Functional ankle range of motion but not peak Achilles tendon force diminished with heel-rise and jumping tasks after Achilles tendon repair

Abstract

Background:

Deficits in sporting performance after Achilles tendon repair may be due to changes in musculotendinous unit structure, including tendon elongation and muscle fascicle shortening.

Hypothesis/Purpose:

The purpose of this study was to discern whether Achilles tendon rupture reduces triceps surae force generation, alters functional ankle range of motion, or both during sport-related tasks. We hypothesized that individuals after Achilles tendon repair lack the functional ankle range of motion needed to complete sport-related tasks.

Study Design:

Cross-sectional study with within-subject control

Methods:

Individuals 1-3 years post Achilles tendon rupture with open repair were included. Participants (n=11) completed a heel-rise task and three jumping tasks. Lower extremity biomechanics were analyzed using motion capture. Between limb differences were tested using paired t-test.

Results:

Pelvic vertical displacement was reduced during the heel-rise (mean difference: −12.8%, p = 0.026) but not jumping (p>0.1). In the concentric phase of all tasks, peak ankle plantar flexion angle (range of mean difference: −19.2% - −48.8%, p<0.05) and total plantar flexor work was lower (range of mean difference: −9.5% - −25.7%, p<0.05) on the repaired side relative to the uninjured side. There were no significant differences in peak Achilles tendon load or impulse with any of the tasks. There were no differences in plantar flexor work or Achilles tendon load parameters during eccentric phases.

Conclusion:

Impaired task performance or increased demands on proximal joints is observed on the repaired side in tasks isolating ankle function. Tasks that do not isolate ankle function appear to be well-recovered, though functional ankle range of motion is reduced with rupture. Reduced plantar flexor work supports prior reports that an elongated tendon and shorter muscle fascicles caused by Achilles tendon rupture constrain functional capacity. Achilles tendon peak load and impulse were not decreased, suggesting that reduced and shifted functional ankle range of motion (favoring dorsiflexion) underlie performance deficits.

Introduction

Achilles tendon rupture has substantial implications for individuals’ ability to engage in sporting activity. Up to 80% of individuals with Achilles tendon rupture are able to return to some amount of sporting activity.⁴² In elite athletes the return to sport rates tend to be lower, with between 60-70% of National Basketball Association and National Football League athletes returning to sport in the same division,^3,29,39 though return to play rates do seem to be sport-dependent.^12,39,40 Sport performance is also impaired upon return to sport. Professional athletes have been found to have diminished performance ratings after injury compared to baseline^3,12,29,39 and lower performance ratings in the first season following return from Achilles tendon rupture when compared to their uninjured peers.^3,29,39 From a biomechanical standpoint, Achilles tendon ruptures permanently reduce performance during running, jumping, and sporting in recreationally active people.^{8,21,31,41,44,45}

Achilles tendon ruptures stimulate gross structural changes in both the tendon and triceps surae musculature. Following rupture, the Achilles tendon heals in a permanently elongated position^22,33,36 and never restores the material properties of healthy tendon tissue.^2,9,11,43 Achilles rupture does not only affect the tendon, itself, but disrupts the whole muscle-tendon unit. At presentation with Achilles tendon rupture, the triceps surae muscles have shorter fascicle length and increased pennation angles, which persist throughout the first 14 weeks post-injury¹⁹ and have been suggested to drive tendon elongation as the musculotendinous unit tries to restore tension on a healing tendon.¹⁸ Fascicle remodeling and increased pennation persists three to six months post-injury.^1,30 In addition to shorter and more pennate muscle fascicles,²⁴ muscle atrophy^{14,15,24,32,44} and fatty infiltration^14,15 have been reported beyond 1-year post-injury.

Whether structural disruption of the triceps surae muscles after Achilles tendon rupture reduces the triceps surae’s ability to generate force, alters functional ankle range of motion (defined as the available ankle excursion over which the plantar flexors are able to generate adequate force for task completion), or a combination of both during higher level, sport-related tasks is not well-described. Prior work linked muscle-tendon structural changes following Achilles tendon rupture with functional deficits during isokinetic strength testing,^7,10,20 heel-rises,^5,36 and plyometric activity.⁸ The purpose of this study was to determine the effects of Achilles tendon ruptures with surgical repair on tendon loading parameters during a combination of clinical tasks to begin to disentangle the effects of muscle contractility and functional ankle range of motion on higher level task performance.

