Journal of Biomechanics xxx (2018) xxx–xxx

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Journal of Biomechanics
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Short communication

Functional deficits may be explained by plantarflexor remodeling

following Achilles tendon rupture repair: Preliminary findings
Josh R. Baxter ⇑, Todd J. Hullfish, Wen Chao
Department of Orthopaedic Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

a r t i c l e i n f o a b s t r a c t

Article history: Achilles tendon ruptures are common injuries that often lead to long-term functional deficits. Despite the
Accepted 13 August 2018 prevalence of these injuries, the mechanism responsible for limited function has not yet been established.
Available online xxxx Therefore, the purpose of this study was to present preliminary findings that support a hypothesis that
skeletal muscle remodeling is the driving factor of poor outcomes in some patients. Biomechanical and
Keywords: ultrasonography assessments were performed on a patient that presented with poor functional outcomes
Achilles tendon rupture 2.5 years after a surgically-repaired acute Achilles tendon rupture. Single-leg heel raise height was
Ultrasound
decreased by 75% in the affected limb (3.0 cm compared to 11.9 cm) while walking mechanics showed
Muscle morphology
no deficits. Ultrasonography revealed that the affected medial gastrocnemius muscle was less thick
and had shorter, more pennate fascicles compared to the unaffected limb. A simple computational model
of a maximal-effort plantarflexion contraction was employed to test the implications of changes in mus-
cle architecture on single-leg heel raise function. Subject-specific measurements of fascicle length and
pennation were input into the model, which supported these architectural parameters as being drivers
of heel raise function. These preliminary findings support the hypothesis that an Achilles tendon rupture
elicits changes in skeletal muscle architecture, which reduces the amount of work and power the joint
can generate. This multidisciplinary framework of biomechanical, imaging, and computational modeling
provides a unique platform for studying the complex interactions between structure and function in
patients recovering from Achilles tendon injuries.
Ó 2018 Elsevier Ltd. All rights reserved.

1. Introduction Achilles tendon ruptures. To accomplish this, we quantified plan-

Achilles tendon ruptures often lead to long-term functional def-
icits (Lantto et al., 2015a; Leppilahti et al., 2000; Silbernagel et al.,
2012; Willy et al., 2017) despite improved treatment and rehabil-
itation protocols (Kangas et al., 2003; Mandelbaum et al., 1995;
Willits et al., 2010). An elongated tendon following injury is con-
sidered to be a predictor of functional deficits in a single-leg heel
raise during the first year following surgical repair (Silbernagel
et al., 2012). While tendon elongation is an important clinical indi-
cator of patient function, such as single-leg heel raise height
(Silbernagel et al., 2012), the underlying musculoskeletal mecha-
nisms that dictate plantarflexor function in patients treated for
Achilles tendon ruptures remain unclear.
The purpose of this study was to present preliminary findings
utilizing a multidisciplinary framework for linking plantarflexor
remodeling with functional deficits in patients who have suffered
⇑ Corresponding author at: 3737 Market Street, Suite 1050, Philadelphia, PA
19104, USA.
E-mail address: josh.baxter@uphs.upenn.edu (J.R. Baxter).
tarflexor morphology and patient function using an integrated
ultrasonography and motion capture approach (Fukunaga et al.,
2001). Further, we simulated a maximal-effort plantarflexion con-
traction using a computational model (Baxter et al., 2012) to test
the effects of muscle remodeling on plantarflexor function. Using
this framework, we began to build support for future testing of
our hypothesis that long-term functional deficits are associated
with decreased muscle fascicle length and increased pennation.
2. Methodology
A 27-year old male (1.83 m and 84 kg) with a poor clinical out-
come 2.5 years following an acute Achilles tendon rupture partici-
pated in this IRB approved study. The ruptured Achilles tendon on
the right leg was surgically repaired by another provider using an
open-reduction within 1 week of the initial injury. The patient
described inability to participate in recreational activities due to
loss of ankle strength and reported experiencing no pain. Poor clin-
ical outcomes were confirmed using a clinical outcome score

https://doi.org/10.1016/j.jbiomech.2018.08.016
0021-9290/Ó 2018 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Baxter, J.R., et al. Functional deficits may be explained by plantarflexor remodeling following Achilles tendon rupture
repair: Preliminary findings. J. Biomech. (2018), https://doi.org/10.1016/j.jbiomech.2018.08.016
2 J.R. Baxter et al. / Journal of Biomechanics xxx (2018) xxx–xxx

