Relative motion between the flexor digitorum superficialis tendon and subsynovial connective tissue is time dependent

The subsynovial connective tissue is an integral component of flexor tendon gliding in the carpal tunnel, which is strained during longitudinal tendon displacement. We tested the effects of repetition frequency and finger load on flexor tendon function throughout active finger movement. Eleven participants performed metacarpophalangeal joint flexion/extension of the long finger cyclically at three repetition frequencies (0.75, 1.00, 1.25 Hz) and two finger loads (3.5, 7 N). Relative displacement between the flexor digitorum superficialis tendon and subsynovial connective tissue was assessed as the shear‐strain index with color ultrasound throughout the entire time history of finger flexion and extension. In addition, long finger joint angles were measured with electrogoniometry while flexor digitorum superficialis and extensor digitorum muscle activities were measured with fine‐wire electromyography to characterize the finger movements. The shear‐strain index increased with greater finger flexion (p = 0.001), representing higher relative displacement between tendon and subsynovial connective tissue; however, no changes were observed throughout finger extension. The shear‐strain index also increased with higher repetition frequencies (p = 0.013) and finger loads (p = 0.029), further modulating time‐dependent effects during finger flexion versus extension. Using ultrasound, we characterized the time‐dependent response of the shear‐strain index, in vivo, providing valuable data on flexor tendon function during active finger movement. Our results infer greater subsynovial connective tissue strain and shear during repetitive and forceful finger movements. Future research characterizing time‐dependent effects in carpal tunnel syndrome patients may further elucidate the relations between subsynovial connective tissue function, damage, and carpal tunnel syndrome.


| INTRODUCTION
Carpal tunnel syndrome (CTS) is the most common entrapment neuropathy of the distal upper limb with an estimated incidence of 424 cases per 100,000 in the US general population, 2000−2005. 1 However, a pooled analysis of 6 prospective studies involving over 50 workplaces and 4321 workers shows the incidence among US workers that perform hand intensive activities is substantially higher. 2 Epidemiological studies further support forceful and repetitive hand activities as physical risk factors for CTS. [3][4][5] It is well known that CTS is caused by median nerve compression, although the underlying pathomechanics are complex. 6,7 Modelling tendon frictional shear force with adjacent carpal tunnel structures demonstrates a strong relationship with physical risk factors such as force and repetition 8,9 as well as flexor tenosynovitis and CTS. 10 More recently, flexor tendon frictional work in the carpal tunnel has been measured, in vitro, to further elucidate pathomechanisms of CTS. These cadaveric investigations revealed an exponential relationship between tendon frictional work versus tendon displacement. [11][12][13][14][15] Furthermore, strain-dependent characteristics of the adjoining subsynovial connective tissue (SSCT) contributed most to overall tendon frictional work. 11,14 These results emphasize the SSCT as an important extra-synovial gliding mechanism, 16 and further support evidence of SSCT fibrosis and thickening as a causal injury mechanism in CTS. [17][18][19] Ultrasound has been used to assess flexor tendon gliding, in vivo, as a shear-strain index (SSI), representing relative displacement between tendon and adjacent SSCT as a percentage of overall tendon displacement. [19][20][21][22][23][24][25][26][27][28][29][30] Researchers have shown the SSI is related to SSCT thickness 19 and predicts median nerve sensory and motor changes in CTS patients. 21 Furthermore, using both in vitro and in vivo methods, physical risk factors have been shown to influence the SSI, including wrist flexion/extension position, 24,31 speed of work, 32,33 and task duration. 27 While these studies provide valuable information of a plausible injury pathway implicating the SSCT, the SSI has been reported a single metric. Assessing the SSI throughout the entire time course of repetitive finger movement is likely to provide valuable information on the viscoelastic characteristics of the SSCT, including its role in injury development. Furthermore, ultrasound investigation of the SSI is limited with respect to forceful efforts despite its importance as a risk factor of CTS. 5 The purpose of this study was to investigate two wellestablished physical risk factors, repetition frequency and finger load on ultrasound assessment of the SSI throughout the entire time series of a cyclical finger flexion/extension task. We hypothesized that ultrasound assessment would capture timedependent changes representing viscoelastic characteristics of the SSCT, which would be further modulated by the repetition frequency and finger load.

