Superimposing hip extension on knee flexion evokes higher activation in biceps femoris than knee flexion alone

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Abstract

Hamstring muscle function during knee flexion has been linked to hamstring injury and performance. However, it is unclear whether knee flexion alone (KF) requires similar hamstring electromyography (EMG) activity pattern to simultaneous hip extension and knee flexion (HE-KF), a combination that occurs in the late swing phase of sprinting. This study examined whether HE-KF maximal voluntary isometric contraction (MVIC) evokes higher (EMG) activity in biceps femoris long head (BFlh) and semitendinosus (ST) than KF alone. Effects of shank rotation angles were also tested. Twenty-one males performed the above-mentioned MVICs while EMG activity was measured along ST and BFlh. Conditions were compared using a one-way mixed functional ANOVA model under a fully Bayesian framework. Higher EMG activity was found in HE-KF in all shank rotation positions than in KF in the middle region of BFlh (highest in the 9th channel, by 0.022 mV [95%CrI 0.014 to 0.030] in neutral shank position). For ST, this was only observed in the neutral shank position and in the most proximal channel (by 0.013 mV [95%CrI 0.001 to 0.025]). We observed muscle- and region-specific responses to HE-KF. Future studies should examine whether hamstring activation in this task is related to injury risk and sprint performance.

Introduction

The hamstring muscle group is composed of three biarticular muscles, the biceps femoris long head (BFlh), the semitendinosus (ST), and the semimembranosus, as well as one mono-articular muscle, the biceps femoris short head. Besides their function as knee flexors, the bi-articular hamstrings are also strong hip extensors and substantially contribute to horizontal ground reaction force in acceleration running, which is essential for sprint performance (Morin et al., 2015). Hip extension and knee flexion are simultaneously required from the hamstrings in the late swing phase of high-speed running (Chumanov et al., 2011), where these muscles are highly activated (Hegyi et al., 2019b, Higashihara et al., 2010, Yu et al., 2008) and are also vulnerable to strain injury. As running speed increases, electromyography (EMG) activity also increases. This results in similar peak muscle lengths in the highly vulnerable BFlh in the late swing phase (Chumanov et al., 2007) across running speeds, which may be protective against strain injury (Garrett et al., 1987). Therefore, examining hamstring EMG activity is important both from an athletic performance and an injury risk perspective.

EMG activity of hamstring muscles in the late swing of high-speed running can exceed that recorded during a maximal isometric knee flexion (KF) contraction (Hegyi et al., 2019b, Kyröläinen et al., 2005). Higher EMG activity in high-speed running could be due to the fact that the hamstrings are simultaneously generating moments about the hip and knee in the late swing phase (Chumanov et al., 2011), which is not accounted for in traditional maximal KF contractions. It has been suggested that hamstring fascicles act isometrically in late swing of sprinting (Van Hooren and Bosch, 2017). However, there is a lack of experimental evidence about fascicle mechanics in sprinting, so the effect of hip extension should be tested in isolated conditions.

At present, it is unclear whether adding hip extension onto knee flexion would similarly affect the activation of different hamstring muscles. For example, based on some studies using muscle functional magnetic resonance imaging (mfMRI) to examine metabolic activation, Bourne et al. (2018) suggested that BFlh-to-ST activation ratio is higher in hip extension than in knee flexion-based exercises. Accordingly, larger BFlh hypertrophy has been observed after hip extension training on a roman chair than after knee-oriented Nordic hamstring training (Bourne et al., 2017a). These exercises also show preferential activation of the BFlh and ST muscles, respectively, when measured with traditional EMG (Bourne et al., 2017b) or high-density EMG (Hegyi et al., 2019a, Hegyi et al., 2018). Another study showed that hip extension increases the activation of BFlh relative to ST in the Nordic hamstring exercise, at least at a near-fully extended knee angle (Hegyi et al., 2019c). These findings may imply that superimposing hip extension on knee flexion would increase BFlh activation preferentially. However, other studies have reported no clear differences between hip- and knee-oriented exercises in the intermuscular distribution of EMG activity (Bourne et al., 2017b, Hegyi et al., 2019a, McAllister et al., 2014, Tsaklis et al., 2015). Additionally, of all hamstring muscles, the largest difference in muscle size between sprinters and non-sprinters is in ST (Handsfield et al., 2017, Miller et al., 2020), and it is currently unclear whether this is a result of adaptation to sprinting. If so, superimposing hip extension on knee flexion might be expected to target ST muscle rather than BFlh. Thus, superimposing hip extension on knee flexion may increase the activation of either or both of the BFlh and ST.