(Achilles Tendon Total Rupture Score: 49/100, (Nilsson-Helander
et al., 2007)), an evaluation by a fellowship-trained foot and ankle
surgeon, and the inability to perform a single-leg heel raise of at
least 50% of the unaffected side.
Morphological measurements of the medial gastrocnemius
were made on images acquired using ultrasonography (Telemed
SmartUs, Vilnius, Lithuania) on the affected and unaffected sides.
Muscle fascicle pennation, length, and muscle belly thickness
(Fig. 1) were acquired using an 8 MHz linear ultrasound probe (Tel-
emed LV8-5L60N-2, Vilnius, Lithuania) (Baxter and Piazza, 2014).
These measurements of medial gastrocnemius morphology were
acquired with the patient seated in an isokinetic dynomameter
(System 4, Biodex Medical Systems, Shirley, NY) with an extended
knee and ankle held in neutral position. During image acquisition,
the medial gastrocnemius of the affected limb was in a retracted
state that prevented us from imaging the muscle midbelly, which
resulted in aponeuroses that were not parallel. To control for this
transducer position, we decided to image the contralateral muscle
belly at the same position proximal of the muscle-tendon junction,
which also resulted in non-parallel aponeuroses. A single investi-
gator identified the deep and superficial aponeuroses as well as a
single fascicle using a custom-written script (MATLAB, The
Mathworks, Natick, MA). Lines were manually fit to each of these
structures and extrapolated off of the image until the fascicle inter-
sected both deep and superficial aponeuroses to define fascicle
length (lf) (Zhou et al., 2015). The angle between the deep aponeu-
rosis and fascicle was calculated to define muscle pennation (hf)
(Fukunaga et al., 1997). Muscle belly thickness (tf) was calculated
as the distance between the superficial and deep aponeuroses in
the mid-section of the image. Repeated measures of uninjured
plantarflexors in another cohort found these measurements to be
reliable (Appendix). Because the aponeuroses were non-parallel,
we were not able to calculate the change in tendon length based
on measurements of muscle architecture (Fukunaga et al., 2001).
Physiological cross sectional area (PCSA) of the medial gastrocne-
mius muscle was estimated by first calculating muscle volume as
a cylinder (Eq. (1) and normalizing this volume by the fascicle
length (Morse et al., 2005).
Supplementary data associated with this article can be found, in
the online version, at https://doi.org/10.1016/j.jbiomech.2018.08.
016.

2
PCSA ¼ ðp  0:5  tf  ðlf cos hf ÞÞ=lf ð1Þ
Plantarflexor function was assessed through a battery of tests
that consisted of isometric strength testing, walking, and single-
leg heel raises. Isometric plantarflexion strength were tested in
an isokinetic dynamometer with the patient seated with a fully
extended knee and neutrally-aligned ankle (Baxter and Piazza,
2014). Lower extremity biomechanics were quantified during
comfortable speed walking and single-leg heel raises using a
12-camera motion capture system (Raptor series, Motion Analysis
Corporation, Santa Rosa, CA) and 3 force plates (BP600900,
Advanced Mechanical Technology, Inc., Watertown, MA). Fascicle
shortening was synchronously acquired (Appendix) with an
8 MHz ultrasound probe during this battery of functional tests
(Lichtwark and Wilson, 2005). Plantarflexion kinematics, torque,
power, and fascicle shortening dynamics were calculated to estab-
lish the link between muscular and patient function. Peak ankle
plantarflexion, torque, and power were calculated using open-
source musculoskeletal software (Delp et al., 2007) (Opensim
v3.3, Stanford University), and fascicle shortening dynamics were
quantified using a custom-written tracking routine.
The effects of fascicle length and pennation on single-leg heel
raise height were tested using a simple computational model
(Fig. 2A). To simulate a single-leg heel raise, maximal plantarflex-
ion contractions of a foot pushing against a moving wall were sim-
ulated (Baxter et al., 2012). The wall retreated at a constant speed
of 0.15 m/s, which was determined based on the average vertical
velocity of the patient’s pelvis when performing single-leg heel
raises on the unaffected limb. A single hill-type muscle model in
series with an elastic element inserted into the foot and leg seg-
ments. Fascicle lengths and pennation angles were varied within
the ranges of the patients’ affected and unaffected limbs (Table 1)
to isolate the implications of these musculoskeletal parameters on
plantarflexor function. Specifically, fascicle length and pennation
angles were varied from 4 to 11 cm (1 cm increments) and 10 to
40 degrees (10 degree increments), respectively. Tendon slack
lengths were determined geometrically by subtracting the medial

Table 1
Medial gastrocnemius morphology.