Given the elongating of the tendon and shortening of muscle resting length after Achilles tendon rupture, we hypothesized that individuals after Achilles tendon repair lack the functional ankle range of motion needed to complete heel-rise and jumping tasks (Figure 1). Decreased functional ankle range of motion would result in no differences between peak force generation of the muscle (Achilles tendon impulse, peak Achilles tendon load) on the repaired compared to the uninjured side. However, functional ankle range of motion would be reduced and shifted towards more dorsiflexed positions to pre-tension the muscle. We hypothesized that alterations in functional ankle range of motion would be reflected in reduced work done by the plantar flexors (as the peak force would be similar but occur over a shorter fascicle length). In summary, we hypothesized that the ruptured side would have decreased functional ankle range of motion relative to the uninjured side (evidenced by lower ankle excursion, lower peak ankle angle, and lower ankle work; and no side-to-side difference in peak Achilles tendon load or impulse).

Figure 1.

Study hypothesis. Muscle and tendon length directly affect the ability for the plantar flexors to generate force (A). After Achilles tendon rupture, the tendon is elongated and the muscle fascicles are shortened decreasing the excursion over which the muscle is able to contract. To compensate for an elongated tendon and adequately preload the muscle the ankle moves into additional dorsiflexion, decreasing the functional ankle range of motion and shifting it toward dorsiflexion (B). This conceptual framework is supported by literature linking kinetic ankle deficits during concentric angle tasks with structural deficits in both patients¹⁷ and computational models.⁵

Materials and Methods

Study Design and Participants

This is a cross-sectional, retrospective analysis of prospectively collected data. Participants included in this study were enrolled between April and November 2017. This study was approved by the University of Delaware Institutional Review Board. To be included, participants needed to be 1-3 years post Achilles tendon rupture treated with open surgical repair. This timeframe was based on literature suggesting the majority of functional gains are made by 1 year post-injury, with no additional gains between 1 and 2 years post-injury²⁷ and limited gains 1 to 7 years post-injury.⁸ Exclusion criteria were history of post-operative complications including deep vein thrombosis or re-rupture and an inability to jump unilaterally due to pain or injury aside from their Achilles tendon rupture. Participants’ surgical and post-operative rehabilitative treatment was administered per the recommendations of their healthcare providers, and participants did not receive standardized intervention as part of the study.

All data were collected in a single session comprised of questionnaires [the Achilles tendon Total Rupture Score (ATRS)²⁶ and a Physical Activity Scale (PAS)¹³] to characterize participants’ self-reported function and physical activity. Muscle and tendon characteristics were assessed via ultrasound and have been previously reported.⁴⁴ Participants then completed functional testing in which each test was performed unilaterally, including a heel-rise task, counter movement jump (CMJ), drop counter movement jump (DJ), and hopping as these are lower extremity functional tasks that have been found to be valid and reliable in individuals with Achilles tendon injuries.^25,28,35,37 Muscle activation and lower limb biomechanics (but not Achilles tendon load) have been previously reported for the hopping task⁴⁴ and muscle activation has been previously reported for the CMJ task.⁴⁵

The right limb was tested first for all participants in order to quasi-randomize testing of the repaired and uninjured sides. For the heel-rise task, participants were positioned standing unilaterally on a 10 degree incline box. Participants were allowed “2 finger” support on an external bar for balance. Five heel-rises were performed at a rate of 1 heel-rise per second (Figure 2). For the CMJ, participants were instructed to stand unilaterally with their arms folded across their chest and then perform a maximal, vertical jump trying to land in the same place on the force plate. For the DJ, participants again stood unilaterally with their arms folded across their chest on top of a 10 cm box. They were instructed to try to slide off of the front of the box and, upon landing on the floor, perform a maximal, vertical jump. Three repetitions on each leg were completed for the CMJ and DJ tasks. For hopping, participants stood unilaterally with their arms to their sides as if jumping rope. They performed 25 rhythmic jumps at a self-selected pace trying to stay within the same place. Trials were repeated if participants jumped off of the force plate. Two repetitions of the hopping task were completed on each leg.

Figure 2.

Heel-rise task.

