JCLB-03926; No of Pages 8 Clinical Biomechanics xxx (2015) xxx–xxx
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The structural and mechanical properties of the Achilles tendon 2 years after surgical repair Jeam Marcel Geremia a,b,⁎, Maarten Frank Bobbert c, Mayra Casa Nova a, Rafael Duvelius Ott d, Fernando de Aguiar Lemos a, Raquel de Oliveira Lupion a, Viviane Bortoluzzi Frasson e, Marco Aurélio Vaz a a
Exercise Research Laboratory, School of Physical Education, Federal University of Rio Grande do Sul, Porto Alegre, Brazil Faculty of Physical Education Sogipa, Porto Alegre, Brazil Faculty of Human Movement Sciences, Move Research Institute Amsterdam, VU University Amsterdam, Amsterdam, The Netherlands d São Lucas Hospital, Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil e Physique Physiotherapy Center, Porto Alegre, Brazil b c
a r t i c l e
i n f o
Article history: Received 10 December 2014 Received in revised form 3 March 2015 Accepted 4 March 2015 Keywords: Stress–strain relation Achilles tendon rupture Immobilization Tendon healing Ultrasound
a b s t r a c t Background: Acute ruptures of the Achilles tendon affect the tendon's structural and mechanical properties. The long-term effects of surgical repair on these properties remain unclear. Purpose: To evaluate effects of early mobilization versus traditional immobilization rehabilitation programs 2 years after surgical Achilles tendon repair, by comparing force-elongation and stress–strain relationships of the injured tendon to those of the uninjured tendon. Methods: A group of males with previous Achilles tendon rupture (n = 18) and a group of healthy male controls (n = 9) participated. Achilles tendon rupture group consisted of patients that had received early mobilization (n = 9) and patients that had received traditional immobilization with a plaster cast (n = 9). Comparisons of tendon structural and mechanical properties were made between Achilles tendon rupture and healthy control groups, and between the uninjured and injured sides of the two rehabilitation groups in Achilles tendon rupture group. Ultrasound was used to determine bilaterally tendon cross-sectional area, tendon resting length, and tendon elongation as a function of torque during maximal voluntary plantar flexion. From these data, Achilles tendon force-elongation and stress–strain relationships were determined. Findings: The Achilles tendon rupture group uninjured side was not different from healthy control group. Structural and mechanical parameters of the injured side were not different between the Achilles tendon rupture early mobilization and the immobilization groups. Compared to the uninjured side, the injured side showed a reduction in stress at maximal voluntary force, in Young's modulus and in stiffness. Interpretation: Two years post-surgical repair, the Achilles tendon mechanical properties had not returned to the uninjured contralateral tendon values. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction The incidence of Achilles tendon (AT) acute ruptures has risen mainly due to an increased participation in sports-related activities (Huttunen et al., 2014; Lantto et al., 2015). Open repair is one of various techniques used for the treatment of AT acute ruptures (Rosenzweig and Azar, 2009). This technique has been used successfully (Del Buono et al., 2014), provides good strength to the repaired tendon and low re-rupture rates (Del Buono et al., 2014; Inglis et al., 1976), and is usually followed by a traditional rehabilitation program. This program
⁎ Corresponding author at: Exercise Research Laboratory (LAPEX), Federal University of Rio Grande do Sul (UFRGS), Rua Felizardo, 750, Bairro Jardim Botânico, CEP: 90690-200, Porto Alegre, RS, Brazil. E-mail address: [email protected] (J.M. Geremia).
involves ankle immobilization with a plaster cast (PC) that is removed 6 weeks after surgery (Maffulli et al., 2003a). Tendons adapt to physical activity regimens (Barone et al., 2009; Fouré et al., 2013; Kubo et al., 2000, 2012). Immobilization causes a reduction of collagen synthesis and an increase in collagen degradation (Kangas, 2007). This reduces the size and number of collagen bundles as well as water and glycosaminoglycan content (Kannus et al., 1997). Furthermore, damaged and healed tendons contain a greater proportion of weaker type III collagen, while normal tendons are composed of type I collagen (characterized by a higher tensile strength) (Kannus et al., 1997). Thus, the immobilization and the healing process can affect the tendon mechanical properties as a whole (Kannus et al., 1997). Early mobilization has been proposed to accelerate tendon repair (Maffulli et al., 2003a,b). The best physical therapy program after AT repair should allow for early weight bearing and joint mobilization, and minimize the abovementioned deleterious effects to the tendon.
http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005 0268-0033/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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Nonetheless, evidence of functional recovery, together with structural and mechanical tendon properties from different rehabilitation programs, seems to be lacking in the current literature. Long-term studies evaluating the AT's structural and mechanical properties after surgical repair are also scarce. Studies have shown that, long after surgery, muscle strength is still reduced (Bressel and McNair, 2001; Maffulli et al., 2003a), tendon morphology has not returned to normal (Maffulli et al., 2001; Rosso et al., 2013), and the functional deficits persist (Olsson et al., 2011). Knowledge of these long-term effects is important because patients are released from rehabilitation to return to their normal activities 6 months post-surgery on average without a clear assessment of their tendon structural and mechanical properties. Evidence for restoration of the AT structural (cross-sectional area—CSA, tendon length—TL) and mechanical (stress, strain, stiffness, Young's modulus) properties in these patients are scarce (Bressel and McNair, 2001). Moreover, the lack of well-defined rehabilitation programs further emphasizes the clinical relevance of determining the exact effects of well-defined rehabilitation programs on these AT structural and mechanical properties, as well as these programs' effectiveness by way of their effects on these properties. The purpose of this study was to determine if early physical rehabilitation of surgically repaired Achilles tendon ruptures leads to different long-term (more than 2 years after surgical repair) structural and mechanical results than traditional post-surgical techniques. Specifically, we addressed the following questions: (1) Are the long-term effects of early mobilization different from those of a traditional rehabilitation program? (2) Are the force-elongation and stress–strain relationships of the injured tendon in patients 2 years after surgical repair different from those of the uninjured AT? Based on the literature (Kannus et al., 1997) we hypothesize that previously injured tendons display inferior structural and mechanical properties than uninjured tendons, which constitutes an increased risk for AT re-injury. 2. Materials 2.1. Subjects The study, conducted according to the provisions of the Declaration of Helsinki, was approved by the ethics and research committee of two Brazilian universities (Protocols 07/04008 and 13202). In order to show a between-rehabilitation groups difference, G* Power 3 software (Kiel University, Germany; effect size = 0.33; significance level = 0.05; required power = 0.80) estimated a sample size of 18 subjects (n = 9 per group). Eighteen patients, admitted to the University Hospital for a unilateral AT rupture (ATR) from June 2008 to July 2009, signed an informed consent form prior to participation in the study. An orthopedic surgeon, based on clinical examination (positive Thompson test), established the diagnosis of total acute ATR. Surgical repair occurred within 15 days after injury, and more than 2 years (29 (4.1 months)) prior to the study. In selecting subjects for the ATR group, we excluded patients who suffered from arterial insufficiency, diabetes, autoimmune disease, and patients who used systemic antibiotics or steroids or showed any other clinical contraindication to perform maximum voluntary contractions on a dynamometer. Nine of the ATR subjects completed a short-term physical therapy (STPT) program, starting 2 weeks after the surgery and lasting 6 weeks, during which a removable brace was used. As at the time of the study there were no well-defined rehabilitation programs available, we decided to aim only at range of motion (ROM) gain in order to avoid possible AT re-rupture. Therefore, therapy sessions, three times per week in the six-week period, included one to two hours of exercises for regaining ROM and muscular endurance (Table 1). The other nine ATR subjects, who were matched in age and anthropometric measurements to patients in the STPT group, completed a PC immobilization program. After surgery, they were immobilized with