Unaffected Affected %Change

Fascicle length 11.2 cm 4.6 cm 59%
Pennation 13 degrees 34 degrees 162%
Thickness 2.9 cm 2.2 cm 24%
PCSA 6.4 cm2 3.2 cm2 51%
Fig. 1. Ultrasound images of the medial gastrocnemius muscle were analyzed to
quantify the fascicle length, pennation angle, and thickness (not shown for clarity). PCSA – physiologic cross sectional area.

1
muscle force (F / F0)

Ftoe ↑ fascicle length ↓ pennation

lfascicle = [4,5,...,11] cm

θfascicle = [10,20,30,40]° 0.5

0.15 m/s

Fmuscle
0
0 25 50 0 25 50
A θankle B plantarflexion (˚) C plantarflexion (˚)

Fig. 2. (A) A single-leg calf raise was simulated using a computational model of a foot maximally plantarflexing against a retreating wall. (B) Increasing fascicle lengths and
(C) decreasing pennation increases the amount of muscle force that can be generated throughout the simulated single-leg calf raise. (B) pennation and (C) fascicle lengths
were held constant at 10 degrees and 5 cm, respectively, to characterize the effects of changing a single muscular parameter. Muscle forces are presented as a ratio of the peak
isometric force of the muscle (F/F0). Simulations were stopped when the muscle was unable to generate ground reaction forces that exceeded the scaled body weight of the
subject (horizontal dashed line) or when the ankle reached 50 degrees of plantarflexion.

Please cite this article in press as: Baxter, J.R., et al. Functional deficits may be explained by plantarflexor remodeling following Achilles tendon rupture
repair: Preliminary findings. J. Biomech. (2018), https://doi.org/10.1016/j.jbiomech.2018.08.016
 J.R. Baxter et al. / Journal of Biomechanics xxx (2018) xxx–xxx 3

1 affected medial gastrocnemius muscle had an estimated PCSA

muscle force (F / F0)

approximately one-half the magnitude of the unaffected muscle.
Plantarflexor function was markedly different between the
affected and unaffected sides during isometric strength testing
0.5 and single-leg heel raises but not during walking (Table 2). Isomet-
ric plantarflexor strength was 47% less in the affected side com-
3° 15° >50° pared to the unaffected side. While the fascicles of the affected
0 limb shortened 1.9 cm compared to 5.1 cm on the unaffected limb
0 25 50 (63% decrease), relative fascicle shortening (41–46% resting
lengths) was similar between sides (Table 2). Plantarflexion
muscle power (P / P0)

motion, torque, and power were similar between the affected

0.4
0.2
0 ence of peak plantarflexor torque, this 75% decrease in single-leg
0 25 50
plantarflexion (˚)
Fig. 3. Patient-specific fascicle length, pennation, and muscle PCSA values of the
unaffected (solid line), affected (dashed line), and affected muscle with decreased
PCSA (dotted line) were tested in the simulation of a single-leg heel raise. Relative
muscle force (F/F0, top) and power (P/P0, bottom) were greatly diminished with the
shorter, more pennate, and less thick muscles experimentally measured in the
patient’s affected limb. Peak plantarflexion simulated for each muscle condition is
represented with vertical dashed lines. Relative force and power was normalized by
the peak isometric force and power of the unaffected muscle, respectively.
gastrocnemius optimal fiber length from the muscle-tendon unit
length when the ankle was positioned in neutral position to mimic
the in vivo measurements (Baxter et al., 2012). Simulations began
with the ankle neutrally aligned and completed when either the
muscle stopped generating sufficient force to elevate the body or
when plantarflexion exceeded 50 degrees. Because we only mod-
eled the medial gastrocnemius – which comprises approximately
24% of the triceps surae total force (Arnold et al., 2010) – we set
the ground reaction force threshold for elevating the body at
196 N (23.8% of average body weight) (Fig. 3).
3. Results
The affected limb demonstrated observable architectural differ-
ences in the medial gastrocnemius muscle compared to the unaf-
fected limb (Table 1). Medial gastrocnemius fascicle length was
59% less, pennation was 162% greater, and thickness was 24% less
compared to the medial gastrocnemius of the unaffected limb. The
and unaffected limbs during walking at 1.05 m/s. Medial gastroc-
nemius fascicles of each limb isometrically contracted (<1 cm)
throughout the stance phase. Severe deficiencies in plantarflexion
motion, power, and muscle shortening explained a 70% decrease
in single-leg heel raise height on the affected side (Table 2). The
patient was only able to elevate his body 3 cm on the affected limb
compared to 11.9 degrees on his unaffected side. Despite no differ-
heel raise height was explained by a 62% decrease in plantarflexor
power. An 82% decrease of medial gastrocnemius fascicle shorten-
ing was measured using ultrasonography during the single-leg heel
raise (Table 2).
Simulated single-leg heel raise function was found to be posi-
tively influenced by longer and less pennate fascicles (Fig. 2). Long
fascicles with little pennation (measured in the unaffected limb)
produced simulated heel-raises that were not constrained by insuf-
ficient muscle force. However, when the shorter and more pennate
fascicles that were measured in the affected limb (Table 1) were
tested in the model, the simulation generated less force and power,
which resulted in a simulated heel-raise that stopped at 15 degrees
plantarflexion (Fig. 3). When the peak muscle force was reduced by
50% to simulate the measured decrease in PCSA of the test subject,
the model was only able to complete a single-leg heel raise of 3
degrees of plantarflexion.
4. Discussion
These preliminary findings rationalize the further testing of our
hypothesis that long-term functional deficits are associated with
decreased muscle fascicle length and increased pennation in
patients that suffer Achilles tendon ruptures. We found that differ-
ences in plantarflexor architecture may explain long-term func-
tional deficits in patients that are surgically treated for an
Achilles tendon rupture. Clinical measures of function, such as
the single-leg heel raise, directly test the plantarflexors ability to
actively shorten and perform positive work (Flanagan et al.,
2005; Österberg et al., 1998). On the other hand, cyclic activities,

