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Original Research

Adaptation to Damaging Dance and Repeated-Sprint Activity in Women

Brown, Meghan A.1; Howatson, Glyn1,2; Keane, Karen M.1; Stevenson, Emma J.1

Author Information
Journal of Strength and Conditioning Research: September 2016 - Volume 30 - Issue 9 - p 2574-2581
doi: 10.1519/JSC.0000000000001346
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Abstract

Introduction

Exercise-induced muscle damage (EIMD) is associated with many sport and exercise activities. This manifests as muscle soreness, inflammation, and detriments in muscle functionality, which can reduce subsequent performance potential (12). Attenuating the symptoms and/or enhancing recovery from EIMD are therefore highly desirable in physically active populations. Despite these potential issues, skeletal muscle has the ability to rapidly adapt after exercise and indices of muscle damage are attenuated after a second bout of exercise, which is commonly termed the repeated bout effect (RBE). This phenomenon has been demonstrated to occur within 1–2 days (21) and can extend for several months after the initial bout (22). Although the mechanisms are not fully understood, the RBE has been attributed to neural, connective, or cellular adaptations (including adaptation in excitation-contraction coupling and the inflammatory response) or, more likely, a combination of these (12,17). Thus, although the symptoms associated with EIMD are often thought to be detrimental, they play a crucial role in the adaptive process; in fact, associated neuromuscular adaptation is suggested to be the most effective means of attenuating future negative effects of EIMD (12,17).

The RBE has been extensively researched in men; however, data concerning women is limited. This is particularly important because estrogen is widely considered to be responsible, in part, for attenuating symptoms of muscle damage in women and could influence a number of factors including effects on muscle membrane integrity (32). In addition, the secondary inflammatory response may be sex dependent, with reports of sex differences in leukocyte and cytokine infiltration into skeletal muscle after exercise (25,32). As a result, the initial physiological stress and ensuing recovery and adaptation associated with EIMD in women are likely to differ compared to men.

Many studies investigating the RBE have used eccentric protocols that exercise single-muscle groups with isolated contractions using isokinetic dynamometry. Although these effectively induce muscle damage, they lack application to athletic paradigms. Although some have explored the RBE using sport-specific protocols (for instance, intermittent-sprint exercise (15), drop jump protocols (8), and downhill running (4)), other muscle-damaging activities that can be directly applied to sport and exercise stimuli warrant further investigation. For instance, dance, and multiple sprint sports such as soccer, rugby, and basketball—popular activities that are participated in both recreationally and professionally—involve eccentric-biased activities (9,13,24,33). Although these exercise modes differ in a number of respects (for instance, dance is characterized by complex movement sequences often prechoreographed, whereas the nature of repeated-sprint sports means that movements are much more unpredictable), they both involve changes in velocity and direction; previously shown to elicit muscle damage. Although these activities have been shown to elicit muscle damage (1,9,13,28), little is known about the adaptation associated with their participation. Given the demands of training and performance, individuals involved in these activities would benefit from an increased understanding of how repeated exposure of activity-specific stimuli can influence the symptoms of muscle damage, recovery, and adaptation.

The aim of this study was to elucidate whether dance-specific and repeated-sprint exercise designed to induce muscle damage can confer a protective effect against a subsequent bout of identical activity in physically active women. It was hypothesized that, despite their differences, the EIMD observed after a second bout of each activity would be lower than the first bout and that the responses of each activity would be similar.

Methods

Experimental Approach to the Problem

Participants were randomly assigned to 1 of 2 muscle-damaging exercise groups; either a dance-specific exercise bout or a sport-specific repeated-sprint protocol. A battery of common markers of muscle damage was measured before, immediately after (0 hours), and 24, 48, and 72 hours after muscle damage. In a RBE design, a subsequent bout of identical exercise and dependent measures was conducted approximately 4 weeks (27 ± 4 days) after the first bout to ensure that subjects had fully recovered from the initial bout and were in the same (early to mid-luteal) phase of the menstrual cycle. This allowed for examination of the damage response and, more specifically, the RBE provided by the initial damaging bout. Participants were tested at the same time on subsequent days (±1 hour) to account for diurnal variation. Participants were asked to avoid strenuous exercise, alcohol, caffeine, nutritional supplements, and any anti-inflammatory drugs or alternative treatments (e.g., massage or cold water immersion) 48 hours before and for the 72-hour recovery period after each exercise bout.