Shank rotation during knee flexion is another factor that may alter the interplay between hamstring muscles. EMG signals recorded during isometric knee flexion show that the medial (semimembranosus and ST) and lateral hamstrings (BFlh and biceps femoris short head) can be preferentially activated by adjusting shank rotation (Jónasson et al., 2016). Of the medial hamstrings, ST seems to be more sensitive to shank rotation than semimembranosus (Mohamed et al., 2003). Furthermore, during exercises requiring submaximal hamstring excitation, external and internal rotation of the leg increases the relative activity of the lateral and medial hamstrings, respectively (Beuchat and Maffiuletti, 2019, Lynn and Costigan, 2009).

Based on the above observations, it seems plausible that some MVIC variations, including hip extension and/or shank rotation, evoke higher maximal voluntary isometric EMG activity in the BFlh and ST muscles than knee flexion alone. In this study, we hypothesised that hip extension superimposed on knee flexion MVIC would result in higher hamstring EMG activity than during knee flexion only MVIC. We assumed that internal shank rotation would further increase ST activity, while external rotation would further increase BFlh activity. According to recent studies, proximo-distal distribution of EMG activity in these muscles is heterogeneous in several exercises (Hegyi et al., 2019a, Hegyi et al., 2018, Schoenfeld et al., 2015), as well as in running (Hegyi et al., 2019b). This suggests that the examined MVIC variations may alter muscle activation in certain muscle regions only, which was also tested in this study.

Section snippets

Participants

Twenty-one young male university students (age 26.3 ± 4.2 yrs, height 1.86 ± 0.04 m; body mass 85.9 ± 10.8 kg; mean ± SD) who were engaged in strength training and recreational running on a weekly basis participated in this study. Exclusion criteria were known history of hamstring strain, previous anterior cruciate ligament injury, and any current musculoskeletal or metabolic disorder. All participants provided written informed consent for this study, which was approved by the ethics committee

Electromyography activity

HD-EMG data from ST and BFlh were treated as one-dimensional spatial functional data, and each reflected an outcome variable. The dependent variable was the MVIC conditions (9 levels). Let yijx denote the jth functional observation in the ith MVIC condition, where a one-way mixed functional ANOVA model with a random subject-intercept of the following form was fitted:yijx=μx+αix+μjx+eijxwhere μx is the grand mean function,αix is the ith level main effect function, μjx is the random intercept for

Fatigue

There were no significant differences in EMG activity in ST or BFlh during KF at the start and end of session A or B (Fig. 2). However, there was a reduction in knee flexor torque at the end compared to the start of session A by −7.8 Nm (95%CrI −15.3 to −0.3), whereas the change in session B of −5.0 Nm (95%CrI −12.6 to 2.7) was not statistically significant.

Knee flexion vs other MVICs

Fig. 3 and Fig. 4 represent the EMG activity of ST and BFlh, respectively. Fig. 5 shows the pairwise differences between KF and each of the

Discussion

This study confirmed our assumption that hip extension superimposed on knee flexion (HE-KF) evokes higher BFlh EMG activity than knee flexion alone (KF) during a maximal voluntary isometric contraction. This difference was most pronounced in the mid-region of BFlh. However, a superior effect of hip extension on knee flexion was not evident in ST, except in the most proximal channel. Differences between internal and external rotation were observed mainly in the proximal (KF) or middle (HE-KF)

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

András Hegyi is a post-doctoral research fellow at the University of Nantes, France. He received his MSc in kinesiology from the Semmelweis University, Hungary in 2013 then received a biomechanics PhD from the University of Jyväskylä, Finland in 2020. His research interests lie in the area of motor control and muscle-tendon function in humans. His current research focuses on sprint performance and its association with muscle size, architecture, strength, and coordination of the lower extremity

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  • Cited by (0)

    András Hegyi is a post-doctoral research fellow at the University of Nantes, France. He received his MSc in kinesiology from the Semmelweis University, Hungary in 2013 then received a biomechanics PhD from the University of Jyväskylä, Finland in 2020. His research interests lie in the area of motor control and muscle-tendon function in humans. His current research focuses on sprint performance and its association with muscle size, architecture, strength, and coordination of the lower extremity in elite athletes from sprint-based sports.