the ankle in gravitational equinus; weight bearing was not allowed. Two weeks post-operatively, when the swelling was reduced, the cast was removed and the patient was immobilized in the same position with a new PC. Four weeks post-operatively, the ankle was plastered in neutral position (i.e., with the sole of the foot perpendicular to the shank), and weight bearing was encouraged. Six weeks postoperatively, the PC was removed and the patients received instructions on how to perform a home-exercise program, consisting of active exercises and stretches to improve ankle ROM, and resistance and balance exercises (Table 2). At the time of the study, more than 2 years after the surgery, all patients were fully functional and received no further treatment. Patients were allocated into groups based on practical considerations. Individuals who lived close to the university and could come to the laboratory on a daily basis were enrolled in the STPT program, whereas individuals who lived in other cities were enrolled into the PC group. Nine healthy subjects served as controls (CTR). Subjects in the CTR group had no history of lower limb injury and were matched in age and anthropometric measurements (height and body mass) to patients in both STPT and PC groups. 2.2. Experiment outline In the experimental session, the subjects' body mass, height, and leg length (defined as the distance between popliteal crease and the center of the lateral malleolus) were determined. Both legs were tested in the experimental session. Subjects were asked about the leg they used to kick a ball, which was considered the dominant leg; this way of establishing leg dominance was preferred over asking, for example, about handedness (Elias et al., 1998). After applying surface electromyography (EMG)-electrodes over m. tibialis anterior and several skin markers on the back of the leg, the subject was seated in a dynamometer (Biodex Medical Systems, New York, USA) with the knee fully extended (180°) (Karamanidis and Arampatzis, 2006) and the hip flexed at 85°. The ankle was kept in neutral position (tibia perpendicular to the sole, ankle angle 90°) (Karamanidis and Arampatzis, 2006), the plantar/ dorsiflexion axis was aligned with the axis of rotation of the dynamometer, and the foot was firmly fixed to the dynamometer's footplate to prevent the calcaneus from lifting off the footplate. Velcro straps stabilized the thigh and trunk. In this position, we measured (1) AT structural properties using ultrasound while the subject was relaxed, (2) AT elongation using ultrasound during isometric plantar flexion ramp contractions as a function of ankle joint torque, and (3) the relationship between tibialis anterior EMG and dorsiflexion torque, to be used for correction of the ankle torque for an antagonistic dorsiflexion torque of this muscle during the plantar flexion ramp contractions. All ultrasound data were collected using a linear probe (60 mm, 7.5 MHz—Aloka, Tokyo, Japan) connected to an ultrasound system (SSD 4000, 51Hz,Aloka Inc., Japan), and the images were recorded by an external DVD unit (R130/XAZ, 32Hz, Inc. Samsung Seoul, South Korea). A small bag containing conductive gel was used as interface between the probe and the skin for better visualization. From the data collected, we calculated the relationship between AT elongation and AT force, as well as AT Young's modulus. Details of each of these measurements and calculations are provided below. Six subjects (ATR group, n = 3; and CTR group, n = 3) were measured twice on two separate days to determine test–retest reliability of measures used. The timeline and content of the experimental session are shown in Fig. 1. 2.3. AT structural properties The AT structural properties, i.e., CSA and TL, were determined while the subject was sitting relaxed. To obtain CSA, the ultrasound probe was placed perpendicular to the tendon and three transverse images were obtained at 2 cm, 4 cm, and 6 cm from the tendon's insertion on the
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
J.M. Geremia et al. / Clinical Biomechanics xxx (2015) xxx–xxx
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Table 1 Short-term physical therapy (STPT) program. Week Exercise description
Mode Series Reps or Load Duration
1–4 5–6 1–4 3–4 5–6 5–6 1–3 4 4 5–6
Hip ab-adduction, hip flexion (SP). Contralateral hip was maintained flexed. Hip ab-adduction, hip flexion (SP). Contralateral hip maintained flexed. Metatarsal-phalangeal and interphalangeal joints flexion and extension (SP). Stretching exercise for the dorsal and plantar flexors (SP). Stretching exercise for the dorsal and plantar flexors (SP). Plantar flexor muscles stretching. Inversion–eversion, ankle plantar flexion–dorsiflexion exercises, the knee extended (SP). Inversion–eversion, ankle plantar flexion–dorsiflexion exercises, knee flexed over a pillow (SP). Resistance exercises with elastic band: eversion, inversion, plantar flexion and dorsiflexion (SP). Resistance exercises with elastic band: eversion, inversion, plantar flexion and dorsiflexion (SP).
A A P/A P P P P/A P/A A A
1 2 3 4 5–6 3 4 5–6 5
Gait training with partial support (three-point gait). Gait training with partial support (two-point gait) Gait training with full support—with crutches. Gait training with full support—no crutches. Full support gait—no orthosis. Knee flexion exercise in orthostasis. Knee flexion exercise in orthostasis. Knee flexion exercise in orthostasis. Proprioceptive training: weight transfer latero-lateral, anterior–posterior and posterior–anterior to postural imbalances. Proprioceptive training: mini trampoline balance in a single side, first static, followed by over ball. Unipodal support training: patient raises the weight on the operated side. Stair climbing training: step by step, place first the healthy and then the operated side. Stair descent training: step by step, place first the operated and then the healthy side. Bipedal squat exercise: holding with both hands onto the cross-bar, perform squats, never exceeding the toe line. Bipedal heel rise: up and down on the feet. Cryotherapy with compression and ankle elevation (SP).
A A A A A A A A A
6 5 5 5 6 6 1–6
A A A A A A
2–3 3 2–3 3 5 3 2–3 2–3 2 2
15–20 20 15–20 20 s 20 s 20 s 15–20 15–20 15 15
1 kg @ 4th week 2–3 kg
2 3 3
15 15 20
2 2
10 10 20 min
5% body weight 10–20% body weight
1 kg 2–3 kg
A = active. P = passive. Reps = repetitions. SP = supine position.
calcaneus (Arya and Kulig, 2010). CSA was defined as the average of these three measurements. TL was defined as the distance between the insertion on the calcaneus and the myotendinous junction obtained with the muscle at rest and the ankle joint in neutral position (Arya and Kulig, 2010). TL was obtained using a modified overlapping images method (Urlando and Hawkins, 2007), for which skin markers were placed at 5 cm intervals starting at the calcaneus and moving in longitudinal direction up the leg to the myotendinous junction of the medial head of gastrocnemius. The marker spacing was such that in any image two adjacent landmarks were visible: in the first image the AT insertion and the first marker, in the second image the first and the second markers, and so on, and in the last image the last marker and myotendinous junction. The ultrasound images were superimposed and aligned with help of the markers using the GIMP program (GIMP 2.6.11, GNU Image Manipulation Program). The ImageJ program (National Institutes of Health, Bethesda, Maryland, USA. http://imagej.nih. gov/ij/) was used to measure the CSA and TL.
