- Email: [email protected]
Effects of submaximal and maximal long-lasting contractions on the compliance of vastus lateralis tendon and aponeurosis in vivo
Available online at www.sciencedirect.com
Journal of Electromyography and Kinesiology 19 (2009) 476–483 www.elsevier.com/locate/jelekin
Effects of submaximal and maximal long-lasting contractions on the compliance of vastus lateralis tendon and aponeurosis in vivo Anne Charlotte Ullrich a
a,b
, Lida Mademli a, Adamantios Arampatzis
a,*
Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Carl-Diem-Weg 6, 50933 Cologne, Germany b Department II of Anatomy, Medical Faculty, University of Cologne, Joseph-Stelzmann-str. 9, 50931 Cologne, Germany Received 11 August 2006; received in revised form 24 August 2007; accepted 19 October 2007
Abstract The present study investigated the effects of submaximal sustained and maximal repetitive contractions on the compliance of human vastus lateralis (VL) tendon and aponeurosis in vivo using two different fatiguing protocols. Twelve male subjects performed three maximum voluntary isometric contractions (MVC) of the knee extensors before and after two fatiguing protocols on a dynamometer. The first fatiguing protocol consisted of a long-lasting sustained isometric knee extension contraction at 25% MVC until failure (inability to hold the defined load). The second fatiguing protocol included long-lasting isokinetic (90/s) knee extension contractions, where maximum moment was exerted and failure was proclaimed when this value fell below 70% of unfatigued maximum isokinetic moment. Ultrasonography was used to determine the elongation and strain of the VL tendon and aponeurosis. Muscle fatigue was indicated by a significant decrease in maximum resultant knee extension moment (p < 0.05) observed during the MVCs after both long-lasting contractions. No significant (p > 0.05) differences in elongation and strain of the VL tendon and aponeurosis were found, when compared every 300 N (tendon force) before and after the fatiguing protocols. The present data indicate, that the VL tendon and aponeurosis in vivo do not suffer from changes in the compliance neither after long-lasting static mechanical loading (strain 3.2%) nor after long-lasting cyclic mechanical loading (strain 6.2–5.5%). 2007 Elsevier Ltd. All rights reserved. Keywords: Fatigue; Tendon compliance; Knee extension; Ultrasonography
1. Introduction Previous studies in vitro reported an alteration of tendon mechanical properties after cyclic loading at low strain values (Rigby, 1964; Schatzmann et al., 1998), suggesting that tendon became less compliant, due to a change in the rest length. Conversely, Kubo et al. (2001a,b) showed in vivo that the tendon compliance increased after repetitive longlasting contractions at high and low force production levels. Tendons show visco-elastic and plastic mechanical behaviour (Ettema, 1998; Rigby et al., 1959). Ettema (1998) distinguished between (a) pure elastic behaviour, independent of any long term changes in the tissue, (b) slow viscous behav*
Corresponding author. Fax: +49 221 4971598. E-mail address: [email protected] (A. Arampatzis).
1050-6411/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2007.10.008
iour, characterised by slow restoration of the specimen to its slack length and (c) plastic deformation of a tissue. Abrahams (1967) found in vitro that ‘‘residual strain’’, only appears if tendon strain increases into the ‘‘final’’ region of the stress–strain curve. This region commences beyond 4% tendon strain (Abrahams, 1967). In vitro (De Zee et al., 2000; De Zee and Voigt, 2001) and in situ (Ettema, 1997) studies reported that after submaximal repetitive contractions provoking tendon strain beneath this level, tendons were not subjected to any change in the compliance that is relevant for muscle function. This result was confirmed in vivo, certifying that submaximal fatiguing contractions had no effect on tendon compliance (Mademli et al., 2006). Contrary to this, in vitro studies (Wang et al., 1995; Wang and Ker, 1995) applying tendon strain beyond 2– 4%, reported changes in mechanical (i.e. compliance) and
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
in structural properties (i.e. wave form of the collagen fibres) of the tendon and aponeurosis. As in vitro results do not totally reflect in vivo conditions (Harris et al., 1966; Viidik, 1973), there is a deficiency in the knowledge of the effect of high strain repetitive exercises and further differences between long-lasting low and high strain exercises on the mechanical properties of the tendon and aponeurosis in vivo. Any change in tendon compliance would affect the muscle force generating potential due to force–length (Alexander and Bennet-Clark, 1977) and force–velocity relationships (Alexander, 2002; Bobbert, 2001). Furthermore changes in the compliance of tendon and aponeurosis during repetitive long duration contractions like running and cycling might affect the safety factor of the tendon and with this its injury risk. Therefore we examined the effects of submaximal and maximal long-lasting mechanical loading on the compliance of vastus lateralis tendon and aponeurosis in vivo, using a sustained isometric and a repetitive isokinetic fatiguing protocol. We hypothesise that changes in the compliance of tendon and aponeurosis in vivo are negligible after a sustained long-lasting submaximal contraction, inducing low strain located within the toe-region of the stress–strain curve. Furthermore we hypothesise that the compliance of the tendon and aponeurosis will be affected after repetitive long-lasting maximal contractions, inducing strain values higher than 4%. 2. Methods 2.1. Experimental protocol Twelve male endurance-trained subjects (cyclists) participated in the study (age: 25 ± 3 years, body mass: 72.3 ± 4.7 kg and body height: 179.9 ± 6.4 cm) after giving their informed consent
477
in compliance with the rules of the local scientific board. None of the subjects had suffered a neuromuscular or musculoskeletal injury within one year prior to the experiment. The subjects were seated on a dynamometer (Biodex-System3, Biodex Medical Systems Inc., USA) with the hip at 140 and their left leg at 100 knee angle respectively. Approximately in this position maximum knee extension moments are achieved (Herzog and Ter Keurs, 1988; Herzog et al., 1990). For warm-up the subjects exerted five submaximal and three maximum voluntary isometric contractions within 2–3 min. After warm-up the experimental protocol started (Fig. 1). The subjects performed an unfatigued maximum voluntary isometric knee extension contraction (MVC-U) lasting 4–5 s. To assist the subjects in holding the moment-plateau, real time visual feedback of the exerted moment was given. Then the subjects performed ten isokinetic contractions at 90/s in a range of motion of 90–180 knee angle. The subjects were instructed to perform the first five contractions submaximally with progressively increasing force in order to perform five maximal contractions in the end. The greatest moment value was considered the maximum isokinetic moment. Real time visual feedback of the exerted moment was also given during these contractions. The first fatiguing protocol (fatigue 1) consisted of a sustained submaximal isometric contraction in the same position as during the MVC-U (knee angle: 100, hip angle: 140). The 25% level of the MVC-U was displayed on the feedback monitor as target. The subjects were instructed to match the displayed lines on the monitor, representing their own and the target moment. Failure was set to be the inability to hold the defined load for more than 3 s despite strong verbal encouragement by the investigators. Between 1.5 and 2 min after task failure a second isometric MVC at 100 knee and 140 hip angle was performed (MVC-F1). After 15 min recovery the maximal fatiguing trial was started (fatigue 2). The subjects had to perform repetitive isokinetic knee extension contractions (knee angle 90–180, hip angle 140) with an angular velocity of 90/s, where maximum moment was exerted. The pre-exercise unfatigued maximum isokinetic moment was set as target and displayed as a red mark on the screen. Seventy percent
Fig. 1. The experimental set-up consisted of a warm-up period, three maximum voluntary knee extension contractions (MVC) and two fatiguing tasks: (a) a submaximal sustained isometric knee extension contraction at 25% of MVC-U until failure and (b) repetitive isokinetic knee extension contractions, where maximum moment was exerted and fatigue was proclaimed when this value fell below 70% of the unfatigued maximum isokinetic moment. The unfatigued maximum isokinetic moment was defined by the greatest moment value achieved during five maximal isokinetic contractions.
