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J Appl Physiol 97: 1908-1914, 2004. First published June 25, 2004; doi:10.1152/japplphysiol.00084.2004
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Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo

Jens Bojsen-Møller,1 Philip Hansen,1 Per Aagaard,1 Ulla Svantesson,2 Michael Kjaer,1 and S. Peter Magnusson1

1Sports Medicine Research Unit/Team Danmark Test Center, Bispebjerg Hospital, University of Copenhagen, 2400 Copenhagen NV, Denmark; and 2Department of Orthopaedics, University of Gothenburg 405 30, Sweden

Submitted 26 January 2004 ; accepted in final form 16 June 2004


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The human triceps surae muscle-tendon complex is a unique structure with three separate muscle compartments that merge via their aponeuroses into the Achilles tendon. The mechanical function and properties of these structures during muscular contraction are not well understood. The purpose of the study was to investigate the extent to which differential displacement occurs between the aponeuroses of the medial gastrocnemius (MG) and soleus (Sol) muscles during plantar flexion. Eight subjects (mean ± SD; age 30 ± 7 yr, body mass 76.8 ± 5.5 kg, height 1.83 ± 0.06 m) performed maximal isometric ramp contractions with the plantar flexor muscles. The experiment was performed in two positions: position 1, in which the knee joint was maximally extended, and position 2, in which the knee joint was maximally flexed (125°). Plantarflexion moment was assessed with a strain gauge load cell, and the corresponding displacement of the MG and Sol aponeuroses was measured by ultrasonography. Differential shear displacement of the aponeurosis was quantified by subtracting displacement of Sol from that of MG. Maximal plantar flexion moment was 36% greater in position 1 than in position 2 (132 ± 20 vs. 97 ± 11 N·m). In position 1, the displacement of the MG aponeurosis at maximal force exceeded that of the Sol (12.6 ± 1.7 vs. 8.9 ± 1.5 mm), whereas in position 2 displacement of the Sol was greater than displacement of the MG (9.6 ± 1.0 vs. 7.9 ± 1.2 mm). The amount and "direction" of shear between the aponeuroses differed significantly between the two positions across the entire range of contraction, indicating that the Achilles tendon may be exposed to intratendinous shear and stress gradients during human locomotion.

triceps surae; Achilles tendon; ultrasound; connective tissue mechanical properties; tendon shear strain; intratendinous stress

THE HUMAN TRICEPS SURAE muscle-tendon structure is intricate in constitution and function, with three separate muscle compartments that merge via their aponeuroses into a common tendon to ultimately insert on the calcaneus. The combined forces generated by the triceps surae muscles during locomotion are transmitted to the Achilles tendon and may reach 1,400–2,600 N during walking and 3,100–5,330 N during running (13, 15, 34). It has been suggested that these large forces imposed on the tendon contribute to various loading-related pathologies such as tendinopathy (19), although the exact etiology remains largely intangible. Consequently, a more detailed understanding of the intrinsic contraction properties of the multipart triceps surae structure may contribute to the development of future treatment paradigms and/or prophylactic intervention models.

Information on the mechanical properties and function of the aponeurosis and tendon have traditionally been based on measurements on animal (10, 22, 23, 33) and human cadaver studies (7, 31, 37). Advances in imaging technology have recently enabled in vivo investigation of these properties (14), and two recent reports on humans have shown that the strain of the free Achilles tendon is considerably greater than that of the aponeurosis during voluntary contractions in vivo (12, 27). However, to what extent activation of the individual muscles of the triceps surae complex influences aponeurosis and tendon strain remains unknown.

A previous in vitro study demonstrated that differences in medial and lateral forces in the Achilles tendon can be observed when single muscles of the triceps surae were subjected to force (1), and Kawakami et al. (20) have reported nonuniform changes in estimated muscle length in vivo between the triceps surae muscle compartments. Uneven shortening of the muscles and nonuniform tendon force would theoretically result in intratendinous shear strain and cause sliding between planes of tissue layers parallel to the acting forces. Because the triceps surae includes the gastrocnemii muscles, which cross both the ankle and knee joints, and the soleus muscle, which crosses the ankle joint alone, the relative contribution of these muscles to the tendon force will be influenced by the degree of knee flexion (9). Contraction-induced intratendinous shear strain is presently not quantifiable in vivo. However, displacement of the insertion aponeurosis during muscle contractions may be assessed with ultrasonography (14, 21, 26, 28), and, because the collagen fibers of the aponeurosis fuse distally to become free tendon structures, any difference in displacement at the level of the aponeuroses may be manifested as shear strain at the level of the tendon.