2.4. AT elongation as a function of ankle joint torque during plantar flexion contractions After the determination of CSA and TL, the probe was supported by a custom-made cast, positioned at the myotendinous junction of the gastrocnemius medial head, and secured to the leg by bandages (Arya and Kulig, 2010). A skin marker was placed between the probe and the skin; if the probe was displaced relative to the marker during a contraction, that contraction was repeated. After performing three plantar flexion ramp maximal voluntary isometric contractions (MVCs) for familiarization and to preconditioning the muscle-tendon complex (Magnusson et al., 2001), the subject performed two plantar flexion ramp MVCs, lasting 10 s each (Magnusson et al., 2001), during which torque, EMG, and ultrasound data were collected. From these two contractions, the highest peak torque was taken as the maximum torque that subjects could produce, as well as the corresponding level of tibialis anterior EMG and tendon elongation (see below). A timing system (HORITA
Table 2 Home exercises program performed in the plaster cast (PC) group after 6 weeks of immobilization. Week Exercise description 1–3 1–3 1–3 4 5 6 4–6 4–6
Sitting on the floor with your legs extended. Ankle movements for heel up and down. Standing, holding a chair and distributing your weight equally in your legs. Climb up and down on your toes. Standing, holding on to a chair, support your body only in the operated side. Climb up and down on tiptoes. Standing, holding a table (or a chair), perform knee flexion and extension with both legs. Standing, holding a table (or a chair), perform knee flexion and extension with both legs. Start exercise performing 3 sets of 10 repetitions and progress to 3 sets of 30 repetitions. Standing, holding a table (or a chair), perform knee flexion and extension with both legs. Start exercise performing 3 sets of 10 repetitions and progress to 3 sets of 30 repetitions. Standing, try to maintain your body supported on the operated side and perform knee flexion and extension. Standing, healthy side positioned forward with knee flexed, the operated side with knee extended and ankle maximally dorsiflexed while elongating calf muscles.
Mode Series Reps or duration A A
3 3
20 20
A A A
3 3 3
20 10 10–30
A
3
10–30
A P
3 5
20 20 s
A = active. P = passive. Reps = repetitions.
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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J.M. Geremia et al. / Clinical Biomechanics xxx (2015) xxx–xxx
Fig. 1. Timeline and content of the experimental session and measurements. CSA = cross-sectional area. TL = tendon length. MVC = maximal voluntary contraction. EMG = electromyography.
Video Stop Watch VS-50; HORITA Company Inc., USA) was utilized to synchronize ultrasound images to the torque and EMG signals. The movement of myotendinous junction was taken to represent AT elongation.
2.5. Relationship between tibialis anterior EMG and dorsiflexion torque The torque recorded by the dynamometer is the net ankle joint torque, which is not equal to the torque produced by the plantar flexors if the antagonistic tibialis anterior is active as well. For this reason, we corrected for the dorsiflexion torque of tibialis anterior using a relationship between tibialis anterior EMG and dorsiflexion torque. To measure the EMG, bipolar electrodes (Ag/AgCl, Meditrace, Kendall, Canada) were placed at the proximal third of the muscle according to the recommendations of SENIAM (http://www.seniam.org/). The EMG signals were amplified (AMT-8, Bortec Biomedical Ltd., Canada) and digitized at 2000 Hz simultaneously with the torque signal of the dynamometer (Windaq data collection system, DATAQ Instruments, Akron, OH, USA, 16-bit). To establish a relationship between tibialis anterior EMG and dorsiflexion torque, three extra measurements were taken (Mademli and Arampatzis, 2005): (a) while the subject was relaxed, and while the subject produced a dorsiflexion torque that resulted in an EMG amplitude that was (b) smaller and (c) higher than the value measured when the subject produced the ramped plantar flexion MVC. The EMG signals obtained during these three conditions were filtered using a 10- to 500-Hz band-pass filter, root mean square (RMS) values were calculated, and a linear relationship was fitted between the RMSvalues and the corresponding dorsiflexion torque. With the help of this relationship we estimated the dorsiflexion torque of tibialis anterior during the plantar flexion contractions on the basis of EMG, and corrected the net ankle joint torque to achieve the true plantar flexion torque.
2.6. Calculation of AT force, elongation, stiffness, strain, and Young's modulus AT force during the ramp plantar flexion contraction was calculated by dividing the total ankle plantar flexor torque, after correction for the tibialis anterior torque, by AT moment arm. Following previous studies (Kubo et al., 2005; Muraoka et al., 2005), the moment arm was taken to be 11% of leg length. To determine AT elongation, the images monitoring the location of the gastrocnemius myotendinous junction were translated from DVD format into AVI format by BitRipper software (Binotex, USA). Using the Virtual Dub software (Avery Lee, USA), the AVI file was screened frame by frame in order to select the desired images. The myotendinous junction displacement was tracked using the ImageJ software. AT force and elongation were extracted at 0%, 20%, 40%, 60%, 80%, and 100% of maximal AT force (Arya and Kulig, 2010). The slope of the AT force-
elongation curve between 60% and 80% of the maximum AT force was taken to represent AT stiffness. To obtain the stress, AT force was divided by CSA, and to obtain the strain, AT elongation during the plantar flexion ramp MVC was divided by TL. Stress and strain values were also obtained at 0%, 20%, 40%, 60%, 80%, and 100% of the maximal AT force (Arya and Kulig, 2010), and the slope of the stress–strain curve between 60% and 80% of the maximum stress was taken to represent Young's modulus. 2.7. Statistical analysis Test–retest reliability of CSA, TL, and AT elongation of the six subjects who were tested twice was calculated using a two-way random effects intra-class correlation coefficient model. A two-way ANOVA for repeated measures was utilized to test for differences between the PC and STPT groups. The factors were groups (PC and STPT) and sides (uninjured and injured). Age, height, and body mass were compared between CTR and ATR groups using a Student t-test for independent samples. The tendon structural and mechanical properties were compared between CTR and ATR groups using a two-way ANOVA. The factors were groups (CTR and ATR) and sides (dominant, non-dominant, uninjured, and injured). When significant groups × side effects were found, separate statistical analyses were performed. First, the dominant and non-dominant sides in the CTR group were compared to each other and to the uninjured side in the ATR group by means of a one-way ANOVA. Subsequently, the uninjured and injured sides of the ATR were compared using a Student t-test for independent samples (parametric data) or a Mann–Whitney U test (non-parametric data). Data were tested for normality using the Shapiro–Wilk test. All tests were performed using SPSS 17.0, at a level of significance of α ≤ 0.05. 3. Results Groups were similar for age [CTR = 44.4 (3.4 years); ATR = 45.3 (2.0 years); p = 0.812)], height [(CTR = 175.3 (1.2 cm); ATR = 173.4 (1.1 cm); p = 0.274)] and body mass [(CTR = 80.0 (4.2 kg); ATR = 84.3 (1.9 kg); p = 0.301)]. The intra-class correlation coefficients were 0.99 (p b 0.001) for the TL, 0.99 (p b 0.001) for the CSA, and 0.98 (p b 0.001) for the tendon elongation. It seems safe to say, therefore, that the measurements were reliable. Both groups (STPT and PC) showed a similar between-sides behavior, with smaller values on the injured side compared to the uninjured side for force (effect size = 0.823), stiffness (effect size = 0.578) (Fig. 2A), stress (effect size = 0.946) and Young's modulus (effect size = 0.857) (Fig. 2B), and larger values for CSA (effect size = 0.904). However, no between-group difference was found in any of the variables (Table 3), and therefore the two patient groups were combined into one ATR group. The CTR group was included in the study in order to assess possible changes in the uninjured side of the ATR group. There was no difference
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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force and stiffness were 21% (effect size = 1.379) and 20% (effect size = 1.081) (respectively) lower on the injured side than on the uninjured side. However, the corresponding tendon elongation was not different (Table 4). There was no difference in TL between the injured and uninjured sides. CSA on the injured side was 113% higher than on the uninjured side (effect size = −3.536). Fig. 3(B) shows the stress–strain relationship of the dominant and non-dominant sides of the CTR group and of the injured and uninjured sides of the ATR group. There was no difference in strain at maximum isometric force. Maximal stress and Young's modulus were lower by 60% (effect size = 3.457) and 58% (effect size = 2.321), respectively, in the injured compared to the uninjured side, with no difference between the CTR group sides and the uninjured side of the ATR group. 4. Discussion
Fig. 2. Achilles tendon force-elongation (A) and stress–strain (B) relationships in the plaster cast (PC) and short-term physical therapy (STPT) groups. Vertical and horizontal error bars are SE of the force and elongation data, respectively.