478
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
of this moment was also displayed on the screen to mark the instant of task failure. When the subjects failed to produce more than 70% of this unfatigued maximum isokinetic moment in three sequential trials, fatigue was declared. The subjects were able to observe their exerted moment on the monitor and were verbally encouraged to achieve maximum force and longer endurance times. Again 1.5– 2 min after task failure a third MVC was performed (MVC-F2). 2.2. Measurement of the knee joint moment The moments were measured using the Biodex-dynamometer. Prior to each contraction the knee joint axis and the axis of the dynamometer were carefully aligned. The axis of rotation of the knee joint was defined to be parallel to the axis of the dynamometer and passing through the midpoint of the line connecting the lateral and medial femoral condyles. Although effort was made to limit any joint movement during the contraction, the knee joint changed its position. This shift significantly influences the resultant joint moments (Arampatzis et al., 2004). To account for this, the resultant moments around the knee joint were calculated through inverse dynamics (Arampatzis et al., 2004). The Vicon 624 System (Vicon motion Systems, United Kingdom) recorded kinematic data using eight cameras operating at 120 Hz. Reflective markers were placed on the following body landmarks: lateral and medial malleolus, most prominent points of the lateral and medial femoral condyles, trochanter major, crista iliaca on the tuberclum iliacum, axis of the dynamometer and the lever arm of the dynamometer. The correction of the measured moment due to gravitational forces was determined for all subjects by obtaining a passive knee joint rotation before each knee extension contraction. The exact method for calculating the resultant joint moment has been described previously (Arampatzis et al., 2004). The influence of the simultaneous activation of the hamstrings (HA), working as antagonists during the knee extension contraction on the resultant joint moment, was taken into account by establishing a relationship between HA EMG-amplitude and exerted moment, whilst working as agonists. The moment generated due to antagonistic coactivation during the knee extension effort was quantified by assuming a linear relationship between surface EMG amplitude of the knee flexor muscles and moment (Baratta et al., 1988) measured during one relaxed condition and two different submaximal knee flexion contractions (Mademli et al., 2004). The coactivation of vastus lateralis (VL), vastus medialis (VM) and rectus femoris (RF) during submaximal knee flexion was within the noise level of the EMG signal, indicating no coactivation during the knee flexion contractions. In the following text the maximum knee joint moments will include the effect of knee joint axis alteration relative to the dynamometer axis, the effect of the gravitational force, and the effect of the hamstring coactivation. The patellar tendon force (PTF) during the contraction was calculated by dividing the knee joint moment by the tendon moment arm. The lever arm of the patellar tendon was calculated as a function of the knee angle using the data provided by Herzog and Read (1993). The kinematic data were interpolated using quintic splines to achieve a common frequency with the moment and EMG signals (3000 Hz). 2.3. Measurement of the EMG-activity The myoelectric activities of the VL, VM, RF and HA muscles were recorded by means of preamplified (bandwidth 10–500 Hz) bipolar EMG leadoffs. Adhesive surface electrodes (Ag/AgCl)
with an electrolytic gel interface and a pickup surface of 0.8 cm2 were positioned above the midpoint of the muscle belly (2 cm inter-electrode distance). Care was taken above the VL muscle belly to avoid interference of the electrodes and the ultrasound probe. The skin was carefully prepared (shaved and cleaned with alcohol) to reduce skin impedance. The electrodes were further secured to the skin with elastic tape together with the preamplifier to reduce motion artefacts. Before the experiment started, the EMG signals from each muscle were checked online for mechanical artefacts by passively shaking the leg. Additionally several functional tests (e.g. contractions against manual resistance in knee extension and flexion) were performed to determine whether a good signal was obtained from each muscle. The preparation was repeated when artefacts or a poor signal were observed. All knee extension contractions were performed within one testing period and no electrode replacement was necessary during the measurements. The Vicon System registered the EMG signals at a sampling rate of 3000 Hz during the MVCs. The root mean square (RMS) was calculated from the raw signal over a 1 s period at the plateau of the calculated tendon force. 2.4. Measurement of the tendinous tissue elongation A 7.5 MHz linear array ultrasound probe (Aloka SSD 4000, 43 Hz, resolution 0.4 · 0.7 mm) was used to visualize the distal tendon and aponeurosis of VL during MVC-U and 1.5–2 min after the fatiguing protocols during MVC-F1 and MVC-F2. The ultrasound probe was placed above the VL muscle belly at about 50% of its length. A marker that could be identified on the ultrasound image was fixed to the skin to examine any motion of the probe relative to the skin during the contraction (Fig. 2). The exact protocol for the analysis of the tendinous tissue elongation during knee extension is described in detail elsewhere (Stafilidis et al., 2005). To synchronise the video data (ultrasound images) with the data from the Vicon System, a synchronization box (Peak Performance Technologies) was used. The experiment leader triggered an analogue signal (0–5 V) manually, which was displayed on the video images and simultaneously captured by the Vicon System. The video tapes were digitised every single frame using video analysis software (Simi Motion 5.0, SIMI Motion GmbH). The elongation of the VL tendon and aponeurosis was defined as the displacement of a cross-point (insertion of a fascicle into the deeper aponeurosis) along the visualised deeper aponeurosis relative to the skin marker. As mentioned above, it has been reported that during maximal ‘‘isometric’’ knee extension efforts it is extremely difficult to completely prevent any joint angular displacement, despite using external fixations (Arampatzis et al., 2004; Bojsen-Møller et al., 2003; Stafilidis et al., 2005). This joint angular dispacement has a significant influence on the measured elongation of the VL tendon and aponeurosis (BojsenMøller et al., 2003; Stafilidis et al., 2005). In order to correct the measured elongation of the VL tendon and aponeurosis their motion was captured by the ultrasound probe during a passive motion (same as used for the correction for the gravitational forces) and recorded on video tape for further analysis. The difference in elongation between the values measured during the MVC and the values due to joint angular displacement represent the elongation of the tendon plus aponeurosis due to the exerted force at each maximal knee extension trial (corrected elongation, Fig. 3). The choice of the examined cross-point on the ultrasound image does not influence the estimation of the strain when the rest (initial) length is known (Stafilidis et al., 2005). The rest length
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
479
Fig. 2. Ultrasound image of the relaxed VL at about 50% length of its muscle belly. The elongation of the VL tendon and aponeurosis was defined as the distance travelled by a cross-point along the visualised deeper aponeurosis during the maximal isometric knee extension effort. The marker between the skin and the ultrasound probe was used to register any motion of the probe relative to the skin during the MVCs.
was defined as the length of the path between the tuberositas tibia (defined as the origin of the patella tendon) and the cross-point at the VL muscle belly. In order to estimate the rest length, the distance of the curved path along the skin from the tuberositas tibia to a marker on the skin was measured using flexible measuring tape. The reported reproducibility of ultrasound measurements from earlier studies is high (coefficient of variation <3.2%, Bojsen-Møller et al., 2003). In our department we proved the accuracy of the ultrasound method several times by digitising the same trial by different examiners. The difference ranged from 1.0 mm to 1.2 mm at a resolution of the ultrasound images of 0.4 · 0.7 mm. Elongation and strain of the VL tendon and aponeurosis during MVC-U, MVC-F1 and MVC-F2 were identified and analysed at the maximum calculated tendon force and every 300 N. This procedure allowed us to compare the elongation and the strain between the MVC before and after the fatiguing tasks at the same given tendon force. Fig. 3. Mean curves (n = 12) of the measured elongation (measured), the corrected elongation considering the joint angular displacement (corrected), and the passive elongation due to joint angular displacement (passive) of the VL tendon and aponeurosis during maximum voluntary isometric contraction. tmax: Time to achieve maximum tendon force.
2.5. Statistics Differences between the maximum values of the knee joint moment, calculated tendon force, elongation and strain of the VL
480
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
tendon and aponeurosis during MVC-U, MVC-F1 and MVC-F2 were checked using a one way analysis of variance (ANOVA) for repeated measures. All values were collected from all subjects (n = 12), except maximal elongation and strain at MVC-F2, which lack one subject due to a visualising problem in the ultrasound picture. The level of significance was set at a = 0.05. When statistically significant differences were found the parameters were compared using the pairwise Bonferroni correction. The same statistical procedure was applied to data of elongation and strain of the tendon and aponeurosis, which was determined in steps of 300 N of the PTF, resulting in eight steps from 0 N to 2100 N. The 300 N steps were taken using the raw data of the MVC moment of each subjects and determining the simultaneous value of the digitised tendon elongation at the respective time. The last step corresponds to the maximum common tendon force achieved by all subjects. In the text and tables the data are presented as means ± 1SD (standard deviation), in the figures the data are presented as means ± 1SEM (standard error of mean).
the three examined knee extensor muscles during the MVCs were compared by drawing the ratio from RF/VL, RF/VM and VM/VL. The ratios showed no significant alteration after the long-lasting contractions (Fig. 4). The rest length of VL tendon and aponeurosis was 350.5 ± 22.5 mm. Maximal elongation and strain during the MVCs after the fatiguing tasks showed a statistically significant (p < 0.05) decrease compared to the values found during MVC-U (Table 1). Strain and elongation of VL estimated during MVC before and after each fatiguing protocol at any 300 N step of the tendon force showed no statistically significant differences (p > 0.05). Strain values are displayed in Fig. 5 and elongation values are displayed in Table 2.