| Experimental design
We used a comparative research design to investigate the effects of three repetition frequencies and two finger loads on flexor digitorum superficialis (FDS) tendon−SSCT relative displacement as the SSI via color imaging during the entire time course of a cyclical long finger flexion/extension task. This study provided Level II evidence via a balanced repeated measures design where each participant performed all conditions within the protocol.

| Participants
A convenience sample of 12 young healthy participants provided written informed consent, which was approved by the Hamilton Integrated Research Ethics Board. However, the data for one participant was omitted due to equipment failure; therefore, the analyzed data set in this paper includes 11 participants. A survey was administered to screen for health conditions that influence tendon gliding in the carpal tunnel as exclusion criteria. 23,24,27,34 Participant characteristics were also documented, 35 which are reported in

| Experimental protocol
The experimental setup was similar to previous studies that investigated the SSI. 23,24,27 Briefly, participants were seated at the T A B L E 1 Participant characteristics and dimensions of the forearm, hand, and long finger (n = 11; 6 males; 5 females). testing apparatus and chair height was adjusted to maintain ∼120°of right elbow flexion with the arm at the side (∼0°of shoulder abduction). The forearm was supinated and immobilized with a splint.
A custom handgrip (diameter-3.5 cm) and Velcro strapping fixed the index, ring, and little fingers in a mid-flexed position; the long finger (third digit) was able to move freely ( Figure 1). Velcro also attached the handgrip to the testing apparatus, which kept the handgrip in a set position to fix the wrist joint in a neutral position (∼0°).
Each participant performed metacarpophalangeal (MCP) joint flexion/extension with the long finger in six experimental conditions, including three repetition frequencies (0.75, 1.00, and 1.25 Hz) and two finger loads (3.5 and 7 N). The frequencies corresponded to those in previous studies, 19,20,28 and met the definition of repetitive work. 36 The loads were selected based on pilot testing with different constant force springs, which also represented forceful exertions for this task. 36

| Statistics
The primary outcome of interest in this study was the SSI, which was tested in a four-way repeated measures analysis-of-variance (ANOVA).
The independent variables were movement direction (finger flexion vs. 3 | RESULTS

| SSI
FDS tendon and SSCT displacements were both bell-shaped throughout the MCP joint flexion/extension task of the long finger ( Figure 3A). Tendon displacement was 13.7 ± 0.8 mm (mean ± 95% CI) and SSCT displacement was 9.6 ± 1.0 mm averaged over all experimental conditions and trials.
There was a significant movement direction by tendon displacement quartile interaction on the SSI (F 1.1,11.0 = 17.5, p = 0.001).
During finger flexion, the SSI increased from 19.4 ± 5.8% in the first quartile to 32.0 ± 6.0% in the fourth quartile, with the greatest increase between the first and second quartiles. However, the SSI did not change throughout the range of motion during finger extension ( Figure 4). These time history differences resulted from diverging FDS tendon and SSCT displacements during finger extension versus flexion, particularly in the first quartile.

| MCP and PIP joint angles
To further characterize the cyclical long finger task, MCP joint flexion angle changes were 33.7 ± 5.6°and accessory PIP joint flexion angle changes were 8.6 ± 3.1°averaged over all experimental conditions and trials. MCP joint flexion followed a symmetrical bell-shaped profile ( Figure 3B). PIP joint flexion curves were more variable, although the peak angle generally occurred near the transition from flexion to extension of the cyclical long finger task (~50% cycle time).
MCP and PIP joint flexion angles were not significantly affected by repetition frequency or finger load (Table 2).

