Running-related muscle activation patterns and tibial acceleration across puberty

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Abstract

This study examined whether differences exist in tibial acceleration transients and electromyography (EMG) variables during running across female pubertal development. Sixty-four girls classified as pre- (n = 19), early/mid- (n = 22) and late/post-pubertal development (n = 23) ran in a laboratory whilst EMG data were recorded from quadriceps, hamstring and calf muscle groups, and acceleration transients from a triaxial accelerometer. The late/post-pubertal girls exhibited delayed vastus lateralis onset (mean difference (MD) = 0.02, 95% CI = 0.008, 0.34 ms)) compared to pre-pubertal girls, lower vastus lateralis pre-activation (MD = 7.02, 95% CI = 12.63, 1.42%) compared to early/mid-pubertal girls, and longer time to peak (TTP) anterior/posterior (A/P) tibial acceleration compared to pre-pubertal girls (MD = 0.02, 95% CI = 0.006, 0.03 s). By contrast, late/post-pubertal girls demonstrated earlier semitendinosus onset compared to both early/mid- (MD = 0.02, 95% CI = 0.03, 0.005 ms) and pre-pubertal girls (MD = 0.02, 95% CI = 0.04, 0.007 ms). No other between-group differences were found for peak A/P, vertical and TTP vertical tibial acceleration (p > 0.05). Subsequently, regression analysis revealed that EMG variables accounted for approximately 34% (R2 = 0.34) of the variance in TTP A/P tibial acceleration. These findings highlight that neuromuscular recruitment patterns and kinetics differ across female pubertal development while running and should be further explored in the context of adolescent female musculoskeletal injuries.

Introduction

Growth of the musculoskeletal system during puberty leads to adaptations in long bone, cartilage and muscle that do not occur simultaneously, and may contribute to a higher risk of musculoskeletal injury during adolescence (Faust, 1977, Tanner, 1986, Michaud et al., 2001). In fact, pubertal musculoskeletal injuries increase by approximately 10% from pre-puberty to post-puberty (Michaud et al., 2001), with overuse injuries reported to affect females more than males (Stracciolini et al., 2014). Although a causal relationship between pubertal development and overuse musculoskeletal injuries is not well established, the aforementioned studies highlight that growth-related changes, particularly during female pubertal development, may be a contributing factor.

Recently, emerging evidence has highlighted that neuromuscular and biomechanical changes begin to occur during female pubertal development (Barber-Westin et al., 2006, Myer et al., 2010, Wild et al., 2012, Wild et al., 2013b). Despite the variation in tasks evaluated across studies (i.e., running versus landing), higher external hip and knee joint moments (Wild et al., 2016, Sayer et al., 2018), decreased hamstring muscle strength (Wild et al., 2013a, Wild et al., 2013b) and delayed onset of vastus medialis activation (Wild et al., 2016) have been observed in girls at later compared to earlier stages of puberty. While these findings indicate that female pubertal development may be associated with potentially suboptimal changes in neuromuscular function, there remains a lack of substantive evidence to support these claims. Hence, further research investigating neuromuscular performance across pubertal development stages during dynamic tasks is required.

Tibial ‘shock’ and lower limb muscle activation patterns across female pubertal stages are two areas requiring further investigation. ‘Shock’ is a biomechanical term used to describe the magnitude and rate of lower extremity loading during the contact phase of dynamic tasks (Lafortune et al., 1996, Coventry et al., 2006). For example, during the early stance phase of running, the tibia undergoes a rapid ‘shock’ (typically measured by accelerometers mounted on the proximal tibia) that must be absorbed by both passive structures (i.e., soft tissues, cartilage, synovial fluid and bone) and active muscles (Mizrahi and Susak, 1982, Lafortune et al., 1996, Coventry et al., 2006). Importantly, controlled muscular contraction is the most effective way of dissipating potentially harmful tibial acceleration transients moving up the kinetic chain (Mizrahi and Susak, 1982). Support for this notion is provided from novel neuromusculoskeletal modelling research by Saxby and colleagues (Saxby et al., 2016a, Saxby et al., 2016b), in which the surrounding lower limb musculature was shown to contribute to 80% of tibiofemoral joint loads while running, with the remaining 20% due to external forces. Hence, it stands to reason that muscle activation patterns measured via electromyography (EMG) may play an important role in regulating the magnitude and timing of tibial ‘shock’ during running.

No previous studies have examined tibial ‘shock’ and associated muscle activation patterns during running across the stages of female pubertal development. However, Dufek and colleagues (2008) reported that running-related impact attenuation measured using a uniaxial accelerometer was approximately 40% lower in pubertal compared to pre-pubertal girls (Dufek et al., 2008). Whilst these findings provide some evidence that puberty may influence tibial acceleration while running, this study only measured a single, undefined plane and failed to implement appropriate pubertal classification methods (Tanner et al., 1976, Tanner, 1986). Other studies have investigated the influence of female development on external knee joint moments during running and landing, and have reported higher joint moments at latter stages of puberty (Wild et al., 2016, Sayer et al., 2018). For instance, we recently reported that girls at late/post-pubertal development run with approximately 12–18% higher external knee extension moments than their pubertal and pre-pubertal counterparts (Sayer et al., 2018). Moreover, other research has found that girls increase their landing-related vertical ground reaction force (GRF) as they progress through puberty (Swartz et al., 2005, Hewett et al., 2006, Quatman et al., 2006). Given that vertical and sagittal plane GRFs are major contributors to joint moments that may contribute to knee injury (Pairot-de-Fontenay et al., 2019), and the magnitude and timing of tibial acceleration transients are closely associated with the peak GRF’s (Elvin et al., 2007, Crowell et al., 2010), it is plausible that pubertal differences in running-related tibial ‘shock’ may also exist.

