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Relationship between wire EMG activity, muscle length, and torque of the hamstrings Olfat Mohamed a,*, Jacquelin Perry b, Helen Hislop c a Department of Physical Therapy, California State University, 1250 Bellflower Boulevard, Long Beach, CA 90840-5603, USA b Pathokinesiology Laboratory, Rancho Los Amigos National Rehabilitation Center, Downey, CA, USA c Department of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, USA Received 8 January 2002; accepted 28 June 2002 Abstract Objective. To determine the effect of change of muscle length on the torque and wire electromyographic activity of six knee flexor muscles. Design. Maximum isometric knee flexion torque and wire EMG data were collected at nine different positions. Background. In vivo EMG–length–tension relationship is difficult to determine because of the interaction between muscle length and moment arm. The study of two-joint muscles allows the change of muscle length at one joint while preserving stable mechanical relationships at the other. This model facilitates understanding of length–tension and EMG–length relationship in vivo. Methods. Nineteen subjects performed maximum isometric knee flexion contraction at nine positions of varying hip and knee angles. Wire EMG activity was recorded from semitendionsus, semimembranosus, long and short head of the biceps femoris, gracilis and sartorious muscles. Results. As the two-joint hamstrings were lengthened, torque was significantly increased. Maximum isometric torque ranged from 257 to 716 kg cm. The ratio of the torque values to EMG activity of all muscles was increased at longer muscle lengths. A change in the muscle length of the two-joint hamstrings did not produce a consistent change of EMG activity. The short head of the biceps femoris and sartorius muscles increased their activity as the angle of knee flexion increased. Conclusions. Maximum torque of knee flexion occurs at the most lengthened position of the hamstrings. EMG activity did not consistently change with the change in muscle length. Relevance Understanding in vivo length–tension relationship and associated EMG activity is important for designing rehabilitation pro- tocols, tendon lengthening and transfer and interpretation of EMG data. Published by Elsevier Science Ltd. Keywords: Length–tension relationship; EMG–length relationship; Electromyography; Hamstrings; Knee flexion torque 1. Introduction Understanding length-tension relationships in human muscle is important for assisting the design of tendon transfer, rehabilitation and training procedures. Fur- thermore understanding the effect of change in mus- cle length on the electromyographic (EMG) activity recorded from muscle is essential in the functional in- terpretation of EMG data during different activities. Muscles are not attached to the skeleton at their opti- mum length. The in vivo length–tension relationship is complicated by several anatomical and mechanical fac- tors. As a joint rotates, the synchronous change in muscle length and effective moment arm at the joint re- sult in torque variations. The interrelationship between these two variables, namely muscle length and moment arm appear to be different in different muscles. The in situ length–tension curves in the cat hindlimb muscles have all been found to follow the pattern of the ascending limb of the force–length relationship [1,2]. However, frog semitendinosus occupy the descending limb of the force– length curve [3]. In humans, gastrocnemius and wrist *Corresponding author. E-mail address: osm@csulb.edu (O. Mohamed). 0268-0033/02/$ - see front matter Published by Elsevier Science Ltd. PII: S0268-0033 (02 )00070-0 Clinical Biomechanics 17 (2002) 569–579 www.elsevier.com/locate/clinbiomech flexor torque increased with increased muscle length [4,5]. Wrist extensors however, followed the classical length–tension curve with an ascending limb, a plateau and a descending limb through the physiologic range of motion [5]. Based on their mathematical model Chang et al. found that forces generated by the biceps brachii and brachialis increased in the more flexed joint posi- tion (descending limb of length–tension relationship) and the brachioradialis pursued the ascending limb of length–tension relationship [6]. The fact that joint angles vary during motion, thereby continually altering the moment arm, is a confounding problem when examining the effect of changes in muscle length on EMG and torque. Investigating two-joint muscles provides an advantage because of the oppor- tunity to alter the muscle length at one joint while re- taining stable mechanics at the other joint. With this in mind, several investigators studied the effect of change of angle at one joint on torque production at the other joint. These reports have included the effects of altering the knee angle on hip extensor torque [7–9], and the hip angle on knee extensor [10,11] or knee flexor torque [11,12] and also the knee angle on plantar flexion torque [13–15]. Elongation of the two-joint muscles was ac- companied with greater torque production in most cases. Measured torque values at any joint, is the sum of torques of several muscles. The level of participation of these muscles at different angles is an important factor that affects the torque values measured at the joint. Sensing the electrical signal of these muscles indicates their relative level of participation. An extensive body of literature is available on the relationship between EMG activity and graduated muscle force with some authors reporting a linear relationship [16–22] and others re- porting more complex curvilinear relationships [22,23]. In these investigations, muscle length generally was kept constant, a situation which is not analogous to that present during most functional physical activities. Studies that have investigated the relationship be- tween muscle length and myoelectric activity yielded disparate results. Some researchers reported a decrease in EMG activity as the muscle length increased [12,16,24] while others reported no change