in any of the structural or mechanical properties between the sides of the CTR group and the uninjured side of the ATR group (Table 4), indicating that the changes in activity level following the injury and during the rehabilitation period had no long-term effect on the AT properties on the uninjured side. The force-elongation (Fig. 3A) and stress–strain (Fig. 3B) relationships of the injured AT differed from those of the uninjured AT. Maximal
The purpose of the study was to determine if early physical rehabilitation of surgically repaired Achilles tendon ruptures leads to different long-term structural and mechanical results than traditional postsurgical techniques. No difference was found in any of the variables between the patients who underwent the STPT program and patients subjected to PC immobilization, suggesting that the type of rehabilitation made no long-term (more than 24 month post-operative) difference. Considering that many surgeons do not favor an early rehabilitation program for fear of possible AT complications (e.g., re-rupture), the results of this study are reassuring: our early rehabilitation program (Table 1) is safe as no re-rupture was observed in our STPT group. In addition, our STPT program allowed for early weight bearing and permitted patients to remove the orthosis; this allowed them to move the ankle and the foot of the injured limb and perform their daily life activities, which improved comfort during the rehabilitation period. Previous studies (Kannus et al., 1997; McNair et al., 2013) have shown that the mechanical properties of ruptured tendons are affected; they are more compliant than healthy tendons. Early weight bearing has been suggested as a way to prevent tendons from becoming compliant and preserve ankle functionality. However, McNair et al. (2013) compared the isokinetic plantar flexor torque (240°/s) and tendon stiffness between two groups of subjects that followed either a weight bearing or a non-weight bearing rehabilitation protocol after AT surgical repair. The authors found no between-group differences in torque production and in tendon stiffness 6 months post-surgery. Affected sides presented smaller isokinetic torques and tendon stiffness (20% and 20–40% deficit, respectively) than the contralateral uninjured side. According to the authors, the decrease in tendon stiffness was associated with the decrease in plantar flexor muscles force. In our study, both groups presented a reduction in plantar flexor force, which appears to have contributed to the observed reduction in tendon stiffness. McNair et al. (2013) also suggest
Table 3 Achilles tendon structural and mechanical properties of the uninjured (U) and injured (I) sides in the plaster cast (PC) and short-term physical therapy (STPT) groups [mean (standard deviation)].
Structural Properties Tendon length (mm) CSA (mm2) Mechanical properties Force (N) Elongation (mm) Stiffness (N/mm) Stress (MPa) Strain (%) Young's modulus (MPa)
PC (U) (n = 9)
PC (I) (n = 9)
STPT (U) (n = 9)
STPT (I) (n = 9)
Group effect, p value
Side effect, p value
Group vs. side, p value
240.33 (12.69) 63.49 (11.75)
243.23 (13.18) 138.22 (20.59)⁎
236.87 (6.06) 61.67 (2.37)
243.51 (18.01) 128.09 (32.64)⁎
0.787 0.395
0.079 b0.001
0.730 0.275
2884.07 (349.36) 14.75 (3.97) 231.53 (51.85) 47.38 (11.38) 5.92 (1.68) 994.24 (358.23)
2342.24 (484.48)⁎ 14.29 (3.45) 200.39 (30.70)⁎ 17.38 (3.11)⁎ 5.68 (1.56) 403.32 (88.81)⁎
3293.87 (626.56) 16.34 (4.00) 227.69 (49.93) 53.85 (10.69) 6.86 (1.56) 848.85 (260.57)
2555.51 (214.72)⁎ 15.37 (4.18) 165.58 (32.89)⁎ 22.77 (6.19)⁎ 6.45 (2.11) 369.74 (95.63)⁎
0.089 0.469 0.165 0.123 0.326 0.306
b0.001 0.630 0.011 b0.001 0.622 b0.001
0.468 0.800 0.369 0.844 0.838 0.374
CSA = cross-sectional area. ⁎ Difference between injured and uninjured sides within groups.
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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J.M. Geremia et al. / Clinical Biomechanics xxx (2015) xxx–xxx
Table 4 Achilles tendon structural and mechanical properties of the dominant (D) and non-dominant (Non-D) sides in the control group (CTR), uninjured (UN), and injured (IN) sides in the Achilles tendon rupture group (ATR) [mean (standard deviation)].
Structural Properties Tendon length (mm) CSA (mm2) Mechanical properties Force (N) Elongation (mm) Stiffness (N/mm) Stress (MPa) Strain (%) Young's modulus (MPa)
CTR (D) (n = 9)
CTR (Non-D) (n = 9)
ATR (UN) (n = 18)
ATR (IN) (n = 18)
Two-Way ANOVA CTR vs. ATR p value
One-Way ANOVA D vs. Non-D vs. UN p value
Specific test UN vs. IN p value
235.05 (6.49) 58.73 (6.86)
235.19 (15.70) 61.62 (8.80)
238.60 (9.72) 62.58 (8.28)
243.37 (14.71) 133.16 (26.98)⁎
0.267 n.a.
n.a. 0.512
n.a. b0.001
3117.84 (604.58) 15.21 (2.58) 210.73 (49.40) 53.54 (10.58) 6.58 (1.04) 885.18 (214.31)
3060.86 (380.12) 16.11 (4.84) 220.41 (38.01) 50.05 (6.34) 6.86 (1.92) 762.23 (169.59)
3088.97 (535.38) 15.54 (3.95) 229.61 (49.42) 50.62 (11.22) 6.39 (1.64) 921.55 (312.95)
2448.88 (379.73)⁎ 14.83 (3.76) 182.99 (35.69)⁎ 20.08 (5.50)⁎ 6.07 (1.84) 386.53 (91.18)⁎
n.a. 0.674 n.a. n.a. 0.865 n.a.
