European Journal of Applied Physiology (2019) 119:73–83 https://doi.org/10.1007/s00421-018-4000-2 ORIGINAL ARTICLE Antagonist muscle architecture and aponeurosis/tendon strain of biceps femoris long head during maximal isometric efforts Eleftherios Kellis1 Received: 11 June 2018 / Accepted: 25 September 2018 / Published online: 3 October 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Introduction Examination of the mechanical behavior of the hamstrings when acting as antagonists provides information about loading of this muscle group and its role for joint stability during forceful quadriceps contractions. The aim of this study was to quantify biceps femoris long head fascicle length (FL), angle of pennation (PA) and distal tendon/aponeurosis strain during maximum voluntary contraction efforts of the knee extensors using real-time ultrasound. Methods Fourteen participants performed passive joint movements and maximum voluntary knee extension and flexion efforts of the knee flexors at 0°, 45° and 90° of knee flexion. An ultrasound probe was used to visualize FL, PA and tendon/ aponeurosis strain from the distal part of the muscle. Results Two-way analysis of variance designs indicated that: (a) antagonist BFlh tendon/aponeurosis strain increased sig- nificantly up to 2.77 ± 1.25% relative to rest (p < 0.05). The FL increased non-significantly (2.86 ± 6.81%) while the PA was unaltered during isometric MVC efforts of the knee extensors (p > 0.05) (b) FL, PA and tendon/aponeurosis strain of the BFlh when acting as antagonist were not significantly affected by knee joint angular position (p > 0.05). Conclusions Antagonist hamstring function takes the form of a lengthened tendon/aponeurosis, no fascicle shortening and submaximal neural activation. Future research could examine whether exercise interventions that aim to alter tendon/ aponeurosis mechanical properties of the hamstrings when acting as antagonists are beneficial for injury prevention and rehabilitation. Keywords Hamstrings · Architecture · Ultrasound · Muscle mechanics · Agonist and antagonist · EMG activity · Isometric contraction Abbreviations Introduction BFlh Biceps femoris long head EMG Electomyography Hamstring muscle function is important for the perfor- FL Fascicle length mance of demanding skills, such as high-intensity sprinting FLe Effective fascicle length or changes in direction (Thelen et al. 2005; Opar and Ser- MVC Maximum voluntary contraction pell 2014). Alterations in hamstring activation during late LMTU Muscle–tendon unit length swing phase of running may be critical for hamstring injury PA Pennation angle (Timmins et al. 2014). Early and sufficient activation of the RMS Root mean square hamstrings prior to ground contact is considered important US Ultrasound for controlling knee joint stability (Gazendam and Hof 2007; Kellis and Liassou 2009). The function of the hamstrings as antagonists during maximal efforts of the knee extensors has been extensively Communicated by Toshio Moritani. examined using electromyography (EMG) (Baratta et al. 1988; Kellis and Baltzopoulos 1997). These studies have * Eleftherios Kellis [email protected] shown that antagonist activation during isometric and isoki- netic tests can reach 15% of maximum voluntary contraction 1 Laboratory of Neuromechanics, Department of Physical (MVC) value (Baratta et al. 1988; Kellis and Baltzopoulos Education and Sport Sciences at Serres, Aristotle University 1997; Kellis et al. 2014). Using EMG-based models, the of Thessaloniki, TEFAA Serres, Serres 62100, Greece Vol.:(0123456789)1 3 74 European Journal of Applied Physiology (2019) 119:73–83 predicted antagonist torque of the hamstrings could account Examination of the mechanical behavior of the muscle for approximately 5–13% of the torque recorded by the isoki- fascicles and the tendinous tissue of the hamstrings may netic dynamometer (Kellis and Baltzopoulos 1997; Kellis provide interesting information regarding the mechanisms 2003; Kellis and Katis 2008). However, the EMG signal of force production of this muscle when acting as antagonist. provides an indication of neural activation of the muscle and This could be useful for the understanding of the mechani- cannot describe the role of the non-contractile components. cal loading of the hamstrings during maximal contractions Like any striated muscle, the force exerted by the ham- of the quadriceps and the role of this load for knee joint strings is a result of both contractile and passive (in-series stability. Consequently, the purpose of this study was to and parallel elastic) components of the muscle. During quantify BFlh muscle and tendon/aponeurosis architecture an isometric knee flexion contraction, the biceps femoris during agonist and antagonist contractions. Based on the long head (BFlh) muscle fascicles shorten by as much as reviewed literature, the following hypotheses were tested: 20% (Bennett et al. 2014) while distal tendon/aponeurosis (a) that FL of the BFlh would increase while PA would be lengthens up to 7% (Kellis 2016). These data, however, may unaltered during antagonist