10) were measured at 4 time points (preexercise, immediately postexercise, 4 hours post, and 24 hours post). Diet was controlled. Compared with NoV, WBV increased (p < 0.01) muscle soreness at 24 hours postexercise in both the UE (2.2 ± 1.7 vs. 0.6 ± 0.9) and LE (2.0 ± 1.5 vs. 0.7 ± 0.7). Muscle torque was decreased immediately postexercise (p < 0.05) in the UE and LE at 0°·s−1 and in the UE at 240°·s−1, but there was no difference between exercise treatments. The exercise session caused significant but small increases in IL-1β and IL-6 but with no differences between exercise treatments. Interleukin-10 was increased with WBV (2.9 ± 2.0 to 3.6 ± 1.9 pg·ml−1; p < 0.03). These data suggest that the addition of WBV to exercise has little effect on muscle function and damage, soreness, or inflammation.

Exercise Nutrition Research Laboratory, School of Kinesiology, Faculty of Health Sciences, Western University, London, Ontario, Canada

Address correspondence to Tom J. Hazell, tom.hazell@uleth.ca.

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Introduction

Whole-body vibration (WBV) is an exercise or rehabilitation tool that uses a ground-based platform generating vertical oscillations that result in reflexive muscle contractions (7,15,34). Vibration exposure directed to the body through the feet has demonstrated positive muscle training and rehabilitation effects likely because of the associated vibration-induced increases in muscle activity (1,7,16,17,26,34,35), blood flow (21,24,25), and muscle temperature (10,11,19).

Both regional and WBVs (via a ground-based platform) have been used in rehabilitation settings to either prevent (3) or treat (23) exercise-induced muscle damage. Synchronous WBV (35 Hz, 5 mm) applied during a static semisquat (100° knee flexion) immediately before maximal isokinetic eccentric exercise of the knee extensors attenuated delayed onset muscle soreness (DOMS), strength reduction, soreness, and plasma creatine kinase (CK) concentration compared with no vibration (2). Further, stimulating lower body muscles directly with either reciprocating (35 Hz, 2 mm [31]) or synchronous (40 Hz, 5 mm [6]) WBV after muscle-damaging exercise can reduce perceived pain, interleukin-6 (IL-6), and histamine compared to no-vibration treatment. Consequently, WBV might have a value as a treatment for DOMS.

There is also research demonstrating that WBV increases muscle activity significantly (1,16,17,26,35), but whether WBV induces any muscle soreness, inflammation, or damage is unknown. Recently, Gojanovic et al. (14) demonstrated that a total body workout (static and dynamic squats, push-ups, toe raises; 27-minute work in 39 minutes) with reciprocating WBV (26 Hz, 15 mm) can increase CK concentration (5 of 20 participants doubled baseline values). However, this study could not determine if this increase in CK was because of the WBV or the exercise routine itself. The purpose of this study was to determine if adding WBV via a ground-based platform to a body mass resistive exercise session affects postexercise muscle function, soreness, and inflammation.

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Methods

Experimental Approach to the Problem

This study investigated whether the increased muscle contractions elicited during WBV exercise result in any effects on muscle function, inflammation, and soreness. Muscle function (isometric and isokinetic strength) and subjective muscle soreness were assessed in both the upper (UE [triceps]) and lower (LE [quadriceps]) extremities while muscle inflammation was assessed via inflammatory cytokines (IL-1β, IL-6, IL-10). All outcome measures were assessed at 4 time points (preexercise, immediately postexercise, 4 hours post, and 24 hours post). The 30-minute WBV exercise session consisted of upper and lower body exercises (15 minutes of exercise: 15 minutes of rest) using body mass as the resistance.

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Subjects

Healthy male kinesiology students (age: 25 ± 3.5 years, height: 179 ± 7.2 cm, weight: 81 ± 7.9 kg; mean ± SD; n = 10) completed 2 separate 24-hour study periods incorporating a WBV exercise session or the same exercise session without vibration (NoV). No physical activity or caffeine ingestion was permitted for at least 48 hours before participation and both physical activity and diet (see below) were controlled throughout the experiment. All the participants were nonsmokers, physically active but not involved in an exercise training program at the time of data collection (and for at least 4 months before the study), none had any contraindications to WBV according to the manufacturer's criteria (i.e., diabetes, epilepsy, gall or kidney stones, acute inflammations, cardiovascular diseases, joint implants, recent thrombosis, or tumors), and all passed the Physical Activity Readiness Questionnaire health survey (38). The study was completed in spring and summer (May–August). The Health Sciences Office of Research Ethics at Western University approved this study, and all the participants gave their informed written consent before participation.