Subjects

After institutional ethical approval, 29 healthy physically active women from a university dance team volunteered for a larger scale study examining the muscle damage response to sprint and dance-specific exercise; these data are presented elsewhere (1). A subset of 21 participants (mean ± SD age 19 ± 1 years [age range 18–21 years]; stature 164 ± 4 cm; mass 58.6 ± 6.2 kg; and body mass index 21.8 ± 2.2 kg·m2) completed a repeated bout of the dance-specific exercise bout (n = 10) or sport-specific repeated-sprint protocol (n = 11) and the data of both bouts of these 21 participants are reported in the present study. Participants gave written, informed consent after a general health-screening questionnaire to confirm the absence of any physiological conditions that would exclude them from the study. Participants were regularly active (8.9 ± 4.1 h·wk−1), including typically attending dance rehearsals twice per week (5.9 ± 3.2 hours). A 3-day food diary and activity log completed before testing determined that there were no differences in physical activity levels or energy and macronutrient intakes between participants. Volunteers were asked to replicate their reported diets and activity levels as closely as possible throughout the testing period, and this was confirmed with a second 3-day food diary and activity log completed midway through the 4-week recovery period. Moreover, participant characteristics were remeasured to ensure that no differences were evident between exercise bouts (all characteristics are displayed in Table 1). A questionnaire determined menstrual cycle phase; all testing took place during the early to mid-luteal phase or where applicable in the 14 days before a withdrawal bleed. This also identified the contraceptive use of participants; 13 were using an oral combination pill (all monophasic), 5 were using a progesterone-only pill/implant/injection, and 3 were normally menstruating.

Table 1.
Table 1.:
Participant characteristics, mean ± SD.*

Procedures

Exercise Protocols

Participants completed a standardized warm-up, followed by 5 minutes to perform any personal stretches and prepare themselves for the assigned protocol. The subject-specific warm-up on the initial day was noted so this could be replicated throughout testing. The originally described dance performance fitness test (DPFT) (26) was extended, as described previously (1), to involve the repetition of a dance phrase representative of contemporary dance at a tempo of 106 b·min−1; with each 10 × 1-minute phrase separated by a 2-minute rest period. The sport-specific repeated-sprint test (SSRS), described in full previously (9), briefly comprises 15 × 30-meter sprints departing every 65 seconds with a rapid 10-meter deceleration phase. Both the adapted DPFT protocol and the SSRS protocol were shown to induce muscle damage previously in this population (1). Standardized instructions and strong verbal encouragement from the investigator to encourage maximal effort were provided throughout each muscle-damaging protocol. In a RBE design, each participant completed a subsequent bout of identical muscle-damaging exercise approximately 4 weeks after the first bout. Protocols and measurement of dependent variables were completed in an indoor sporting facility, and the environmental conditions were controlled (17.7 ± 0.2° C and 1,012.1 ± 8.4 hpa).

Delayed-Onset Muscle Soreness

Subjective delayed-onset muscle soreness (DOMS) was measured using a 200-mm visual analog scale (9) from “no soreness” to “unbearably sore” anchored at each end of the scale. Participants were required to indicate on the line the level of perceived active lower limb soreness felt during a 90° squat.

Limb Girth

An anthropometric tape measure (Bodycare Products, Warwickshire, United Kingdom) was used to determine muscle swelling in the lower limbs. Girths at the calf (measured at its largest girth at baseline) and midthigh (located as midway between the inguinal crease and the superior border of the patella) of the right leg were recorded. These locations on the skin were marked with permanent marker on the initial day of each bout to ensure consistency on subsequent days. The mean of 2 measures at each site was used for analysis. Calf and midthigh girth intraexaminer percentage coefficients of variation (%CVs) were <1%.

Muscle Function

Subjects completed 3 countermovement jumps (CMJ) and 3 drop jumps (for measurement of reactive strength index [RSI]) using a light timing system (Optojump; Microgate, Bolzano, Italy). For CMJ, participants were asked to squat down and jump vertically and maximally, keeping their hands on their hips throughout. For RSI (jump height [cm] ÷ ground contact time [seconds]), subjects were instructed to drop from a height of 30 cm and on landing, to perform a 2-footed jump maximally with minimum contact time. Each effort was separated by 60 seconds of rest, and the peak CMJ and RSI were used for analysis.

Knee extensor peak force of the participants' right leg was measured using a strain gauge (MIE Digital Myometer; MIE Medical Research Ltd, Leeds, United Kingdom) to determine maximal voluntary isometric contraction (MVC). While in a seated position, the strain gauge was wrapped immediately above the malleoli and attached to a plinth on a purpose-built chair. The knee joint angle was standardized at 90° using a goniometer and confirmed before each contraction. Subjects were asked to complete 3 MVCs lasting 3 seconds, interspersed with 30 seconds of rest. The peak force of the 3 MVCs was used for analysis.