3. Results During the sustained isometric submaximal fatiguing protocol the time to failure was 4.67 ± 1.87 min (range from 2.16 to 8.73 min) and during the repetitive isokinetic maximal fatiguing protocol 5.67 ± 4.98 min (range from 2.0 to 20.52 min), respectively. Both maximum resultant knee extension moments, achieved during the MVCs after the two fatiguing trials, were statistically significant lower (p < 0.05) compared to the pre-fatigue state (Table 1). The decrease of maximum exerted knee extension moment was about 28% after fatigue 1 and 21% after fatigue 2, confirming an ongoing state of muscle fatigue 1.5–2 min after the fatiguing tasks. Similar to the knee joint moment the calculated tendon force during the MVC was statistically significant lower (p < 0.05) after fatigue 1 and fatigue 2 compared to the pre-fatigue condition (Table 1). Additionally, the achieved maximum knee extension moment and the calculated tendon force after fatigue 1 were statistically significant (p < 0.05) lower than after fatigue 2 (Table 1). The RMS values of the EMG activity of
Fig. 4. Ratios EMGRMS (means ± SEM) from VL, VM and RF during the MVCs prior to (MVC-U), after isometric (MVC-F1) and after isokinetic (MVC-F2) long-lasting mechanical loading (n = 12). The ratios were taken as ratio RF/VL, ratio RF/VM and ratio VM/VL.
Table 1 Comparison of maximum values of the examined parameters during the unfatigued MVC (MVC-U) and during the MVCs after isometric (MVCF1) and isokinetic fatiguing protocol (MVC-F2) MVC-U Moment (N m) Tendon force (N) Elongation (mm) Strain (%)
154.4 ± 47.3 3517 ± 747 26.8 ± 5.1 7.7 ± 1.5
MVC-F1
MVC-F2 a
111.3 ± 35.5 2610 ± 701a 23.6 ± 6.1a 6.8 ± 1.7a
123.4 ± 29.0a,b 2860 ± 550a,b 24.5 ± 5.4a 7.1 ± 1.6a
Means ± SD, n = 12. Moment – maximum exerted moment from the knee extensor muscles during maximum voluntary isometric contraction (MVC). Tendon force – maximum calculated tendon force during MVC. Elongation – maximal elongation of the tendon and aponeurosis of the VL during MVC. Strain – maximal strain of the tendon and aponeurosis of the VL during MVC. a Significant different to MVC-U (p < 0.05). b Significant different to MVC-F1 (p < 0.05).
Fig. 5. Strain (means ± SEM) of VL tendon and aponeurosis determined in steps of 300 N and at the maximum of the calculated tendon force during the unfatigued MVC (MVC-U) and during the MVCs after isometric (MVC-F1) and isokinetic fatiguing protocol (MVC-F2). The curve ends at 2100 N, which corresponds to the maximum calculated tendon force achieved by all subjects during the MVCs (n = 12).
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483 Table 2 Elongation (mean ± SD) of the VL tendon and aponeurosis determined in steps of 300 N of the calculated tendon force during the MVCs prior to (MVC-U), after isometric (MVC-F1) and after isokinetic (MVC-F2) longlasting mechanical loading Tendon force (N)
MVC-U elongation (mm)
MVC-F1 elongation (mm)
MVC-F2 elongation (mm)
0 300 600 900 1200 1500 1800 2100
0.0 4.2 ± 2.5 8.1 ± 3.8 11.7 ± 4.6 14.9 ± 4.9 17.5 ± 5.3 19.8 ± 5.6 21.9 ± 5.9
0.0 3.8 ± 1.7 7.3 ± 2.8 10.9 ± 3.8 14.2 ± 4.1 17.0 ± 5.0 19.6 ± 6.0 20.9 ± 5.8
0.0 4.2 ± 3.0 7.9 ± 4.4 11.3 ± 5.1 14.6 ± 5.3 17.9 ± 5.8 20.2 ± 6.4 21.8 ± 6.5
The table ends at 2100 N, which corresponds to the maximum 300 N step of the calculated tendon force achieved by all subjects during the MVCs (n = 12).
4. Discussion The main result of the present study is that elongation and strain of VL tendon and aponeurosis show no significant alterations between any of the compared force levels (steps of 300 N from 0 N to 2100 N) of the MVCs neither 1.5–2 min after the long-lasting isometric submaximal contraction nor 1.5–2 min after the long-lasting isokinetic maximal contractions. This outcome gives proof to our first hypothesis, confirming that 1.5–2 min after the submaximal fatiguing trial at 25% of the maximum isometric knee extension moment (fatigue 1) the tendon did not show any significant alteration in its compliance. At this level of contraction the mean calculated tendon force was 879 ± 187 N and the corresponding tendon strain was about 3.2% (Fig. 5). The strain remains within the limit of 4%, which is supposed to be the threshold when ‘‘residual strain’’ occurs in tendons, according to earlier in vitro studies (Abrahams, 1967). The result matches more recent in vitro (De Zee et al., 2000) and in vivo (Mademli et al., 2006) studies, using long term dynamic loading with a natural loading profile at low strain, reporting that the effect on the compliance of the tendon was negligible. It is well known that in the toe-region, increasing strain under tensile testing provokes a smaller increase in stress due to straightening out of the wavy crimp of the tendinous structure (Diamant et al., 1972; Rigby et al., 1959; Viidik and Ekholm, 1968). According to Viidik and Ekholm (1968), increasing tendon strain within the toe-region reflects a gradually increasing recruitment of collagen fibres. This has been interpreted to be a mechanism of collagen fibres to resist creep at low stress levels (Thornton et al., 2002). Therefore we can conclude that the capacity of the VL tendon and aponeurosis to resist force remained unaffected after the sustained submaximal fatiguing protocol. Contrary to our second hypothesis even after the isokinetic fatiguing protocol (fatigue 2), which was performed from 100% to 70% of unfatigued maximum isokinetic
481
moment, the tendon was not subjected to any change in compliance. The maximum calculated tendon forces during the isokinetic protocol were between 2177 ± 516 N and 1693 ± 242 N. The corresponding strain of the VL tendon and aponeurosis during the isokinetic fatiguing protocol was 6.2–5.5% tendon strain (Fig. 5). Thus tendon strain did not remain at the toe-region, but proceeded into the quasi-linear region, which occurs after the completion of recruitment of fibres and involves the stretching of the straightened fibres (Viidik and Ekholm, 1968). In vitro studies examining the mechanical properties of tendon have reported that preconditioning is usually manifested as a right shift of the load–elongation curve and that afterwards the load–elongation relationship of soft tissues reaches a steady state (Fung, 1993). In a similar manner, recently Maganaris (2003) found in vivo that tendon elongation at a given tendon force changed in the first five contractions and reached a plateau thereafter. In our protocol, the warm up period with the three isometric MVCs and the five maximal isokinetic contractions prior to the fatiguing protocols can serve as a possible explanation why tendon compliance was not altered during long-lasting repetitive contractions. Additionally in vitro studies reported that cyclic loading by constant applied stress on the tendon at 5–6% initial strain values has a negligible effect on the achieved strain during the first 40 min (Wren et al., 2003). In the present study the subjects were able to sustain the repetitive isokinetic maximal fatiguing protocol for 5.67 ± 4.98 min. With respect to Wren et al. (2003), the achieved endurance times of our subjects might indicate that load–elongation relationship of tendon and aponeurosis did not overcome the steady state. It seems that the effects of muscle fatigue limit the number of repetitive strain cycles in vivo and that muscle fatigue occurs before changes in tendon mechanical properties. This fact together with the preconditioning is possibly the main reason why cyclic loading from 6.2% to 5.5% strain did not affect tendon compliance. The calculation of tendon force by means of moment arm values from the literature (Herzog and Read, 1993) could be a methodological limitation of the study, because of inter individual anatomical differences. As we compared the subjects with themselves before and after the fatiguing protocols this potential error would be systematic and might not influence the presented findings. Furthermore, as mentioned above, we measured tendon mechanical properties 1.5–2 min after the fatiguing protocols. Therefore, possible alterations in tendon compliance during the fatiguing protocols, withering within this time gap, would stay undetected. Therefore we can only exclude changes in tendon compliance 1.5–2 min after the fatiguing trials. Moreover, although Rigby (1964) reported that after submaximal preconditioning the tendon recovers after 10 min rest, 15 min recovery might not be enough to completely discard all effects of the isometric fatiguing protocol. However this should not affect the conclusions of the present study, since no alteration was found in
