- Email: [email protected]
Achilles tendon loading during weight bearing exercises
Accepted Manuscript Achilles tendon loading during weight bearing exercises Naghmeh Gheidi, Thomas W. Kernozek, John D. Willson, Andrew Revak, Keith Diers PII:
S1466-853X(17)30339-5
DOI:
10.1016/j.ptsp.2018.05.007
Reference:
YPTSP 898
To appear in:
Physical Therapy in Sport
Received Date: 3 August 2017 Revised Date:
18 April 2018
Accepted Date: 8 May 2018
Please cite this article as: Gheidi, N., Kernozek, T.W., Willson, J.D., Revak, A., Diers, K., Achilles tendon loading during weight bearing exercises, Physical Therapy in Sports (2018), doi: 10.1016/ j.ptsp.2018.05.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Achilles tendon loading during weight bearing exercises
Naghmeh Gheidi, Ph.D.1,2* (e-mail: [email protected])
John D. Willson, PT, Ph.D.3 (e-mail: [email protected]) Andrew Revak, DPT. 1 (e-mail: [email protected])
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Keith Diers, DPT, ATC.1(e-mail: [email protected])
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Thomas W. Kernozek, Ph.D., FACSM2, (e-mail: [email protected])
1. Department of Exercise and Sport Science, University of Wisconsin-La Crosse, La Crosse, USA
2. La Crosse Institute for Movement Science, Physical Therapy Program, Department of Health Professions, University of Wisconsin-La Crosse, La Crosse, USA.
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3. Department of Physical Therapy, East Carolina University, Greenville, USA.
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*Corresponding author: Naghmeh Gheidi, Ph.D, Department of Exercise and Sport Science, University of Wisconsin-La Crosse, 161 Mitchell Hall, E0010 - 1820 Pine street, La Crosse, WI, USA, 54601, Phone (608) 785 – 8182 Fax (608) 785-8172 (email: [email protected])
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Achilles tendon loading during a weight bearing exercises
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ACCEPTED MANUSCRIPT ABSTRACT
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Objective: Compare the estimated Achilles tendon (AT) loading using a
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musculoskeletal model during commonly performed weight bearing therapeutic
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exercises.
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Design: Controlled laboratory study.
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Setting: University biomechanics laboratory.
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Participants: Eighteen healthy males (Age:22.1±1.8 years, height:177.7±8.4 cm,
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weight =74.29±11.3 kg).
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Main Outcome Measure(s): AT loading was estimated during eleven exercises:
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tandem, Romberg, and unilateral standing, unilateral and bilateral heel raising, unilateral
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and bilateral jump landing, squat, lunge, walking, and running while moving the ankle
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through each subjects range of motion. Kinematic and kinetic data were recorded at
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180 Hz and 1800Hz respectively. These data were then used in a musculoskeletal model
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to estimate force in the triceps surae. AT cross-sectional images were measured by
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ultrasound to determine AT stress. A repeated measures multivariate analysis of
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variance (α=0.05) was used on AT loading variables.
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Results: Squat and unilateral jump landing were the most different in AT stress. Peak
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AT stress variables were generally greater during more dynamic, unilateral exercises
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compared to more static, bilateral exercises.
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Conclusions: Bilateral, more static exercises resulted in less AT loading and may serve
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as a progression during the rehabilitation compared to more dynamic, unilateral
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exercises.
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Keywords: Kinematics, Kinetics, Strain, Therapeutic Exercise, and Rehabilitation.
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ACCEPTED MANUSCRIPT INTRODUCTION
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Achilles tendon (AT) rupture and Achilles tendinopathy both are increasingly
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common injuries, particularly among runners, males, and those 30-50 years old
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(Ganestam, Kallemose, Troelsen, & Barfod, 2016; Lantto, Heikkinen, Flinkkilä,
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Ohtonen, & Leppilahti, 2015; Sobhani, Dekker, Postema, & Dijkstra, 2013).
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Conservative management of both AT rupture and tendinopathy are now routinely
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recommended (Egger & Berkowitz, 2017; Huttunen, Kannus, Rolf, Felländer-Tsai, &
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Mattila, 2014). The latest clinical practice guidelines for the treatment of Achilles pain,
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stiffness, and muscle power deficits provide the strongest recommendation to exercise
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therapy for treatment (Carcia, Martin, Houck, & Wukich, 2010). The mechanical loading of injured tendons through exercise therapy is
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recognized as a key consideration for tendon tissue reparative and constructive
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processes (Arampatzis, Karamanidis, Mademli, & Albracht, 2009; Kjaer et al., 2005).
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However, mechanical loads of excessive magnitude, duration, or frequency provided
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without sufficient time for adaptation are also associated with AT injury (Maganaris,
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Chatzistergos, Reeves, & Narici, 2017). Thus, for effective tissue healing, it appears
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necessary for people with AT disorders to experience exercises at an appropriate dose
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based on the current tendon material properties and stage of tendon healing. A clinical
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approach to AT exercise prescription is to adjust the magnitude, duration, and rate of
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tendon loading based on patient subjective response to treatment (Silbernagel, Thomeé,
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Eriksson, & Karlsson, 2007). Knowledge of AT stress characteristics across a spectrum
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of common rehabilitation exercises is fundamental to this approach as a basis for
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appropriate recommendations to either increase or decrease the remodeling stimulus for
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each patient. To date, however, no study has assessed AT loading during a variety of
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ACCEPTED MANUSCRIPT common weight-bearing exercises often performed during rehabilitation programs using
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the same computational methods. Our aim was to compare estimated AT loading and
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ankle range of motion during several exercises to inform exercise progression for the
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safe and progressive loading of the AT following rupture and tendinopathy. METHODS
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Subjects
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Eighteen healthy and physically active males were examined in our study (Age:
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22.1±1.8 years, height: 177.7±8.4 cm, weight: 74.29±11.3 kg, and Tegner activity level:
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6.22 ± 1.11).
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squared=0.715 in G*Power (3.0.10, Germany) revealed that a sample size of 13 would
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be sufficient to achieve to power 0.8. Subjects with a prior surgical history to either
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lower extremity within the past year, injury to either lower extremity within the past 6
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months that prevented participation in typical activities or greater than 1 day, less than 5
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on Tegner activity level scale, or current pain in the lower extremity or the trunk were
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excluded. Each subject was informed of the study procedures, benefits, and potential
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risks and signed an informed consent form approved by the Institutional Review Board
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at the University prior to participation.
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Protocol
A GE LOGIQ P6 Ultrasound (General Electric, Waukesha, WI, USA) was used
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in measuring AT cross-sectional area (CSA) of the right leg. Each subject was
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positioned in prone on a treatment table with their ankle in a neutral position as
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measured with a hand-held goniometer (Koivunen-Niemelä & Parkkola, 1995).
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Ultrasound gel (Aquasonic Clear, Fairfield, New Jersey, USA) was applied to the ML6-
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area on the subject’s skin. AT cross-sectional area images were then scaled and
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measured using ImageJ software (National Institutes of Health, Bethesda, MD, USA).
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All participants were fitted with a standard model of footwear (Model 625, New
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Balance, Boston, MA) and tight fitting clothing for testing. Forty-seven reflective
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markers (Vannatta & Kernozek, 2015) were placed on the subject’s skin or clothing for
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testing. A brief warm-up was performed while walking at a self-paced speed on a
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treadmill (CX-445T, Cybex, Boston, MA). Exercises were demonstrated, with specific
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instructions being provided by the same researcher for each subject. The right leg was
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always assessed for all participants and was placed on one of the four force plates flush
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with the laboratory floor. Subjects performed several practice repetitions for each of the
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exercises prior to testing and then performed five consecutive repetitions for all 11
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exercises performed in a random order. The exercises included tandem, Romberg, and
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unilateral standing (U-Standing), unilateral and bilateral heel rising, unilateral and
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bilateral jump landing, squat, forward lunge, walking, and running. The trials were
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repeated if there was poor timing of the exercise compared to a metronome used for
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pacing or participant was unable to perform the exercise sufficiently based on researcher
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observation. A one-minute rest period was incorporated into the transition between
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exercises. During bilateral exercises, participants were asked to attempt equal weight
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bearing on both lower extremities that were positioned each on a separate force plate.
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The following descriptions highlight the specific performance criteria of each
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exercise. To be consistent, all standing activities (tandem, Romberg, and U-Standing)
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were performed for approximately 4 seconds (tandem (3.92±0.36 s), U-Standing
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(4.02±0.36 s), and Romberg (4.22±0.92 s)). During the tandem stance, each subject
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heel to toe. During the Romberg stance, each subject stood upright with feet together.