| Finger force and muscle activity
Finger force throughout the MCP joint flexion/extension task produced a sinusoidal-shaped curve ( Figure 3C).  Table 2).
FDS muscle activity measured via fine-wire EMG mirrored the finger force profile throughout the flexion/extension movement with the longer finger ( Figure 3D). ED muscle activity was relatively low for the entire movement; however, activity was higher near the beginning and end of the movement cycle. Average FDS muscle activity was significantly greater in the high compared to the low finger loading condition (F 1,10 = 7.6, p = 0.02; low load-23.0 ± 9.6% MVC; high load-  resistance have also demonstrated highly viscoelastic characteristics. [11][12][13][14][15] We previously observed differences in tendon frictional work during simulated proximal tendon displacement with SSCT loading versus distal tendon displacement with SSCT unloading. 13 As well, researchers have showed that higher flexor tendon velocities produce increased gliding resistance. 12  however, relative displacement was linear during finger extension.
These results are consistent with our current study, which found a nonlinear increase in the SSI during finger flexion, whereas relative displacement was uniform throughout finger extension.
Overall, our findings fit with the SSCT as a microvacuolar system to facilitate tendon gliding through its multiple layers of collagen interconnected by small perpendicular fibrils and surrounding gel-like matrix. 16 Proximal tendon displacement results in sequential loading of the SSCT, starting with the deepest layers closest to the tendon followed by more superficial layers via load transfer through interconnecting fibrils. 26,32,41 However, it has been suggested that unloading the SSCT during distal tendon displacement results in a more uniform relaxation of the fibrils and layers. 32   Note: Superscript letters (a,b) denote significant differences between repetition frequency conditions (0.75, 1.00, 1.25 HZ).
T A B L E 3 Mean (±95% CI) FDS and ED muscle activity normalized to 100% MVC during cyclical long finger movement. We found a significant main effect of finger load on the SSI, which was previously documented in the cadaveric carpal tunnel. 14 Average and peak FDS muscle activity measured via fine-wire EMG were both significantly greater in the high (7 N) versus low (3.5 N) finger load condition, confirming greater musculotendon loading.
Furthermore, electrogoniometry confirmed that MCP and PIP joint kinematics were not significantly different between the high and low finger load conditions, lending further credence that the SSI increased as a function of the finger load. Plausible causes may be related to viscoelastic strain and creep with greater musculotendon loading 45 as well as increased dorsopalmar flexor tendon displacements in the carpal tunnel. 46 Regardless of the precise mechanism(s), we found the SSI increased independently with both repetition frequency and finger load, suggesting a greater likelihood of shear injury during repetitive and forceful finger movements.
There were a few limitations of this study. Color imaging is very sensitive to the angle of insonation between the ultrasound beam and the movement direction of anatomical structures (FDS tendon or SSCT). We steered the ultrasound beam 20°and applied a gel wedge to increase the angle of insonation to approximately 60°. 47 We previously evaluated accuracy and reliability in vitro using similar methods. 32 However, further assessing reliability of the SSI during a repetitive (cyclical) finger flexion task, in vivo, may expand future applications of this method. Second, fine-wire EMG confirmed FDS muscle activity was greater in the high finger load condition compared to the low finger load condition. However, high variability was observed in the EMG, which limited our analyses to average and peak values throughout the cyclical finger movement. Reporting these basic metrics prevented time-dependent analyses of goniometry and EMG data. Nonetheless, quantifying the effects of repetition frequency and finger load via two-way ANOVA provided context with respect to the forceful efforts of the repetitive MCP joint flexion/extension task of the long finger. Finally, the participant sample was relatively small (n = 11), due to the invasive nature of fine-wire EMG. However, the effects of repetition frequency and finger load were expected to be large from previous study by our research group. 14,32 As such, the study was sufficiently powered, while providing comprehensive characterization of the finger movements performed by the participants via electrogoniometry and fine-wire EMG.
In summary, we found time-dependent changes in finger flexion versus finger extension during active long-finger movements on the SSI. Higher repetition frequencies and finger loads also increased the SSI. Time-dependent changes likely represent viscoelastic characteristics of the SSCT due to the sequential loading of its layers via interconnecting fibrils and its gel-like matrix. 16