482
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
the examined tendinous properties after the fatiguing protocols. As it is well known from the literature, creep can influence the initial length of the tendon and thereby it might affect its compliance (Schwerdt et al., 1980). If we suspect that creep occurred during the fatiguing protocols, this might have changed the rest length of the tendon. Experimentally, due to ultrasound methodology, it is very difficult to assign the same cross-point in the ultrasound picture at the VL aponeurosis before and after the fatiguing protocols in order to detect possible rest length changes. Hence alternatively we digitised pennation angle and fascicle length at rest before and after the long-lasting contractions. The pennation angle was defined as the angle of insertion of the muscle fascicles into the deeper aponeurosis and the fascicle length as the length of the fascicular path between the insertions of the fascicle into the upper and deeper aponeurosis. Pennation angle and fascicle length did not show statistically significant alterations after fatigue 1 or fatigue 2, therefore possible changes of the rest length, which could have affected tendon compliance, could be excluded. Finally, since we determined strain and elongation of the VL tendon and aponeurosis, but we calculated tendon force of the overall quadriceps femoris muscle, any change in the relative contribution of the VL, VM and RF to tendon force prior to and after the long-lasting contractions, might have affected the strain–force relationship. The ratios of the RMS showed no significant differences after the fatiguing trials, suggesting that the presented results, regarding the effect of long-lasting static as well as cyclic loading on tendon compliance, stayed unaffected (Fig. 4). In conclusion the results show that the VL tendon and aponeurosis do not suffer from changes in the compliance in vivo, neither after long-lasting static mechanical loading (strain 3.2%) nor after long-lasting cyclic mechanical loading (strain 6.2–5.5%). References Abrahams M. Mechanical behaviour of tendon in vitro, a preliminary report. Med Biol Eng 1967;5:433–43. Alexander RMcN, Bennet-Clark HC. Storage of elastic strain energy in muscle and other tissues. Nature 1977;265:114–7. Alexander RMcN. Tendon elasticity and muscle function. Comp Biochem Physiol 2002;A133:1001–11. Arampatzis A, Karamanidis K, DeMonte G, Stafilidis S, MoreyKlapsing G, Bru¨ggemann G P. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomech 2004;19:277–83. Baratta R, Solomonow M, Zhou B H, Letson D, Chuinard R, D’Ambrosia R. Muscular coactivation: the role of the antagonist musculature in maintaining knee stability. The Am J Sports Med 1988;16:113–22. Bobbert MF. Dependence of human squat jump performance on the series elastic compliance of the triceps surae: a stimulation study. The J Exp Biol 2001;204:533–42. Bojsen-Møller J, Hansen P, Aagaard P, Kjaer M, Magnusson SP. Measuring mechanical properties of the vastus lateralis tendonaponeurosis complex in vivo by ultrasound imaging. Scand J Med Sci Sports 2003;13:259–65.
De Zee M, Bojsen-Mo¨ller F, Voigt AM. Dynamic viscoelastic behavior of lower extremity tendons during stimulated running. J App Physiol 2000;89:1352–9. De Zee M, Voigt AM. Moment dependency of the series elastic stiffness in the human plantar flexor measured in vivo. J Biomech 2001;43: 1399–406. Diamant J, Keller A, Baer E, Litt M, Arridge RGC. Collagen: ultrastructure and its relation to mechanical properties as a function of ageing. Proc Roy Soc 1972;180(B):293–315. Ettema GJC. Mechanical behaviour of rat skeletal muscle during fatiguing stretch-shortening cycles. Exp Physiol 1997;82:107–19. Ettema GJC. A new method to measure elastic properties of plastic viscoelastic connective tissue. Med Eng Phys 1998;20:308–14. Fung YC. Biomechanics. 2nd ed. Mechanical properties of living tissues. New York, Berlin, Heidelberg: Springer-Verlag; 1993. Harris EH, Walker LB, Bass BR. Stress–strain studies in cadavric human tendon and an anomaly in the Young’s modulus thereof. Med Biol Eng 1966;4:253–9. Herzog W, Ter Keurs HEDJ. A method for the determination of the force–length relation of selected in vivo human skeletal muscles. Eur J Physiol 1988;411:637–41. Herzog W, Abrahamse SK, Ter Keurs HEDJ. Theoretical determination of force–length relations of intact human skeletal muscles using the cross bridge model. Eur J Physiol 1990;416:113–9. Herzog W, Read LJ. Lines of action and moment arms of the major forcecarrying structures crossing the human knee joint. J Anatomy 1993;182(Pt2):213–30. Kubo K, Kanehisa H, Kawakami Y, Fukunaga T. Effects of repeated muscle contaction on the tendon structures in humans. Eur J Appl Physiol 2001a;84:162–6. Kubo K, Kanehisa H, Kawakami Y, Fukunaga T. Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo. J Appl Physiol 2001b;91:277–82. Maganaris CN. Tendon conditioning: artefact or property? Proc Biol Sci/ The Roy Soc 2003;270(Suppl. 1):S39–42. Mademli L, Arampatzis A, Morey-Klapsing G, Bru¨ggemann GP. Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J Electromyogr Kinesiol 2004;14:591–7. Mademli L, Arampatzis A, Walsh M. Effects of muscle fatigue on the compliance of the gastrocnemius medialis tendon and aponeurosis. J Biomech 2006;59:426–34. Rigby BJ, Hirai N, Spikes JD, Eyring H. The mechanical properties of rat tail tendon. The J Gen Physiol 1959;43:265–83. Rigby BJ. Effect of cyclic extension on the physical properties of tendon collagen and its possible relation to biological ageing of collagen. Nature 1964;202:1072–4. Schatzmann L, Brunner P, Sta¨ubli HU. Effects of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg, Sports Traumatol, Arthrosc 1998;6(Suppl. 19): 56–61. Schwerdt H, Constantinesco A, Chambron J. Dynamic viscoelastic behavior of the human tendon in vitro. J Biomech 1980;13:912–3. Stafilidis S, Karamanidis K, Morey-Klapsing G, DeMonte G, Bru¨gemann GP, Arampatzis A. Strain and elongation of the vastus lateralis aponeurosis and tendon in vivo during maximal isometric contraction. Eur J Appl Physiol 2005;94:317–22. Thornton GM, Shrive NG, Frank CB. Ligament creep recruits fibres at low stresses and lead to modulus-reducing fibre damage at higher creep stresses: a study in rabbit medial collateral ligament model. J Orthopaed Res 2002;20:967–74. Viidik A, Ekholm R. Light and electron microscopic studies of collagen fibres under strain. Zeitschrift fu¨r Anatomie und Entwicklungsgeschichte 1968;127:154–64. Viidik A. Functional properties of collagenous tissues. Int Rev Connective Tissue Res 1973;6:127–215. Wang XT, Ker RF, Alexander RMcN. Fatigue rupture of wallaby tail tendons. J Exp Biol 1995;198:847–52.
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483 Wang XT, Ker RF. Creep rupture of wallaby tail tendons. J Exp Biol 1995;198:831–45. Wren TA, Lindsey DP, Beaupre GS, Carter DR. Effects of creep and cyclic loading on the mechanical properties and failure of human achilles tendons. Ann Biomed Eng 2003;31:710–7.
Anne Charlotte Ullrich, ne´e Niemeyer, finished her practical year at the University Hospital of Cologne (Germany) and graduated in medicine from the University of Cologne in November 2007. In 2003 she joined the institute of Biomechanics and Orthopaedics at the German Sport University of Cologne where she is writing her doctoral thesis on responses of the muscle–tendon unit’s mechanical properties during and after long lasting mechanical loading.
Lida Mademli graduated in sport science from the Aristotle University of Thessaloniki (Greece) in 2002. The same year she moved to Cologne (Germany), where she joined the institute of Biomechanics and Orthopaedics at the German Sport University of Cologne. She is enjoying a grant for making her Ph.D. thesis on the age related effects of fatigue on the neuromechanical properties of the muscle– tendon unit and the postural stability after sudden perturbations.
483
Adamantios Arampatzis received his Ph.D. at the German Sport University of Cologne in 1995. He is the head of the research group focusing on the neuromechanics of the human muscoloskeletal system at the Institute of Biomechanics and Orthopaedics from the German Sport University Cologne. Among his research interests are the adaptation potential of the human system to physical activity and the influence of the neuromechanical capacity of the muscoloskeletal system on motor task behaviour during daily and sport activities.