0.973 n.a. 0.612 0.720 n.a 0.337
0.001 n.a. 0.03 b0.001 n.a. b0.001
CSA = cross-sectional area. Specific test = t-test or Mann–Whitney U test. n.a., not applicable. ⁎ Difference between UN and IN sides.
that strength-training programs focused on muscle hypertrophy would be valuable to improve tendon stiffness. However, as our rehabilitation programs (STPT, PC) focused on ROM gain rather than on muscle strengthening exercises, apparently they did not promote sufficient overload in the healing tendons of both groups to produce the desired long-term AT structural and mechanical adaptations for complete recovery.
Fig. 3. Achilles tendon force-elongation (A) and stress–strain (B) relationships in the control (CTR) and Achilles tendon rupture (ATR) groups. Vertical and horizontal error bars are SE of the stress and strain data, respectively.
The results of this study show that approximately 2 years and 6 months after surgical repair the AT material properties had still not fully recovered. Maffulli et al. (2003a) evaluated the isometric plantar flexor strength in patients with a complete AT rupture that were subjected to different rehabilitation protocols (immobilization and accelerated). Twenty-one months after surgical repair, these authors found a significant muscle strength deficit in the injured side of both groups compared to the uninjured side. Maffulli et al. (2003b) and Bressel and McNair (2001) emphasize that the observed reduction in force production might be associated with the different lifestyle adopted by the subjects after the injury, as some of them apparently avoided systematic physical activity fearing new ruptures or complications. Although we did not evaluate the subjects' lifestyle in our study, our results show a lack of recovery in the structural and functional properties of the plantar flexor group in the injured side, which has important clinical implications. The CTR group was included in the study in order to assess possible changes in the uninjured side of the ATR group. Overall, the uninjured side of the ATR group appeared similar to the dominant and nondominant sides of the CTR group; any changes in activity level that might have occurred after the injury on the injured side had no longterm effects on the uninjured tendon. This suggests that lifestyle did not change, that the changes in AT properties of the injured limb were directly related to the injury itself, and that the changes in properties on the injured side have something to do with structural changes in the tendon. The second question that we addressed was whether the forceelongation and the stress–strain relationships of the injured tendon differed from those of the uninjured tendon. Tendon elongation and tendon strain at MVC were similar at the injured and uninjured sides in the ATR group. However, similar elongation and strain were reached at lower tendon force and tendon stress on the injured side than on the uninjured side, evidencing that injured tendons are more compliant than uninjured tendons. The fact that both stiffness and Young's modulus were smaller on the injured side than on the uninjured side further supports the idea that tendon material is more compliant on the injured side, in contrast to previous findings that did not take into consideration the AT structural parameters to determine these mechanical properties (Bressel and McNair, 2001). The greater tendon compliance on the injured side, which may come with a higher risk of tendon re-rupture, seems to be in line with histological findings reported in the literature. It has been shown that the main content of uninjured tendons is type I collagen, while repaired tendons contain a greater proportion of type III collagen (Maffulli et al., 2000). Type I collagen is characterized by a higher tensile strength (Maffulli and Almekinders, 2007), which promotes the ability
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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to support larger loads, while type III collagen has a lower tensile strength. Kannus et al. (1997) reported that injured tendons might not reach an optimum orientation of collagen fibers, at least not during short-term rehabilitation protocols. It is unclear what happens in the long-term, due to the lack of literature on well-defined long-term rehabilitation protocols aimed at promoting favorable structural and mechanical changes during tendon healing. We also think that new insights are necessary in the field of tendon rehabilitation to optimize the return to a healthy condition. There are two aspects to this: (1) we want the best outcome possible in terms of tendinous tissue itself, and (2) we want to reach this best outcome as quickly as possible by optimization of the rehabilitation program. The ideal protocol assures early return to function, patient comfort, and return of tendon structure and mechanical properties to normal values. The STPT program used here seems suitable to achieve the first and second goals, but not the third. When tendon force is normalized by CSA, large differences are found between injured and uninjured sides in the ATR group (Fig. 3B). Tendon thickening after AT surgical repair is a common finding. Our results showed that CSA was 113% larger on the injured side than on the uninjured side. Changes in tendon thickness seem to be present several months post-surgical repair, and our results agree with those of other studies (Maffulli et al., 2003a; Möller et al., 2002), indicating that the healed tendon is structurally different. Our methods to obtain the force-elongation and stress–strain curves of the AT have some limitations. According to previous studies, the moment arm does not remain constant during MVCs (Maganaris et al., 1998), and rotations in the joints can occur (Magnusson et al., 2001). Nevertheless, our values were similar to values obtained in studies in which error-reduction techniques were used (Arya and Kulig, 2010; Kubo et al., 2012; Magnusson et al., 2001; Stenroth et al., 2012; Waugh et al., 2012). The non-invasive method for assessing the mechanical properties of human tendon by real-time ultrasound scanning has often been used and the results obtained vary greatly (Maganaris et al., 2008). According to Maganaris et al. (2008), this variation is probably caused by inter-study methodological differences, which demonstrates the importance of a careful comparison of different studies. Interestingly, we did not find the characteristic toe region in the forceelongation and stress–strain curves. According to Maffulli and Almekinders (2007), this region is associated with forces that reduce the resting crimp angle of collagen fibers without causing further fiber stretching. The seated position we adopted with full knee extension can generate initial forces on the AT (Stenroth et al., 2012), which could have pre-stretched the collagen fibers. Evaluators were not blinded to the patients' allocation into the groups. Although few studies (Möller et al., 2002; Rosso et al., 2013) had their evaluators blinded to the patients' allocation into the groups, this is a limitation that can influence the study's internal validity. However, we do not believe that this limitation influenced the clinical relevance of our study. Most studies in the field fail to clearly describe the rehabilitation program used and do not report the mechanical properties of the sutured AT post-surgery. By showing that these properties are still different from a normal or a healthy tendon even more than 2 years after surgery, our study contributes to the existing knowledge in the area of tendon structural and mechanical properties. 5. Conclusion Early physical rehabilitation did not lead to long-term AT structural and mechanical differences when compared to traditional postsurgical techniques. However, more than 2 years after surgical repair the previously injured tendons are still structurally and mechanically different from healthy tendons. Our early rehabilitation protocol did not lead to deleterious effects on the sutured tendons and can be safely used for post-surgery treatment. Finally, further study is necessary to design long-term rehabilitation protocols that make injured tendons return to a healthy condition.
7
Acknowledgments The authors would like to acknowledge Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Programa Ciências Sem Fronteiras (CSF) e Financiadora de Estudos e Projetos (FINEP) from Brazil for financial support, and Valdirene Gambarra da Silva for technical help during patient recruitment.