A pilot study (see MATERIALS AND METHODS) on human cadaver material confirmed that the proximal part of the soleus and gastrocnemius aponeuroses are separate structures, and it was therefore hypothesized that the gastrocnemius and soleus aponeuroses can undergo differential displacement, which would further be influenced by knee joint position. Consequently, the purpose of the present study was to investigate the influence of knee joint position on the patterns and magnitude of displacement of the gastrocnemius and soleus aponeuroses during isometric muscle actions in vivo.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
An in vitro pilot study was performed on five cadavers to investigate the intrinsic connective tissue structures of the triceps surae (Figs. 1 and 2). In all cadaver specimens, the soleus and gastrocnemius aponeuroses were separate structures proximal to their common junction, as the compartments were easily separated. This in vitro observation supported the initial hypothesis that sliding between soleus and gastrocnemius aponeuroses is mechanically possible during muscular contraction. However, approaching the aponeurosis junction in a distal direction, transverse collagen structures were observed constituting a gradual increase in "firmness" of the aponeurosis connection (Fig. 1). The transverse structures were not apparent in all cadavers (Fig. 2) confirming previous observations (18, 30) that individual variation exists regarding the structure of the soleus-gastrocnemius aponeurosis junction.



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  		Fig. 1. Medial view of a cadaver dissection of the gastrocnemius-soleus junction proximal to the Achilles tendon. Collagen structures connecting the 2 separate aponeuroses (interaponeurosis connections) increase distally toward the aponeurosis junction. These were not apparent on all cadavers (see Fig. 2), and it was in most cases possible to completely separate the aponeuroses until the junction by firm insertion of a finger into the interaponeurosis space. These structures likely exhibit dissimilar mechanical properties in vivo; however, the effects of cadaver fixation on the strength and stiffness of the transverse collagen structures remain to be investigated.

 


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  		Fig. 2. Medial view of a cadaver dissection of the lower leg, illustrating the most common type of junction between the gastrocnemius and soleus muscles (18, 30). The 2 structures contribute equally to the Achilles tendon. On this cadaver specimen, the junction was well defined and had minimal connecting aponeurosis structures proximal to the junction.

 
Subjects.   Eight healthy male subjects with a mean ± SD age, body mass, and height of 30 ± 7 yr, 76.8 ± 5.5 kg, and 1.83 ± 0.06 m, respectively, volunteered for the study. The subjects were recreational athletes accustomed to various physical activities, including running and cycling. All subjects were informed about the study procedures and provided their informed consent before participation. The local ethics committee approved the experimental procedures.

Experimental setup.   The experimental setting consisted of two custom-built rigid steel frames in which isometric plantar flexor force and tendon-aponeurosis mechanical properties were examined. All tests were performed unilaterally (right leg) with the subtalar joint in the anatomically neutral position and with the tibia at a 90° angle to the sole of the foot. One steel frame was necessary for each knee joint position. 1) The extended-knee frame enabled subjects to be seated with the knee fully extended and the hip flexed to ~70°. This experimental device has been described in detail previously (28). 2) The flexed-knee frame allowed firm vertical fixation of the lower leg while subjects were seated with the knee joint flexed to 125 ± 4° and hip joint flexed to ~100° (Fig. 3). In both devices, the foot rested against an adjustable, steel footplate with the mechanical axis of rotation collinear with the lateral malleolus. Subjects did not wear shoes during testing, and the design of the foot plates prevented displacement of the foot on the footplate during plantar flexion efforts. To assess plantar flexion moment (N·m), a strain gauge load cell was attached between the footplate and the steel frame at a known distance from the axis of rotation.



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  		Fig. 3. Experimental setting consisted of 2 custom-built rigid steel frames allowing isometric plantar flexion contractions with extended knee (left) and maximally flexed knee (right). The steel frames enabled firm fixation of the experimental leg, thereby minimizing any joint movement during contraction efforts. The adjustable footplate was aligned such that the axis of rotation corresponded to that of the ankle joint. All tests were performed unilaterally with the right leg. The ultrasound transducer (A) was strapped securely to the skin, and plantar flexor moment was obtained with a strain gauge (B) that was connected to the adjustable footplate.