Participants completed a single maximal effort 30-meter sprint, and sprint time was recorded. The sprint was initiated from a line 30-cm behind the start line to prevent false triggering of the timing gates (Brower telemetric timers; Brower timing systems, Draper, UT, USA).

The 15 × 30-meter sprint times of those completing the SSRS were also recorded to determine total sprint time, mean sprint time, and rate of fatigue using the following formula (7):

Fatigue index (%) = (100 × [total sprint time/ideal sprint time]) − 100, in which total sprint time = sum of sprint times from all sprints and ideal sprint time = the number of sprints × fastest sprint time.

Creatine Kinase

Twenty participants consented to blood collection; n = 10 in both groups. Where data for single time points were missing because of sampling error (9 of 210 samples [<5%]), linear interpolation was used to complete the data set. Blood samples were collected by means of venepuncture from the antecubital fossa area into a 10-ml EDTA vacutainer. The samples were centrifuged at 3,000 RCF for 15 minutes at 4° C (Alegra X-22 Centrifuge; Beckman Coulter, Bucks, United Kingdom). Plasma was extracted, and stored immediately at −80° C for later analysis. Plasma CK concentrations were determined spectrophotometrically (Roche Modular; Roche Diagnostics, Burgess Hill, United Kingdom); the analytical range for this method was 7–2,000 IU·L and the interassay and intra-assay %CVs were <2%. The reference range for adult women is 10–160 IU·L.

Statistical Analyses

All results are presented as mean ± SEM. To account for interindividual variability, limb girths, CMJ, RSI, MVC, and sprint performance were expressed as a percentage change relative to baseline. Statistical software (IBM SPSS v21; IBM, Armonk, NY, USA) was used for inferential analysis and significance was accepted at the p ≤ 0.05 a priori. Mauchly's test assessed the sphericity of the data and, where appropriate, violations were corrected using the Greenhouse–Geisser adjustment. Raw baseline values were compared between bouts for each group using paired samples t-tests to assess any training effect. Total sprint time, mean sprint time, and fatigue scores were also compared between bouts in the SSRS group using paired samples t-tests. A mixed factor repeated-measures analysis of variance (group, 2 × bout, 2 × time, 5) was performed on all variables (except total sprint time, mean sprint time, and fatigue) using group as the between-subject factor, and bout and time as within-subject factors to analyze differences between groups and bouts. Where significant effects occurred, least significant difference post hoc analysis was performed. Partial eta-squared () effect sizes are also presented to provide magnitude of effects; 0.010, 0.059, and >0.138 were considered to represent small, medium, and large effects, respectively (27).

Results

There were no differences in baseline values between bout 1 and bout 2. For illustrative purposes, data not presented in figures (limb girth, CMJ, RSI, and MVC) are presented in Table 2. Participants completed the DPFT at a tempo of 106 b·min−1 during both bouts, and paired samples t-tests determined no differences between bouts 1 and 2 of the SSRS protocol for total sprint time (81.60 ± 1.00 seconds vs. 82.43 ± 0.96 seconds), mean sprint time (5.43 ± 0.07 seconds vs. 5.50 ± 0.06 seconds), and fatigue (3.82 ± 0.42% vs. 3.77 ± 0.43%), demonstrating that exercise intensity was maintained. Time effects were observed for all dependent variables (all p < 0.01).

Table 2.
Table 2.:
Absolute values for limb girth, CMJ, RSI, and MVC after bouts 1 and 2 of DPFT (n = 10) and SSRS (n = 11), mean ± SEM.*†

Delayed-Onset Muscle Soreness

Muscle soreness increased immediately after exercise and peaked 24 hours after EIMD in both groups after bouts 1 and 2 (Figure 1). However, DOMS was higher during bout 1 compared with bout 2 (F1,19 = 11.5, p = 0.003, and = 0.38), where DOMS was attenuated at 0, 24, and 48 hours after EIMD (F2.5,47.7 = 4.7, p = 0.009, and = 0.20). The magnitude of change in DOMS 48, and 72 hours after bout 2 was greater for DPFT compared with SSRS (F2.5,47.7 = 4.5, p = 0.010, and = 0.19).

Figure 1.
Figure 1.:
Muscle soreness in response to muscle-damaging exercise after dance performance fitness test (DPFT) (n = 10) and sport-specific repeated-sprint test (SSRS) (n = 11). Values are presented as mean ± SEM. ϕDenotes significant bout effect. *Denotes significantly different from bout 1 independent of group. #Denotes significantly different between groups compared to bout 1. Significance at the p ≤ 0.05 level.