Journal of Electromyography and Kinesiology 19 (2009) 476–483 www.elsevier.com/locate/jelekin
Effects of submaximal and maximal long-lasting contractions on the compliance of vastus lateralis tendon and aponeurosis in vivo Anne Charlotte Ullrich a
a,b
, Lida Mademli a, Adamantios Arampatzis
a,*
Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Carl-Diem-Weg 6, 50933 Cologne, Germany b Department II of Anatomy, Medical Faculty, University of Cologne, Joseph-Stelzmann-str. 9, 50931 Cologne, Germany Received 11 August 2006; received in revised form 24 August 2007; accepted 19 October 2007
Abstract The present study investigated the effects of submaximal sustained and maximal repetitive contractions on the compliance of human vastus lateralis (VL) tendon and aponeurosis in vivo using two different fatiguing protocols. Twelve male subjects performed three maximum voluntary isometric contractions (MVC) of the knee extensors before and after two fatiguing protocols on a dynamometer. The first fatiguing protocol consisted of a long-lasting sustained isometric knee extension contraction at 25% MVC until failure (inability to hold the defined load). The second fatiguing protocol included long-lasting isokinetic (90/s) knee extension contractions, where maximum moment was exerted and failure was proclaimed when this value fell below 70% of unfatigued maximum isokinetic moment. Ultrasonography was used to determine the elongation and strain of the VL tendon and aponeurosis. Muscle fatigue was indicated by a significant decrease in maximum resultant knee extension moment (p < 0.05) observed during the MVCs after both long-lasting contractions. No significant (p > 0.05) differences in elongation and strain of the VL tendon and aponeurosis were found, when compared every 300 N (tendon force) before and after the fatiguing protocols. The present data indicate, that the VL tendon and aponeurosis in vivo do not suffer from changes in the compliance neither after long-lasting static mechanical loading (strain 3.2%) nor after long-lasting cyclic mechanical loading (strain 6.2–5.5%). 2007 Elsevier Ltd. All rights reserved. Keywords: Fatigue; Tendon compliance; Knee extension; Ultrasonography
1. Introduction Previous studies in vitro reported an alteration of tendon mechanical properties after cyclic loading at low strain values (Rigby, 1964; Schatzmann et al., 1998), suggesting that tendon became less compliant, due to a change in the rest length. Conversely, Kubo et al. (2001a,b) showed in vivo that the tendon compliance increased after repetitive longlasting contractions at high and low force production levels. Tendons show visco-elastic and plastic mechanical behaviour (Ettema, 1998; Rigby et al., 1959). Ettema (1998) distinguished between (a) pure elastic behaviour, independent of any long term changes in the tissue, (b) slow viscous behav*
Corresponding author. Fax: +49 221 4971598. E-mail address: [email protected] (A. Arampatzis).
1050-6411/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2007.10.008
iour, characterised by slow restoration of the specimen to its slack length and (c) plastic deformation of a tissue. Abrahams (1967) found in vitro that ‘‘residual strain’’, only appears if tendon strain increases into the ‘‘final’’ region of the stress–strain curve. This region commences beyond 4% tendon strain (Abrahams, 1967). In vitro (De Zee et al., 2000; De Zee and Voigt, 2001) and in situ (Ettema, 1997) studies reported that after submaximal repetitive contractions provoking tendon strain beneath this level, tendons were not subjected to any change in the compliance that is relevant for muscle function. This result was confirmed in vivo, certifying that submaximal fatiguing contractions had no effect on tendon compliance (Mademli et al., 2006). Contrary to this, in vitro studies (Wang et al., 1995; Wang and Ker, 1995) applying tendon strain beyond 2– 4%, reported changes in mechanical (i.e. compliance) and
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
in structural properties (i.e. wave form of the collagen fibres) of the tendon and aponeurosis. As in vitro results do not totally reflect in vivo conditions (Harris et al., 1966; Viidik, 1973), there is a deficiency in the knowledge of the effect of high strain repetitive exercises and further differences between long-lasting low and high strain exercises on the mechanical properties of the tendon and aponeurosis in vivo. Any change in tendon compliance would affect the muscle force generating potential due to force–length (Alexander and Bennet-Clark, 1977) and force–velocity relationships (Alexander, 2002; Bobbert, 2001). Furthermore changes in the compliance of tendon and aponeurosis during repetitive long duration contractions like running and cycling might affect the safety factor of the tendon and with this its injury risk. Therefore we examined the effects of submaximal and maximal long-lasting mechanical loading on the compliance of vastus lateralis tendon and aponeurosis in vivo, using a sustained isometric and a repetitive isokinetic fatiguing protocol. We hypothesise that changes in the compliance of tendon and aponeurosis in vivo are negligible after a sustained long-lasting submaximal contraction, inducing low strain located within the toe-region of the stress–strain curve. Furthermore we hypothesise that the compliance of the tendon and aponeurosis will be affected after repetitive long-lasting maximal contractions, inducing strain values higher than 4%. 2. Methods 2.1. Experimental protocol Twelve male endurance-trained subjects (cyclists) participated in the study (age: 25 ± 3 years, body mass: 72.3 ± 4.7 kg and body height: 179.9 ± 6.4 cm) after giving their informed consent
477
in compliance with the rules of the local scientific board. None of the subjects had suffered a neuromuscular or musculoskeletal injury within one year prior to the experiment. The subjects were seated on a dynamometer (Biodex-System3, Biodex Medical Systems Inc., USA) with the hip at 140 and their left leg at 100 knee angle respectively. Approximately in this position maximum knee extension moments are achieved (Herzog and Ter Keurs, 1988; Herzog et al., 1990). For warm-up the subjects exerted five submaximal and three maximum voluntary isometric contractions within 2–3 min. After warm-up the experimental protocol started (Fig. 1). The subjects performed an unfatigued maximum voluntary isometric knee extension contraction (MVC-U) lasting 4–5 s. To assist the subjects in holding the moment-plateau, real time visual feedback of the exerted moment was given. Then the subjects performed ten isokinetic contractions at 90/s in a range of motion of 90–180 knee angle. The subjects were instructed to perform the first five contractions submaximally with progressively increasing force in order to perform five maximal contractions in the end. The greatest moment value was considered the maximum isokinetic moment. Real time visual feedback of the exerted moment was also given during these contractions. The first fatiguing protocol (fatigue 1) consisted of a sustained submaximal isometric contraction in the same position as during the MVC-U (knee angle: 100, hip angle: 140). The 25% level of the MVC-U was displayed on the feedback monitor as target. The subjects were instructed to match the displayed lines on the monitor, representing their own and the target moment. Failure was set to be the inability to hold the defined load for more than 3 s despite strong verbal encouragement by the investigators. Between 1.5 and 2 min after task failure a second isometric MVC at 100 knee and 140 hip angle was performed (MVC-F1). After 15 min recovery the maximal fatiguing trial was started (fatigue 2). The subjects had to perform repetitive isokinetic knee extension contractions (knee angle 90–180, hip angle 140) with an angular velocity of 90/s, where maximum moment was exerted. The pre-exercise unfatigued maximum isokinetic moment was set as target and displayed as a red mark on the screen. Seventy percent
Fig. 1. The experimental set-up consisted of a warm-up period, three maximum voluntary knee extension contractions (MVC) and two fatiguing tasks: (a) a submaximal sustained isometric knee extension contraction at 25% of MVC-U until failure and (b) repetitive isokinetic knee extension contractions, where maximum moment was exerted and fatigue was proclaimed when this value fell below 70% of the unfatigued maximum isokinetic moment. The unfatigued maximum isokinetic moment was defined by the greatest moment value achieved during five maximal isokinetic contractions.