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Each subject stood upright on their right leg with their hands at their sides during U-
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Standing. Each exercise was performed with the participant’s eyes open. During the
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squat, forward lunges (FL), unilateral heel raising (U-HR) and bilateral heel raising (B-
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HR), unilateral and bilateral forward-backward jumping exercises, subjects began in
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standing with their feet shoulder width apart on each force plate. During squatting, they
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were asked to have their thighs reach approximately parallel to the floor and for the
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forward lunge have their right knee achieve approximately a 90 degree angle. The
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forward stepping distance of the lunge to the force plate was scaled to a distance of
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three of the participant’s foot lengths. Front knee was required to stay behind toe to
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keep the tibia more vertical. The subject performed the lunge until knee of the trailing
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leg was located just above ground (about 1-3 inches). The rate of each exercise was
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paced with a metronome set at 0.5 Hz where approximately 1 second was used for the
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raising portion and 1 second for the lowering portion of each exercise. AT compression
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at end range dorsiflexion has been associated with insertional Achilles tendinopathy
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(Chimenti, Flemister, Tome, McMahon, & Houck, 2016). Therefore, B-HR and U-HR
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exercises were performed on a level surface rather than on an incline or edge of a step.
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Participants moved their ankle through their available range of motion when completing
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these exercises. Performing heel raising exercises from a level surface is also consistent
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with early rehabilitation exercises that address midportion Achilles tendinopathy
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(Silbernagel et al., 2007). The participants attempted to maintain while equal weight
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bearing throughout the B-HR exercise. For the jump landing tasks, subjects jumped
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forward with both feet over a 16 cm barrier and landed on both feet for bilateral
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ACCEPTED MANUSCRIPT jumping and landing (B-Jump-Land). For unilateral jumping and landing (U-Jump-
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Land), they performed the same exercise on one leg. They were asked to maintain
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stability for 2 seconds and then jump backward for each exercise where only the
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forward landing and backward jumping motions were analyzed. Based on visual
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observation, if any aspect of the left foot made contact with the ground during the
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unilateral exercises, the exercise was repeated. During walking and running trials, the
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subject walked or ran at constant speed of 1.4m/s±5% for walking and 3.5m/s±5% for
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running based on photocells interfaced with a digital clock.
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A random number generator was used to determine the order of exercise
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execution. Five successful trials of each exercise were completed. Only data from the
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right lower extremity were analyzed.
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Instrumentation
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Kinematic data were recorded at 180 Hz with 15 Motion Analysis cameras
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(Motion Analysis Corporation, Santa Rosa, CA, USA) surrounding the measurement
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space. Synchronized kinetic data were collected from one of four force platforms
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(Model 4080, Bertec Corporation, Columbus, OH, USA) sampled at 1800Hz. The
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kinematic and kinetic data, and muscle forces were calculated from a 44 degree of
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freedom (DOF) musculoskeletal model with 18 rigid segments using the Human Body
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Model (HBM, Motek Medical, Amsterdam, Netherlands). This model uses a head as a
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single segment with 3-DOF relative to the thorax, a trunk as three segments (pelvis,
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mid-trunk and thorax) with 3-DOF, upper arms with 6-DOF relative to thorax, elbow
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with 2-DOF, wrist with 2-DOF and pelvis segment with 6-DOF and able to rotate and
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translate in all three dimensions with respect to the ground (van den Bogert,
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Geijtenbeek, Even-Zohar, Steenbrink, & Hardin, 2013). The hip was a ball-in-socket
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tibiofemoral translations and non-sagittal rotations were both constrained as a function
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of knee flexion. Each foot segment had 2-DOF. The inertial characteristics of the
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musculoskeletal model segments were based on participants’ total body mass and
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segment lengths. Three hundred muscle tendon units were represented (86 in the legs,
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204 in the arms and 10 in the trunk) where the muscle insertion points, wrapping points,
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and moment arms were based on Delp et al., 1990. HBM utilizes a full body marker set
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that provides an estimate of force output from 300 muscles, although for this project we
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examined solely the lower leg muscles.
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HBM used global optimization to determine skeletal model kinematics then joint
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moments were obtained from equations of motion. Within the inverse dynamics
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processing algorithm, the residual loads, three forces and three moments on the pelvis
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were minimized. For each time step, the muscle forces were estimated from the joint
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moments by minimizing a static cost function where the sum of squared muscle
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activations was related to maximum muscle strengths (van den Bogert et al., 2013).
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The muscle forces from HBM were then used to quantify total AT force by
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summing the muscle forces of the medial and lateral gastrocnemius and soleus during
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the stance phase of each exercise. The AT stress was calculated by dividing the AT
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force by the participant specific AT cross-sectional area. Peak stress rate was
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determined from the instantaneous slope of the stress versus the time curve. The total
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AT force impulse (AT impulse) was calculated by integrating the AT force time graph
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by trapezoid rule. The ankle ROM was the total amount of joint excursion during
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stance.
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Statistical Analysis
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ACCEPTED MANUSCRIPT A repeated measures multivariate analysis of variance (MANOVA) with an
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alpha set to 0.05 was used to compare the AT stress, AT stress rate, AT force, ankle
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range of motion, and AT impulse across the 11 exercises. Follow-up univariate tests
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were then performed between each exercise. Finally, the Bonferroni procedure was used
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for pairwise comparisons between exercises for each dependent variable. All statistical
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procedures were performed using SPSS software (Version 23, IBM, Armonk, NY).
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RESULTS
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The MANOVA revealed differences between tasks (Wilk’s lambda=0.006, p-
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value<0.001). The univariate follow-up tests indicated differences in peak AT stress,
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AT force, AT stress rate, ankle ROM, and AT impulse over 1s for all 11 exercises.
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Table 1 shows the mean and standard deviation for peak AT stress, AT force,
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AT stress rate, ankle ROM, and AT impulse for each exercise. The Romberg standing
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position had the lowest ROM (0.26±0.15°) followed by the tandem stance (0.45±0.22°).
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Table 2 shows the percentage differences, effect size, and pairwise comparisons between AT loading variables and ankle ROM during each exercise.
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Insert Table 2 about here.
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Figure 1 depicts the AT stress throughout each exercise. It is observable that the
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timing of peak AT stress was somewhat unique between each exercise. However, some
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showed similar AT loading profiles but with different magnitudes like the B-Jump-Land
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and U-Jump-Land (at 0-30% for landing, ≈80-100% for jumping) and during the stance
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phase of walking and running. The peak AT stress for the B-Land-Jump and U-Jump-
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Land occurred during the jumping portion of the exercise. Similarly, for running and
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stress during the Romberg, U-Standing and tandem displayed somewhat uniform
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loading patterns since muscle force requirements were solely needed for postural
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control and required little participant change in motion as they were tested in a more
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static and set position. During both heel raise exercises (B-HR and U-HR), the peak AT
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stress occurred during raising portion rather than lowering while the FL showed a rather
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unique pattern where the peak AT stress occurred during raising (≈70%).
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Insert Figure 1 about here.
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Figure 2A depicts the peak AT stress in order of magnitude for all exercises.
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Categories were determined from AT stress based on statistical differences between
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exercises. Therefore, squat and Romberg with lowest stress were in the first category,
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followed by FL, B-HR, tandem, and U-Standing in the second category. Walking, B-
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Jump-Land, U-HR, and walking were in the third category. U-Jump-Land had the
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largest AT stress and was in the fourth category.
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Ankle ROM was presented in order of AT stress (Figure 2B). Ankle ROM did
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not demonstrate a similar order where the Romberg, tandem, and U-Standing had the
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lowest motion followed by running and walking. The FL, U-Jump-Land, and B-Jump-
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Land had highest ROM whereas the U-HR, Squat, B-HR, and FL were generally in the
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middle.
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Figure 2C depicts the AT stress rate in order of AT stress. Tandem, Romberg,
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U-Standing, and the squat showed similar and the lowest stress rate. FL, B-HR, and U-
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HR were similar but with a higher stress rate. Running and U-Jump-Land showed the
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highest stress rate of all exercises. The AT stress rate in order of magnitude was largely
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similar to the AT stress ordering of the exercises. Insert Figure 2 about here.
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Table 3 shows the AT impulse. One repetition of U-Jump-Land and U-HR
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showed the highest impulse. One second of the Romberg exercise, and one step walking
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and running showed the lowest impulse.
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Insert Table 2 about here.
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Figure 3, depicts a progressive order of loading based on magnitude. The
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magnitude for all variables (AT stress, AT stress rate, AT impulse, and ROM) was
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divided by their respective peak exercise to normalize each of these data. The
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Polynomial (order 3) trend lines appear to show a pattern of possible progressive order
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based on AT stress, AT stress rate, AT impulse and ROM magnitude. These data are
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based on our results presented in Table 2. This order starts with standing or balanced
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based exercises with minimal loading variables and ROM such as the Romberg,
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Tandem and U-Standing. These exercises may be appropriate as a first stage of
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progression. The second phase of progression may include the squat, B-HR, and FL
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with a higher load, impulse and ROM.
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Insert Figure 3 about here.