Limb Girth

There were no differences between groups or bouts for calf girth; however, thigh girth was larger immediately after the DPFT compared with after SSRS independent of bout (F4,76 = 4.0, p = 0.005, and = 0.18).

Muscle Function

Reductions in CMJ, RSI, and MVC peaked immediately after EIMD in both bouts with the exception of MVC in the SSRS group, which reached lowest levels 24 hours after bout 1. These measures of muscle functionality progressively recovered to near baseline values with no differences between groups or bouts. Interestingly, sprint time improved (F1,19 = 8.6, p = 0.008, and = 0.31) after bout 2 independent of group (Figure 2), where recovery was greater 24, 48, and 72 hours compared with bout 1 (F4,76 = 6.2, p < 0.001, and = 0.25). Both groups improved sprint time beyond baseline measures 72 hours after EIMD in bout 2 (−1.5 ± 0.7% and −1.2 ± 0.6% for DPFT and SSRS, respectively.

Figure 2.
Figure 2.:
Sprint time in response to muscle-damaging exercise after the DPFT (n = 10) and SSRS (n = 11). Values are presented as mean ± SEM. ϕDenotes significant bout effect. *Denotes significantly different from bout 1 independent of group. Significance at the p ≤ 0.05 level.

Creatine Kinase

Circulating CK was increased and reached peak concentrations 24 hours after both bouts in both exercise groups (Figure 3). Although the SSRS group experienced higher average CK levels, this was not different from the DPFT group and CK was lower 24, 48, and 72 hours after the repeated bout compared with bout 1 independent of group (F2.0,36.4 = 5.2, p = 0.010, and = 0.23).

Figure 3.
Figure 3.:
Creatine kinase in response to muscle-damaging exercise after DPFT (n = 10) and SSRS (n = 10) groups. Values are presented as mean ± SEM. *Denotes significantly different from bout 1 independent of group. Significance at the p ≤ 0.05 level.

Discussion

This investigation was the first to examine the RBE associated with dance and repeated-sprint exercise in healthy active women. Although EIMD was evident in a repeated bout of both dance and sprint activity, this was less than the initial bout. As anticipated, there were lower levels of muscle soreness, reduced concentrations of circulating CK, and, although only evident with one performance variable, an attenuation of the detriments in muscle function with a second bout of both exercise protocols.

A reduction in soreness after the second bout of exercise has been observed in other investigations in women (5,20,23). Some authors propose that DOMS is likely related to the secondary inflammatory response (14). The increase in tissue osmotic pressure associated with inflammation results in the sensitizing of afferent nociceptive fibers thought to magnify feelings of soreness and pain (14). Therefore, the dampened DOMS reported after a subsequent bout of both exercise protocols (in addition to subjects becoming accustomed to the sensation of soreness (3)) is perhaps attributable to cellular adaptation relating to the secondary inflammatory response. Indeed, neutrophil and monocyte activation has been shown to be diminished with a subsequent bout of eccentric exercise (2). Interestingly, those completing the DPFT experienced greater reductions in DOMS in the later recovery period after the second bout. Intuitively, the habituation to dance-type activity may be responsible for an improved RBE in the DPFT group. A recent study in young women demonstrated that in comparison with a nonexercising group, muscle soreness was reduced after a repeated bout of eccentric exercise when regular training (similar to the damaging exercise) was undertaken between bouts (6). The authors suggested that the concomitant reduction in exercise-induced inflammation that they observed may largely explain this difference. These findings suggest that perhaps the continued dance training that participants completed between bouts resulted in a sport-specific adaptation in the group performing the dance-based acute bout; as indicated by the higher reduction in DOMS. Although such adaptation is plausible, because no systemic inflammatory markers were measured, this remains speculative and to be fully elucidated. In addition, a reduced inflammatory response may be merely a consequence of a reduction in the initial mechanical disruption in the repeated bout.

Thigh girth increased immediately after both bouts of the DPFT but not after SSRS. Intuitively, this might suggest a greater blood flow and/or secondary inflammatory response associated with the dance-type activity. However, as calf girth was unaffected, this is unlikely and the differences in the nature and demands of the exercise protocols are more likely responsible for the variance in muscle swelling.