contractions, (b) antagonist ten- not apply to conditions where the muscle acts as antago- don/aponeurosis strain would increase from rest to MVC, nist, because in the latter condition, the neural activation is and (c) that FL, PA and tendon/aponeurosis strain of the submaximal and the muscle–tendon unit may lengthen due antagonist muscle contractions would differ between joint to maximum force exertion by the agonist muscle (quadri- angular positions tests. ceps) (Simoneau et al. 2012). Consequently, it is possible that when acting as antagonist, muscle fascicles and tendon/ aponeurosis show a different mechanical behavior from the Methods one predicted based on corresponding agonist contraction data. Participants The mechanics of antagonist muscle co-contraction have received less attention in the literature (Simoneau et al. 2012; A total of 14 males (age 20.1 ± 0.3 years; mass 81.5 ± 2.3 kg; Raiteri et al. 2015). Particularly, Simoneau et al. (2012) height 1.77 ± 0.02 m) volunteered to participate in this study found that when acting as antagonists, the fascicle length after signing written informed consent. The participants (FL) of the gastrocnemius remained relatively unchanged were healthy, and they had no injury of the lower limbs while the tibialis anterior FL increased approximately by including history of hamstring strain or any other muscle or 5%. Nevertheless, at the same level of activation, the FL ligamentous injury of the knee. The participants were physi- was greater and pennation angle (PA) was smaller, during cally active, but they did not engage in a specific sport or antagonist than during agonist contractions. This was attrib- exercise program during the measurement period. The pro- uted to a change in joint position which increased FL and cedures are confirmed with the Declaration of Helsinki and cancelled fascicle shortening when the muscle co-contracts were approved by the University ethics review committee. (Simoneau et al. 2012). This was confirmed by Raiteri et al. (2015) who reported insignificant changes in FL of ankle Procedure muscles when acting as antagonists. To our knowledge, the changes in muscle architecture and tendon strain when the The tests were performed on a Cybex (Humac Norm, CSMI, hamstrings function as antagonists are unknown. MA, USA) dynamometer with the subject in the prone posi- Τhe contribution of the tendon and muscle to the mechan- tion. The axis of rotation of the dynamometer was carefully ical properties of the muscle–tendon unit varies depending aligned with the approximate center of rotation of the knee, on the changes in initial length (Herbert and Crosbie 1997; on the posterior aspect of the lateral femoral condyle. Axis Herbert et al. 2002; Hoang et al. 2007; Kwah et al. 2012). alignment was checked both at rest and maximum contrac- Antagonist hamstring muscle activation and predicted tions to reduce errors occurring due to joint movement. A moment of force vary with joint angle, being greater near twin-axis goniometer (Model TSD 130B, Biopac Systems, knee extension than more flexed knee joint angles (Kel- Inc., Goleta, CA, USA) was used to record knee angular lis and Baltzopoulos 1997; Kellis 2003; Kellis and Katis position (0° = full knee extension). The goniometry signal 2008). In addition, changes in neuromuscular properties of was fed through BNC connectors (Model CLB107, Biopac the muscle during isometric contractions may depend on the Systems) to a 12-bit analog-to-digital converter sampling initial muscle length (Muraoka et al. 2004) and this effect at a rate of 1000 Hz per channel using the Acknowledge differs between the hamstrings and the quadriceps (Hannah (version 3.9.1, Biopac Systems) software. Ultrasonic images et al. 2014). Consequently, during agonist contractions of from the BFlh were recorded using an ultrasonic appara- the quadriceps, a different response of BFlh may be expected tus (SSD-3500, ALOKA, Japan) with an electronic linear than when acting as agonist muscle itself. array probe of 10 MHz wave frequency and a length of 6 cm. 1 3 European Journal of Applied Physiology (2019) 119:73–83 75 Dynamometer torque and knee joint angular position were the position was marked on the skin. This location allowed simultaneously recorded at 1000 Hz. The video-capturing visualization of the most distal fascicles and intermediate module of the system software allowed simultaneous record- tendon of the BFlh. An echo absorptive marker was placed ing of the ultrasound video images at a rate of 30 Hz. in the US field of view such that any random movement of The EMG signal from the BFlh was collected using a pair the probe is recorded. Ultrasound video footages were auto- of bipolar bar surface electrodes (inter-electrode distance matically stored in digital format by the software. 1 cm, TSD 150B, Biopac System Inc., Goleta, CA, USA) In each video ultrasound footage, using a video-based which were positioned on the BFlh muscle belly, proximally software (Max Traq Lite version 2.09, Innovision Systems, to the US probe. The skin was shaved and cleaned with alco- Inc., Columbiaville, Mich.