Walking and UHR may be in the third phase of progression, even though the
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impulse appears higher. During the final phase of progression, running and jumping
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may be recommended. These two last phases of progression and exercises appear to be
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supported
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Silbernagel et al., 2007; Strom & Casillas, 2009), within physical therapy assessments
in common rehabilitation regimens (Nilsson-Helander et al., 2010;
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based on the strength of the triceps surae and AT (Kountouris & Cook, 2007), and in
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AT injury prevention training(Kraemer & Knobloch, 2009). DISCUSSION
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Our aim was to compare the estimated AT loading variables and ankle ROM
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during common weight bearing exercises used in AT rehabilitation programs. Based on
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significant differences in peak stress obtained in this study, exercises were organized
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into 4 distinct categories. The first included the squat and Romberg, the second tandem,
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FL, U-Standing, and B-HR. Walking, B-Jump-Land, U-HR, and walking were in the
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third category. U-Jump-Land had the largest AT stress and was in the fourth category
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alone. In general, our AT force values are well below the reported AT failure load
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range of 4617-5579N (Wren, Yerby, Beaupré, & Carter, 2001). The order of the AT
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stress rate largely followed the order of AT stress. As expected range of motion
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requirements for the different exercises were lowest for the more static exercises.
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Standing activities generally displayed lower AT stress. During standing the
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body center of gravity often is located anterior to the ankle (Opila, Wagner, Schiowitz,
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& Chen, 1988), where the plantar flexor muscles provide tension to maintain balance.
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Cheung, Zhang, & An (2006) estimated AT force equivalent to .75 BW during bilateral
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standing using a finite element model which were slightly lower than our results of 0.91
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BW, 1.93 BW, and 2.18 BW AT force during Romberg, Tandem and U-standing,
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respectively. Interestingly, changing from a Romberg to tandem standing for the
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posterior limb increased AT force nearly 70% in our study. This was likely related to
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the more anterior location of the center of pressure for the posterior limb while in
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tandem standing. We did not analyze the anterior limb for tandem standing but would
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suspect AT stress to be lower. It has been shown that a 70 mm anterior shift in center of
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AT force (Cheung et al., 2006). Although ankle range of motion and AT rate did not
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show any differences between the Romberg and tandem standing, all loading variables
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were higher during tandem.
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Heel raising exercises are common during the initial phase of some AT
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tendinopathy rehabilitation programs (Silbernagel et al., 2007) and also indicated in the
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second and third phase of AT rupture rehabilitation program (Nilsson-Helander et al.,
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2010; Strom & Casillas, 2009). Peak AT force and stress were lower during bilateral
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(1375.0 N, 44.6 MPa) compared to U-HR (2903.0 N, 95.1 MPa). Rees, Lichtwark,
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Wolman, & Wilson (2008), reported similar AT force (≈ 2900 and 3100 N) as in our
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investigation (2903.3 N) during a U-HR and lowering exercise. Arya & Kulig (2010),
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reported similar AT force and stress (≈2250 N (2.94 BW), 40 MPa) estimated from the
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plantar flexor moment during a maximal effort isometric contraction against a
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dynamometer. Maganaris & Paul (2002), using a 90% maximal isometric contraction of
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the plantar flexors, reported a maximal force and stress on the AT of 875 N (1.19 BW)
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and 32.4 MPa where tendon forces were estimated from the moment generated based on
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tendon travel methods. In addition, Geremia et al., (2015) also estimated AT loading
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during a maximal plantarflexion contraction after a short term bout of physical therapy
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and reported an average stress of 53.9 MPa for a healthy control group using similar
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methods as the previous study.
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Our AT loading estimates during walking (2701.1 N (3.71BW), 86.2 MPa) were
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generally larger compared to previous studies. Finni, Komi, & Lukkariniemi (1998),
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reported AT force of 1480±560 N during walking at 1.5±0.2m/s1. They measured AT
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force by optic fiber techniques which may help explain the lower magnitudes compared
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that we observed (86.17 MPa). Also, there were differences in AT cross section area
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compared to our study which also can influence AT stress measures. Even though, they
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used the same methods to measure AT cross section area (ultrasonography), they
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reported a much larger mean AT cross section area (74 mm2) while in our study the
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peak AT cross section area was smaller (62 mm2). Their participants were five men and
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three women while we measured 18 men. Akizuki, Gartman, Nisonson, Ben-Avi, &
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McHugh (2001) reported AT forces of 553 N (0.73 BW) during typical walking. Our
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higher estimated AT force can likely be explained the difference in methodology as they
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used EMG to estimate AT force.
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AT injuries are particularly common among runners and running is considered
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to be an important aspect of rehabilitation programs for individuals hoping to return to
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sports (Silbernagel et al., 2007). The peak AT force in the present study while running
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at 3.5 m/s was approximately 4.15 BW using computer modeling based estimation,
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which is comparable to direct measurements of AT force (5.2 BW) during running at
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3.9 m/s (Komi, 1990) but slightly lower than other previous estimates of AT force
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during running. Estimated peak AT force were estimated to be between 4.5-7.2 BW
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using inverse dynamics methods of different running speeds (Sinclair, Taylor, & Atkins,
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2015; Scott & Winter, 1990; Willy, Halsey, Hayek, Johnson, & Willson, 2016; Farris,
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Buckeridge, Trewartha, & McGuigan, 2012). Peak AT force determined using
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musculoskeletal modeling based estimates of muscle force with different optimization
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methods have ranged between 5.3-8.0 BW when running at speeds between 3.5-4.4 m/s
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(Almonroeder, Willson, & Kernozek, 2013; Edwards, Gillette, Thomas, & Derrick,
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2008; Miller, Gillette, Derrick, & Caldwell, 2009). However, direct comparisons
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computer modeling techniques. For example, computer simulations of muscle force
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from optimization techniques include numerous assumptions and rely on many
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mathematical models to represent the musculoskeletal system. An advantage of the
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current study is that all of the exercises were subject to the same methods, facilitating a
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more direct comparison between exercises.
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Given the historical prescription of heel raises as part of a rehabilitation program
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for AT disorders, and the prevalence of Achilles tendinopathy among runners, a
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comparison of the mechanical stimulus between these two activities appears to be
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clinically relevant. Based on our results, the peak AT stress and force were similar
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between running and unilateral heel raises. However, the AT stress rate and impulse
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were significantly different between these activities. The AT stress rate was over four
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times greater during running but the impulse was over four times greater for the heel
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raise exercise. Despite the lower AT impulse for heel raises compared to that of a single
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stance phase during running, it is important to note that the common rehabilitation dose
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of 3 sets of 10 repetitions for heel raises results in a cumulative AT impulse that is only
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6% of the total AT impulse that a typical runner may experience over the course of a 30
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minute run (based on 176 steps/min at 3.5 m/s) (Willy et al., 2016). In order to mimic
303
the overall AT impulse of a 30-minute run, an individual would need to perform an
304
estimated 482 unilateral heel raises. Therefore, although unilateral heel lifts closely
305
mimic the peak magnitude of the mechanical stimulus during running in this study, this
306
exercise differs greatly in other important loading characteristics related to tendon
307
stiffness (stress rate) and total tendon energy transfer (impulse).
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ACCEPTED MANUSCRIPT Some studies have reported loads on the AT during hopping and jumping.
309
Lichtwark & Wilson (2005), reported peak AT force between 3500-400 N using in-vivo
310
methods during single limb hopping. Fukashiro, Komi, Järvinen, & Miyashita (1995) in
311
another in-vivo study reported a peak AT force of 3786 N during hopping over a 7cm
312
barrier. Our unilateral jump showed higher AT force (4864 N (6.68 BW)) in
313
comparison. We believe this discrepancy can be addressed by different involved
314
methods of measuring AT force as well as different barrier heights as we used a 16 cm
315
barrier. Jumping over a higher barrier likely requires higher muscle forces imparted to
316
the AT.
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All exercises chosen in this study are commonly used in rehabilitation programs;
318
many include both a concentric and eccentric phase. Eccentric training has been used
319
extensively in these programs for decreasing tendon pain and functional improvement
320
(Maffulli, Longo, Loppini, Spiezia, & Denaro, 2010). However, the review by Couppe
321
et al reported that tendon adaptations may depend on the number of repetitions at an
322
appropriate load, movement speed, and exercise duration regardless of muscle
323
contraction type (Couppé, Svensson, Silbernagel, Langberg, & Magnusson, 2015). In
324
addition, there some studies reporting no AT loading differences between the
325
concentric/eccentric phases of a heel raising and lowering exercise(Henriksen, Aaboe,
326
Bliddal, & Langberg, 2009; Rees et al., 2008). Henriksen et al., 2009 stated that the
327
applied external load is of primary importance in specifying the tendon load rather than
328
muscle contraction type.
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329
The main purpose for our study was to compare some common weight bearing
330
rehabilitation exercises used for AT injuries. Rehabilitation protocols historically aim to
331
provide a progressive prescription of therapeutic exercises that expose patients to an
17
ACCEPTED MANUSCRIPT appropriate load for tissue adaptation for the safe return to daily activities and sport.