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Familiarization

Before any testing, the participants performed a familiarization session to acclimate to the sensation of WBV. A demonstration of proper technique for each of the dynamic exercises to be performed in the exercise session occurred, and practice of these movements was undertaken until performance was consistent and correct. This session also had the participants maintain static positions of these exercises with exposure to 30 seconds of the WBV stimulus.

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Exercise Session

A dynamic body mass resistive exercise session involving most of the major muscle groups of both the upper and lower body was studied. The exercises for the lower body included squats (feet on the platform; descent to ∼90°, ascent to ∼160°), single leg lunges for each leg (lead foot on the platform; descent to ∼90°, ascent ∼160°), and hamstring bridges (laying supine, feet on the platform and repetitions involving elevating the trunk as high as possible). The upper body exercises included push-ups and triceps dips (hands on the platform; descent to ∼90°, ascent to ∼180°). Blocks were used for the upper body exercises, lunges, and hamstring bridges enabling the hands or feet that were off the platform to be at the same height as the platform. Body mass was the resistance for all exercises. A 1:1 exercise to recovery ratio (30-second exercise: 30-second recovery) was used. We have previously demonstrated that this exercise session increases 24-hour oxygen consumption significantly demonstrating its potential as an exercise modality (18). The exercise session was based on the traditional 60 seconds on and 60 seconds off (1:1 work to rest ratio) used with WBV exercise for most prior lower body exercise programs and 30 seconds on: 30 seconds off for upper body dynamic exercises (push-ups and triceps dips) because 60 seconds proved to be very difficult.

Specifically, the participants completed 5 sets of each of a total of 6 exercises paced by a metronome at a rate of 0.5 reps·s−1 resulting in 15 minutes of exercise during the 30-minute protocol. A goniometer was adhered with double-sided tape to the lateral side of the left knee and left elbow to ensure consistent dynamic movements.

The WBV stimulus was applied using a WAVE platform (Whole-body Advanced Vibration Exercise, Windsor, ON, Canada). This platform generates a synchronous (vertical; strictly the z-axis) vibration stimulus whereby the platform oscillates up and down uniformly (33). The WBV stimulus was set at a frequency of 45 Hz and a peak-to-peak displacement of 2 mm (verified via single frame analysis of high-speed video), which we have shown previously to increase leg skeletal muscle electromyography significantly (16,17). Importantly, the platform has a load-leveling system based on body mass (regardless of body mass this places the vibration platform in the same initial position using inflatable air bladders), so each subject received the same vibration stimulus. We have verified system performance with masses up to 180 kg (data not shown). The NoV exercise session was performed on the same platform but with the vibration turned off.

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Experimental Protocol

The participants completed 2 separate 24-hour data collection periods separated by 4 weeks (WBV exercise session vs. NoV). The treatments were rotated systematically to avoid order effects. The participants arrived at the laboratory (0830 hours), ate a prescribed breakfast (0830–0900 hours—see below for details), had a resting blood sample taken from a forearm vein, completed baseline (preexercise) assessments of muscle function (knee and elbow extensors), and filled out a muscle soreness questionnaire (see below). Then, they completed the 30-minute exercise routine with or without vibration (0930–1000 hours) and the same measurements were repeated (Figure 1) immediately postexercise (1000 hours); 4 hours postexercise (1400 hours); and 24 hours postexercise (0900 hours next day). Lunch (between 1200 and1300 hours) was provided to each subject (see details below). During exercise recovery data collection (measures #3–4), the participants were allowed to leave the laboratory but refrained from any additional exercise until all measures were completed the next day. Dinner was eaten at the same time on both testing days (1700–1800 hours).

Figure 1

Figure 1

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Diet

All the subjects were provided the same breakfast and lunch in the laboratory. For breakfast, the subjects consumed 29 kJ·kg−1 meal (∼72% carbohydrate, 15% fat, and 13% protein) consisting of yogurt (150 g), orange juice (236 ml), and cereal (16 kJ·g−1). For lunch, the subjects ate a 46 kJ·kg−1 meal (∼55% carbohydrates, 27% fat, and 18% protein) consisting of a submarine sandwich (6 in.; meatball), 1% chocolate milk (500 ml), and cereal bar (16 kJ·g−1). Further, they recorded their evening food intake (64 kJ·kg−1 meal; ∼41% carbohydrate, 31% fat, and 28% protein) on the first experimental day and reproduced it for the subsequent treatment.