in EMG activity at different muscle lengths [22,25]. Only few investigations have been directed toward a comprehensive analysis of the interaction of the three factors of muscle length, muscle torque and concomitant EMG activity [12,15,16]. These studies have used surface, unipolar wire or con- centric needle EMG methods. Surface and monopolar electrodes are susceptible to crosstalk [13,26,27], while concentric needle technique does not allow for sampling the same motor units in different trials. This investiga- tion used a fine wire bipolar technique, which has the advantage of recording the same group of motor units through the change of joint angle. This study used a two-joint muscle model in which the length of the hamstrings was altered at the hip while keeping a constant lever arm at the knee. The main hypothesis of this study was that an increase in the length of the hamstring muscles would result in an in- creased torque with a decreased EMG output over that recorded at shorter lengths. 2. Methods EMG activity of six knee flexor muscles and isometric knee flexion torque were recorded from the dominant lower extremity of a group of normal healthy women. Data were collected during manual muscle testing and during maximum isometric knee flexion at varying po- sitions of the hip and knee. 2.1. Subjects Nineteen healthy adult women between the ages of 22 and 36 years volunteered for the study. Participants reported no history or signs of musculoskeletal or neu- rological dysfunction that would affect motor perfor- mance involving either lower extremity. 2.2. Instrumentation Myoelectric activity (EMG) of each muscle, was sensed by a pair of 50-lm insulated nickel–chromium alloy wire electrodes with hookedends. The paired wires were threaded through a single 1.5 in., 25 gauge, dis- posable needle. The electrode assembly was sterilized before use and discarded following insertion. The prox- imal ends of both wires were connected to a 2 cm2 pad that contained the ground plate taped to the ipsilateral leg near the insertion site. Shielded cables extending from the pads (one for each muscle) carried the signals to a telemetry package worn around the subject’s waist. Within this package the signals were differentially am- plified, filtered and transmitted by a six-channel FM– FM telemetry unit (Model 2600, Biosentry Telemetry INC, Torrance, CA, USA). The Telemetry system had a common mode rejection ratio of 58 dB. The modulation of each channel was adjusted to insure 100–1000 Hz frequency responses. The signals from these modulated channels then were telemetered to a multichannel on- line digital acquisition system using a DEC 11/23 com- puter (Digital Equipment Co., Maynard MA, USA). The computer sampled each channel at 2500 Hz. The filter system band passed the data from 80 to 1000 Hz, thus eliminating any 60 Hz or low frequency noise. Calibration was achieved by passing a 1 V, 400 Hz signal through the ground electrodes; a baseline noise level above 50 mV was not accepted. The instrumentation also included seven monitoring oscilloscopes, which allowed immediate viewing of the data. 570 O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 Knee flexor torque was measured using a Cybex II dynamometer (Lumex Co., Ronkonkoma, NY, USA). The dynamometer was attached to a table with an ad- justable back support which accommodated differing thigh lengths and could recline backward from 90� to 180�, and forward from 90� to 70�. The resistance arm of the dynamometer was adjustable to different leg lengths and was capable of being locked in varying degrees of knee flexion. The speed adjustment was set at 0 rad/s to provide an immovable dynamometer arm. Calibration of the dynamometer was performed using a series of certified weights placed on the dynamometer’s lever arm against which the torque output of the device was compared. A Dual Beam oscilloscope (Model 502A Tektronix Inc., Oregon, USA) was connected to the dynamometer and was used to provide an instant visual feedback of torque values to the subject. The oscillo- scope had two horizontal fluorescent beams; one was ‘‘static’’ and could be set at any desired level on the screen while the other beam moved to represent the amount of torque exerted at the dynamometer arm. A video camera and cassette recorder were used to docu- ment and store all steps in the study of each subject. 2.3. Procedure 2.3.1. Subject preparation and electrode insertions A training session was scheduled about an hour be- fore testing to familiarize the subject with the dyna- mometer and the visual feedback system. Height and weight (without shoes) were measured to the nearest cm, and to the nearest 0.5 kg, respectively. The leg that the subject used to kick a ball was determined as the dom- inant lower extremity. Straight leg raise (SLR) range of the dominant lower extremity was measured by a hand- held goniometer with the subject supine. Because of the study requirement to avoid passively stretching the knee flexor muscles, the full range of SLR was considered to be 10� less than the passive full range for each subject. Thus, for this study SLR equalled passive SLR minus 10�. Subjects with a SLR range equal to, or more than 90� were designated as the ‘‘long’’ muscle group. Those subjects with a SLR range of <90� were classified as having ‘‘short’’ hamstrings. All electrode insertions were in the dominant lower extremity, the wire electrode pairs were placed using Basmajian’s single needle technique [28] into the following six muscles; semitendinosus, semimembranosus, biceps fermoris (long head), biceps femoris (short head), sartorius and gracilis. After each insertion, the subject was asked to produce several contractions of that muscle to secure the wires. The wires were taped to the skin leaving a loose loop to assure that under high torque the electrodes would not be displaced. The proximal ends of the wires were at- tached to the ground electrode–telemetry system. Elec- trode placement was confirmed with a mild electrical current administered through the inserted wires to cause a visible or palpable contraction of each muscle. After confirmation of electrode placement the subject was asked to walk across the walkway at different speeds to ensure that the electrodes were settled within the muscles and to observe if discomfort existed that might have altered the normal pattern of walking. In any such case, the electrodes causing the discomfort were moved or replaced. 