Biomechanical Analysis

Lower limb and pelvic kinematics and kinetics were assessed using 8-cameras (Nexus, Vicon, oxford, United Kingdom) and 2 in-ground force plates (Bertec Corporation, Columbus, OH, USA). Kinematics were collected at 120 Hz and kinetics were collected at 1080 Hz. Retroreflective markers were placed on the foot (1^st and 5^th metatarsal heads, posterior heel), ankle (medial and lateral malleoli), knee (medial/lateral femoral condyles), and hip/pelvis (greater trochanter, anterior superior iliac spine) with tracking clusters on the shank, thigh, and sacrum.³⁸

Lower limb kinematics and kinetics were calculated using a constrained kinematic model using a previously described approach.⁴ Briefly, a generic musculoskeletal model (gait 2392)³⁴ was scaled using each participant’s bodyweight and markers placed over anatomic landmarks. After scaling body segments of each participant, we moved these models into the anatomic position by fitting the experimental data collected during a standing trial using best practices.¹⁶ Next, inverse kinematics quantified lower extremity motion and inverse dynamics quantified lower extremity kinetics during each of the movement trials. The change in pelvic height during each activity was calculated to quantify movement performance. Pelvic height was defined as the vertical distance of the center of the pelvis from the ground. We used OpenSim’s pelvis body coordinate system origin, which is based on the ASIS and PSIS landmarks. Using this peak height, the concentric and eccentric phases of each activity were analyzed and phases were resampled to 101 data points (MATLAB 2019b, The Mathworks, Natick, MA). Impulse was calculated as the area under the load-time curve and work as the area under the load-displacement curve (trapz function in MATLAB). To characterize joint kinetics and Achilles tendon loading across participants, kinetic variables were normalized by participant bodyweight for Achilles tendon peak load and impulse and by participant bodyweight multiplied by participant stature for joint kinetics including peak torque and joint work. After calculating the ankle joint moments generated during these activities, Achilles tendon load was calculated by dividing these moments by an Achilles tendon moment arm of 5 cm²³ and normalized tendon load by participant bodyweight. Achilles tendon peak load and impulse loading are reported to characterize the loads applied to the tendon. Because we did not quantify triceps surae shortening dynamics with ultrasound imaging, we decided to report joint-level work.

Statistical Analysis

Descriptive statistics [mean(SD)] are reported for each of the variables of interest. Differences in Achilles tendon load parameters between repaired and uninjured sides were examined using one-tailed paired t-tests. A one-tailed test was used as it is understood that ankle performance is impaired after Achilles tendon rupture. Differences in hip and knee joint biomechanics between repaired and uninjured sides were examined using two-tailed paired t-tests. Significance was established a priori as an alpha level of 0.05. A conservative estimate of ten participants were needed to power the study at an alpha level of 0.05 and power of 0.95, based on previously reported effect sizes observed in between limb biomechanical comparisons of individuals after Achilles tendon rupture.⁴¹

Results

Participant Characteristics

Participants (10 male, 1 female) had a mean(SD) body mass index of 25.9(1.0) kg/m² and were 43.6(2.7) years of age. Participants were 17(6) months from repair at the time of study participation, with a mean(SD) time from rupture to surgery of 11(10) days. The right side was ruptured in 5 participants, and the left side was ruptured in 6 participants. Participants scored a mean(SD) of 88.8(4.5) of 100 points on the ATRS and 5.0(0.5) on the Physical Activity Scale corresponding to the description, “moderate exercise at least 3 hours a week, e.g. tennis, swimming, jogging, etc.”

Heel-Rise Ankle Performance

Participants had significantly less pelvic displacement (the change in vertical pelvic position from the start of the movement to the peak vertical position of the movement) during the heel-rise task on the injured relative to the uninjured side. During the concentric phase, peak ankle angle and ankle excursion was significantly lower on the repaired side (Figure 3, Table 1). Total plantar flexor work was lower on the repaired side, but there were no statistically significant differences in peak Achilles tendon load or Achilles tendon impulse between injured and uninjured sides (Figure 4, Table 1).

Figure 3.

Plantar flexor angle during the concentric phase for each of the clinical tasks. Plantar flexion is positive, traces represent bootstrapped 95% confidence intervals. * indicates p < 0.05 for between limb comparison.

Table 1.

Ankle mechanics during concentric and eccentric phases of functional tasks.