333
Despite our exclusion criteria specifying the study of asymptomatic and healthy
334
subjects, perhaps future work should consider the use of the VISA-A questionnaire as it
335
is a valid and reliable index (Robinson et al., 2001) to further screen out individuals
336
with AT tendinopathy. A limitation of this study is that we were not able to include all
337
exercises identified in our survey of published rehabilitation protocols (Nilsson-
338
Helander et al., 2010; Silbernagel et al., 2007; Strom & Casillas, 2009). To our
339
knowledge, however, this is the first study to compare a wide variety of weight bearing
340
exercises common to several AT rehabilitation protocols using the same methodology.
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As a conclusion, it seems our results support the recommended progression of
342
loading for AT tendinopathy by increasing the speed of movement or increasing the
343
magnitude of load (Maffulli, Renstrom, & Leabetter, 2005). A progressive prescription
344
of weight bearing therapeutic exercises during rehabilitation may provide the tendon a
345
gradual stimulus for adaptation.
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ACCEPTED MANUSCRIPT Tables: Table 1: Mean ± standard deviation) for peak Achilles tendon (AT) stress, AT force, AT stress rate, ankle range of motion (ROM), and AT force impulse during each exercise performance.
Squat Romberg FL B-HR Tandem U-Standing Walk B-Jump-Land U-HR Run U-Jump-Land
18.23±8.10 21.43±6.98 40.96±18.89 44.60±11.89 46.05±18.88 52.17±12.93 86.17±28.32 91.90±35.98 95.07±33.73 97.80±50.83 158.55±71.60
0.77±0.35 0.91±0.3 1.72±0.74 1.89±0.41 1.93±0.74 2.18±0.38 3.71±1.29 3.88±1.43 3.98±1.06 4.15±2.03 6.68±2.66
AT Stress Rate (MPa/s) Mean±sd 35.30±18.20 17.61±6.00 128.18±65.48 220.46±111.47 16.77±8.62 18.29±8.58 403.42±163.20 1173.67±618.30 296.03±185.56 1200.11±561.11 1985.73±1036.60
Ankle ROM (°)
AT Force Impulse (BW*s)
RI PT
AT Force (BW)
31.57±5.39 0.26±0.15 39.27±8.48 31.73±5.55 0.45±0.22 0.95±0.62 18.39±4.69 46.37±8.28 30.44±7.19 13.30±5.37 41.14±6.78
SC
AT Stress (MPa)
M AN U
Exercise
3.68±2.13 0.72±0.22 4.1±2.2 3.02±0.80 1.40±0.45 1.66±0.28 1.63±0.50 3.80±1.53 7.26±1.60 2.04±1.64 10.01±5.68
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Note: FL = forward lunge, B=Bilateral, HR=Heel Raise, Land=Landing, U=Unilateral
ACCEPTED MANUSCRIPT Table 2: Percentage differences in Achilles tendon (AT) stress, AT force, rate of AT stress rate, ankle range of motion (ROM), and AT force impulse when performing each exercise. * means p-value<0.05. # means Cohen’s d effect size>0.08 (large effect size) AT Stress
AT Stress Rate
AT Force
AT Force Impulse
Ankle ROM
AT Stress
Romberg Run UStanding Squat Tandem
140.25*# 67.10#
-24.07
-23.59
150.05*#
190.55*#
84.72*#
76.80*# -11.67
76.31*# -11.51
113.63*# 153.72*#
21.74# 195.47*#
10.80 98.18*#
25.33#
-55.63*#
FL
76.68*#
77.14*#
160.62*#
16.58#
-7.59
Romberg Run UStanding
124.36*# -6.22
124.01*# -6.72#
194.09*# -2.23
197.77*# 110.84*#
136.28*# 60.27#
55.15*#
56.11*#
193.86*#
191.97*#
78.39*#
U-HR
-79.56*#
-79.30*#
-79.14*#
Squat
133.79*#
133.76*#
188.32*#
37.98*#
3.21
U-JumpLand
117.88*#
118.10*#
Tandem
66.47*#
67.13*#
194.37*#
196.16*#
92.31*#
Walk
-71.12*#
-73.30*#
-3.39
-2.54
119.43*#
41.48*#
-62.57*#
Run
128.11*#
128.06*#
175.75*# 103.55*# 164.22*#
-53.23*#
-53.03*#
-51.41*#
11.95
-89.93*#
UStanding
-83.53*#
-82.20*#
-3.79
Squat
16.14
16.67
-66.87*#
Tandem
-72.97*# 126.42*# 152.37*# 120.34*#
-71.83*# 125.56*# 152.04*# 121.21*#
7.89#
U-JumpLand Walk UStanding
-50.06*#
-50.66*#
SC
M AN U
97.68*#
86.41*#
79.93*#
FL
8.51#
9.42#
52.94#
-21.24#
-30.34
Romberg
70.18*#
70*#
170.41*#
196.75*#
123*#
-74.72*#
-74.83*#
137.92*#
81.86*#
38.73
U-JumpLand
-15.65
-14.25
169.36*#
188.37*#
58.12*#
Walk
84.21*#
144.79*#
0.51
-19.70
#
-2.09
171.72*
-72.27*#
-71.21*#
-29.26
112.018*#
111.79*#
Walk
-63.58*#
Tandem
#
#
73.03*#
194.49*#
186.91*#
37.21
U-HR
2.83
4.18
120.86*#
-78.37*#
-65.45*#
U-JumpLand
-47.40*#
-46.72*#
-49.32#
102.28*#
112.26*# 132.28*#
-92.48*#
Walk
12.64
11.20
99.37*#
-32.12*#
22.34
178.56*# 196.65*# 184.04*#
194.17*# 195.67*# 190.45*#
135.34*# 150.92*#
132.46*#
76.43*#
143.99*#
107.29*#
-86.56*#
-85.93*#
71.17*#
194.38*#
89.76*#
U-HR
-112.46*# -158.75*#
-26.32*#
Walk
130.153*#
157.38*# 193.01*# 167.82*#
3.64
U-JumpLand
135.16*# 158.66*# 131.25*#
52.76*#
77.21#
Squat
96.42*#
95.59*#
-63.48#
188.32*#
-75.66*#
Tandem
12.46
12.17
8.67#
71.43#
16.99
176.72*# 196.35*# 182.65*#
187.89*# 190.97*# 180.35*#
125.56*# 143.10*#
Walk
-49.15*#
-51.96*#
-31.85
71.95*#
53.23*#
101.58*#
-77.45*#
-57.34#
-58.65*#
1.82
Tandem
UJumpLand
U-HR
-69.47*#
-69.37*#
U-JumpLand
109.97*#
110.34*#
Walk
-60.69*#
-63.12*#
Walk
59.15*#
57.17*#
#
134.55*# -64.15*# 163.91*# 173.16*#
-81.44*#
-65*#
-100.97*#
Tandem
-29.90*#
-78.99*#
188.57*#
*
U-JumpLand
137.15*#
-95.65#
137.40*#
-25.83*#
-58.44*#
Squat
192.33*# 114.05*# 196.73*# -53.52# 196.61*# 197.49*# 194.42*#
20.54
160.03*#
-58.27*#
62.24*#
86.21*#
173.33*#
-82.49*#
U-HR
60.85*#
72.42*#
194.0*#
4.15
U-JumpLand
7.02
-83.77*#
126.66*#
73.30*
U-HR
9.82
177.54*# 196.45*# 183.27*# 148.11*# -30.71
U-HR
-4.65
49.35*
194.41*
EP
-3.20
Tandem
U-HR
Run
83.94*#
TE D
Squat
Romberg
4.48#
UStanding
RI PT
22.87
FL
37.49*
6.44#
AT Force Impulse
Percentage Differences (%) 61.60*# 151.68*# 197.37*# # -82.79* -161.4*# 98.80*#
136.75*
Walk
Ankle ROM
62.61*# -81.93*#
68.98*
Run
B-HR
#
96.30*
U-JumpLand
Squat
#
AT Stress Rate
B-HR
U-HR
U-Standing
#
AC C
B-Jump-Land
Percentage Differences (%) #
AT Force
-15.18
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Table 3: Mean ± standard deviation for peak AT force impulse per step during running and walking, over 1 second for standing exercises, and per repetition during Squat, FL, B-HR, U-HR, and Jump-Lands.
Per Repetition 1.21±0.33 2.91±0.66
AT Force Impulse (BW*s) B-JumpU-JumpWalk Run Land Land Per Step 1.52±0.63 4.00±2.34 0.97±0.30 0.60±0.49
Romberg
Tandem
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0.72±0.22
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1.64±0.91
B-HR
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1.47±0.88
FL
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Squat
In 1 sec 1.40±0.45
UStanding 1.66±0.28
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HIGHLIGHTS: Bilateral and standing exercises resulted in less AT loading.
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Ankle ROM did not demonstrate a similar order of magnitude as AT loading.
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Progressive weight bearing exercises start with standing or balanced based exercises with
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minimum AT loading and ROM. -
Squats, BHR, and FL then Walking and UHR may be appropriate for the second and
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Running and jumping may be recommended in the final phase of rehabilitation.
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third phases of rehabilitation.
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Ethical approval This study was approved by the Ethics Committee on the use of human subjects in research at the University of Wisconsin - La Crosse. All participants provided informed consent prior to
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participation.