 
Experimental design and procedures.   After careful preparation of the skin by light abrasion and cleansing with alcohol, pregelled bipolar Ag-AgCl surface electrodes (type QN-10-A, Medicotest, Ølstykke, Denmark) were placed over the distal half of the muscle bellies of the medial gastrocnemius, lateral gastrocnemius, soleus, and tibialis anterior. Electrodes were positioned parallel to the approximated fiber direction with a 20-mm interelectrode distance. A reference electrode was placed over the facies medialis of the tibia. An electrical goniometer (G180, Penny and Giles, Biometrics, Gwent, UK) was placed laterally across the ankle joint to monitor joint angle. The goniometer was firmly secured with tape over the distal part of the fifth metatarsal and the distal-lateral part of the fibula.

The subjects were positioned tightly in the extended-knee frame, which was individually adjusted so that no hip or knee joint movement and no vertical displacement between the lower back and the backrest occurred during the plantar flexion efforts. An ultrasound probe (7.5-MHz linear array B-mode, width and depth resolution, 0.51 and 0.34 mm, respectively; Sonoline Sienna, Siemens, Erlangen, Germany) was fitted into a custom-made rigid cast that was secured onto the skin of the subjects in the sagittal plane at a distance of 286 ± 20 mm from the heel pad. The probe was positioned so that fascicles of both the distal medial gastrocnemius and the more profound soleus were visible within the ultrasound image. In accordance with previous reports (26, 28), the ultrasound probe did not shift position during muscular contraction.

Five forceful plantar flexion contractions were performed as preconditioning of the triceps surae muscle-tendon complex (29). After preconditioning, the subjects performed three isometric contractions by gradually increasing plantar flexor force over a 10-s period from a relaxed state to maximal effort. Each ramp trial was separated by a 2-min rest, during which the subjects were allowed to flex the knee joint. In a separate experiment performed to correct for ankle joint movement, an investigator rotated the foot about the ankle joint from ~5° of plantar flexion to 5° of dorsiflexion, while the subject remained relaxed (passive trial). The electromyogram (EMG) signals were evaluated online to ensure that no muscle activation occurred during the passive trial. To assess the level of coactivation in the antagonist muscle during the plantar flexor ramp contractions, the subjects performed three maximal voluntary dorsiflexion contractions. For this task, a rigid strap was placed over the dorsal and distal part of the metatarsals and connected to the strain gauge cell, enabling concurrent measurement of dorsiflexor force and muscle EMG. Each dorsiflexor effort lasted ~5 s separated by a 2-min rest period.

Subsequently, the subjects were placed in the flexed-knee frame and the above-described procedures were repeated: after the lower leg was firmly fixed in a vertical position over the horizontal foot, the subjects performed five maximal preconditioning contractions with the plantar flexor muscles, three isometric 10-s force ramps, and one passive trial. Finally, a passive baseline sweep was performed to determine the weight of the foot and foot plate.

The duration of the total experimental session was ~120 min/subject and involved in total 16 plantar flexor and 6 dorsiflexor contractions.

Data sampling and signal processing.   EMG activity was registered during all tasks by using custom-made amplifiers with a frequency response of 20 Hz to 10 kHz and 1:1 preamplifiers. The EMG signals obtained during the ramp contractions and passive trials were full-wave rectified, integrated, and averaged with a time constant of 200 ms online (3). EMG, force, and joint angle data were sampled at 50 Hz during these tasks to match the frequency of the video frame capturing, whereas during dorsiflexor trials force, goniometer, and EMG signals were recorded at 1 kHz. For subsequent analysis, the force, EMG, and goniometer data were stored on a personal computer using an external analog-to-digital converter (DT 2801A, Data Translation). The ultrasound S-VHS video images obtained during ramp and passive trials were simultaneously and continuously sampled at a rate of 50 Hz on a separate computer utilizing frame-by-frame capturing software (Matrox Marvel G400-TV, Dorval, Canada). The two computers were interconnected to enable synchronous sampling, by use of a custom-built trigger device that provided a visual marker on the ultrasound video image and simultaneously initiated sampling of the force, EMG, and goniometer signals via the analog-to-digital converter (5, 27).