2.3.2. Manual muscle testing Manual muscle testing for the medial and lateral hamstrings and the gracilis muscle was performed with the subject in the prone lying position [29]. For the medial hamstring and gracilis muscles, maximum resis- tance to knee flexion was applied with the subject’s knee flexed to 75� and the leg medially rotated. For lateral hamstring muscles, the knee was flexed with the leg laterally rotated. The manual muscle test for the sartorius muscle was conducted with the subject in a sitting position at the edge of the plinth. Hip flexion was maximally resisted at the lower one-third of the thigh, while the other hand of the investigator prevented the pelvis from tilting poste- riorly. This modified sartorius test was chosen over the traditional test because a comparison of techniques showed that the selected procedure generated the highest EMG. 2.3.3. Dynamometer testing Torque and EMG data were collected during a series of nine combinations of hip and knee positions (Fig. 1). Maximum isometric knee flexion was performed with the knee at 0�, 45� and 90� while the hip was at 0� of flexion. The same knee angles were tested with the hip flexed to 90� and to the angle of SLR range minus 10�. Fig. 1. The nine test positions. O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 571 For ease of recording and comprehension the nine positions were coded in a four-digit sequence. The first two digits indicate hip angle and the last two digits represent knee angle (Fig. 1). For example: hip 0�, knee 0� ¼ 00–00, hip SLR, knee 45� ¼ SLR–45 and hip 90�, knee 90� ¼ 90–90. 2.3.3.1. Test sequence. A preset randomization order for maximum testing was prepared for each subject, which ensured: (1) that the same number of subjects performed each sequence and (2) avoidance of frequent changes of subject position between sitting and lying. Following recording knee flexor torque and EMG activity at all three knee angles in the first randomly selected hip po- sition, the same test procedure was then repeated at the second and then the third hip position with the knee angle again randomly ordered. For every position, the axis of the dynamometer arm was aligned with the axis of the knee joint (at the level of the femoral epicondyle). A baseline measurement was recorded with the leg resting on the cuff so that the torque produced by the weight of the leg would not be added to that produced by the contraction of the knee flexor muscles. After securing the test position, the monitoring oscilloscope used by the subject was set so that its two horizontal fluorescent beams were super- imposed at the baseline. The subject then was instructed to try as hard as she could to move the ‘‘dynamic torque beam’’ as high on the screen as possible. Verbal en- couragement was given during all tests. In each position, two maximum isometric contractions, of 5 s each, were performed. The highest torque value of the two testing trials was used for analysis. Stabilization of subjects was provided in a variety of ways, a firm wedge shaped pad was placed under the kneesurface, a pelvic strap was used to counteract dis- placement of the pelvis and another strap was placed firmly over the midthigh. The back support and seat depth were adjusted individually for each subject adding to her stability and comfort. The subject was encour- aged to grip the table for further support. 2.3.3.2. Target torque. Target torque testing was per- formed after the maximum knee flexion test in the po- sition of hip at 0�, knee at 90� (the shortest position for the hamstrings). The torque value achieved in that po- sition (00–90) was recorded and then the subject was asked to match it in the two following positions: hip at 90�, knee at 90�, and hip at SLR, knee at 0�, using the same visual feedback from the oscilloscope. 2.4. Data analysis 2.4.1. EMG data processing and quantification Digitization of the data was accomplished with the aid of a DEC 11/23 minicomputer with an AD converter to transfer the EMG signal into a discrete numerical output. All EMG data were digitized at 2500 samples per second. The digitized data were integrated using a VAX computer 750. The integration program first cal- culated the mean signal from the resting EMG trial to establish a noise threshold for each channel of EMG. The noise threshold value which then was subtracted for the remaining trials to correct for any DC interference in the signal form. The corrected values were rectified and summed to produce the integrated value of the EMG for each 1/50th second. Data from the manual muscle test were processed to yield a normalization factor against which subsequent EMG data were compared. EMG values from the isometric testing were expressed as a percentage of the maximum EMG obtained during the manual muscle test and abbreviated as %MMT. Torque data for each trial were printed out at 0.02 s intervals for the 5-s duration of the test. The mean value of the highest torque in any 1 s, and the EMG data associated with that interval, were used for analysis. 2.4.2. Statistical analysis A detailed screening analysis was performed on tor- que data and on the EMG data for all muscles. A two- way repeated measures analysis of variance (ANOVA) was employed to determine if there was a significant difference in torque or EMG data from all tested mus- cles between the group with long muscles (>90�) and the group with short muscles (<90�). The other factor was the testing angle. A two-way repeated measures ANOVA was used to determine the effect of hip and knee position on the torque and EMG data. Preliminary analysis revealed a significant interaction between the positions of the two joints. Consequently the effect of each joint was studied separately using one-way repeated measures ANOVA. Because separate analysis was done for each joint which required examining the same data twice, Bonferroni adjustment was made to ensure an overall alpha level of 0.05. A repeated measures ANOVA was also conducted to compare the EMG at target torque. All statistical procedures were conducted with the BMDP software program (Statistical Software Inc, Los Angeles, USA). 