Variable	Concentric			Eccentric
	Repaired	Uninjured	p-value	Repaired	Uninjured	p-value
Heel-rise
Pelvis height (m)	0.09±0.01	0.10±0.01	0.026*
Peak ankle angle (degrees)	17.9±5.0	26.1±5.5	0.001*	17.5±4.8	26.0±5.5	0.001*
Ankle excursion (degrees)	39.2±5.8	52.0±6.9	0.002*	39.6±5.6	51.9±7.3	0.001*
Plantar flexor work (J/kg)	1.80±0.22	2.35±0.29	0.009*	−1.13±0.22	−1.42±0.29	0.985
Achilles tendon – peak (bodyweights)	3.84±0.27	3.74±0.20	0.372	3.49±0.29	3.48±0.22	0.410
Achilles tendon – impulse (bodyweight*s)	2.11±0.30	2.00±0.29	0.528	2.55±0.25	2.44±0.25	0.408
Counter Movement Jump
Pelvis height (m)	0.26±0.04	0.31±0.04	0.227
Peak ankle angle (degrees)	42.1±7.4	46.3±6.6	0.020*	−6.0±4.7	−5.5±3.9	0.498
Ankle excursion (degrees)	78.9±9.6	81.0±8.9	0.039*	30.3±6.4	28.4±4.7	0.316
Plantar flexor work (J/bodyweight)	3.55±0.52	4.57±0.67	0.050*	−0.26±0.19	−0.37±0.16	0.360
Achilles tendon – peak (bodyweights)	5.40±0.48	5.60±0.46	0.325	4.85±0.75	4.39±0.67	0.557
Achilles tendon – impulse (bodyweight*s)	1.60±0.15	1.62±0.21	0.645	1.53±0.28	1.20±0.22	0.514
Drop Jump
Pelvis height (m)	0.20±0.3	0.24±0.04	0.130
Peak ankle angle (degrees)	36.2±7.8	43.5±8.0	0.034*	34.1±6.3	44.0±7.8	0.044*
Ankle excursion (degrees)	70.3±10.3	78.1±9.3	0.086	68.6±8.6	74.5±7.9	0.085
Plantar flexor work (J/bodyweight)	3.26±0.48	4.13±0.66	0.033*	−1.90±0.57	−2.39±0.42	0.969
Achilles tendon – peak (bodyweights)	6.97±0.90	7.47±1.10	0.360	6.97±0.98	7.43±1.08	0.326
Achilles tendon – impulse (bodyweight*s)	1.24±0.17	1.35±0.21	0.323	0.94±0.14	0.92±0.14	0.381
Hopping
Pelvis height (m)	0.20±0.02	0.20±0.02	0.576
Peak ankle angle (degrees)	23.9±4.5	29.6±5.6	0.010*	18.0±3.6	21.4±4.3	0.025*
Ankle excursion (degrees)	52.0±6.1	61.6±7.7	0.061	47.1±5.5	55.1±6.9	0.150
Plantar flexor work (J/bodyweight)	2.96±0.36	3.23±0.43	0.021*	−1.36±0.25	−1.51±0.28	0.940
Achilles tendon – peak (bodyweights)	7.12±0.83	7.12±0.87	0.191	7.19±0.84	7.19±0.95	0.203
Achilles tendon – impulse (bodyweight*s)	0.89±0.09	0.89±0.10	0.254	0.69±0.08	0.72±0.08	0.339

Values are mean±SD. Plantar flexor work, Achilles tendon peak load and impulse are normalized to bodyweight.

^*indicates p-value < 0.05

Figure 4.

Achilles tendon load profiles for each of the clinical tasks. Plantar flexion is positive, traces represent bootstrapped 95% confidence intervals.

Similar to the concentric phase, during the eccentric phase the injured ankle had significantly lower peak ankle angle and ankle excursion (Table 1). There were no statistically significant differences in total plantar flexion work, peak Achilles tendon load, or Achilles tendon impulse between injured and uninjured sides (Table 1).

Jumping Ankle Performance

There were no differences in pelvis vertical trajectory with jumping on the injured compared to uninjured side during any of the jumping tasks (Table 1).