S1466-853X(17)30339-5
DOI:
10.1016/j.ptsp.2018.05.007
Reference:
YPTSP 898
To appear in:
Physical Therapy in Sport
Received Date: 3 August 2017 Revised Date:
18 April 2018
Accepted Date: 8 May 2018
Please cite this article as: Gheidi, N., Kernozek, T.W., Willson, J.D., Revak, A., Diers, K., Achilles tendon loading during weight bearing exercises, Physical Therapy in Sports (2018), doi: 10.1016/ j.ptsp.2018.05.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Achilles tendon loading during weight bearing exercises
Naghmeh Gheidi, Ph.D.1,2* (e-mail: [email protected])
John D. Willson, PT, Ph.D.3 (e-mail: [email protected]) Andrew Revak, DPT. 1 (e-mail: [email protected])
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Keith Diers, DPT, ATC.1(e-mail: [email protected])
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Thomas W. Kernozek, Ph.D., FACSM2, (e-mail: [email protected])
1. Department of Exercise and Sport Science, University of Wisconsin-La Crosse, La Crosse, USA
2. La Crosse Institute for Movement Science, Physical Therapy Program, Department of Health Professions, University of Wisconsin-La Crosse, La Crosse, USA.
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3. Department of Physical Therapy, East Carolina University, Greenville, USA.
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*Corresponding author: Naghmeh Gheidi, Ph.D, Department of Exercise and Sport Science, University of Wisconsin-La Crosse, 161 Mitchell Hall, E0010 - 1820 Pine street, La Crosse, WI, USA, 54601, Phone (608) 785 – 8182 Fax (608) 785-8172 (email: [email protected])
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Achilles tendon loading during a weight bearing exercises
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ACCEPTED MANUSCRIPT ABSTRACT
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Objective: Compare the estimated Achilles tendon (AT) loading using a
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musculoskeletal model during commonly performed weight bearing therapeutic
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exercises.
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Design: Controlled laboratory study.
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Setting: University biomechanics laboratory.
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Participants: Eighteen healthy males (Age:22.1±1.8 years, height:177.7±8.4 cm,
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weight =74.29±11.3 kg).
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Main Outcome Measure(s): AT loading was estimated during eleven exercises:
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tandem, Romberg, and unilateral standing, unilateral and bilateral heel raising, unilateral
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and bilateral jump landing, squat, lunge, walking, and running while moving the ankle
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through each subjects range of motion. Kinematic and kinetic data were recorded at
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180 Hz and 1800Hz respectively. These data were then used in a musculoskeletal model
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to estimate force in the triceps surae. AT cross-sectional images were measured by
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ultrasound to determine AT stress. A repeated measures multivariate analysis of
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variance (α=0.05) was used on AT loading variables.
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Results: Squat and unilateral jump landing were the most different in AT stress. Peak
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AT stress variables were generally greater during more dynamic, unilateral exercises
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compared to more static, bilateral exercises.
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Conclusions: Bilateral, more static exercises resulted in less AT loading and may serve
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as a progression during the rehabilitation compared to more dynamic, unilateral
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exercises.
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Keywords: Kinematics, Kinetics, Strain, Therapeutic Exercise, and Rehabilitation.
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ACCEPTED MANUSCRIPT INTRODUCTION
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Achilles tendon (AT) rupture and Achilles tendinopathy both are increasingly
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common injuries, particularly among runners, males, and those 30-50 years old
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(Ganestam, Kallemose, Troelsen, & Barfod, 2016; Lantto, Heikkinen, Flinkkilä,
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Ohtonen, & Leppilahti, 2015; Sobhani, Dekker, Postema, & Dijkstra, 2013).
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Conservative management of both AT rupture and tendinopathy are now routinely
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recommended (Egger & Berkowitz, 2017; Huttunen, Kannus, Rolf, Felländer-Tsai, &
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Mattila, 2014). The latest clinical practice guidelines for the treatment of Achilles pain,
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stiffness, and muscle power deficits provide the strongest recommendation to exercise
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therapy for treatment (Carcia, Martin, Houck, & Wukich, 2010). The mechanical loading of injured tendons through exercise therapy is
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recognized as a key consideration for tendon tissue reparative and constructive
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processes (Arampatzis, Karamanidis, Mademli, & Albracht, 2009; Kjaer et al., 2005).
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However, mechanical loads of excessive magnitude, duration, or frequency provided
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without sufficient time for adaptation are also associated with AT injury (Maganaris,
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Chatzistergos, Reeves, & Narici, 2017). Thus, for effective tissue healing, it appears
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necessary for people with AT disorders to experience exercises at an appropriate dose
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based on the current tendon material properties and stage of tendon healing. A clinical
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approach to AT exercise prescription is to adjust the magnitude, duration, and rate of
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tendon loading based on patient subjective response to treatment (Silbernagel, Thomeé,
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Eriksson, & Karlsson, 2007). Knowledge of AT stress characteristics across a spectrum
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of common rehabilitation exercises is fundamental to this approach as a basis for
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appropriate recommendations to either increase or decrease the remodeling stimulus for
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each patient. To date, however, no study has assessed AT loading during a variety of
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ACCEPTED MANUSCRIPT common weight-bearing exercises often performed during rehabilitation programs using
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the same computational methods. Our aim was to compare estimated AT loading and
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ankle range of motion during several exercises to inform exercise progression for the
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safe and progressive loading of the AT following rupture and tendinopathy. METHODS
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Subjects
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Eighteen healthy and physically active males were examined in our study (Age:
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22.1±1.8 years, height: 177.7±8.4 cm, weight: 74.29±11.3 kg, and Tegner activity level:
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6.22 ± 1.11).
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squared=0.715 in G*Power (3.0.10, Germany) revealed that a sample size of 13 would
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be sufficient to achieve to power 0.8. Subjects with a prior surgical history to either
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lower extremity within the past year, injury to either lower extremity within the past 6
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months that prevented participation in typical activities or greater than 1 day, less than 5
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on Tegner activity level scale, or current pain in the lower extremity or the trunk were
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excluded. Each subject was informed of the study procedures, benefits, and potential
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risks and signed an informed consent form approved by the Institutional Review Board
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at the University prior to participation.
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Protocol
A GE LOGIQ P6 Ultrasound (General Electric, Waukesha, WI, USA) was used
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in measuring AT cross-sectional area (CSA) of the right leg. Each subject was
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positioned in prone on a treatment table with their ankle in a neutral position as
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measured with a hand-held goniometer (Koivunen-Niemelä & Parkkola, 1995).
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Ultrasound gel (Aquasonic Clear, Fairfield, New Jersey, USA) was applied to the ML6-
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area on the subject’s skin. AT cross-sectional area images were then scaled and
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measured using ImageJ software (National Institutes of Health, Bethesda, MD, USA).
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All participants were fitted with a standard model of footwear (Model 625, New
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Balance, Boston, MA) and tight fitting clothing for testing. Forty-seven reflective
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markers (Vannatta & Kernozek, 2015) were placed on the subject’s skin or clothing for
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testing. A brief warm-up was performed while walking at a self-paced speed on a
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treadmill (CX-445T, Cybex, Boston, MA). Exercises were demonstrated, with specific
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instructions being provided by the same researcher for each subject. The right leg was
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always assessed for all participants and was placed on one of the four force plates flush
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with the laboratory floor. Subjects performed several practice repetitions for each of the
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exercises prior to testing and then performed five consecutive repetitions for all 11
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exercises performed in a random order. The exercises included tandem, Romberg, and
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unilateral standing (U-Standing), unilateral and bilateral heel rising, unilateral and
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bilateral jump landing, squat, forward lunge, walking, and running. The trials were
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repeated if there was poor timing of the exercise compared to a metronome used for
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pacing or participant was unable to perform the exercise sufficiently based on researcher
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observation. A one-minute rest period was incorporated into the transition between
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exercises. During bilateral exercises, participants were asked to attempt equal weight
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bearing on both lower extremities that were positioned each on a separate force plate.
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The following descriptions highlight the specific performance criteria of each
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exercise. To be consistent, all standing activities (tandem, Romberg, and U-Standing)
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were performed for approximately 4 seconds (tandem (3.92±0.36 s), U-Standing
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(4.02±0.36 s), and Romberg (4.22±0.92 s)). During the tandem stance, each subject
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heel to toe. During the Romberg stance, each subject stood upright with feet together.
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Each subject stood upright on their right leg with their hands at their sides during U-
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Standing. Each exercise was performed with the participant’s eyes open. During the
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squat, forward lunges (FL), unilateral heel raising (U-HR) and bilateral heel raising (B-
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HR), unilateral and bilateral forward-backward jumping exercises, subjects began in
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standing with their feet shoulder width apart on each force plate. During squatting, they
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were asked to have their thighs reach approximately parallel to the floor and for the
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forward lunge have their right knee achieve approximately a 90 degree angle. The
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forward stepping distance of the lunge to the force plate was scaled to a distance of
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three of the participant’s foot lengths. Front knee was required to stay behind toe to
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keep the tibia more vertical. The subject performed the lunge until knee of the trailing
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leg was located just above ground (about 1-3 inches). The rate of each exercise was
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paced with a metronome set at 0.5 Hz where approximately 1 second was used for the
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raising portion and 1 second for the lowering portion of each exercise. AT compression
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at end range dorsiflexion has been associated with insertional Achilles tendinopathy
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(Chimenti, Flemister, Tome, McMahon, & Houck, 2016). Therefore, B-HR and U-HR
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exercises were performed on a level surface rather than on an incline or edge of a step.