3. Results 3.1. Subject description The mean age for the group of 19 subjects was 27 years (range: 22–36 years), the mean height was 162 cm (range: 141–173 cm) and the mean weight was 61 kg. The maximum SLR measurement ranged from 70 to 106� with mean of 90�. There were two subjects with a left dominant lower extremity whereas in 17 subjects the right lower extremity was dominant. 572 O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 3.2. Repeated trials The EMG and torque values from the first trial of maximum isometric knee flexion in all nine tested posi- tions were significantly correlated with those obtained during the second trial (P < 0:0001). The correlation coefficients ranged from 0.91 to 0.97 for the torque values and from 0.77 to 0.99 for the EMG of all tested muscles. The majority (80%) of the correlations coeffi- cients were equal to or greater than 0.90 for EMG of all muscles in all positions. 3.3. Effect of inherent hamstring length on EMG and torque SLR range was significantly different between the long and short group (P < 0:00001). Age, weight and height data, however, did not contribute to significant differences between the two groups. The mean SLR range for the short group was 82.6 (SD, 6.3�) and for the long group was 98.8 (SD, 4.1�). According to responses on the screening questionnaire there was no discernible difference between the two groups in their customary lifestyle or recreational activity patterns. The two groups did not vary significantly with respect to EMG activity in any of the investigated muscles (P > 0:05). Neither were there significant differences in torque values between the two groups (P > 0:05). The lack of any significant differences related to inherent muscular length led to the dissolution of the grouping and all 19 subjects were treated thereafter as a single group. 3.4. Effect of change of hip positions on maximum isometric knee flexion torque Regardless of knee position, the extended hip posi- tion (0�) was always associated with significantly less torque than that recorded in the two flexed hip positions (SLR and 90) (Table 1, Fig. 2). For example, with the knee at 0�, peak torque with the hip at 0� was 581 kg cm, which was significantly lower than the 680 and 637 kg cm obtained in the SLR and 90� hip angles respec- tively. Similarly with the knee at 45� and hip at 0�, the value for maximum torque was 467 kg cm, which was significantly lower than the 719 and 716 recorded at the SLR and 90�. There was no significant difference be- tween the two sitting positions (SLR and 90�) with the knee at 45� (Table 1). 3.5. Effect of change of knee positions on maximum isometric knee flexion torque Flexion at 90� was the only knee position that influ- enced flexor muscle torque independent of hip angle, as the maximum isometric flexor torque was the least at all three hip positions. At the extended hip position (0�), all subjects generated their highest torque when the knee was fully extended (0�). The group mean was 580 kg cm. The magnitude of torque values declined significantly as knee flexion increased to 45� (467 kg cm) and fell to its lowest value at 90� (257 kg cm). Differences between the three knee angles were statistically significant (P < 0:05) (Table 1, Fig. 2). In the two sitting positions (hip SLR and 90�) the 90� knee angle, was associated with significantly lower mean torque values than the other two knee positions (0� and 45�). The highest mean knee flexion torque values were generated when the knee was at 45� with the hip at SLR and 90�. For example, with the hip at 90�, the three knee angles of 0�, 45� and 90� were associated with torque values of 637, 716 and 462 respectively; the differences Table 1 Maximum isometric knee flexion torque (kg cm), comparison of three hip and three knee positions Hip position Mean (SEM) Significant multiple comparison Knee 0� Knee 45� Knee 90� 0� 580 (33.4) 467.6 (30.5) 256.5 (24.1) Knee 0� versus 45�, 90� Knee 45� versus 90� SLR 680 (38.5) 719.2 (41.6) 437.1 (31.6) Knee 90� versus 0�, 45� 90� 637 (32.6) 716.1 (47.1) 461.5 (32.5) Knee 0� versus 45�, 90� Knee 45� versus 90� Fig. 2. Maximum isometric knee flexion torque at three positions of the knee and two hip angles (mean, SEM). O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 573 were significant between the three knee angles (Table 1, Fig. 2). 3.6. Effect of the most lengthened position on knee flexion torque When the hamstring muscles were tested in their most elongated positions (knee fully extended), the slight differences in length incurred when the hip varied be- tween SLR and 90� did not significantly alter knee flexion torque (P > 0:05). Fourteen of the 19 subjects regardless of their range of SLR, produced equal or slightlygreater torque at the SLR–00 versus the 90–00 position. 3.7. Effect of change of hip and knee position on EMG activity of the two-joint hamstrings The EMG activity of the two-joint hamstrings at maximum effort was not altered significantly with the change in hip angle at the three knee positions (P > 0:05). The only exception was the decreased ac- tivity of the semimembranosus where the mean value was 75% MMT with the hip at 0� as opposed to 90% MMT at the other two hip angles (Table 2). Similarly, the change in knee position did not significantly affect the EMG activity of the two-joint hamstrings, except for the semitendinosus where the mean EMG values were 68% MMT in the most lengthened position (90–00) compared to 86% in the most shortened position (00–90). 