478
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
of this moment was also displayed on the screen to mark the instant of task failure. When the subjects failed to produce more than 70% of this unfatigued maximum isokinetic moment in three sequential trials, fatigue was declared. The subjects were able to observe their exerted moment on the monitor and were verbally encouraged to achieve maximum force and longer endurance times. Again 1.5– 2 min after task failure a third MVC was performed (MVC-F2). 2.2. Measurement of the knee joint moment The moments were measured using the Biodex-dynamometer. Prior to each contraction the knee joint axis and the axis of the dynamometer were carefully aligned. The axis of rotation of the knee joint was defined to be parallel to the axis of the dynamometer and passing through the midpoint of the line connecting the lateral and medial femoral condyles. Although effort was made to limit any joint movement during the contraction, the knee joint changed its position. This shift significantly influences the resultant joint moments (Arampatzis et al., 2004). To account for this, the resultant moments around the knee joint were calculated through inverse dynamics (Arampatzis et al., 2004). The Vicon 624 System (Vicon motion Systems, United Kingdom) recorded kinematic data using eight cameras operating at 120 Hz. Reflective markers were placed on the following body landmarks: lateral and medial malleolus, most prominent points of the lateral and medial femoral condyles, trochanter major, crista iliaca on the tuberclum iliacum, axis of the dynamometer and the lever arm of the dynamometer. The correction of the measured moment due to gravitational forces was determined for all subjects by obtaining a passive knee joint rotation before each knee extension contraction. The exact method for calculating the resultant joint moment has been described previously (Arampatzis et al., 2004). The influence of the simultaneous activation of the hamstrings (HA), working as antagonists during the knee extension contraction on the resultant joint moment, was taken into account by establishing a relationship between HA EMG-amplitude and exerted moment, whilst working as agonists. The moment generated due to antagonistic coactivation during the knee extension effort was quantified by assuming a linear relationship between surface EMG amplitude of the knee flexor muscles and moment (Baratta et al., 1988) measured during one relaxed condition and two different submaximal knee flexion contractions (Mademli et al., 2004). The coactivation of vastus lateralis (VL), vastus medialis (VM) and rectus femoris (RF) during submaximal knee flexion was within the noise level of the EMG signal, indicating no coactivation during the knee flexion contractions. In the following text the maximum knee joint moments will include the effect of knee joint axis alteration relative to the dynamometer axis, the effect of the gravitational force, and the effect of the hamstring coactivation. The patellar tendon force (PTF) during the contraction was calculated by dividing the knee joint moment by the tendon moment arm. The lever arm of the patellar tendon was calculated as a function of the knee angle using the data provided by Herzog and Read (1993). The kinematic data were interpolated using quintic splines to achieve a common frequency with the moment and EMG signals (3000 Hz). 2.3. Measurement of the EMG-activity The myoelectric activities of the VL, VM, RF and HA muscles were recorded by means of preamplified (bandwidth 10–500 Hz) bipolar EMG leadoffs. Adhesive surface electrodes (Ag/AgCl)
with an electrolytic gel interface and a pickup surface of 0.8 cm2 were positioned above the midpoint of the muscle belly (2 cm inter-electrode distance). Care was taken above the VL muscle belly to avoid interference of the electrodes and the ultrasound probe. The skin was carefully prepared (shaved and cleaned with alcohol) to reduce skin impedance. The electrodes were further secured to the skin with elastic tape together with the preamplifier to reduce motion artefacts. Before the experiment started, the EMG signals from each muscle were checked online for mechanical artefacts by passively shaking the leg. Additionally several functional tests (e.g. contractions against manual resistance in knee extension and flexion) were performed to determine whether a good signal was obtained from each muscle. The preparation was repeated when artefacts or a poor signal were observed. All knee extension contractions were performed within one testing period and no electrode replacement was necessary during the measurements. The Vicon System registered the EMG signals at a sampling rate of 3000 Hz during the MVCs. The root mean square (RMS) was calculated from the raw signal over a 1 s period at the plateau of the calculated tendon force. 2.4. Measurement of the tendinous tissue elongation A 7.5 MHz linear array ultrasound probe (Aloka SSD 4000, 43 Hz, resolution 0.4 · 0.7 mm) was used to visualize the distal tendon and aponeurosis of VL during MVC-U and 1.5–2 min after the fatiguing protocols during MVC-F1 and MVC-F2. The ultrasound probe was placed above the VL muscle belly at about 50% of its length. A marker that could be identified on the ultrasound image was fixed to the skin to examine any motion of the probe relative to the skin during the contraction (Fig. 2). The exact protocol for the analysis of the tendinous tissue elongation during knee extension is described in detail elsewhere (Stafilidis et al., 2005). To synchronise the video data (ultrasound images) with the data from the Vicon System, a synchronization box (Peak Performance Technologies) was used. The experiment leader triggered an analogue signal (0–5 V) manually, which was displayed on the video images and simultaneously captured by the Vicon System. The video tapes were digitised every single frame using video analysis software (Simi Motion 5.0, SIMI Motion GmbH). The elongation of the VL tendon and aponeurosis was defined as the displacement of a cross-point (insertion of a fascicle into the deeper aponeurosis) along the visualised deeper aponeurosis relative to the skin marker. As mentioned above, it has been reported that during maximal ‘‘isometric’’ knee extension efforts it is extremely difficult to completely prevent any joint angular displacement, despite using external fixations (Arampatzis et al., 2004; Bojsen-Møller et al., 2003; Stafilidis et al., 2005). This joint angular dispacement has a significant influence on the measured elongation of the VL tendon and aponeurosis (BojsenMøller et al., 2003; Stafilidis et al., 2005). In order to correct the measured elongation of the VL tendon and aponeurosis their motion was captured by the ultrasound probe during a passive motion (same as used for the correction for the gravitational forces) and recorded on video tape for further analysis. The difference in elongation between the values measured during the MVC and the values due to joint angular displacement represent the elongation of the tendon plus aponeurosis due to the exerted force at each maximal knee extension trial (corrected elongation, Fig. 3). The choice of the examined cross-point on the ultrasound image does not influence the estimation of the strain when the rest (initial) length is known (Stafilidis et al., 2005). The rest length
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
479
Fig. 2. Ultrasound image of the relaxed VL at about 50% length of its muscle belly. The elongation of the VL tendon and aponeurosis was defined as the distance travelled by a cross-point along the visualised deeper aponeurosis during the maximal isometric knee extension effort. The marker between the skin and the ultrasound probe was used to register any motion of the probe relative to the skin during the MVCs.
was defined as the length of the path between the tuberositas tibia (defined as the origin of the patella tendon) and the cross-point at the VL muscle belly. In order to estimate the rest length, the distance of the curved path along the skin from the tuberositas tibia to a marker on the skin was measured using flexible measuring tape. The reported reproducibility of ultrasound measurements from earlier studies is high (coefficient of variation <3.2%, Bojsen-Møller et al., 2003). In our department we proved the accuracy of the ultrasound method several times by digitising the same trial by different examiners. The difference ranged from 1.0 mm to 1.2 mm at a resolution of the ultrasound images of 0.4 · 0.7 mm. Elongation and strain of the VL tendon and aponeurosis during MVC-U, MVC-F1 and MVC-F2 were identified and analysed at the maximum calculated tendon force and every 300 N. This procedure allowed us to compare the elongation and the strain between the MVC before and after the fatiguing tasks at the same given tendon force. Fig. 3. Mean curves (n = 12) of the measured elongation (measured), the corrected elongation considering the joint angular displacement (corrected), and the passive elongation due to joint angular displacement (passive) of the VL tendon and aponeurosis during maximum voluntary isometric contraction. tmax: Time to achieve maximum tendon force.
2.5. Statistics Differences between the maximum values of the knee joint moment, calculated tendon force, elongation and strain of the VL
480
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
tendon and aponeurosis during MVC-U, MVC-F1 and MVC-F2 were checked using a one way analysis of variance (ANOVA) for repeated measures. All values were collected from all subjects (n = 12), except maximal elongation and strain at MVC-F2, which lack one subject due to a visualising problem in the ultrasound picture. The level of significance was set at a = 0.05. When statistically significant differences were found the parameters were compared using the pairwise Bonferroni correction. The same statistical procedure was applied to data of elongation and strain of the tendon and aponeurosis, which was determined in steps of 300 N of the PTF, resulting in eight steps from 0 N to 2100 N. The 300 N steps were taken using the raw data of the MVC moment of each subjects and determining the simultaneous value of the digitised tendon elongation at the respective time. The last step corresponds to the maximum common tendon force achieved by all subjects. In the text and tables the data are presented as means ± 1SD (standard deviation), in the figures the data are presented as means ± 1SEM (standard error of mean).
the three examined knee extensor muscles during the MVCs were compared by drawing the ratio from RF/VL, RF/VM and VM/VL. The ratios showed no significant alteration after the long-lasting contractions (Fig. 4). The rest length of VL tendon and aponeurosis was 350.5 ± 22.5 mm. Maximal elongation and strain during the MVCs after the fatiguing tasks showed a statistically significant (p < 0.05) decrease compared to the values found during MVC-U (Table 1). Strain and elongation of VL estimated during MVC before and after each fatiguing protocol at any 300 N step of the tendon force showed no statistically significant differences (p > 0.05). Strain values are displayed in Fig. 5 and elongation values are displayed in Table 2.