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Participants moved their ankle through their available range of motion when completing
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these exercises. Performing heel raising exercises from a level surface is also consistent
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with early rehabilitation exercises that address midportion Achilles tendinopathy
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(Silbernagel et al., 2007). The participants attempted to maintain while equal weight
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bearing throughout the B-HR exercise. For the jump landing tasks, subjects jumped
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forward with both feet over a 16 cm barrier and landed on both feet for bilateral
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Land), they performed the same exercise on one leg. They were asked to maintain
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stability for 2 seconds and then jump backward for each exercise where only the
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forward landing and backward jumping motions were analyzed. Based on visual
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observation, if any aspect of the left foot made contact with the ground during the
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unilateral exercises, the exercise was repeated. During walking and running trials, the
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subject walked or ran at constant speed of 1.4m/s±5% for walking and 3.5m/s±5% for
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running based on photocells interfaced with a digital clock.
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A random number generator was used to determine the order of exercise
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execution. Five successful trials of each exercise were completed. Only data from the
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right lower extremity were analyzed.
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Instrumentation
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Kinematic data were recorded at 180 Hz with 15 Motion Analysis cameras
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(Motion Analysis Corporation, Santa Rosa, CA, USA) surrounding the measurement
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space. Synchronized kinetic data were collected from one of four force platforms
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(Model 4080, Bertec Corporation, Columbus, OH, USA) sampled at 1800Hz. The
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kinematic and kinetic data, and muscle forces were calculated from a 44 degree of
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freedom (DOF) musculoskeletal model with 18 rigid segments using the Human Body
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Model (HBM, Motek Medical, Amsterdam, Netherlands). This model uses a head as a
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single segment with 3-DOF relative to the thorax, a trunk as three segments (pelvis,
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mid-trunk and thorax) with 3-DOF, upper arms with 6-DOF relative to thorax, elbow
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with 2-DOF, wrist with 2-DOF and pelvis segment with 6-DOF and able to rotate and
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translate in all three dimensions with respect to the ground (van den Bogert,
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Geijtenbeek, Even-Zohar, Steenbrink, & Hardin, 2013). The hip was a ball-in-socket
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tibiofemoral translations and non-sagittal rotations were both constrained as a function
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of knee flexion. Each foot segment had 2-DOF. The inertial characteristics of the
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musculoskeletal model segments were based on participants’ total body mass and
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segment lengths. Three hundred muscle tendon units were represented (86 in the legs,
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204 in the arms and 10 in the trunk) where the muscle insertion points, wrapping points,
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and moment arms were based on Delp et al., 1990. HBM utilizes a full body marker set
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that provides an estimate of force output from 300 muscles, although for this project we
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examined solely the lower leg muscles.
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HBM used global optimization to determine skeletal model kinematics then joint
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moments were obtained from equations of motion. Within the inverse dynamics
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processing algorithm, the residual loads, three forces and three moments on the pelvis
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were minimized. For each time step, the muscle forces were estimated from the joint
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moments by minimizing a static cost function where the sum of squared muscle
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activations was related to maximum muscle strengths (van den Bogert et al., 2013).
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The muscle forces from HBM were then used to quantify total AT force by
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summing the muscle forces of the medial and lateral gastrocnemius and soleus during
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the stance phase of each exercise. The AT stress was calculated by dividing the AT
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force by the participant specific AT cross-sectional area. Peak stress rate was
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determined from the instantaneous slope of the stress versus the time curve. The total
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AT force impulse (AT impulse) was calculated by integrating the AT force time graph
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by trapezoid rule. The ankle ROM was the total amount of joint excursion during
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stance.
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Statistical Analysis
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alpha set to 0.05 was used to compare the AT stress, AT stress rate, AT force, ankle
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range of motion, and AT impulse across the 11 exercises. Follow-up univariate tests
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were then performed between each exercise. Finally, the Bonferroni procedure was used
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for pairwise comparisons between exercises for each dependent variable. All statistical
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procedures were performed using SPSS software (Version 23, IBM, Armonk, NY).
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RESULTS
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The MANOVA revealed differences between tasks (Wilk’s lambda=0.006, p-
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value<0.001). The univariate follow-up tests indicated differences in peak AT stress,
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AT force, AT stress rate, ankle ROM, and AT impulse over 1s for all 11 exercises.
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Table 1 shows the mean and standard deviation for peak AT stress, AT force,
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AT stress rate, ankle ROM, and AT impulse for each exercise. The Romberg standing
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position had the lowest ROM (0.26±0.15°) followed by the tandem stance (0.45±0.22°).
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Table 2 shows the percentage differences, effect size, and pairwise comparisons between AT loading variables and ankle ROM during each exercise.
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Insert Table 2 about here.
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Figure 1 depicts the AT stress throughout each exercise. It is observable that the
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timing of peak AT stress was somewhat unique between each exercise. However, some
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showed similar AT loading profiles but with different magnitudes like the B-Jump-Land
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and U-Jump-Land (at 0-30% for landing, ≈80-100% for jumping) and during the stance
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phase of walking and running. The peak AT stress for the B-Land-Jump and U-Jump-
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Land occurred during the jumping portion of the exercise. Similarly, for running and
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stress during the Romberg, U-Standing and tandem displayed somewhat uniform
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loading patterns since muscle force requirements were solely needed for postural
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control and required little participant change in motion as they were tested in a more
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static and set position. During both heel raise exercises (B-HR and U-HR), the peak AT
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stress occurred during raising portion rather than lowering while the FL showed a rather
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unique pattern where the peak AT stress occurred during raising (≈70%).
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Insert Figure 1 about here.
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Figure 2A depicts the peak AT stress in order of magnitude for all exercises.
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Categories were determined from AT stress based on statistical differences between
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exercises. Therefore, squat and Romberg with lowest stress were in the first category,
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followed by FL, B-HR, tandem, and U-Standing in the second category. Walking, B-
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Jump-Land, U-HR, and walking were in the third category. U-Jump-Land had the
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largest AT stress and was in the fourth category.
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Ankle ROM was presented in order of AT stress (Figure 2B). Ankle ROM did
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not demonstrate a similar order where the Romberg, tandem, and U-Standing had the
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lowest motion followed by running and walking. The FL, U-Jump-Land, and B-Jump-
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Land had highest ROM whereas the U-HR, Squat, B-HR, and FL were generally in the
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middle.
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Figure 2C depicts the AT stress rate in order of AT stress. Tandem, Romberg,
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U-Standing, and the squat showed similar and the lowest stress rate. FL, B-HR, and U-
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HR were similar but with a higher stress rate. Running and U-Jump-Land showed the
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highest stress rate of all exercises. The AT stress rate in order of magnitude was largely
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similar to the AT stress ordering of the exercises. Insert Figure 2 about here.
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Table 3 shows the AT impulse. One repetition of U-Jump-Land and U-HR
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showed the highest impulse. One second of the Romberg exercise, and one step walking
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and running showed the lowest impulse.
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Insert Table 2 about here.
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Figure 3, depicts a progressive order of loading based on magnitude. The
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magnitude for all variables (AT stress, AT stress rate, AT impulse, and ROM) was
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divided by their respective peak exercise to normalize each of these data. The
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Polynomial (order 3) trend lines appear to show a pattern of possible progressive order
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based on AT stress, AT stress rate, AT impulse and ROM magnitude. These data are
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based on our results presented in Table 2. This order starts with standing or balanced
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based exercises with minimal loading variables and ROM such as the Romberg,
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Tandem and U-Standing. These exercises may be appropriate as a first stage of
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progression. The second phase of progression may include the squat, B-HR, and FL
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with a higher load, impulse and ROM.
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Insert Figure 3 about here.
Walking and UHR may be in the third phase of progression, even though the
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impulse appears higher. During the final phase of progression, running and jumping
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may be recommended. These two last phases of progression and exercises appear to be
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supported
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Silbernagel et al., 2007; Strom & Casillas, 2009), within physical therapy assessments
in common rehabilitation regimens (Nilsson-Helander et al., 2010;
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based on the strength of the triceps surae and AT (Kountouris & Cook, 2007), and in
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AT injury prevention training(Kraemer & Knobloch, 2009). DISCUSSION
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Our aim was to compare the estimated AT loading variables and ankle ROM
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during common weight bearing exercises used in AT rehabilitation programs. Based on
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significant differences in peak stress obtained in this study, exercises were organized
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into 4 distinct categories. The first included the squat and Romberg, the second tandem,
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FL, U-Standing, and B-HR. Walking, B-Jump-Land, U-HR, and walking were in the
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third category. U-Jump-Land had the largest AT stress and was in the fourth category
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alone. In general, our AT force values are well below the reported AT failure load
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range of 4617-5579N (Wren, Yerby, Beaupré, & Carter, 2001). The order of the AT
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stress rate largely followed the order of AT stress. As expected range of motion
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requirements for the different exercises were lowest for the more static exercises.