3.8. Effect of change of hip and knee positions on EMG activity of the other three knee flexors The change in hip position did not affect the EMG activity of the short head of biceps femoris. Knee angle change, however, resulted in significantly less EMG at the extended knee position (0�) compared to the other two knee-flexed positions (45� and 90�). This pattern was consistent in all three hip positions (Table 3). Altering the hip position affected the sartorius muscle only when the knee was at 0�. Significantly less activity was recorded when both the hip and knee were at the extended position 00–00, compared to the other hip-flexed positions (90� and SLR) (Table 3). Regardless of hip position, the extended knee angle (0�) was always associated with significantly less EMG activity in the sartorious muscle compared to the other flexed knee positions (Table 3). Gracilis activity did not significantly change with the change in hip position at the three tested knee angles. The change in knee position significantly affected its activity only with the hip at 0�, as the knee 0� position was associated with significantly less EMG than the other two positions (45, 90) (Table 3). 3.9. EMG Activity at target torque Reproduction of the maximum knee flexion torque recorded at the most shortened hamstring position (00– 90) in an intermediate (90–90) and then at the length- Table 2 EMG of the hamstring muscles Comparison of three knee and three hip positions EMG %MMT Mean (SEM) Knee 0� Knee 45� Knee 90� Hip at 0� STEN 77.7 (6.5) 89.4 (6.6) 87.3 (7.6) SMEM 86.2 (5.9) 94.3 (6.3) 75.3 (7.5)a BFLH 87.0 (6.8) 91.7 (7.9) 75.7 (8.1) Hip at SLR STEN 77.3 (7.0) 84.0 (8.4) 88.8 (7.6) SMEM 82.8 (6.3) 79.1 (5.8) 90.2 (5.9) BFLH 76.5 (4.8) 79.2 (6.0) 66.8 (7.4) Hip at 90� STEN 67.9 (6.3)b 80.2 (7.8) 86.2 (6.4) SMEM 82.2 (5.1) 81.6 (5.1) 90.0 (5.5) BFLH 74.6 (5.9) 75.9 (5.6) 70.8 (6.2) Abbreviations: BFLH¼ long head of biceps femoris, BFSH¼biceps femoris short head, GRAC¼ gracilis, MMT¼manual muscle test, SART¼ sartorius, SEM¼ standard error of the mean, SMEM¼ semimembranosus, STEN¼ semitendinosus, TQ¼ torque. a Significant multiple comparison, with Bonferoni adjustment with knee 90�; hip 0� versus hip SLR, 90�. b Significant multiple comparison, with Bonferoni adjustment with hip 90�; knee 0� versus 90�. Table 3 EMG of the other knee flexor muscles Comparison of three hip and three knee positions EMG %MMT Mean (SEM) Knee 0� Knee 45� Knee 90� Hip at 0� BFSH 66.8 (6.8)a 104.1 (7.7) 97.8 (8.4) SART 26.1 (4.9)a ;b 50.3 (7.8) 61.6 (11.4) GRAC 84.1 (7.6)a 102.8 (8.1) 104.4 (7.6) Hip at SLR BFSH 76.9 (6.0)c 98.0 (6.3) 104.7 (9.5) SART 43.5 (6.7)c 61.2 (8.4) 63.6 (7.3) GRAC 84.7 (8.4) 90.4 (9.7) 97.8 (8.3) Hip at 90� BFSH 67.4 (5.7)d 90.4 (7.8) 107.0 (10.8) SART 38.7 (6.6)d 61.6 (8.4) 69.8 (8.4) GRAC 81.4 (8.1) 89.3 (9.7) 102.0 (10.8) Abbreviations: see Table 2. a Significant multiple comparison with Bonferroni adjustment with hip at 0�; knee 0� versus 45�, 90�. b Significant multiple comparison with Bonferroni adjustment with knee at 0�; hip 0� versus SLR, 90�. c Significant multiple comparison with Bonferroni adjustment with hip at SLR; knee 0� versus 45�, 90�. d Significant multiple comparison with Bonferroni adjustment hip 90�; knee 0� versus 45�, 90�. 574 O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 ened position (SLR–00), showed significantly decreased EMG activity with lengthening of all investigated mus- cles. The difference was statistically significant between the three positions (P < 0:0001) with only one exception for the sartorius muscle (Fig. 3). There was no significant difference in the EMG activity of the sartorius between the most shortened and the intermediate positions, however, there was a statistically significant drop of ac- tivity at the SLR–00 position. The mean activity of the semitendinosus muscle decreased from 86% MMT at the most shortened position (00–90) to 60% MMT when the muscle was at an intermediate length position (90– 90). At the lengthened position (SLR–00) the semiten- dinosus exhibited an activity level of only 22% MMT (a 76% drop from the value recorded at the shortened po- sition; 00–90) (Fig. 3). The mean EMG activity of the semimembranosus muscle at the shortened position (00– 90), the intermediate position (90–90) and the lengthened position (SLR–00) were 78%, 53% and 28% of MMT, respectively. The long head of the biceps femoris muscle exhibited mean EMG values of 76% at SLR–00; 38% at 90–90; and 23% at 00–90. The short head of the biceps femoris and gracilis muscles followed the same pattern. 4. Discussion 4.1. Effect of inherent muscle length on isometric knee flexor torque Comparison of maximum isometric torque values between the long hamstring group and those with short hamstrings revealed no differences in any test position. This finding is in disagreement with data reported by Gossman et al., who found that subjects with short hamstrings produced greater peak torque than did those with long hamstrings [30]. In a later study however, they collected similar data on men and women and found no difference due to hamstring length in both groups [31]. Gossman et al. alluded to a gender bias in the first study as the reason for the disparate results. Hornsby et al. reported that women with ‘‘tight’’ triceps surae muscles produced significantly greater maximal plantar flexion torque than comparable women with loose calf muscles [32]. These differences held true both with the knee flexed and extended. Hornsby con- cluded that the triceps surae muscles of the tight group exerted more force as a result of the combined action of active and passive elements of muscle; the contribution of the passive elements (connective tissue, etc.) was es- pecially significant since two of the test positions (0� and 7� dorsiflexion) required greater than the available dorsiflexion range of the tight group ()15� to )6� of neutral) [32]. Thus, they had to force the foot of the tight group into the test position, which caused force re- cording before the development of any voluntary effort. In our study, a baseline measurement was taken with the subject in the test position. Recording of data started during voluntary contraction. We found no significant reduction in the EMG activity of the two-joint hamstring muscles between the short and long groups. Neither was there evidence to support an increased contribution of the one-joint muscle (biceps femoris short head), which suggests that both groups had a similar strategy to reach maximum knee flexion torque. 