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Muscle Function Tests

The muscle function (torque) measures consisted of maximal voluntary isometric and isokinetic contractions for both the knee (intraclass correlation: 0.92 for isometric; 0.90 for 60°·s−1; 0.92 for 240°·s−1) and elbow extensors (ICC: 0.95 for isometric; 0.90 for 60°·s−1; 0.93 for 240°·s−1) using a Biodex Multi-Joint System 3 dynamometer (Biodex System 3 Pro, Biodex Medical Systems, Shirley, NY, USA). To test the knee extensors, the participants performed 3 maximal isometric knee extensions at 90° of knee flexion. Each repetition was held for 3 seconds (120 seconds of passive rest was provided between repetitions). Five minutes of passive rest separated the isometric and isokinetic tests. The isokinetic contractions (60–180° range of motion) were performed at 2 velocities: 60 and 240°·s−1. The participants performed 5 maximal contractions at each angular velocity separated by 3 minutes of passive rest. The torque was recorded throughout the entire range of motion (60–180°). To test the elbow extensors, a similar protocol was employed, except that the isometric tests were performed at 60° of elbow flexion. Verbal encouragement was provided during all muscle function tests to ensure maximal exertion.

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Muscle Inflammation

For the measurement of IL-1β, IL-6, and IL-10, a 6-ml blood sample (BD Vacutainer K2 ethylenediaminetetraacetic acid Blood Collection Tube [lavender top]; Becton, Dickinson and Company, Franklin Lakes, NJ, USA) was collected at each testing time point (preexercise, postexercise, 4 hours postexercise, and 24 hours postexercise) from a forearm vein. Samples were immediately centrifuged at 3500 rpm for 15 minutes at 4° C (Allegra 21R, Beckman Coulter, Brea, CA, USA); the plasma aliquots were transferred to polypropylene freezer vials and frozen and stored at −80° C for later analyses. Each cytokine was determined by specific enzyme-linked immunosorbent assay kits (Millipore, Billerica, MA, USA).

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Muscle Soreness

To measure muscle soreness, the participants rated their perceived degree of soreness for both the knee and elbow extensors at all 4 time points, using a linear 0- to 10-point scale (4,39). A rating of 0 indicated no soreness and a rating of 10 indicated extreme soreness.

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Statistical Analyses

All data were analyzed using Sigma Stat for Windows (version 3.5; Systat Software Inc., Point Richmond, CA, USA) or SAS (version 9.2, Cary, NC, USA). Two-way repeated measures analyses of variance (treatment × time) were used to investigate the differences in muscle function and the markers of muscle inflammation at all measurement points. Post hoc tests were performed using Tukey's Honestly Significant Difference tests, where necessary. A Kruskal-Wallis test was used to determine differences in muscle soreness. All data are presented as mean ± SD, and the level of statistical significance was set at p ≤ 0.05.

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Results

Isometric Muscle Function

There was no interaction for quadriceps muscle function (p = 0.963; Figure 2A) or main effect for exercise mode (p = 0.78), but there was a main effect for time of measure (p = 0.03). Both the immediate postexercise (p = 0.04) and 24 hours postexercise measures (p = 0.04) were lower than preexercise values.

Figure 2

Figure 2

There was no interaction for triceps muscle function (p = 0.97; Figure 2A) or main effect for exercise mode (p = 0.71), but there was a main effect for time (p = 0.01). The immediate postexercise time point was lower than the preexercise (p = 0.02) and the 24 hours postexercise measures (p = 0.02).

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Isokinetic Muscle Function (60°·s−1)

There was no interaction for quadriceps muscle function at 60°·s−1 (p = 0.97; Figure 2B) and no main effects for exercise mode (p = 0.66) or time (p = 0.32).

Similarly, there was no interaction for triceps isokinetic muscle function at 60°·s−1 (p = 0.44; Figure 2B) and no main effects for exercise mode (p = 0.77) or time (p = 0.07).

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Isokinetic Muscle Function (240°·s−1)

There was no interaction for quadriceps muscle function at 240°·s−1 (p = 0.95; Figure 2C) and no main effects for exercise mode (p = 0.71) or time (p = 0.07).