Analysis of aponeurosis displacement.   On the ultrasound images, the triceps surae aponeurosis structure is visible as two parallel hyperechoic lines at an oblique angle to the skin surface (Fig. 4). Echoes corresponding to the muscle fascicles of the soleus and medial gastrocnemius can be observed in the classical pennate pattern inserting at their respective aponeuroses at which interfascicle connective tissue can be defined as hyperechoic aponeurosis fixed points.



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  		Fig. 4. Ultrasound images of the plantar flexor muscles obtained at rest (A) and at plantar flexion moment of ~50 N·m (B) in the extended-knee position. The soleus and gastrocnemius insertion aponeuroses (note the separation of aponeuroses) can be seen as high-echogenic transverse structures across the images, separating the muscle compartments of the gastrocnemius and soleus. The aponeuroses continue distally (right) to form the gastrocnemius and soleus junction and ultimately the Achilles tendon. Two fascicle fixed points are identified in A and B. Note that displacement of the gastrocnemius aponeurosis exceeds that of the soleus at 50 N·m because of the extended-knee joint position.

 
The longitudinal displacement of such fixed points during graded contractions was considered to represent the magnitude of deformation of the combined aponeurosis and free tendon distal to this point (14, 17, 27, 28) (Fig. 4). Before analysis of the displacement, each video sequence was carefully evaluated to identify five to nine high-echogenic fixed points in the medial gastrocnemius and soleus compartments, respectively, which were observable throughout the entire ramp contraction. Because it has previously been shown that there is no difference in aponeurosis displacement between two subsequent maximal efforts (27), the sequence exhibiting the most clearly visible fixed points from the three video sequences recorded in each trial was selected for further analysis. Displacement was measured with an automated tracking software using a pyramidal implementation of the Lukas-Kanade feature tracking (6); this provided a frame-by-frame displacement of the defined fixed points. This method has previously been described and evaluated in detail (5, 16, 27). For each trial, the selected ultrasound video sequence was analyzed three times for displacement of the medial gastrocnemius aponeurosis. Subsequently, the same sequence in a given contraction was analyzed three times for displacement of the soleus aponeurosis. The single analysis sequence yielding the greatest maximal displacement (5) for medial gastrocnemius and soleus was used for further analysis.

It has been reported that passive angular joint movement results in considerable aponeurosis displacement (27, 28, 35). Thus, if any ankle joint movement should occur in the direction of plantar flexion during the ramp contractions, the observed aponeurosis displacement would be attributed to both joint angular rotation and contraction-related tissue deformation. To correct for contamination of the displacement due to joint movement, individual ratios of the aponeurosis displacement relative to joint angular movement (mm/°) were obtained from the passive trials, by plotting fascicle displacement as a function of ankle joint angle (27, 28). The correction factor was determined separately for the soleus and medial gastrocnemius muscles in the two knee joint positions. This correction procedure could not be performed for one subject because of erroneous goniometer data.

Calculation of plantar flexion moment.   Plantarflexion moment was calculated by multiplying the strain gauge force by the perpendicular distance to the axis of joint rotation. In the flexed-knee position, where the foot and foot plate were situated in the horizontal plane, strain gauge force was corrected for the effect of gravity on the foot plate and forefoot. To correct for the force contributed by coactivation of the antagonist muscle (m. tibialis anterior) during the graded plantarflexion contractions (27, 28), a linear relation was assumed between EMG amplitude and muscle tension (24, 36).

Calculation of interaponeurosis shear displacement.   For each subject, the relations between plantar flexion moment and aponeurosis displacement for both the soleus and medial gastrocnemius aponeuroses were established in the two knee joint positions. In both positions, interaponeurosis shear displacement at the site of the triceps surae where the ultrasound probe was located was determined by subtracting the displacement of the soleus aponeurosis from the displacement of the medial gastrocnemius aponeurosis throughout the entire range of contraction effort.