For the concentric phase of the CMJ, ankle angle peak and excursion were significantly lower on the repaired side (Table 1). Plantar flexor work was lower on the repaired side, but there were no differences in Achilles tendon peak load or impulse. There were no between-limb differences observed in any measure during the eccentric phase (Table 1).

For the concentric phase of the DJ, ankle angle peak but not excursion was significantly lower on the repaired side (Table 1). Concentric work was lower on the repaired side, but there were no between-limb differences in Achilles tendon peak load or impulse. Ankle angle peak was lower on the repaired side during the eccentric phase, but there were no between limb differences in ankle peak, plantar flexor work, or Achilles tendon peak load or impulse during the eccentric phase (Table 1).

For the concentric phase of the hopping task, ankle angle peak but not excursion was significantly lower on the repaired side. Concentric plantar flexor work was lower on the repaired side, but there were no differences in peak Achilles tendon load or Achilles tendon impulse. In the eccentric phase, peak ankle angle was significantly lower on the repaired side but there were no between-limb differences in ankle excursion. Similar to the other jumping tasks, there were no between limb differences in plantar flexor work or Achilles tendon peak load or impulse during the eccentric phase (Table 1).

Hip and Knee Contributions to Heel-Rise and Jumping Performance

There were no differences in knee or hip work between sides during the concentric phase of any task with the exception of combined proximal lower extremity (hip and knee, together) work during the concentric phase of hopping (between limb comparison for combined lower extremity – heel-rise: mean difference=7.0%, p=0.369; CMJ: mean difference=18.1%, p=0.496; DJ: mean difference=2.5%, p=0.664; hop: mean difference=41.6%, p=0.006) (Table 2).

Table 2.

Hip and knee work during concentric phase of functional tasks.

Work (J)	Repaired	Uninjured	p-value
Heel-rise
Hip	0.015±0.011	0.069±0.027	0.302
Knee	0.172±0.061	0.117±0.046	0.818
Counter Movement Jump
Hip	1.520±0.383	0.868±0.204	0.781
Knee	0.974±0.213	1.073±0.315	0.714
Drop Jump
Hip	0.459±0.140	0.394±0.134	0.595
Knee	0.606±0.171	0.784±0.321	0.781
Hopping
Hip	0.135±0.042	0.089±0.032	0.984
Knee	0.347±0.082	0.328±0.102	0.986

Values are mean±SD.

Discussion

This study is the first to disentangle functional ankle range from plantar flexor strength by assessing lower extremity biomechanics during higher level strength and plyometric tasks commonly used in the rehabilitation progression to return individuals to sporting activities after Achilles tendon rupture. In tasks that isolate ankle function like the heel-rise and hopping tasks, participants demonstrate either impaired task performance (evidenced by lower pelvic displacement during the heel-rise task) or increased demands on the more proximal joints (evidenced by comparable jump height between sides but increased proximal limb peak load and work on the repaired side). Tasks that do not isolate ankle function – such as the counter movement jump and drop jump – appear to be well-recovered though functional ankle range of motion is reduced by 19-48% on the repaired side.

The concentric phase was consistently more affected by Achilles tendon rupture across all tasks, with a 20-26% deficit in plantar flexor work on the repaired side. Achilles tendon peak load and impulse were not decreased, however. Taken together, these findings suggest that reduced and shifted functional ankle range of motion (favoring a more dorsiflexed range) underlie heel-rise and jumping performance deficits in a group of individuals who had recovered well based on self-reported function following injury. This points to the need to reduce tendon elongation and restore muscle length of the triceps surae after Achilles tendon rupture – to address musculature that is short but not necessarily weak for improved performance with sport-related activities.

A combination of shortened muscle fascicle length and tendon elongation is one potential explanation for impaired functional ankle range of motion as the muscle has less excursion to contract, particularly affecting performance with tasks like heel-rises which emphasize end-range plantar flexion.^5,6,10 Functional deficits resulting from this imbalance in length-tension relationships of the myotendinous unit is supported by moderate to strong relationships between muscle fascicle length and isometric plantar flexion torque at 14 weeks post-injury.¹⁷ Functionally, isolated calf strength deficits that are more pronounced in greater amounts of plantarflexion have been observed with dynamometry, correlating strongly with muscle atrophy.¹⁴ Tendon elongation has been suggested to underlie changes to walking,^2,43 running,^8,21,41 and jumping mechanics throughout the course of recovery.^31,41,44,45 Additionally, moderate to strong relationships between tendon elongation and deficits in triceps surae isometric strength, particularly at end-range plantarflexion, have been observed even in individuals greater than 10 years post-injury.¹⁵ Combined with the results of the present study, it seems that the triceps surae musculature continues to be able to have capacity to produce force but over a limited range pointing to the need to intervene with the goal of restoring muscle and tendon length, likely very early after rupture.