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Standing activities generally displayed lower AT stress. During standing the
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body center of gravity often is located anterior to the ankle (Opila, Wagner, Schiowitz,
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& Chen, 1988), where the plantar flexor muscles provide tension to maintain balance.
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Cheung, Zhang, & An (2006) estimated AT force equivalent to .75 BW during bilateral
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standing using a finite element model which were slightly lower than our results of 0.91
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BW, 1.93 BW, and 2.18 BW AT force during Romberg, Tandem and U-standing,
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respectively. Interestingly, changing from a Romberg to tandem standing for the
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posterior limb increased AT force nearly 70% in our study. This was likely related to
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the more anterior location of the center of pressure for the posterior limb while in
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tandem standing. We did not analyze the anterior limb for tandem standing but would
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suspect AT stress to be lower. It has been shown that a 70 mm anterior shift in center of
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AT force (Cheung et al., 2006). Although ankle range of motion and AT rate did not
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show any differences between the Romberg and tandem standing, all loading variables
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were higher during tandem.
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Heel raising exercises are common during the initial phase of some AT
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tendinopathy rehabilitation programs (Silbernagel et al., 2007) and also indicated in the
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second and third phase of AT rupture rehabilitation program (Nilsson-Helander et al.,
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2010; Strom & Casillas, 2009). Peak AT force and stress were lower during bilateral
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(1375.0 N, 44.6 MPa) compared to U-HR (2903.0 N, 95.1 MPa). Rees, Lichtwark,
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Wolman, & Wilson (2008), reported similar AT force (≈ 2900 and 3100 N) as in our
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investigation (2903.3 N) during a U-HR and lowering exercise. Arya & Kulig (2010),
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reported similar AT force and stress (≈2250 N (2.94 BW), 40 MPa) estimated from the
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plantar flexor moment during a maximal effort isometric contraction against a
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dynamometer. Maganaris & Paul (2002), using a 90% maximal isometric contraction of
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the plantar flexors, reported a maximal force and stress on the AT of 875 N (1.19 BW)
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and 32.4 MPa where tendon forces were estimated from the moment generated based on
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tendon travel methods. In addition, Geremia et al., (2015) also estimated AT loading
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during a maximal plantarflexion contraction after a short term bout of physical therapy
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and reported an average stress of 53.9 MPa for a healthy control group using similar
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methods as the previous study.
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Our AT loading estimates during walking (2701.1 N (3.71BW), 86.2 MPa) were
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generally larger compared to previous studies. Finni, Komi, & Lukkariniemi (1998),
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reported AT force of 1480±560 N during walking at 1.5±0.2m/s1. They measured AT
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force by optic fiber techniques which may help explain the lower magnitudes compared
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that we observed (86.17 MPa). Also, there were differences in AT cross section area
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compared to our study which also can influence AT stress measures. Even though, they
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used the same methods to measure AT cross section area (ultrasonography), they
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reported a much larger mean AT cross section area (74 mm2) while in our study the
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peak AT cross section area was smaller (62 mm2). Their participants were five men and
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three women while we measured 18 men. Akizuki, Gartman, Nisonson, Ben-Avi, &
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McHugh (2001) reported AT forces of 553 N (0.73 BW) during typical walking. Our
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higher estimated AT force can likely be explained the difference in methodology as they
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used EMG to estimate AT force.
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AT injuries are particularly common among runners and running is considered
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to be an important aspect of rehabilitation programs for individuals hoping to return to
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sports (Silbernagel et al., 2007). The peak AT force in the present study while running
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at 3.5 m/s was approximately 4.15 BW using computer modeling based estimation,
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which is comparable to direct measurements of AT force (5.2 BW) during running at
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3.9 m/s (Komi, 1990) but slightly lower than other previous estimates of AT force
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during running. Estimated peak AT force were estimated to be between 4.5-7.2 BW
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using inverse dynamics methods of different running speeds (Sinclair, Taylor, & Atkins,
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2015; Scott & Winter, 1990; Willy, Halsey, Hayek, Johnson, & Willson, 2016; Farris,
280
Buckeridge, Trewartha, & McGuigan, 2012). Peak AT force determined using
281
musculoskeletal modeling based estimates of muscle force with different optimization
282
methods have ranged between 5.3-8.0 BW when running at speeds between 3.5-4.4 m/s
283
(Almonroeder, Willson, & Kernozek, 2013; Edwards, Gillette, Thomas, & Derrick,
284
2008; Miller, Gillette, Derrick, & Caldwell, 2009). However, direct comparisons
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ACCEPTED MANUSCRIPT between studies should be made with caution due to differences in running speed and
286
computer modeling techniques. For example, computer simulations of muscle force
287
from optimization techniques include numerous assumptions and rely on many
288
mathematical models to represent the musculoskeletal system. An advantage of the
289
current study is that all of the exercises were subject to the same methods, facilitating a
290
more direct comparison between exercises.
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Given the historical prescription of heel raises as part of a rehabilitation program
292
for AT disorders, and the prevalence of Achilles tendinopathy among runners, a
293
comparison of the mechanical stimulus between these two activities appears to be
294
clinically relevant. Based on our results, the peak AT stress and force were similar
295
between running and unilateral heel raises. However, the AT stress rate and impulse
296
were significantly different between these activities. The AT stress rate was over four
297
times greater during running but the impulse was over four times greater for the heel
298
raise exercise. Despite the lower AT impulse for heel raises compared to that of a single
299
stance phase during running, it is important to note that the common rehabilitation dose
300
of 3 sets of 10 repetitions for heel raises results in a cumulative AT impulse that is only
301
6% of the total AT impulse that a typical runner may experience over the course of a 30
302
minute run (based on 176 steps/min at 3.5 m/s) (Willy et al., 2016). In order to mimic
303
the overall AT impulse of a 30-minute run, an individual would need to perform an
304
estimated 482 unilateral heel raises. Therefore, although unilateral heel lifts closely
305
mimic the peak magnitude of the mechanical stimulus during running in this study, this
306
exercise differs greatly in other important loading characteristics related to tendon
307
stiffness (stress rate) and total tendon energy transfer (impulse).
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ACCEPTED MANUSCRIPT Some studies have reported loads on the AT during hopping and jumping.
309
Lichtwark & Wilson (2005), reported peak AT force between 3500-400 N using in-vivo
310
methods during single limb hopping. Fukashiro, Komi, Järvinen, & Miyashita (1995) in
311
another in-vivo study reported a peak AT force of 3786 N during hopping over a 7cm
312
barrier. Our unilateral jump showed higher AT force (4864 N (6.68 BW)) in
313
comparison. We believe this discrepancy can be addressed by different involved
314
methods of measuring AT force as well as different barrier heights as we used a 16 cm
315
barrier. Jumping over a higher barrier likely requires higher muscle forces imparted to
316
the AT.
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All exercises chosen in this study are commonly used in rehabilitation programs;
318
many include both a concentric and eccentric phase. Eccentric training has been used
319
extensively in these programs for decreasing tendon pain and functional improvement
320
(Maffulli, Longo, Loppini, Spiezia, & Denaro, 2010). However, the review by Couppe
321
et al reported that tendon adaptations may depend on the number of repetitions at an
322
appropriate load, movement speed, and exercise duration regardless of muscle
323
contraction type (Couppé, Svensson, Silbernagel, Langberg, & Magnusson, 2015). In
324
addition, there some studies reporting no AT loading differences between the
325
concentric/eccentric phases of a heel raising and lowering exercise(Henriksen, Aaboe,
326
Bliddal, & Langberg, 2009; Rees et al., 2008). Henriksen et al., 2009 stated that the
327
applied external load is of primary importance in specifying the tendon load rather than
328
muscle contraction type.
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329
The main purpose for our study was to compare some common weight bearing
330
rehabilitation exercises used for AT injuries. Rehabilitation protocols historically aim to
331
provide a progressive prescription of therapeutic exercises that expose patients to an
17
ACCEPTED MANUSCRIPT appropriate load for tissue adaptation for the safe return to daily activities and sport.
333
Despite our exclusion criteria specifying the study of asymptomatic and healthy
334
subjects, perhaps future work should consider the use of the VISA-A questionnaire as it
335
is a valid and reliable index (Robinson et al., 2001) to further screen out individuals
336
with AT tendinopathy. A limitation of this study is that we were not able to include all
337
exercises identified in our survey of published rehabilitation protocols (Nilsson-
338
Helander et al., 2010; Silbernagel et al., 2007; Strom & Casillas, 2009). To our
339
knowledge, however, this is the first study to compare a wide variety of weight bearing
340
exercises common to several AT rehabilitation protocols using the same methodology.