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Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
The structural and mechanical properties of the Achilles tendon 2 years after surgical repair Jeam Marcel Geremia a,b,⁎, Maarten Frank Bobbert c, Mayra Casa Nova a, Rafael Duvelius Ott d, Fernando de Aguiar Lemos a, Raquel de Oliveira Lupion a, Viviane Bortoluzzi Frasson e, Marco Aurélio Vaz a a
Exercise Research Laboratory, School of Physical Education, Federal University of Rio Grande do Sul, Porto Alegre, Brazil Faculty of Physical Education Sogipa, Porto Alegre, Brazil Faculty of Human Movement Sciences, Move Research Institute Amsterdam, VU University Amsterdam, Amsterdam, The Netherlands d São Lucas Hospital, Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil e Physique Physiotherapy Center, Porto Alegre, Brazil b c
a r t i c l e
i n f o
Article history: Received 10 December 2014 Received in revised form 3 March 2015 Accepted 4 March 2015 Keywords: Stress–strain relation Achilles tendon rupture Immobilization Tendon healing Ultrasound
a b s t r a c t Background: Acute ruptures of the Achilles tendon affect the tendon's structural and mechanical properties. The long-term effects of surgical repair on these properties remain unclear. Purpose: To evaluate effects of early mobilization versus traditional immobilization rehabilitation programs 2 years after surgical Achilles tendon repair, by comparing force-elongation and stress–strain relationships of the injured tendon to those of the uninjured tendon. Methods: A group of males with previous Achilles tendon rupture (n = 18) and a group of healthy male controls (n = 9) participated. Achilles tendon rupture group consisted of patients that had received early mobilization (n = 9) and patients that had received traditional immobilization with a plaster cast (n = 9). Comparisons of tendon structural and mechanical properties were made between Achilles tendon rupture and healthy control groups, and between the uninjured and injured sides of the two rehabilitation groups in Achilles tendon rupture group. Ultrasound was used to determine bilaterally tendon cross-sectional area, tendon resting length, and tendon elongation as a function of torque during maximal voluntary plantar flexion. From these data, Achilles tendon force-elongation and stress–strain relationships were determined. Findings: The Achilles tendon rupture group uninjured side was not different from healthy control group. Structural and mechanical parameters of the injured side were not different between the Achilles tendon rupture early mobilization and the immobilization groups. Compared to the uninjured side, the injured side showed a reduction in stress at maximal voluntary force, in Young's modulus and in stiffness. Interpretation: Two years post-surgical repair, the Achilles tendon mechanical properties had not returned to the uninjured contralateral tendon values. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction The incidence of Achilles tendon (AT) acute ruptures has risen mainly due to an increased participation in sports-related activities (Huttunen et al., 2014; Lantto et al., 2015). Open repair is one of various techniques used for the treatment of AT acute ruptures (Rosenzweig and Azar, 2009). This technique has been used successfully (Del Buono et al., 2014), provides good strength to the repaired tendon and low re-rupture rates (Del Buono et al., 2014; Inglis et al., 1976), and is usually followed by a traditional rehabilitation program. This program
⁎ Corresponding author at: Exercise Research Laboratory (LAPEX), Federal University of Rio Grande do Sul (UFRGS), Rua Felizardo, 750, Bairro Jardim Botânico, CEP: 90690-200, Porto Alegre, RS, Brazil. E-mail address: [email protected] (J.M. Geremia).
involves ankle immobilization with a plaster cast (PC) that is removed 6 weeks after surgery (Maffulli et al., 2003a). Tendons adapt to physical activity regimens (Barone et al., 2009; Fouré et al., 2013; Kubo et al., 2000, 2012). Immobilization causes a reduction of collagen synthesis and an increase in collagen degradation (Kangas, 2007). This reduces the size and number of collagen bundles as well as water and glycosaminoglycan content (Kannus et al., 1997). Furthermore, damaged and healed tendons contain a greater proportion of weaker type III collagen, while normal tendons are composed of type I collagen (characterized by a higher tensile strength) (Kannus et al., 1997). Thus, the immobilization and the healing process can affect the tendon mechanical properties as a whole (Kannus et al., 1997). Early mobilization has been proposed to accelerate tendon repair (Maffulli et al., 2003a,b). The best physical therapy program after AT repair should allow for early weight bearing and joint mobilization, and minimize the abovementioned deleterious effects to the tendon.
http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005 0268-0033/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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Nonetheless, evidence of functional recovery, together with structural and mechanical tendon properties from different rehabilitation programs, seems to be lacking in the current literature. Long-term studies evaluating the AT's structural and mechanical properties after surgical repair are also scarce. Studies have shown that, long after surgery, muscle strength is still reduced (Bressel and McNair, 2001; Maffulli et al., 2003a), tendon morphology has not returned to normal (Maffulli et al., 2001; Rosso et al., 2013), and the functional deficits persist (Olsson et al., 2011). Knowledge of these long-term effects is important because patients are released from rehabilitation to return to their normal activities 6 months post-surgery on average without a clear assessment of their tendon structural and mechanical properties. Evidence for restoration of the AT structural (cross-sectional area—CSA, tendon length—TL) and mechanical (stress, strain, stiffness, Young's modulus) properties in these patients are scarce (Bressel and McNair, 2001). Moreover, the lack of well-defined rehabilitation programs further emphasizes the clinical relevance of determining the exact effects of well-defined rehabilitation programs on these AT structural and mechanical properties, as well as these programs' effectiveness by way of their effects on these properties. The purpose of this study was to determine if early physical rehabilitation of surgically repaired Achilles tendon ruptures leads to different long-term (more than 2 years after surgical repair) structural and mechanical results than traditional post-surgical techniques. Specifically, we addressed the following questions: (1) Are the long-term effects of early mobilization different from those of a traditional rehabilitation program? (2) Are the force-elongation and stress–strain relationships of the injured tendon in patients 2 years after surgical repair different from those of the uninjured AT? Based on the literature (Kannus et al., 1997) we hypothesize that previously injured tendons display inferior structural and mechanical properties than uninjured tendons, which constitutes an increased risk for AT re-injury. 2. Materials 2.1. Subjects The study, conducted according to the provisions of the Declaration of Helsinki, was approved by the ethics and research committee of two Brazilian universities (Protocols 07/04008 and 13202). In order to show a between-rehabilitation groups difference, G* Power 3 software (Kiel University, Germany; effect size = 0.33; significance level = 0.05; required power = 0.80) estimated a sample size of 18 subjects (n = 9 per group). Eighteen patients, admitted to the University Hospital for a unilateral AT rupture (ATR) from June 2008 to July 2009, signed an informed consent form prior to participation in the study. An orthopedic surgeon, based on clinical examination (positive Thompson test), established the diagnosis of total acute ATR. Surgical repair occurred within 15 days after injury, and more than 2 years (29 (4.1 months)) prior to the study. In selecting subjects for the ATR group, we excluded patients who suffered from arterial insufficiency, diabetes, autoimmune disease, and patients who used systemic antibiotics or steroids or showed any other clinical contraindication to perform maximum voluntary contractions on a dynamometer. Nine of the ATR subjects completed a short-term physical therapy (STPT) program, starting 2 weeks after the surgery and lasting 6 weeks, during which a removable brace was used. As at the time of the study there were no well-defined rehabilitation programs available, we decided to aim only at range of motion (ROM) gain in order to avoid possible AT re-rupture. Therefore, therapy sessions, three times per week in the six-week period, included one to two hours of exercises for regaining ROM and muscular endurance (Table 1). The other nine ATR subjects, who were matched in age and anthropometric measurements to patients in the STPT group, completed a PC immobilization program. After surgery, they were immobilized with