From a clinical standpoint, it seems important to be conscientious that the rehabilitation approach for returning to sport incorporates a variety of sport-specific maneuvers to develop task-related motor plans given the differences in compensatory strategies observed across tasks. The results of this study support the importance of restoring functional ankle range of motion after Achilles tendon rupture with repair. Determining whether focusing rehabilitation on restoring functional ankle range of motion or on compensatory strategies may require consideration not only of tendon length but also muscle fascicle length as a prognostic indicator of rehabilitation potential. It is not known the extent to which muscle functional length is able to be remediated by rehabilitation, so proximal lower extremity strengthening may be particularly important in individuals with short muscle fascicle length and elongated tendon length to prepare individuals who will require proximal compensatory strategies to engage in sport activity. This is in line with previous literature supporting the need for proximal strengthening due to increased loads at the knee during plyometric tasks after Achilles tendon rupture.^41,44 Additionally, because muscle and tendon length become abnormal very early after Achilles rupture, developing new surgical techniques to restore muscle fascicle length may be beneficial in improving muscle functional length later in recovery.

There are a few limitations to this study that are important to consider. This study was designed using the uninjured side as a within subject control. An uninjured control group was not included to limit variables that could confound the analysis (i.e. physical activity level, body mass index, age, etc.). It is possible that individuals in this study could have modified their heel-rise or jumping strategy bilaterally in response to their Achilles rupture, reducing the effect of presence of rupture in this analysis. Compared to previously published data in healthy participants,⁴ the participants included in this study had similar or slightly increased peak Achilles tendon load (% difference based on means from repaired side in this group to controls: heel-rise=28%, CMJ=10%, DJ=27%, hop=7%) and similar or reduced Achilles tendon impulse (% difference based on means from repaired side in this group to controls: heel-rise=2%, CMJ= −33%, DJ= −59%, hop= −32%). Additionally, while all participants underwent open surgical repair and some form of post-operative rehabilitation, surgical technique and rehabilitation was not standardized. Including individuals treated per standard of care rather than intervention delivered as part of the study likely reflects the clinical reality of patients with Achilles tendon rupture treated with open repair. We estimated Achilles tendon load by dividing ankle torque by a constant length moment arm of 5 cm.²³ However, we do not expect this approximation to impact the findings because we used paired t-tests.

In summary, the findings of this study suggest that individuals with well-recovered self-reported function continue to demonstrate substantial deficits in concentric ankle excursion and work after Achilles tendon repair, though Achilles impulse and peak Achilles tendon force is restored to the uninjured side. Taken together, this suggests that even after one year following injury, at a time when most athletes have returned to sporting activity,⁴² altered length tension relationships within the triceps surae musculotendinous unit limit the functional ankle range of motion available to an athlete. Future studies investigating restoring muscle and tendon length-tension relationship early after injury and promoting recovery of functional ankle range of motion throughout the course of recovery are needed to optimize athlete performance particularly in tasks isolating ankle plantar flexor function.

Clinical Relevance:

These findings point to the need to reduce tendon elongation and restore muscle length of the triceps surae after Achilles tendon rupture – to address musculature that is short but not necessarily weak for improved performance with sport-related activities.

What is known about the subject:

• Achilles tendon rupture results in tendon elongation and muscle fascicle shortening

• Tendon elongation is associated with impaired heel-rise and jump performance

• During repeated jumping tasks and jogging lower extremity work shifts from the ankle to the knee

What this study adds to existing knowledge:

• With tasks using ankle plantar flexion, either lower extremity work shifts proximally or task performance is impaired

• The concentric phase of heel-rise and jumping tasks is most affected after rupture

• Plantar flexor work in the concentric phase is reduced, but Achilles tendon impulse and peak load is largely maintained

• These findings suggest that it is not the muscle’s ability to generate force that is affected but the effect of impaired length-tension relationships which limit functional ankle range of motion