To date, only one study has investigated neuromuscular recruitment patterns across the stages of female pubertal development. Wild et al. (2016) reported delayed onset of vastus medialis, but no difference in rectus femoris, hamstrings, medial gastrocnemius and tibialis anterior muscles during single limb landing as girls progressed through pubertal development. Although these findings may suggest muscle activation patterns do not change across female pubertal development, this study did not investigate distinct pubertal groups (i.e., pre, mid and late/post-pubertal stages), and used a landing task rather than running. Therefore, a more comprehensive analysis of running-related muscle recruitment strategies is needed to determine if differences exist between pubertal groups and, given the link between muscle recruitment and dissipation of tibial acceleration transients (Mizrahi and Susak, 1982, Lafortune et al., 1996, Coventry et al., 2006), to establish if muscle activation patterns contribute to any differences in the timing and magnitude of peak tibial acceleration.

The primary aim of this study was to examine whether girls classified as pre-pubertal, early/mid-pubertal and late/post-pubertal exhibit differences in lower limb muscle activation patterns (i.e., onset and amplitude) and the timing and magnitude of peak anterior and vertical tibial acceleration transients during barefoot running. The secondary aim was to explore relationships between measures of muscle activation and tibial acceleration adjusted for pubertal development stage. Our primary hypothesis was that girls in the late/post-pubertal group would exhibit both increased anterior and vertical peak tibial acceleration, as well as delayed onset and lower amplitude of quadriceps, hamstrings and gastrocnemius muscles compared to early/mid- and pre-pubertal girls. Our secondary hypothesis was that an inverse relationship would exist between the onset and amplitude of lower limb muscle activation and the magnitude and time to peak (TTP) of anterior and vertical peak tibial acceleration as pubertal stage advances.

Section snippets

Study population

Sixty-four recreationally active females were recruited from the student body at the University of Melbourne, local schools, community centres and sporting facilities. Inclusion criteria were: (i) aged 7–25 years old; (ii) participating in regular physical activity (>30 min of moderate and/or vigorous activities daily); and, (iii) healthy weight (body mass index < 30 kg/m2). Exclusion criteria were: (i) history of lower limb injury, knee pain or medical condition affecting walking, running and

Results

Demographic characteristics for the cohort, according to stage of puberty, are presented in Table 1. As expected, differences were found for age, mass and height (p < 0.05), whereby the late/post-pubertal girls were taller, heavier and older than their early/mid- and pre-pubertal counterparts (p < 0.05, Table 1). There were no differences in estradiol concentration between the three groups. (p > 0.05).

Discussion

Female pubertal development is associated with neuromuscular and biomechanical changes (Barber-Westin et al., 2006, Myer et al., 2010, Wild et al., 2012, Wild et al., 2013b) that are postulated to contribute to the higher incidence of musculoskeletal injury amongst pubescent girls and young women (Michaud et al., 2001). Given the lack of studies reporting the association between pubertal development, muscle activation and tibial acceleration during running, the present study provides further

Conclusion

This study reports altered muscle activation patterns and a longer TTP A/P acceleration in girls at the latter stages of female pubertal development. Latter stages of pubertal development and earlier ST onset were predictors of a longer TTP A/P acceleration. It is not known if these differences in muscle activation patterns and TTP A/P acceleration have implications for musculoskeletal running injuries which future prospective studies should examine.

Declaration of Competing Interest

All authors declare no conflict of interest and at no stage did any of funding organizations influence study design, data collection or analysis of results.

Acknowledgements

This research was supported by an Australian Research Council (ARC) linkage grant (LP150101041) in conjunction with Asics Oceania Pty Ltd. TS was supported by an NHMRC Australian Government Research Training Program Scholarship (APP1075881). KLB is the recipient of a NHMRC Principal Research Fellowship (#1058440). RSH is funded by an ARC Future Fellowship (FT130100175). ALB is the recipient of a NHMRC Career Development Fellowship (#1053521). Thank you to Karine Fortin for her incredible effort

Dr. Tim Sayer is a Lecturer in Physiotherapy at The University of Melbourne, Australia and a Clinical Director at Melbourne CBD Physiotherapy. His educational background includes a Bachelor of Science (Hons), Doctor of Physiotherapy (DPT) and Doctor of Philosophy (PhD) from the University of Melbourne, Australia. His research has focussed on the effect of female pubertal development on running and landing-related lower limb biomechanics, which subsequently may lead to adolescent knee injuries.

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