3. Results During the sustained isometric submaximal fatiguing protocol the time to failure was 4.67 ± 1.87 min (range from 2.16 to 8.73 min) and during the repetitive isokinetic maximal fatiguing protocol 5.67 ± 4.98 min (range from 2.0 to 20.52 min), respectively. Both maximum resultant knee extension moments, achieved during the MVCs after the two fatiguing trials, were statistically significant lower (p < 0.05) compared to the pre-fatigue state (Table 1). The decrease of maximum exerted knee extension moment was about 28% after fatigue 1 and 21% after fatigue 2, confirming an ongoing state of muscle fatigue 1.5–2 min after the fatiguing tasks. Similar to the knee joint moment the calculated tendon force during the MVC was statistically significant lower (p < 0.05) after fatigue 1 and fatigue 2 compared to the pre-fatigue condition (Table 1). Additionally, the achieved maximum knee extension moment and the calculated tendon force after fatigue 1 were statistically significant (p < 0.05) lower than after fatigue 2 (Table 1). The RMS values of the EMG activity of
Fig. 4. Ratios EMGRMS (means ± SEM) from VL, VM and RF during the MVCs prior to (MVC-U), after isometric (MVC-F1) and after isokinetic (MVC-F2) long-lasting mechanical loading (n = 12). The ratios were taken as ratio RF/VL, ratio RF/VM and ratio VM/VL.
Table 1 Comparison of maximum values of the examined parameters during the unfatigued MVC (MVC-U) and during the MVCs after isometric (MVCF1) and isokinetic fatiguing protocol (MVC-F2) MVC-U Moment (N m) Tendon force (N) Elongation (mm) Strain (%)
154.4 ± 47.3 3517 ± 747 26.8 ± 5.1 7.7 ± 1.5
MVC-F1
MVC-F2 a
111.3 ± 35.5 2610 ± 701a 23.6 ± 6.1a 6.8 ± 1.7a
123.4 ± 29.0a,b 2860 ± 550a,b 24.5 ± 5.4a 7.1 ± 1.6a
Means ± SD, n = 12. Moment – maximum exerted moment from the knee extensor muscles during maximum voluntary isometric contraction (MVC). Tendon force – maximum calculated tendon force during MVC. Elongation – maximal elongation of the tendon and aponeurosis of the VL during MVC. Strain – maximal strain of the tendon and aponeurosis of the VL during MVC. a Significant different to MVC-U (p < 0.05). b Significant different to MVC-F1 (p < 0.05).
Fig. 5. Strain (means ± SEM) of VL tendon and aponeurosis determined in steps of 300 N and at the maximum of the calculated tendon force during the unfatigued MVC (MVC-U) and during the MVCs after isometric (MVC-F1) and isokinetic fatiguing protocol (MVC-F2). The curve ends at 2100 N, which corresponds to the maximum calculated tendon force achieved by all subjects during the MVCs (n = 12).
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483 Table 2 Elongation (mean ± SD) of the VL tendon and aponeurosis determined in steps of 300 N of the calculated tendon force during the MVCs prior to (MVC-U), after isometric (MVC-F1) and after isokinetic (MVC-F2) longlasting mechanical loading Tendon force (N)
MVC-U elongation (mm)
MVC-F1 elongation (mm)
MVC-F2 elongation (mm)
0 300 600 900 1200 1500 1800 2100
0.0 4.2 ± 2.5 8.1 ± 3.8 11.7 ± 4.6 14.9 ± 4.9 17.5 ± 5.3 19.8 ± 5.6 21.9 ± 5.9
0.0 3.8 ± 1.7 7.3 ± 2.8 10.9 ± 3.8 14.2 ± 4.1 17.0 ± 5.0 19.6 ± 6.0 20.9 ± 5.8
0.0 4.2 ± 3.0 7.9 ± 4.4 11.3 ± 5.1 14.6 ± 5.3 17.9 ± 5.8 20.2 ± 6.4 21.8 ± 6.5
The table ends at 2100 N, which corresponds to the maximum 300 N step of the calculated tendon force achieved by all subjects during the MVCs (n = 12).
4. Discussion The main result of the present study is that elongation and strain of VL tendon and aponeurosis show no significant alterations between any of the compared force levels (steps of 300 N from 0 N to 2100 N) of the MVCs neither 1.5–2 min after the long-lasting isometric submaximal contraction nor 1.5–2 min after the long-lasting isokinetic maximal contractions. This outcome gives proof to our first hypothesis, confirming that 1.5–2 min after the submaximal fatiguing trial at 25% of the maximum isometric knee extension moment (fatigue 1) the tendon did not show any significant alteration in its compliance. At this level of contraction the mean calculated tendon force was 879 ± 187 N and the corresponding tendon strain was about 3.2% (Fig. 5). The strain remains within the limit of 4%, which is supposed to be the threshold when ‘‘residual strain’’ occurs in tendons, according to earlier in vitro studies (Abrahams, 1967). The result matches more recent in vitro (De Zee et al., 2000) and in vivo (Mademli et al., 2006) studies, using long term dynamic loading with a natural loading profile at low strain, reporting that the effect on the compliance of the tendon was negligible. It is well known that in the toe-region, increasing strain under tensile testing provokes a smaller increase in stress due to straightening out of the wavy crimp of the tendinous structure (Diamant et al., 1972; Rigby et al., 1959; Viidik and Ekholm, 1968). According to Viidik and Ekholm (1968), increasing tendon strain within the toe-region reflects a gradually increasing recruitment of collagen fibres. This has been interpreted to be a mechanism of collagen fibres to resist creep at low stress levels (Thornton et al., 2002). Therefore we can conclude that the capacity of the VL tendon and aponeurosis to resist force remained unaffected after the sustained submaximal fatiguing protocol. Contrary to our second hypothesis even after the isokinetic fatiguing protocol (fatigue 2), which was performed from 100% to 70% of unfatigued maximum isokinetic
481
moment, the tendon was not subjected to any change in compliance. The maximum calculated tendon forces during the isokinetic protocol were between 2177 ± 516 N and 1693 ± 242 N. The corresponding strain of the VL tendon and aponeurosis during the isokinetic fatiguing protocol was 6.2–5.5% tendon strain (Fig. 5). Thus tendon strain did not remain at the toe-region, but proceeded into the quasi-linear region, which occurs after the completion of recruitment of fibres and involves the stretching of the straightened fibres (Viidik and Ekholm, 1968). In vitro studies examining the mechanical properties of tendon have reported that preconditioning is usually manifested as a right shift of the load–elongation curve and that afterwards the load–elongation relationship of soft tissues reaches a steady state (Fung, 1993). In a similar manner, recently Maganaris (2003) found in vivo that tendon elongation at a given tendon force changed in the first five contractions and reached a plateau thereafter. In our protocol, the warm up period with the three isometric MVCs and the five maximal isokinetic contractions prior to the fatiguing protocols can serve as a possible explanation why tendon compliance was not altered during long-lasting repetitive contractions. Additionally in vitro studies reported that cyclic loading by constant applied stress on the tendon at 5–6% initial strain values has a negligible effect on the achieved strain during the first 40 min (Wren et al., 2003). In the present study the subjects were able to sustain the repetitive isokinetic maximal fatiguing protocol for 5.67 ± 4.98 min. With respect to Wren et al. (2003), the achieved endurance times of our subjects might indicate that load–elongation relationship of tendon and aponeurosis did not overcome the steady state. It seems that the effects of muscle fatigue limit the number of repetitive strain cycles in vivo and that muscle fatigue occurs before changes in tendon mechanical properties. This fact together with the preconditioning is possibly the main reason why cyclic loading from 6.2% to 5.5% strain did not affect tendon compliance. The calculation of tendon force by means of moment arm values from the literature (Herzog and Read, 1993) could be a methodological limitation of the study, because of inter individual anatomical differences. As we compared the subjects with themselves before and after the fatiguing protocols this potential error would be systematic and might not influence the presented findings. Furthermore, as mentioned above, we measured tendon mechanical properties 1.5–2 min after the fatiguing protocols. Therefore, possible alterations in tendon compliance during the fatiguing protocols, withering within this time gap, would stay undetected. Therefore we can only exclude changes in tendon compliance 1.5–2 min after the fatiguing trials. Moreover, although Rigby (1964) reported that after submaximal preconditioning the tendon recovers after 10 min rest, 15 min recovery might not be enough to completely discard all effects of the isometric fatiguing protocol. However this should not affect the conclusions of the present study, since no alteration was found in