Statistics.   Two-tailed Wilcoxon's signed-rank tests were used to evaluate the differences in aponeurosis displacement between muscles and between the two knee joint positions. An alpha level of P < 0.05 was considered significant. Results are reported as group means ± SE.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Maximal plantar flexion moment during ramps was greater in the extended-knee position (132 ± 20 N·m) compared with the flexed-knee position (97 ± 11 N·m; P < 0.05). In the extended-knee position, the corresponding aponeurosis displacement at maximal effort for the medial gastrocnemius (12.6 ± 1.7 mm) exceeded that for the soleus (8.9 ± 1.5 mm; P < 0.05), whereas in the flexed-knee position displacement of the soleus (9.6 ± 1.0 mm) was greater than displacement of the medial gastrocnemius (7.9 ± 1.2 mm; P < 0.05) (Fig. 5).



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  		Fig. 5. Plantar flexion moment and aponeurosis displacement for the 2 knee joint positions. Left: maximal moment during ramp contractions in the extended (Ext)-knee and flexed-knee positions. A significant difference in plantar flexion moment was observed between the 2 positions (132 ± 20 N·m vs. 97 ± 11 N·m) because of the lesser capacity of the gastrocnemius muscle in the flexed-knee position. Right: corresponding displacements for the medial gastrocnemius (MG) and the soleus (Sol) aponeuroses in the 2 knee joint positions. In the extended-knee position, displacement of MG exceeded that of Sol (12.6 ± 1.7 vs. 8.9 ± 1.5 mm), whereas the displacement of the Sol was greater than that of the MG (9.6 ± 1.0 vs. 7.9 ± 1.2 mm) in the flexed-knee position. *P < 0.05.

 
When tendon-aponeurosis displacement was analyzed to the greatest common level of plantar flexion moment achieved in the two knee joint positions for each subject, which corresponded to the maximal force in the flexed-knee position, displacement of the medial gastrocnemius aponeurosis (9.0 ± 0.8 mm) exceeded that of the soleus in the extended-knee position (6.2 ± 0.6 mm; P < 0.05), whereas the soleus displacement was greater than that of the medial gastrocnemius in the flexed-knee position (values reported above). Displacement of the soleus aponeurosis was less in the extended-knee position compared with the flexed-knee position (P < 0.05), whereas displacement of the medial gastrocnemius aponeurosis did not differ significantly between the two positions (Fig. 6).



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  		Fig. 6. Aponeurosis displacement for the MG and Sol muscles corresponding to the greatest common effort level of the 2 positions achieved by each subject. At the common effort level, MG displacement exceeded that of Sol in the extended-knee position (9.0 ± 0.8 vs. 6.2 ± 0.6 mm), whereas Sol displacement was greater than that of MG (9.6 ± 1.0 vs. 7.9 ± 1.2 mm) in the flexed-knee position. Furthermore, Sol displacement in the extended position was less than that in the flexed position (P < 0.05), whereas there was no difference between the 2 positions for MG displacement. *P < 0.05.

 
Interaponeurosis shear, which was estimated as the difference in the displacement of the soleus and medial gastrocnemius aponeuroses (soleus displacement subtracted from that of the medial gastrocnemius), was determined for the two knee joint positions at increasing levels of exertion until the greatest common level of plantar flexion moment (Fig. 7). The magnitude of aponeurosis shear displacement differed significantly between the two positions throughout the common range of ramp moments (10–87 N·m).



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  		Fig. 7. Anterior-posterior shear between the MG and Sol aponeuroses. Shear displacement between the 2 aponeuroses was determined by subtracting the displacement of the soleus aponeurosis from that of the medial gastrocnemius throughout ramp contractions in the 2 knee joint positions. In the extended-knee position, displacement of the gastrocnemius exceeded that of the soleus, whereas the opposite occurred in the flexed-knee position. A significant difference was observed between the 2 knee joint positions in the interaponeurosis shear displacement at plantar flexion moments of 10–87 N·m (*P < 0.05). The effect size was reduced at moments >87 N, which could only be achieved by 4 of 8 subjects in the flexed-knee position.

 
The greatest interaponeurosis shear displacement in the extended-knee position (medial gastrocnemius displacement > soleus displacement) was 4.0 ± 0.7 mm, whereas the greatest shear displacement was 2.0 ± 0.5 mm (medial gastrocnemius < soleus) in the flexed-knee position. These values corresponded to ~32% of the maximal displacement of the medial gastrocnemius aponeurosis in the extended-knee position and ~21% of maximal displacement of the soleus aponeurosis in the flexed-knee position.