4.2. Effect of change of hip angle on isometric torque At all tested knee angles there was a significant drop in isometric knee flexion torque when the hip was at 0� as compared to the two sitting positions. The significant decline in knee flexor torque values in supine (hip at 0�) was consistent with previous reports for isometric knee flexion of normal subjects [9,11,12,33,34] and with re- ports on hemiparetic patients [35]. With the knee at a constant momentarm length, two interrelated factors explain the increased torque values found in lengthened muscle. One factor is the non-contractile component of the muscle, which has two elements; one is parallel with the muscle fibers (the endomysium, perimysium and epimysium), while the other is in series with the muscle (tendons and tendon bundles within the muscle, etc.). These connective tissue sleeves, when stretched, produce passive tension that is added to the active tension gen- erated by muscle contraction. At shorter lengths these passive elements are slack and their contribution to tension gradually decreases as the amount of slack in- creases. The second factor is the effectiveness of the contractile element of the muscle; i.e. a length–tension relationship as explained by Huxley’s sliding filament model [36,37]. In this model there is an optimal position at which maximum overlap between the thick and thin filaments occurs which results in production of maximum tension. Lengths shorter or longer than this optimal length accommodate fewer actin–myosin bonds and, therefore, there is a decrease in the produced tension. The hip 0� position lengthens the sartorious muscle. Its small Fig. 3. EMG of all tested muscles at target torque (mean, SEM). O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 575 cross sectional area however, limits its contribution to the knee flexor torque when compared to the hamstrings. 4.3. Effect of change of knee angle on isometric torque The maximum knee flexor torque recorded at 90� of knee flexion was consistently lower than that recorded at the other two knee angles. With the hip extended and the knee at 90� (the most shortened position) the mean torque was only 44% of that recorded at the same hip position with the knee at 0�. In some subjects, the decrement in torque in the most shortened position (00–90�) was more dramatic than others as evidenced by the large standard deviation of torque values at this position. The decreased ability of some subjects to produce torque at the most shortened hamstring length could not be related to discomfort as a result of a tight rectus femoris. Subjects for this study were evaluated for a tight rectus femoris muscle; with the hip at 0� all of the subjects were able to actively flex the knee at least 15� past the 90� required for the shortest test position. Active insufficiency is a possible explanation for decreased flexion torque in the most shortened position. The term active insufficiency refers to a decrease in production of muscle tension when the muscle is contracting at a very short length due to a disadvantageous positioning of the actin and myosin filaments [36,38]. Gordon et al. proposed that at ex- tremely short muscular lengths, the filaments from the opposite Z lines overlap resulting in a marked decrease of tension [38]. The effect of shorter muscle length was more pro- nounced when the hamstring muscles were shortened at both joints than at one joint. In supine with the hip joint at 0�, a decrease in knee flexion angle from 90� to 45� to full extension, resulted in a gradual increase in maxi- mum isometric torque values which reached maximum at full extension. These results are in agreement with previous reports on the knee flexors [9,33,34,39]. With the hip at 0�, the two-joint hamstrings are shortened at the proximal end and additional shortening is caused by increasing the knee flexion angle which greatly reduced the efficiency of muscle contraction. This insufficiency was shown by the 56% reduction in torque values at the 90� flexion angle when compared to full extension. These results are similar to those of Smidt et al. who reported a 43% decrease in peak torque at the 90� angle of knee flexion as compared to the peak torque recorded at 5� of knee flexion [39]. At different angles of knee flexion, Smidt measured lever arm lengths of the knee flexors from serial X-rays. He found that the maximum moment arm of 4.08 cm occurred at 45� of knee flexion. Moment arm lengths decreased with both increase and decrease of knee flexion angle from the 45� position. Although the 45� of knee flexion provided the best mechanical advantage for the hamstrings [39], the maximum isometric torque occurred at full knee extension when the hip was held in extension. It appears that with the hip extended (0�), the hamstrings were more affected by the length change than by the mechanical change of the moment arm at the knee joint. During sitting, however, the knee angle at which the highest mean flexor torque occurred was 45�, and this held true at hip angles of both 90� and SLR. That angle of maximum torque varied, however, between subjects; 12 of 19 subjects produced their maximum torque at the 45� knee angle in the sitting position with the hip at 90�, while the remaining seven subjects generated more tor- que at the 0� knee angle. The variation of the angle at which peak torque occurred during knee flexion between subjects has been pointed out by a number of investi- gators [33,34,40,41]. Walsmsley and Yang commented that nine of their 10 subjects generated their maximum torque at a knee angle of 30�, while one registered the greatest torque at the 0� position. In another study, Bender and Kaplan noted that 13 of 20 subjects created greater torque at 0� but the remaining seven subjects were able