There was no interaction for triceps muscle function at 240°·s−1 (p = 0.69; Figure 2C or main effect for exercise mode, p = 0.96), but there was a main effect for time of measure (p < 0.01). Immediately postexercise was lower than pre (p < 0.01), 4-hour (p < 0.01), and 24 hours postexercise (p = 0.05).

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Muscle Soreness

There was an interaction (p < 0.01; exercise mode × time) for quadriceps muscle soreness (Figure 3A). The WBV exercise session increased muscle soreness at 24 hours post-WBV (2.0 ± 1.5; p < 0.01) vs. NoV (0.7 ± 0.7). This 24-hour time point with WBV exercise was also greater than all previous time points (p < 0.04). The NoV had no effect on quadriceps muscle soreness.

Figure 3

Figure 3

There was also an interaction (p = 0.011; exercise mode × time) for triceps muscle soreness (Figure 3B). The WBV exercise session increased muscle soreness at 24 hours post-WBV (2.2 ± 1.7; p < 0.01) vs. NoV (0.6 ± 0.9). This 24-hour time point with WBV exercise was also greater than all previous time points (p < 0.01). The NoV had no effect on triceps muscle soreness.

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Interleukin-1β

There was no interaction for IL-1β (p = 0.99; Figure 4A), and there was no effect of exercise mode (p = 0.88) or time of measure (p = 0.13).

Figure 4

Figure 4

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Interleukin-6

There was no interaction for IL-6 (p = 0.33; Figure 4B), and there was no effect of exercise mode (p = 0.09), but there was a main effect for time of measure (p < 0.01) where immediately postexercise was increased compared with preexercise (p < 0.01).

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Interleukin-10

There was no interaction for IL-10 (p = 0.42; Figure 4C) and no effect for time (p = 0.38), but there was a main effect for exercise mode (p = 0.03). The WBV exercise session was increased vs. the NoV (p = 0.03).

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Discussion

The addition of WBV to a dynamic exercise session (upper and lower body) with body mass as the resistance resulted in no muscle damage as evidenced by no effects on muscle function or inflammation markers (IL-1β, IL-6, and IL-10) and only a slight increase in muscle soreness 24 hours postexercise compared with the same exercise session with no vibration. The exercises performed were typical of standard body mass resistance training (push-ups, squats, lunges, etc) containing both concentric and eccentric components. Although the addition of WBV to these dynamic exercises has demonstrated increases in skeletal muscle activity (16,17), skin temperature (19), and oxygen consumption and heart rate (18), the increase in exercise intensity results in minimal effects on muscle function, inflammation, soreness, and presumably tissue injury.

In contrast, another recent WBV exercise routine produced a significant increase in plasma CK concentration perhaps indicating muscle injury (14). This study used similar exercises (squats, push-ups, calf raises) as in this study, but the investigators did not have a control group (same exercise routine without WBV), so it is unknown whether the observed increase in CK was because of WBV or the exercise. Further, their subjects were physically inactive, they did not have a familiarization exposure to the WBV protocol, and the CK results were quite variable (significant increases, defined as an increase of at least double the baseline value, were only observed in 5 of 20 subjects).

In this study, we observed a small decrease in muscle torque immediately postexercise (isometric knee and elbow; isokinetic 240°·s−1); however, none of these decreases were significant between experimental conditions indicating that any effect was because of the exercise not the vibration. As muscle torque is often considered the most valid indirect measure of muscle damage (8), these data suggest that any tissue damage resulting from the WBV was minimal. Consequently, it is likely that these small torque decreases immediately postexercise were muscle fatigue related (9), and not the result of muscle damage. Perhaps the small decrease immediately postexercise in the elbow flexors (significant at 240°·s−1 but not at 60°·s−1) was because of the smaller size of the triceps muscle affecting fast but not slow contraction velocity. Although previously we have demonstrated that the addition of vibration to dynamic body mass resistive exercises increases muscle activity (16,17), the current data suggest that WBV exposure does not induce sufficient tissue soreness and injury to affect subsequent muscle function. However, whether WBV exercise affects rates of torque or velocity development warrants future research.