Table 2
Plantarflexor biomechanics.

Unaffected Affected %change

Isometric Strength Torque (N m) 133 N m 70 N m 47%
MG shortening 0.45 (5.1 cm) 0.41 (1.9 cm) M (63%)
Single Leg Heel Raise Plantarflexion 40 degrees 12 degrees 70%
Height (cm) 11.9 cm 3.0 cm 75%
Torque (N m) 140 N m 140 N m M
Power (W) 260 W 100 W 62%
MG shortening 0.48 (5.4 cm) 0.22 (1.0 cm) 54% (82%)
Walking (1.1 m/s) Plantarflexion 17 ± 1 degrees 18 ± 1 degrees M
Torque (N m) 145 ± 6 N m 162 ± 5 N m M
Power (W) 284 ± 20 W 313 ± 57 W M
MG shortening <1 cm <1 cm M

Peak plantarflexor angle, torque, and power. Medial gastrocnemius (MG) relative shortening presented as ratio of absolute shortening/resting length and absolute shortening
(in parentheses). Nominal differences between the affected and unaffected sides (<10%) are denoted by M.

Please cite this article in press as: Baxter, J.R., et al. Functional deficits may be explained by plantarflexor remodeling following Achilles tendon rupture
repair: Preliminary findings. J. Biomech. (2018), https://doi.org/10.1016/j.jbiomech.2018.08.016
4 J.R. Baxter et al. / Journal of Biomechanics xxx (2018) xxx–xxx
such as walking, can be successfully performed with reduced plan-
tarflexor muscle function due to the well-described elastic energy
return of the Achilles tendon (Fukunaga et al., 2001; Ishikawa et al.,
2005). This proposed research framework supports experimental
findings with a computational model, demonstrating that medial
gastrocnemius morphology explains functional deficits when per-
forming a single-leg heel raise.
Traditional gait analysis may be a poor test of patient function
following an Achilles tendon rupture. We observed stereotypical
medial gastrocnemius function during gait (Fukunaga et al.,
2001) demonstrated that the patient walked with minimal muscle
shortening despite severely compromised plantarflexors on the
affected side, which may be compensated for with increased mus-
cle excitation (Appendix). While single-leg heel raises may serve as
better measures of plantarflexor function, reduced heel raise
height may be partly explained by the smaller plantarflexor mus-
cles. Our simulation of the affected muscle with a 51% smaller
PCSA resulted in 3 degrees of plantarflexion (Fig. 3) compared to
12 degrees measured in vivo (Table 1). These differences may be
explained by other plantarflexor muscles, such as the flexor hallu-
cus longus, which is often surgically transferred to the Achilles ten-
don in patients with chronic Achilles tendon ruptures to restore
function (Wapner et al., 2006).
Our findings suggest that the medial gastrocnemius may
undergo remodeling following an Achilles tendon rupture to
restore resting tendon tension, which may lead to shorter and
more pennate plantarflexor muscles and decreased PCSA (Table 1)
– resulting in reduced functional capacity (Fig. 2). Skeletal muscle
has been shown in small animal models to remodel in response to
changes to surrounding musculoskeletal structures, ultimately
changing the number of sarcomeres in series (Burkholder and
Lieber, 1998; Koh and Herzog, 1998). Thus maintaining musculo-
tendinous constraints, in the case of Achilles tendon ruptures
minimizing tendon diastasis, should be a priority, which can be
modified based on surgical technique (Demetracopoulos et al.,
2014) and rehabilitation strategies (Kangas et al., 2007;
Mortensen et al., 1999). Early intervention may be critical to
long-term outcomes (Westin et al., 2016) because tendon elonga-
tion appears to occur within the first 10 weeks of injury (Kangas
et al., 2007; Nyström and Holmlund, 1983). Surgical interventions
(Takahashi et al., 2010) and strength training (Blazevich et al.,
2007; Kawakami et al., 1995; Seynnes et al., 2006) may restore
fascicle morphology and improve patient function. Although it
may seem appealing to increase fascicle length through eccentric