The relation between joint angular rotation and aponeurosis displacement was linear (r > 0.98). The resulting correction factor with the knee extended was 0.68 ± 0.07 mm/° for the medial gastrocnemius and 0.69 ± 0.06 mm/° for the soleus. The corresponding values with the knee flexed were 0.56 ± 0.03 mm/° for the medial gastrocnemius and 0.65 ± 0.04 mm/° for soleus. There was no significant difference in the mean correction factors between muscles or knee joint positions.


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The main finding of the study was that during isometric contractions with the plantar flexor muscles there was a differential displacement between the soleus and gastrocnemius aponeuroses proximal to the junction with the Achilles tendon. When the knee joint was extended, displacement of the medial gastrocnemius aponeurosis exceeded that of the soleus aponeurosis, whereas the converse occurred when the knee joint was flexed. These differences in aponeurosis displacement created a "shear" effect with a direction that was governed by the knee joint position.

The anatomy of the triceps surae is complex and subject to considerable variation between individuals. The lateral and medial compartments of the gastrocnemius gradually coalesce into a broad aponeurosis or tendon lying superficial in the posterior aspect of the lower leg with the independent insertion aponeurosis of the soleus muscle located anteriorly. The cadaver investigation confirmed that the separation of the aponeuroses allows for differential movement of the two contiguous structures in the proximal region. However, minor transverse collagen structures connect the aponeuroses distally, which initiates a gradual merging of the two structures (Fig. 1) to ultimately form the Achilles tendon. Two distinct types of soleus-gastrocnemius junctions have previously been identified; the most common type involves the two structures contributing collagen fibers directly and equally to the Achilles tendon (Fig. 2), in contrast to an alternative arrangement in which the gastrocnemius aponeurosis inserts more proximally into the underlying soleus aponeurosis (18, 30). The collagen fibers originating from the separate aponeuroses initiate a longitudinal rotation at the junction so that the medial fibers are rotated ~90° to become posterior at the calcaneus insertion and the posterior fibers rotate laterally (32); however, the distance that the aponeurosis fibers can be regarded separate structures within the Achilles tendon remains unknown. Also, the anteroposterior tendon diameter, the distance from the soleus-gastrocnemius junction to the calcaneal insertion, and the so-called "free Achilles tendon length" defined as tendon without direct muscle-fiber insertion have been shown to vary between subjects (4, 18, 27). Despite of the fact that the recent use of ultrasonography (14, 20, 21, 26, 28) and magnetic resonance imaging (11, 12) has enabled a more precise in vivo description of the aponeurosis-tendon properties during loading, a comprehensive three-dimensional understanding of the properties and function of the plantar flexor muscles during contraction remains to be achieved.

Arndt et al. (1) examined the medial and lateral forces in the Achilles tendon in vitro during differential loading of the triceps surae muscles. The force in the medial portion of the tendon exceeded that of the lateral portion when the medial gastrocnemius and soleus muscles were loaded, whereas the lateral tendon forces exceeded the medial forces when either the lateral gastrocnemius or the entire triceps surae muscle group was loaded. On the basis of in vivo observations, it has been suggested that, within the tendon, the distribution of force in the anterior-posterior plane may be uneven because of differential patterns of muscle activation as well as with changing knee joint angle due to altered contractile properties of the gastrocnemius muscle (2). However, the purported transverse tendon force gradient and local stress concentrations that may give rise to nonuniform intratendinous strain distribution have not been determined in vivo. Nonetheless, in vivo observations of the displacement of a syringe needle inserted into the free Achilles tendon during plantar flexor contraction efforts (27) resulted in the needle (diameter 0.5 mm, length 25 mm) being deformed, as evident by a sharp angle (unpublished observation), when it was removed. Furthermore, Kawakami et al. (20) observed uneven shortening of separate triceps surae muscles by estimating changes in muscle length from measurements of pennation angle and fascicle length at various knee and ankle joint angles. These results are consistent with the notion that there may be significant intratendinous differential strain during muscular contractions.