The recovery of CMJ, RSI, and MVC was similar after both exercise protocols, and decrements were not mitigated by a previous bout. The decrements of these measures of muscle function were greatest immediately after exercise, with the exception of MVCs during the initial bout of SSRS, which reached lowest levels 24 hours after exercise. The MVC response was surprising, given that the combination of both muscle damage and metabolic fatigue immediately after exercise could result in the greatest decline of neuromuscular function, as demonstrated by the other functional measures. Perhaps the different exercise protocols used in the literature are responsible for this discrepancy. Although the muscles may have been put under maximum stress in the present investigation, the time under tension was far less than during traditional, isolated muscle-contraction models. As a result, the fatigue component might be less evident in these sport-specific protocols. Nonetheless, the results concur with the findings of a recent study demonstrating that well-trained subjects received no protection against decrements in CMJ and MVC after a second bout of intermittent-sprint exercise despite reduced DOMS and their familiarity with the mode of exercise (15). Arguably, these activities are frequently encountered during training and performance in the present study population. Although a homogenous population was recruited to better control for training status and free-living physical activity levels and dietary behaviors, the participants were recruited from a university dance team. Jumps and landing tasks are incorporated in most dance activities (24), and many dance movements are characterized by explosive actions (33). Because the women were physically active and regularly participating in dance, it is conceivable that the training status of subjects in this study may explain the apparent lack of an RBE in these measures. Indeed, the only measure of muscle function to recover more rapidly after the second bout was sprint time and given that the study population were less accustomed with this activity compared to the other performance measures, it is perhaps unsurprising that this was observed in both exercise groups. Moreover, it is possible that the exercise stimuli were not of an adequate intensity to elicit neural adaptations. Indeed, neural adaptations—which manifest as an increase in motor unit activation and/or increased recruitment of slow-twitch fibers to limit myofibrillar disruption—are associated with maximal-intensity contractions (10). Having said this, although arguably small, the observed performance improvement is nevertheless an important consequence of the RBE. The present study is in agreement with a number of investigations reporting that physically active or trained participants experience a RBE (8,10,11,18).

In the present investigation, a 4-week recovery period was chosen not only to maintain exercise intensity between bouts but also to control for menstrual cycle phase. Many investigations in women conduct testing during the early follicular phase where estrogen is at its lowest levels, though still higher than in men. Although this may conveniently control for hormonal effects, this period represents only a quarter of the menstrual cycle (31). The application of the results reported in such studies is therefore limited, particularly as recent evidence suggests that EIMD and recovery may differ between menstrual cycle phases (16,30). If estrogen does indeed play a role in the attenuation of muscle damage and adaptation in women, testing in the luteal phase (where estrogen is markedly elevated) may better observe these effects. Moreover, although menstrual phase in the present study was determined with participants' contraceptive use in mind, it should be noted that some forms of contraception exposes the body to synthetic forms of estrogen and therefore naturally occurring estrogen may be found in lower quantities (19). Indeed, noncontraceptive users (with potentially higher concentrations of biologically active estrogen) have been reported to receive more protection against EIMD compared with oral contraceptive users (29). Although details of contraceptive use have been provided, the lack of control of contraceptive use is a limitation of the present investigation and the reader should interpret the results with this in mind.

Some studies examining the RBE using female subjects do not report how changes in the menstrual cycle were (if at all) accounted for and many investigations using both men and women have combined sexes in treatment groups, failing to acknowledge the potential influence of sex. It is clear that although much more research is required regarding the potential influence of sex in muscle damage, recovery, and adaptation, the accurate reporting of menstrual cycle phase and contraceptive use of female participants is essential to develop our understanding. Nonetheless, the present investigation is in agreement with those who have demonstrated that muscle-damaging exercise can elicit a protective affect against a subsequent damaging exercise bout in women (5,20,23).

Practical Applications

This study aimed to investigate whether physically active women receive a protective effect against indices of EIMD after an identical repeated exposure of dance-type and repeated-sprint exercise. Increases in CK and decrements in muscle soreness and one measure of muscle function were attenuated after a second bout, indicative of an RBE. Perhaps the most interesting finding was that, although there were group divergences in thigh girth and muscle soreness, adaptation from exercise stimuli of this nature was similar. Although limitations warrant consideration (for instance, all participants were trained in dance and their contraceptive use varied), these results add to a growing body of evidence demonstrating that different exercise paradigms can elicit a protective effect against damage for subsequent bouts. Specifically, the findings enhance our understanding of the implications on recovery and adaptation in exercising women. These data have important practical application, suggesting that preconditioning with activity-specific exercise may reduce symptoms of damage and improve recovery with subsequent exposure of the same stimuli. Future research should examine the influence of interventions to further attenuate the damage response experienced after exercise in women.

Acknowledgments

The authors would like to thank the participants for generously giving their time in volunteering to take part in the study.

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Keywords:

recovery; exercise-induced muscle damage; repeated bout effect

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