training, these possible adaptations may not translate to improved
function since the muscle would be forced to operate over the
ascending limb of the force-length curve if the Achilles tendon
length remains elongated.
This study was affected by several limitations. These prelimi-
nary findings propose a mechanism for functional limitations in a
single patient who suffered an acute Achilles tendon rupture. Mor-
phological and functional measurements were not assessed at the
time of injury because this patient was treated for the initial injury
by another provider. It is possible that the unaffected limb under-
went morphological changes in response to an increased workload
to compensate for the functional constraints imposed by the
injured limb; however, prior work does not support this theory
(Howell et al., 1993). Ultrasound imaging of muscle architecture
was acquired with both ankles held in the neutral position, which
may have affected ankle torque (Fath et al., 2010), and therefore
muscle length. Due to the noticeably smaller – and more proximal
– gastrocnemius on the affected limb, we decided to acquire ultra-
sound images the same distance proximal of the muscle tendon
junction on both limbs. This decision may explain the increased
fascicle length on the unaffected limb. However, muscle pennation
of the unaffected limb was within 1 standard deviation of reported
Please cite this article in press as: Baxter, J.R., et al. Functional deficits may be explained by plantarflexor remodeling following Achilles tendon rupture
repair: Preliminary findings. J. Biomech. (2018), https://doi.org/10.1016/j.jbiomech.2018.08.016
values (Baxter and Piazza, 2014), suggesting that ultrasound
images were acquired at an appropriate location. Further, results
from our simple computational model appear to support experi-
mental measures of patient function, further supporting these
large disparities in fascicle lengths, pennation, and muscle thick-
ness between the affected and unaffected side. We did not measure
Achilles tendon elongation with ultrasound and, because of the
non-parallel aponeuroses, were unable to estimate elongation
(Fukunaga et al., 2001); however, the 8 cm deficit in single-leg heel
raise is consistent with an elongated tendon of approximately 4 cm
(Silbernagel et al., 2012). We only measured and modeled the
medial gastrocnemius muscle, which functions differently than
the other plantarflexors (Kawakami et al., 1998); however, plan-
tarflexor atrophy 18 months following Acute Achilles tendon rup-
ture is similar across the three muscles (Heikkinen et al., 2017).
Finally, this patient was an otherwise healthy 24-year old male
at the time of injury; and while nearly two-thirds of acute ruptures
occur in adults younger than 50 years of age (Lantto et al., 2015b),
the injury mechanism and physiologic response to the injury may
vary based on age.
5. Conclusion
Long-term functional deficits in patients who have suffered
acute Achilles tendon ruptures may be partially explained by mor-
phological changes in the medial gastrocnemius muscle. We pro-
pose a combined in vivo and in silico framework to rigorously
quantify muscle remodeling in response to Achilles tendon inju-
ries. This approach provides a means to prospectively study the
implications of injury, treatment, and rehabilitation on plan-
tarflexor function. Using this framework, we hypothesize that
these structural changes are compensatory to tendon elongation.
If correct, minimizing tendon elongation throughout treatment
and rehabilitation is essential for long-term patient function. Link-
ing plantarflexor structure and function in a prospective study is
necessary to optimize treatment and rehabilitation options for
patients with Achilles tendon injuries.
Conflict of interest
None of the Authors have conflicts of interest related to this
study.
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