In accordance with previous results (9), the present study demonstrated that knee joint angle influenced the maximal plantar flexion moment as evidenced by a greater maximal plantar flexion moment (~35%) in the extended-knee position compared with the flexed-knee position. This effect is mainly attributed to the impaired contractile properties of the gastrocnemii muscles in the flexed-knee position because of the shortened muscle length. The present study, however, extends the knowledge of this behavior by demonstrating that during plantarflexion efforts substantial differential aponeurosis displacement occurs throughout the range of force exertion, and even at very low effort levels a difference in aponeurosis displacement was apparent. The difference in displacement between separate aponeuroses within the triceps surae amounted to >30% of the maximal observed displacement, indicating that a considerable "shear potential" exists during movement tasks. The net direction of the aponeurosis shear displacement varied with knee joint position across the range of force exertion. Likely, the observed differential aponeurosis displacement was caused by differences in force output of the medial gastrocnemius and soleus muscles. Alternatively, the aponeurosis behavior could result from a regional difference in mechanical properties of the involved connective tissue structures. However, the similarity of the aponeurosis displacement between muscles and knee joint positions during the passive trials suggests that the differential displacement was mainly due to differences in force exertion between muscles.

It should be noted that the ultrasound image analysis only accounts for two dimensions of aponeurosis displacement during tensile loading. It cannot, therefore, be excluded that unaccounted deformation or displacement occurs in additional planes (12, 38). For example, the width of the (soleus and gastrocnemius) aponeuroses increases with muscular force production (25, 33), and the length changes of the aponeuroses during passive conditions exceed those during an active muscle contraction (23, 33). Moreover, it must be conceded that the present method does not directly assess the magnitude of nonuniform deformation or longitudinal sliding of intratendinous structures in the free Achilles tendon; however, when the effect of joint rotation is eliminated, the observed aponeurosis displacement does reflect deformation of the serially coupled structures that are distal to the measurement site. It has previously been demonstrated that >70% of the total aponeurosis displacement measured at a similar site relates to tendon deformation (27). Therefore, the present data suggest that the plantar flexor contractions also partly produce a nonuniform deformation of collagen fibers within the Achilles tendon (intratendinous shear), although this remains to be experimentally confirmed.

The Achilles tendon is prone to numerous loading-related injuries, such as tendinopathy. The etiology of this syndrome is poorly understood (8, 18), but it has been proposed that intratendinous stress concentrations and the resultant interfibril frictional forces may play a role in tendinopathy (2). Given that this relation exists, it may be speculated that for the healthy muscle-tendon unit the activation strategy is fine-tuned to accommodate optimal force transmission and to minimize interaponeurosis displacement and thus intratendinous shear for each possible constellation of ankle and knee joint position in the physiological range of normal human movement. Furthermore, any disturbance in the activation strategy may result in increased differential aponeurosis displacement and induce excessive intratendinous shear and potential tissue injury. The present data suggest that future studies should focus on the role of intratendinous strain gradients with respect to tendon pathologies. Albeit speculative, the existence of a proximal "focal point" (i.e., a tight transverse junction of collagen fibers) may reduce intratendinous shear and strain gradient in the more distal free tendon, perhaps reducing risk of injury. Alternatively, greater tendon shear and interfibril friction may be expected if the soleus and gastrocnemius aponeuroses remain separate structures further distal into the Achilles tendon. The present methodology permits investigations into the relation between contraction-induced differential aponeurosis displacement and tendon pathologies and further development of treatment and prophylactic strategies.

In conclusion, the present study investigated the mechanical function of the triceps surae with respect to differential displacement of separate aponeuroses during muscular contraction. The data show that substantial displacement was present between the soleus and medial gastrocnemius aponeuroses during maximal plantar flexion contractions, even though the aponeuroses are connected to a common tendon. The results suggest that the Achilles tendon is subjected to intratendinous shear and stress gradients during human locomotion, which may be significant for Achilles tendon pathologies.


   GRANTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This work was supported by the national Danish organization for elite sports Team Danmark and the Danish Research Agency.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Drs. Roger Enoka, Thorsten Rudroff, and Kevin Keenan, Department of Integrative Physiology, University of Colorado, for valuable comments and Dr. Finn Bojsen-Møller, Department of Medical and Functional Anatomy, Biomechanics and Motor Control Laboratory, University of Copenhagen, for generous and insightful help and for assistance with cadaver specimens.


   FOOTNOTES
 

Address for reprint requests and other correspondence: J. Bojsen-Møller, Sports Medicine Research Unit/Team Danmark Test Center, Bispebjerg bakke, 23, bygn 8, Bispebjerg Hospital, 2400 Copenhagen NV, Denmark (E-mail: jbm01{at}bbh.hosp.dk).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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