the ankle in gravitational equinus; weight bearing was not allowed. Two weeks post-operatively, when the swelling was reduced, the cast was removed and the patient was immobilized in the same position with a new PC. Four weeks post-operatively, the ankle was plastered in neutral position (i.e., with the sole of the foot perpendicular to the shank), and weight bearing was encouraged. Six weeks postoperatively, the PC was removed and the patients received instructions on how to perform a home-exercise program, consisting of active exercises and stretches to improve ankle ROM, and resistance and balance exercises (Table 2). At the time of the study, more than 2 years after the surgery, all patients were fully functional and received no further treatment. Patients were allocated into groups based on practical considerations. Individuals who lived close to the university and could come to the laboratory on a daily basis were enrolled in the STPT program, whereas individuals who lived in other cities were enrolled into the PC group. Nine healthy subjects served as controls (CTR). Subjects in the CTR group had no history of lower limb injury and were matched in age and anthropometric measurements (height and body mass) to patients in both STPT and PC groups. 2.2. Experiment outline In the experimental session, the subjects' body mass, height, and leg length (defined as the distance between popliteal crease and the center of the lateral malleolus) were determined. Both legs were tested in the experimental session. Subjects were asked about the leg they used to kick a ball, which was considered the dominant leg; this way of establishing leg dominance was preferred over asking, for example, about handedness (Elias et al., 1998). After applying surface electromyography (EMG)-electrodes over m. tibialis anterior and several skin markers on the back of the leg, the subject was seated in a dynamometer (Biodex Medical Systems, New York, USA) with the knee fully extended (180°) (Karamanidis and Arampatzis, 2006) and the hip flexed at 85°. The ankle was kept in neutral position (tibia perpendicular to the sole, ankle angle 90°) (Karamanidis and Arampatzis, 2006), the plantar/ dorsiflexion axis was aligned with the axis of rotation of the dynamometer, and the foot was firmly fixed to the dynamometer's footplate to prevent the calcaneus from lifting off the footplate. Velcro straps stabilized the thigh and trunk. In this position, we measured (1) AT structural properties using ultrasound while the subject was relaxed, (2) AT elongation using ultrasound during isometric plantar flexion ramp contractions as a function of ankle joint torque, and (3) the relationship between tibialis anterior EMG and dorsiflexion torque, to be used for correction of the ankle torque for an antagonistic dorsiflexion torque of this muscle during the plantar flexion ramp contractions. All ultrasound data were collected using a linear probe (60 mm, 7.5 MHz—Aloka, Tokyo, Japan) connected to an ultrasound system (SSD 4000, 51Hz,Aloka Inc., Japan), and the images were recorded by an external DVD unit (R130/XAZ, 32Hz, Inc. Samsung Seoul, South Korea). A small bag containing conductive gel was used as interface between the probe and the skin for better visualization. From the data collected, we calculated the relationship between AT elongation and AT force, as well as AT Young's modulus. Details of each of these measurements and calculations are provided below. Six subjects (ATR group, n = 3; and CTR group, n = 3) were measured twice on two separate days to determine test–retest reliability of measures used. The timeline and content of the experimental session are shown in Fig. 1. 2.3. AT structural properties The AT structural properties, i.e., CSA and TL, were determined while the subject was sitting relaxed. To obtain CSA, the ultrasound probe was placed perpendicular to the tendon and three transverse images were obtained at 2 cm, 4 cm, and 6 cm from the tendon's insertion on the
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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Table 1 Short-term physical therapy (STPT) program. Week Exercise description
Mode Series Reps or Load Duration
1–4 5–6 1–4 3–4 5–6 5–6 1–3 4 4 5–6
Hip ab-adduction, hip flexion (SP). Contralateral hip was maintained flexed. Hip ab-adduction, hip flexion (SP). Contralateral hip maintained flexed. Metatarsal-phalangeal and interphalangeal joints flexion and extension (SP). Stretching exercise for the dorsal and plantar flexors (SP). Stretching exercise for the dorsal and plantar flexors (SP). Plantar flexor muscles stretching. Inversion–eversion, ankle plantar flexion–dorsiflexion exercises, the knee extended (SP). Inversion–eversion, ankle plantar flexion–dorsiflexion exercises, knee flexed over a pillow (SP). Resistance exercises with elastic band: eversion, inversion, plantar flexion and dorsiflexion (SP). Resistance exercises with elastic band: eversion, inversion, plantar flexion and dorsiflexion (SP).
A A P/A P P P P/A P/A A A
1 2 3 4 5–6 3 4 5–6 5
Gait training with partial support (three-point gait). Gait training with partial support (two-point gait) Gait training with full support—with crutches. Gait training with full support—no crutches. Full support gait—no orthosis. Knee flexion exercise in orthostasis. Knee flexion exercise in orthostasis. Knee flexion exercise in orthostasis. Proprioceptive training: weight transfer latero-lateral, anterior–posterior and posterior–anterior to postural imbalances. Proprioceptive training: mini trampoline balance in a single side, first static, followed by over ball. Unipodal support training: patient raises the weight on the operated side. Stair climbing training: step by step, place first the healthy and then the operated side. Stair descent training: step by step, place first the operated and then the healthy side. Bipedal squat exercise: holding with both hands onto the cross-bar, perform squats, never exceeding the toe line. Bipedal heel rise: up and down on the feet. Cryotherapy with compression and ankle elevation (SP).
A A A A A A A A A
6 5 5 5 6 6 1–6
A A A A A A
2–3 3 2–3 3 5 3 2–3 2–3 2 2
15–20 20 15–20 20 s 20 s 20 s 15–20 15–20 15 15
1 kg @ 4th week 2–3 kg
2 3 3
15 15 20
2 2
10 10 20 min
5% body weight 10–20% body weight
1 kg 2–3 kg
A = active. P = passive. Reps = repetitions. SP = supine position.
calcaneus (Arya and Kulig, 2010). CSA was defined as the average of these three measurements. TL was defined as the distance between the insertion on the calcaneus and the myotendinous junction obtained with the muscle at rest and the ankle joint in neutral position (Arya and Kulig, 2010). TL was obtained using a modified overlapping images method (Urlando and Hawkins, 2007), for which skin markers were placed at 5 cm intervals starting at the calcaneus and moving in longitudinal direction up the leg to the myotendinous junction of the medial head of gastrocnemius. The marker spacing was such that in any image two adjacent landmarks were visible: in the first image the AT insertion and the first marker, in the second image the first and the second markers, and so on, and in the last image the last marker and myotendinous junction. The ultrasound images were superimposed and aligned with help of the markers using the GIMP program (GIMP 2.6.11, GNU Image Manipulation Program). The ImageJ program (National Institutes of Health, Bethesda, Maryland, USA. http://imagej.nih. gov/ij/) was used to measure the CSA and TL.