to generate higher torques at the 45� angle [40]. Inconsistency of the angle of peak torque also has been noted in patients with knee injuries. Mendler et al. wrote that in the sitting position the 45� knee angle was associated with maximum isometric force in half of her subjects [42]. The other half reached their peak torque at 10� of knee flexion (the 0� angle was not tested). These findings suggest an interaction between optimum muscle length and moment arm. The torque values obtained here at the maximum muscle length (90–00) were not different from those obtained at an intermediate length where the muscles had their maximum moment arm at the knee (90–45�). This means that the increased ham- string lever arm compensated for the decrease in muscle length that occurred as a result of flexing the knee from 0� to 45�. That compensatory mechanism was greatly impaired when shortening the hamstrings by extending the hip with the knee flexed, as evidenced by torque decline, which compromised both factors. 4.4. Effect of hip and knee angle on EMG activity of the knee flexors In general, the two-joint hamstring muscles as a group did not show any significant or consistent change in EMG activity with alteration in the length of the muscles by hip or knee joint position changes. One exception was the 16% decline of EMG of the semi- membranosus at the most shortened position (00–90) compared to the two sitting positions (90, SLR). The second exception is the decreased activity of the semi- tendinosus in sitting (hip at 90) with the knee at 0 compared to the other two flexed knee positions. Regarding semimembranosus, similar results have been reported for the gastrocnemius muscle at the knee- 576 O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 flexed position [13,15]. Using single motor unit record- ings Kennedy et al. reported decreased recruitment of the medial gastrocnemius muscle during plantar flexion when the knee was flexed to 90� [15]. This was attributed to the diminished force-producing capabilities of the muscle as a result of its reduced length. When compar- ing the architectural characteristics of the human semi- membranosus to the other two hamstrings, Wickiewicz et al. reported that it had the largest angle of pennation and the shortest fiber length [43]. It is possible that in the most shortened position, some motor units were not active because they are in a position where they can no longer produce active force. An important factor to consider is the change of angle of pennationunder tension; Fukunaga et al. found that the angle of pen- nation increased during isometric contraction in the human vastus lateralis muscle [44]. In other words the capability of motor unit to produce force is affected not only by their inherent architectural features but also by the change in these features during contraction. The decreased activity of the semitendinosus muscle in the most lengthened position (90–00) as compared to the other two knee-flexed positions might be explained by the interaction of the muslce’s length and the ana- tomical location of its tendon. When the knee is fully extended, the semitendinosus tendon lays very close to the axis of the knee joint, providing a poor lever arm for knee flexion. This suggests its insufficiency as a knee flexor; in addition, the muscle is elongated at the both joints. The interaction of these two factors might have caused the observed decline of EMG activity. The general consistency of the EMG activity of the two-joint hamstrings at different muscle lengths at maximum effort, reported in this paper, agree with other reports of normal subjects for the biceps brachii [22,45,46] and the quadriceps muscles [47–50]. Data from a substantial number of investigations are in dis- agreement in that they cite increases of EMG activity at shorter muscle lengths [12,16,20,24,51–53]. The level of force at which EMG was recorded in the various studies is one source of conflict. Andriacchi et al. recorded EMG from the knee flexors and extensors as they re- sponded to constant unidirectional loads that tended to flex or extend the knee [16], more EMG activity was recorded in the hamstring muscles as the knee angle increased. The fact that Andriacchi used constant loads did not mean that the muscle exerted constant effort. A change of joint angles alters both the muscle’s lever arm and length. Resisting a constant load might demand a maximum effort from the muscle at one position, where at other positions it requires only a submaximal effort, which could explain the decrease in EMG activity. The studies that investigated maximum isometric effort at various angles reported no difference between EMG activity as the muscle length changed [22,46–48,50] which is in agreement with the results of this study. Lunnen’s data were in conflict with those of the present study. They found a consistent trend of de- creased activity in the hamstring muscles as the hip angle was increased, but which was only significant when the hip was flexed to 135� (subject sitting and leaning forward) [12]. The decreased EMG activity in Lunnen’s study might have occurred because of the use of surface electrodes. As the hip angle was increased from supine (0�) to sitting (135�), the tendon of the muscle might have been pulled closer to the recording electrodes which may have caused a decrease in the amount of EMG that could be sensed. Significant re- duction of EMG activity has been demonstrated when the recording electrodes were moved away from the center of the muscle and closer to its tendon [27]. In- tramuscular electrodes have been shown to move with the muscle during contraction and length change [45]. Studies on cineplastic muscles also have reported decreased EMG activity with increased muscle length [20,24]. The difficulty of extrapolating results from such a model to normal muscle is that a cineplastic muscle has been detached from its original insertion site and its new attachment confers major shortening on the mus- cle. It has been well documented that induced muscle shortening not only decreases