The observed no or small change in inflammatory markers also suggests the WBV exercise caused little muscle damage. Thus, both exercise sessions studied were not overly strenuous. We did observe a small increase in IL-6 (∼2–3 pg·ml−1) immediately postexercise, but there was no difference between treatments. The IL-6 is an inflammation responsive cytokine released with increasing exercise intensity, duration, and muscle mass involvement (29,30). For comparison purposes, this increase is much less than reported after running a 42-km marathon (∼80 pg·ml−1) (28) or even after a traditional strength exercise session (∼5–6 pg·ml−1) (20) confirming that the exercise bout studied was not very strenuous. For IL-10, there was no effect for time of measure, but there was a main effect for the type of exercise as the WBV session resulted in a greater overall response than did the NoV session. However, consistent with the other inflammation markers, the IL-10 increase (<3.7 pg·ml−1) was small vs. strength exercise (∼5 pg·ml−1) (20). Apparently body mass resistive WBV exercise has little effect on inflammation. However, it is worth noting that IL-10 is an inhibitor of other inflammatory cytokines (32), so its increase with WBV may have minimized any potential increase in the other markers of muscle inflammation measured (IL-1β and IL-6).

We did observe a small increase in muscle soreness 24 hours post-WBV exercise, but the increase was quite modest (rating of ∼2 out of 10 in both the quadriceps and triceps). This observation is consistent with the minimal muscle function and inflammatory response effects observed again indicating the addition of WBV to a moderate intensity body mass resistive exercise routine has minimal effects on muscle function and damage. This may mean that synchronous WBV exercise could be completed more frequently in a training program or that external loads are needed to produce training effects; however, muscle soreness can peak approximately 1–3 days postexercise (37) and whether this small degree of muscle soreness seen in response to the WBV exercise session would increase significantly at 48 or 72 hours remains to be determined. Importantly, it is unlikely that this soreness was because of the novelty of the WBV stimulus as all the subjects completed a familiarization session before the study and several had participated in WBV exercise previously. The current results demonstrating little to no muscle damage and soreness with dynamic WBV exercise session could have important implications for rehabilitation settings as WBV has demonstrated benefits to older adults (22) or those with neurological diseases (multiple sclerosis, Parkinson's disease) (12), fibromyalgia (36), and even chronic obstructive pulmonary disease (13).

The vibration stimulus generated by any ground-based WBV platform activates an afferent feedback response via muscle spindles and 1a afferents, a response akin to the tonic vibration reflex (7,34). The resulting increase in muscle activity via reflexive muscle contractions may be because of greater motor neuron activation/recruitment and increased synchronization of synergist muscles (5,27). However, the absence of soreness and presumably damage with WBV may mean WBV does not affect muscle protein synthesis sufficiently for training adaptations, at least in young healthy men. Future studies should examine older and less fit individuals and the use of external loads to assess more fully the potential applicability of WBV exercise.We used considerable experimental control over each 24-hour data collection period (controlled feeding and physical activity), but there were several limitations to our study. First, because muscle damage can peak 1–3 days postexercise, changes might have occurred after our measurement period. Second, our muscle function testing did not contain an eccentric component, so our evaluation is incomplete. Third, we did not include other muscle damage markers such as plasma CK or lactate dehydrogenase because these have large individual intersubject variability and previous activity provides a substantial protective effect (8). Fourth, although any potential effects of prior isometric contractions on postactivation potentiation would have contributed equally on all testing days, this effect was unmeasured. Finally, even though WBV did not affect peak torque generated by the elbow or knee extensors in this study, the rate of torque and velocity development might have been altered.

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Practical Applications

The addition of WBV to dynamic upper and lower body exercise of sufficient intensity to increase skeletal muscle activity, V[Combining Dot Above]O2, heart rate, and muscle temperature causes little effect on muscle function and damage, soreness or inflammation. This has implications for increased frequency of training and the use of WBV to speed recovery as suggested by Rhea et al. (31). The WBV sessions increase both during and postexercise V[Combining Dot Above]O2 (18), so regular WBV exercise could be beneficial from a fat loss standpoint. Furthermore, WBV exposure could also be a beneficial rehabilitation tool. However, these data also suggest that WBV exercise with body mass resisted movements may not be sufficiently intense to induce muscle hypertrophy at least in young fit individuals. Future research is warranted to determine the value of similar WBV exercise sessions on less fit individuals (sedentary or older adults) as well as whether the addition of external weights can induce training effects in more fit (trained) individuals.

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Acknowledgments

The authors would like to thank Dr. Crystal O. Kean for her help with the muscle function data and Dr. Trevor B. Birmingham for the use of his Biodex dynamometer. The WAVE (Windsor, ON, Canada) donated the platform. No competing financial interests exist.

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Keywords:

muscle soreness; muscle function; IL-6; IL-10; IL-β

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