    Daniel Csala is a PhD student at the University of Physical Education, Hungary and a sport scientist at the Ferencvárosi TC football club. He received his MSc in kinesiology from the University of Physical Education, Hungary in 2019. He is interested in hamstring muscle function and neuromuscular fatigue in football players.

    Bálint Kovács is a PhD student at the University of Physical Education, Hungary. He received his MSc in PE and adaptive PE teaching from the University of Physical Education, Hungary in 2015 then started PhD in biomechanics at the University of Physical Education, Hungary. His current research focuses on the impact of lower leg morphology and function on running economy.

    Annamária Péter is a post-doctoral researcher at the University of Jyväskylä, Finland. She received her MSc in kinesiology in Hungary in 2013 from the Semmelweis University then her PhD in 2019 from the University of Jyväskylä. Her research interests include gait analysis, lower leg muscle activation and muscle-tendon interactions in healthy and clinical conditions such as Achilles tendon rupture.

    Dr Bernard Liew is a Physiotherapist, where he received a PhD in physiotherapy from Curtin University. He currently is a lecturer in Biomechanics at the School of Sport, Rehabilitation and Exercise Sciences, University of Essex, United Kingdom. His research currently lies at the intersection of musculoskeletal pain, movement science, and applied statistical/machine learning.

    Yu (Ryan) Yue is an Associate Professor at Baruch College, The City University of New York. He received his BSc in Statistics from Shanghai University of Finance and Economics in 2003, then received a PhD in Statistics from University of Missouri in 2008. His research has been focusing on Bayesian hierarchical modeling, spatial smoothing techniques, functional neuroimaging data analysis, and quantile regression.

    Taija Finni is a professor of kinesiology and vice dean at the Faculty of Sport and Health Sciences, University of Jyväskylä. She completed PhD in biomechanics at the University of Jyväskylä in 2001 and post-doctoral studies at the University of California. Prof Finni’s research ranges from basic neuromuscular function to translational research related to physical activity and sedentary behavior (OpenKin, CHIPASE). Her ongoing projects relate to muscle-tendon function in healthy and injured people (UNRESAT) and training adaptations of children with cerebral palsy (EXECP), for example. She has over 100 publications and has supervised 11 PhD students to completion and has 6 PhD students currently under supervision. She serves as a senior section editor in Scandinavian Journal of Medicine and Science in Sports and is an active member of the International Society of Biomechanics and the European College of Sport Science. Homepage: https://staff.jyu.fi/Members/finni.

    József Tihanyi is a professor emeritus and Head of the Doctoral Council at the University of Physical Education, Hungary. He graduated from the Hungarian University of Physical Education in 1970 where he was the rector between 1994 and 2001. He has more than 200 publications in the fields of musculuskeletal biomechanics, strength traning and exercise-induced muscle damage. Sixteen of his PhD students graduated and there are three PhD students currently under his supervision. He has been visiting professor at several universities including Zagreb University, Tor Vergata University (Rome), Claude Bernard University (Lyon), Kuwait University and L’Aquila University. Throughout his career he has been a member of the editorial board at several high-impact scientific journals. He was also a Hungarian champion and record holder in high jump and the coach for successful high jumpers.

    Neil Cronin is currently an Associate Professor of biomechanics at the University of Jyväskylä, Finland. He received his PhD from Aalborg University, Denmark, in 2010. He then worked as a post-doctoral researcher at Griffith University, Australia, before returning to Jyväskylä in 2011. He also currently holds adjunct or honorary positions at four institutes, in Finland, the UK and Australia. His main research interests include musculoskeletal imaging, human locomotion, and applications of artificial intelligence to the sport and health domains.

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