maximum muscle force but also changes both active and passive length–tension relationships as the sarcomeres adapt to the new length [54–56]. The literature does not shed any light on the function of the short head of the biceps femoris with which the results of this study could be compared. Such reports as do exist on that one-joint knee flexor muscle, concern its function during normal walking and similar submaximal functional activities. The same comment can be made regarding the sartorius and gracilis muscles. All non-hamstring knee flexors (short head of biceps femoris, sartorius and gracilis) decreased their myo- electric activity at full knee extension. Since the short head of the biceps femoris does not cross the hip, it follows that hip position should have no effect on its function. This was indeed the case, as a change of hip angle at the three tested knee positions did not alter its level of EMG activity. The extended knee angle, how- ever, caused a 34% decrease in activity of the short head compared to the knee-flexed positions. The sartorius on the other hand, should have been influenced by alterations in both hip and knee angles. The maximum activity of the sartorius muscle occurred dur- ing sitting with the knee at 90�, the other more extended hip positions did slightly decrease its level of activity. The difference only was statistically significant between the fully extended and fully flexed hip position with the knee at 0�. This pattern of activity suggested that the flexed hip position favored the sartorius, which is, after all, a flexor muscle at both joints. The gracilis muscle was continu- ously active during maximal efforts and the activity O. Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 577 seemed independent of hip angle and only weakly de- pendent on knee angle. The gracilis is primarily a hip adductor, and according to some sources [29,57] it con- tributes to knee and hip flexion. The data in this study support its contribution to knee flexion. Change in hip angle however, did not result in any major changes in gracilis EMG activity. One possible flaw in this discus- sion may arise from the fact that these two strap-like muscles (sartorius and gracilis) have such a small cross- sectional area that a small EMG difference and a small torque differences might be magnified in importance. The semitendinosus, sartorius and gracilis muscles share a common insertion site at the medial side of upper part of the tibia ‘‘pes anserinus’’. These three muscles had a common response of decreased EMG activity when the knee was fully extended. It is easy to demonstrate on cadaver specimens that during full knee extension the tendons of these three muscles are placed very close to the knee joint axis. The lever arm of these muscles decreases which place them in a less efficient position to produce knee flexion, which may explain their decreased activity at the extended knee angle. 4.5. EMG activity at target torque When the subjects were asked to reproduce, at lengthened positions, the same amount of torque gen- erated in the most shortened position (00–90) the EMG activity significantly decreased. This implied that pro- duction of a given torque in a lengthened position re- quires fewer motor units than the same torque in the shortened position. These results are in agreement with other investigations [12,16]. Using surface electrodes, Lunnen et al. found that the EMG activity of the biceps femoris muscle declined when his subjects reproduced a submaximal torque at a lengthened position [12]. In this study when the two-joint hamstring muscles were elongated, not only were their activity reduced but the short head of the biceps femoris, the sartorius and the gracilis also had a significant drop-off in their level of participation. The reduction of activity was dispersed among the active muscles and no one muscle was re- sponsible alone to meet the torque demand at any po- sition, even when the demand was well below maximum. Major knee flexors contributed more to torque by virtue of their greater cross-sectional area. The minor flexors contributed less by virtue of their smaller cross-sectional area. Contribution of individual muscles to a given effort cannot be measured where multiple muscles act synergistically. 4.6. Generalrelationship of maximum flexion torque to EMG The ratio between torque output and EMG activity may be considered as indication of ‘‘efficiency’’. EMG indicates the number of active muscle fibers and torque is a measure of muscle output. Thus muscles that pro- duce high torque with low EMG are more energy effi- cient than the opposite case. The two-joint hamstrings contributed the most to knee flexion torque by virtue of their large cross-sectional area. 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Mohamed et al. / Clinical Biomechanics 17 (2002) 569–579 579 Relationship between wire EMG activity, muscle length, and torque of the hamstrings Introduction Methods Subjects Instrumentation Procedure Subject preparation and electrode insertions Manual muscle testing Dynamometer testing Test sequence Target torque Data analysis EMG data processing and quantification Statistical analysis Results Subject description Repeated trials Effect of inherent hamstring length on EMG and torque Effect of change of hip positions on maximum isometric knee flexion torque Effect of change of knee positions on maximum isometric knee flexion torque Effect of the most lengthened position on knee flexion torque Effect of change of hip and knee position on EMG activity of the two-joint hamstrings Effect of change of hip and knee positions on EMG activity of the other three knee flexors EMG Activity at target torque Discussion Effect of inherent muscle length on isometric knee flexor torque Effect of change of hip angle on isometric torque Effect of change of knee angle on isometric torque Effect of hip and knee angle on EMG activity of the knee flexors EMG activity at target torque General relationship of maximum flexion torque to EMG References
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