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As a conclusion, it seems our results support the recommended progression of
342
loading for AT tendinopathy by increasing the speed of movement or increasing the
343
magnitude of load (Maffulli, Renstrom, & Leabetter, 2005). A progressive prescription
344
of weight bearing therapeutic exercises during rehabilitation may provide the tendon a
345
gradual stimulus for adaptation.
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ACCEPTED MANUSCRIPT Tables: Table 1: Mean ± standard deviation) for peak Achilles tendon (AT) stress, AT force, AT stress rate, ankle range of motion (ROM), and AT force impulse during each exercise performance.
Squat Romberg FL B-HR Tandem U-Standing Walk B-Jump-Land U-HR Run U-Jump-Land
18.23±8.10 21.43±6.98 40.96±18.89 44.60±11.89 46.05±18.88 52.17±12.93 86.17±28.32 91.90±35.98 95.07±33.73 97.80±50.83 158.55±71.60
0.77±0.35 0.91±0.3 1.72±0.74 1.89±0.41 1.93±0.74 2.18±0.38 3.71±1.29 3.88±1.43 3.98±1.06 4.15±2.03 6.68±2.66
AT Stress Rate (MPa/s) Mean±sd 35.30±18.20 17.61±6.00 128.18±65.48 220.46±111.47 16.77±8.62 18.29±8.58 403.42±163.20 1173.67±618.30 296.03±185.56 1200.11±561.11 1985.73±1036.60
Ankle ROM (°)
AT Force Impulse (BW*s)
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AT Force (BW)
31.57±5.39 0.26±0.15 39.27±8.48 31.73±5.55 0.45±0.22 0.95±0.62 18.39±4.69 46.37±8.28 30.44±7.19 13.30±5.37 41.14±6.78
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AT Stress (MPa)
M AN U
Exercise
3.68±2.13 0.72±0.22 4.1±2.2 3.02±0.80 1.40±0.45 1.66±0.28 1.63±0.50 3.80±1.53 7.26±1.60 2.04±1.64 10.01±5.68
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Note: FL = forward lunge, B=Bilateral, HR=Heel Raise, Land=Landing, U=Unilateral
ACCEPTED MANUSCRIPT Table 2: Percentage differences in Achilles tendon (AT) stress, AT force, rate of AT stress rate, ankle range of motion (ROM), and AT force impulse when performing each exercise. * means p-value<0.05. # means Cohen’s d effect size>0.08 (large effect size) AT Stress
AT Stress Rate
AT Force
AT Force Impulse
Ankle ROM
AT Stress
Romberg Run UStanding Squat Tandem
140.25*# 67.10#
-24.07
-23.59
150.05*#
190.55*#
84.72*#
76.80*# -11.67
76.31*# -11.51
113.63*# 153.72*#
21.74# 195.47*#
10.80 98.18*#
25.33#
-55.63*#
FL
76.68*#
77.14*#
160.62*#
16.58#
-7.59
Romberg Run UStanding
124.36*# -6.22
124.01*# -6.72#
194.09*# -2.23
197.77*# 110.84*#
136.28*# 60.27#
55.15*#
56.11*#
193.86*#
191.97*#
78.39*#
U-HR
-79.56*#
-79.30*#
-79.14*#
Squat
133.79*#
133.76*#
188.32*#
37.98*#
3.21
U-JumpLand
117.88*#
118.10*#
Tandem
66.47*#
67.13*#
194.37*#
196.16*#
92.31*#
Walk
-71.12*#
-73.30*#
-3.39
-2.54
119.43*#
41.48*#
-62.57*#
Run
128.11*#
128.06*#
175.75*# 103.55*# 164.22*#
-53.23*#
-53.03*#
-51.41*#
11.95
-89.93*#
UStanding
-83.53*#
-82.20*#
-3.79
Squat
16.14
16.67
-66.87*#
Tandem
-72.97*# 126.42*# 152.37*# 120.34*#
-71.83*# 125.56*# 152.04*# 121.21*#
7.89#
U-JumpLand Walk UStanding
-50.06*#
-50.66*#
SC
M AN U
97.68*#
86.41*#
79.93*#
FL
8.51#
9.42#
52.94#
-21.24#
-30.34
Romberg
70.18*#
70*#
170.41*#
196.75*#
123*#
-74.72*#
-74.83*#
137.92*#
81.86*#
38.73
U-JumpLand
-15.65
-14.25
169.36*#
188.37*#
58.12*#
Walk
84.21*#
144.79*#
0.51
-19.70
#
-2.09
171.72*
-72.27*#
-71.21*#
-29.26
112.018*#
111.79*#
Walk
-63.58*#
Tandem
#
#
73.03*#
194.49*#
186.91*#
37.21
U-HR
2.83
4.18
120.86*#
-78.37*#
-65.45*#
U-JumpLand
-47.40*#
-46.72*#
-49.32#
102.28*#
112.26*# 132.28*#
-92.48*#
Walk
12.64
11.20
99.37*#
-32.12*#
22.34
178.56*# 196.65*# 184.04*#
194.17*# 195.67*# 190.45*#
135.34*# 150.92*#
132.46*#
76.43*#
143.99*#
107.29*#
-86.56*#
-85.93*#
71.17*#
194.38*#
89.76*#
U-HR
-112.46*# -158.75*#
-26.32*#
Walk
130.153*#
157.38*# 193.01*# 167.82*#
3.64
U-JumpLand
135.16*# 158.66*# 131.25*#
52.76*#
77.21#
Squat
96.42*#
95.59*#
-63.48#
188.32*#
-75.66*#
Tandem
12.46
12.17
8.67#
71.43#
16.99
176.72*# 196.35*# 182.65*#
187.89*# 190.97*# 180.35*#
125.56*# 143.10*#
Walk
-49.15*#
-51.96*#
-31.85
71.95*#
53.23*#
101.58*#
-77.45*#
-57.34#
-58.65*#
1.82
Tandem
UJumpLand
U-HR
-69.47*#
-69.37*#
U-JumpLand
109.97*#
110.34*#
Walk
-60.69*#
-63.12*#
Walk
59.15*#
57.17*#
#
134.55*# -64.15*# 163.91*# 173.16*#
-81.44*#
-65*#
-100.97*#
Tandem
-29.90*#
-78.99*#
188.57*#
*
U-JumpLand
137.15*#
-95.65#
137.40*#
-25.83*#
-58.44*#
Squat
192.33*# 114.05*# 196.73*# -53.52# 196.61*# 197.49*# 194.42*#
20.54
160.03*#
-58.27*#
62.24*#
86.21*#
173.33*#
-82.49*#
U-HR
60.85*#
72.42*#
194.0*#
4.15
U-JumpLand
7.02
-83.77*#
126.66*#
73.30*
U-HR
9.82
177.54*# 196.45*# 183.27*# 148.11*# -30.71
U-HR
-4.65
49.35*
194.41*
EP
-3.20
Tandem
U-HR
Run
83.94*#
TE D
Squat
Romberg
4.48#
UStanding
RI PT
22.87
FL
37.49*
6.44#
AT Force Impulse
Percentage Differences (%) 61.60*# 151.68*# 197.37*# # -82.79* -161.4*# 98.80*#
136.75*
Walk
Ankle ROM
62.61*# -81.93*#
68.98*
Run
B-HR
#
96.30*
U-JumpLand
Squat
#
AT Stress Rate
B-HR
U-HR
U-Standing
#
AC C
B-Jump-Land
Percentage Differences (%) #
AT Force
-15.18
ACCEPTED MANUSCRIPT
Table 3: Mean ± standard deviation for peak AT force impulse per step during running and walking, over 1 second for standing exercises, and per repetition during Squat, FL, B-HR, U-HR, and Jump-Lands.
Per Repetition 1.21±0.33 2.91±0.66
AT Force Impulse (BW*s) B-JumpU-JumpWalk Run Land Land Per Step 1.52±0.63 4.00±2.34 0.97±0.30 0.60±0.49
Romberg
Tandem
RI PT
U-HR
0.72±0.22
TE D
M AN U
SC
1.64±0.91
B-HR
EP
1.47±0.88
FL
AC C
Squat
In 1 sec 1.40±0.45
UStanding 1.66±0.28
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
HIGHLIGHTS: Bilateral and standing exercises resulted in less AT loading.
-
Ankle ROM did not demonstrate a similar order of magnitude as AT loading.
-
Progressive weight bearing exercises start with standing or balanced based exercises with
RI PT
-
minimum AT loading and ROM. -
Squats, BHR, and FL then Walking and UHR may be appropriate for the second and
EP
TE D
M AN U
Running and jumping may be recommended in the final phase of rehabilitation.
AC C
-
SC
third phases of rehabilitation.
ACCEPTED MANUSCRIPT
Ethical approval This study was approved by the Ethics Committee on the use of human subjects in research at the University of Wisconsin - La Crosse. All participants provided informed consent prior to
AC C
EP
TE D
M AN U
SC
RI PT
participation.