482
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483
the examined tendinous properties after the fatiguing protocols. As it is well known from the literature, creep can influence the initial length of the tendon and thereby it might affect its compliance (Schwerdt et al., 1980). If we suspect that creep occurred during the fatiguing protocols, this might have changed the rest length of the tendon. Experimentally, due to ultrasound methodology, it is very difficult to assign the same cross-point in the ultrasound picture at the VL aponeurosis before and after the fatiguing protocols in order to detect possible rest length changes. Hence alternatively we digitised pennation angle and fascicle length at rest before and after the long-lasting contractions. The pennation angle was defined as the angle of insertion of the muscle fascicles into the deeper aponeurosis and the fascicle length as the length of the fascicular path between the insertions of the fascicle into the upper and deeper aponeurosis. Pennation angle and fascicle length did not show statistically significant alterations after fatigue 1 or fatigue 2, therefore possible changes of the rest length, which could have affected tendon compliance, could be excluded. Finally, since we determined strain and elongation of the VL tendon and aponeurosis, but we calculated tendon force of the overall quadriceps femoris muscle, any change in the relative contribution of the VL, VM and RF to tendon force prior to and after the long-lasting contractions, might have affected the strain–force relationship. The ratios of the RMS showed no significant differences after the fatiguing trials, suggesting that the presented results, regarding the effect of long-lasting static as well as cyclic loading on tendon compliance, stayed unaffected (Fig. 4). In conclusion the results show that the VL tendon and aponeurosis do not suffer from changes in the compliance in vivo, neither after long-lasting static mechanical loading (strain 3.2%) nor after long-lasting cyclic mechanical loading (strain 6.2–5.5%). References Abrahams M. Mechanical behaviour of tendon in vitro, a preliminary report. Med Biol Eng 1967;5:433–43. Alexander RMcN, Bennet-Clark HC. Storage of elastic strain energy in muscle and other tissues. Nature 1977;265:114–7. Alexander RMcN. Tendon elasticity and muscle function. Comp Biochem Physiol 2002;A133:1001–11. Arampatzis A, Karamanidis K, DeMonte G, Stafilidis S, MoreyKlapsing G, Bru¨ggemann G P. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomech 2004;19:277–83. Baratta R, Solomonow M, Zhou B H, Letson D, Chuinard R, D’Ambrosia R. Muscular coactivation: the role of the antagonist musculature in maintaining knee stability. The Am J Sports Med 1988;16:113–22. Bobbert MF. Dependence of human squat jump performance on the series elastic compliance of the triceps surae: a stimulation study. The J Exp Biol 2001;204:533–42. Bojsen-Møller J, Hansen P, Aagaard P, Kjaer M, Magnusson SP. Measuring mechanical properties of the vastus lateralis tendonaponeurosis complex in vivo by ultrasound imaging. Scand J Med Sci Sports 2003;13:259–65.
De Zee M, Bojsen-Mo¨ller F, Voigt AM. Dynamic viscoelastic behavior of lower extremity tendons during stimulated running. J App Physiol 2000;89:1352–9. De Zee M, Voigt AM. Moment dependency of the series elastic stiffness in the human plantar flexor measured in vivo. J Biomech 2001;43: 1399–406. Diamant J, Keller A, Baer E, Litt M, Arridge RGC. Collagen: ultrastructure and its relation to mechanical properties as a function of ageing. Proc Roy Soc 1972;180(B):293–315. Ettema GJC. Mechanical behaviour of rat skeletal muscle during fatiguing stretch-shortening cycles. Exp Physiol 1997;82:107–19. Ettema GJC. A new method to measure elastic properties of plastic viscoelastic connective tissue. Med Eng Phys 1998;20:308–14. Fung YC. Biomechanics. 2nd ed. Mechanical properties of living tissues. New York, Berlin, Heidelberg: Springer-Verlag; 1993. Harris EH, Walker LB, Bass BR. Stress–strain studies in cadavric human tendon and an anomaly in the Young’s modulus thereof. Med Biol Eng 1966;4:253–9. Herzog W, Ter Keurs HEDJ. A method for the determination of the force–length relation of selected in vivo human skeletal muscles. Eur J Physiol 1988;411:637–41. Herzog W, Abrahamse SK, Ter Keurs HEDJ. Theoretical determination of force–length relations of intact human skeletal muscles using the cross bridge model. Eur J Physiol 1990;416:113–9. Herzog W, Read LJ. Lines of action and moment arms of the major forcecarrying structures crossing the human knee joint. J Anatomy 1993;182(Pt2):213–30. Kubo K, Kanehisa H, Kawakami Y, Fukunaga T. Effects of repeated muscle contaction on the tendon structures in humans. Eur J Appl Physiol 2001a;84:162–6. Kubo K, Kanehisa H, Kawakami Y, Fukunaga T. Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo. J Appl Physiol 2001b;91:277–82. Maganaris CN. Tendon conditioning: artefact or property? Proc Biol Sci/ The Roy Soc 2003;270(Suppl. 1):S39–42. Mademli L, Arampatzis A, Morey-Klapsing G, Bru¨ggemann GP. Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J Electromyogr Kinesiol 2004;14:591–7. Mademli L, Arampatzis A, Walsh M. Effects of muscle fatigue on the compliance of the gastrocnemius medialis tendon and aponeurosis. J Biomech 2006;59:426–34. Rigby BJ, Hirai N, Spikes JD, Eyring H. The mechanical properties of rat tail tendon. The J Gen Physiol 1959;43:265–83. Rigby BJ. Effect of cyclic extension on the physical properties of tendon collagen and its possible relation to biological ageing of collagen. Nature 1964;202:1072–4. Schatzmann L, Brunner P, Sta¨ubli HU. Effects of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg, Sports Traumatol, Arthrosc 1998;6(Suppl. 19): 56–61. Schwerdt H, Constantinesco A, Chambron J. Dynamic viscoelastic behavior of the human tendon in vitro. J Biomech 1980;13:912–3. Stafilidis S, Karamanidis K, Morey-Klapsing G, DeMonte G, Bru¨gemann GP, Arampatzis A. Strain and elongation of the vastus lateralis aponeurosis and tendon in vivo during maximal isometric contraction. Eur J Appl Physiol 2005;94:317–22. Thornton GM, Shrive NG, Frank CB. Ligament creep recruits fibres at low stresses and lead to modulus-reducing fibre damage at higher creep stresses: a study in rabbit medial collateral ligament model. J Orthopaed Res 2002;20:967–74. Viidik A, Ekholm R. Light and electron microscopic studies of collagen fibres under strain. Zeitschrift fu¨r Anatomie und Entwicklungsgeschichte 1968;127:154–64. Viidik A. Functional properties of collagenous tissues. Int Rev Connective Tissue Res 1973;6:127–215. Wang XT, Ker RF, Alexander RMcN. Fatigue rupture of wallaby tail tendons. J Exp Biol 1995;198:847–52.
A.C. Ullrich et al. / Journal of Electromyography and Kinesiology 19 (2009) 476–483 Wang XT, Ker RF. Creep rupture of wallaby tail tendons. J Exp Biol 1995;198:831–45. Wren TA, Lindsey DP, Beaupre GS, Carter DR. Effects of creep and cyclic loading on the mechanical properties and failure of human achilles tendons. Ann Biomed Eng 2003;31:710–7.
Anne Charlotte Ullrich, ne´e Niemeyer, finished her practical year at the University Hospital of Cologne (Germany) and graduated in medicine from the University of Cologne in November 2007. In 2003 she joined the institute of Biomechanics and Orthopaedics at the German Sport University of Cologne where she is writing her doctoral thesis on responses of the muscle–tendon unit’s mechanical properties during and after long lasting mechanical loading.
Lida Mademli graduated in sport science from the Aristotle University of Thessaloniki (Greece) in 2002. The same year she moved to Cologne (Germany), where she joined the institute of Biomechanics and Orthopaedics at the German Sport University of Cologne. She is enjoying a grant for making her Ph.D. thesis on the age related effects of fatigue on the neuromechanical properties of the muscle– tendon unit and the postural stability after sudden perturbations.
483
Adamantios Arampatzis received his Ph.D. at the German Sport University of Cologne in 1995. He is the head of the research group focusing on the neuromechanics of the human muscoloskeletal system at the Institute of Biomechanics and Orthopaedics from the German Sport University Cologne. Among his research interests are the adaptation potential of the human system to physical activity and the influence of the neuromechanical capacity of the muscoloskeletal system on motor task behaviour during daily and sport activities.