2.4. AT elongation as a function of ankle joint torque during plantar flexion contractions After the determination of CSA and TL, the probe was supported by a custom-made cast, positioned at the myotendinous junction of the gastrocnemius medial head, and secured to the leg by bandages (Arya and Kulig, 2010). A skin marker was placed between the probe and the skin; if the probe was displaced relative to the marker during a contraction, that contraction was repeated. After performing three plantar flexion ramp maximal voluntary isometric contractions (MVCs) for familiarization and to preconditioning the muscle-tendon complex (Magnusson et al., 2001), the subject performed two plantar flexion ramp MVCs, lasting 10 s each (Magnusson et al., 2001), during which torque, EMG, and ultrasound data were collected. From these two contractions, the highest peak torque was taken as the maximum torque that subjects could produce, as well as the corresponding level of tibialis anterior EMG and tendon elongation (see below). A timing system (HORITA
Table 2 Home exercises program performed in the plaster cast (PC) group after 6 weeks of immobilization. Week Exercise description 1–3 1–3 1–3 4 5 6 4–6 4–6
Sitting on the floor with your legs extended. Ankle movements for heel up and down. Standing, holding a chair and distributing your weight equally in your legs. Climb up and down on your toes. Standing, holding on to a chair, support your body only in the operated side. Climb up and down on tiptoes. Standing, holding a table (or a chair), perform knee flexion and extension with both legs. Standing, holding a table (or a chair), perform knee flexion and extension with both legs. Start exercise performing 3 sets of 10 repetitions and progress to 3 sets of 30 repetitions. Standing, holding a table (or a chair), perform knee flexion and extension with both legs. Start exercise performing 3 sets of 10 repetitions and progress to 3 sets of 30 repetitions. Standing, try to maintain your body supported on the operated side and perform knee flexion and extension. Standing, healthy side positioned forward with knee flexed, the operated side with knee extended and ankle maximally dorsiflexed while elongating calf muscles.
Mode Series Reps or duration A A
3 3
20 20
A A A
3 3 3
20 10 10–30
A
3
10–30
A P
3 5
20 20 s
A = active. P = passive. Reps = repetitions.
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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J.M. Geremia et al. / Clinical Biomechanics xxx (2015) xxx–xxx
Fig. 1. Timeline and content of the experimental session and measurements. CSA = cross-sectional area. TL = tendon length. MVC = maximal voluntary contraction. EMG = electromyography.
Video Stop Watch VS-50; HORITA Company Inc., USA) was utilized to synchronize ultrasound images to the torque and EMG signals. The movement of myotendinous junction was taken to represent AT elongation.
2.5. Relationship between tibialis anterior EMG and dorsiflexion torque The torque recorded by the dynamometer is the net ankle joint torque, which is not equal to the torque produced by the plantar flexors if the antagonistic tibialis anterior is active as well. For this reason, we corrected for the dorsiflexion torque of tibialis anterior using a relationship between tibialis anterior EMG and dorsiflexion torque. To measure the EMG, bipolar electrodes (Ag/AgCl, Meditrace, Kendall, Canada) were placed at the proximal third of the muscle according to the recommendations of SENIAM (http://www.seniam.org/). The EMG signals were amplified (AMT-8, Bortec Biomedical Ltd., Canada) and digitized at 2000 Hz simultaneously with the torque signal of the dynamometer (Windaq data collection system, DATAQ Instruments, Akron, OH, USA, 16-bit). To establish a relationship between tibialis anterior EMG and dorsiflexion torque, three extra measurements were taken (Mademli and Arampatzis, 2005): (a) while the subject was relaxed, and while the subject produced a dorsiflexion torque that resulted in an EMG amplitude that was (b) smaller and (c) higher than the value measured when the subject produced the ramped plantar flexion MVC. The EMG signals obtained during these three conditions were filtered using a 10- to 500-Hz band-pass filter, root mean square (RMS) values were calculated, and a linear relationship was fitted between the RMSvalues and the corresponding dorsiflexion torque. With the help of this relationship we estimated the dorsiflexion torque of tibialis anterior during the plantar flexion contractions on the basis of EMG, and corrected the net ankle joint torque to achieve the true plantar flexion torque.
2.6. Calculation of AT force, elongation, stiffness, strain, and Young's modulus AT force during the ramp plantar flexion contraction was calculated by dividing the total ankle plantar flexor torque, after correction for the tibialis anterior torque, by AT moment arm. Following previous studies (Kubo et al., 2005; Muraoka et al., 2005), the moment arm was taken to be 11% of leg length. To determine AT elongation, the images monitoring the location of the gastrocnemius myotendinous junction were translated from DVD format into AVI format by BitRipper software (Binotex, USA). Using the Virtual Dub software (Avery Lee, USA), the AVI file was screened frame by frame in order to select the desired images. The myotendinous junction displacement was tracked using the ImageJ software. AT force and elongation were extracted at 0%, 20%, 40%, 60%, 80%, and 100% of maximal AT force (Arya and Kulig, 2010). The slope of the AT force-
elongation curve between 60% and 80% of the maximum AT force was taken to represent AT stiffness. To obtain the stress, AT force was divided by CSA, and to obtain the strain, AT elongation during the plantar flexion ramp MVC was divided by TL. Stress and strain values were also obtained at 0%, 20%, 40%, 60%, 80%, and 100% of the maximal AT force (Arya and Kulig, 2010), and the slope of the stress–strain curve between 60% and 80% of the maximum stress was taken to represent Young's modulus. 2.7. Statistical analysis Test–retest reliability of CSA, TL, and AT elongation of the six subjects who were tested twice was calculated using a two-way random effects intra-class correlation coefficient model. A two-way ANOVA for repeated measures was utilized to test for differences between the PC and STPT groups. The factors were groups (PC and STPT) and sides (uninjured and injured). Age, height, and body mass were compared between CTR and ATR groups using a Student t-test for independent samples. The tendon structural and mechanical properties were compared between CTR and ATR groups using a two-way ANOVA. The factors were groups (CTR and ATR) and sides (dominant, non-dominant, uninjured, and injured). When significant groups × side effects were found, separate statistical analyses were performed. First, the dominant and non-dominant sides in the CTR group were compared to each other and to the uninjured side in the ATR group by means of a one-way ANOVA. Subsequently, the uninjured and injured sides of the ATR were compared using a Student t-test for independent samples (parametric data) or a Mann–Whitney U test (non-parametric data). Data were tested for normality using the Shapiro–Wilk test. All tests were performed using SPSS 17.0, at a level of significance of α ≤ 0.05. 3. Results Groups were similar for age [CTR = 44.4 (3.4 years); ATR = 45.3 (2.0 years); p = 0.812)], height [(CTR = 175.3 (1.2 cm); ATR = 173.4 (1.1 cm); p = 0.274)] and body mass [(CTR = 80.0 (4.2 kg); ATR = 84.3 (1.9 kg); p = 0.301)]. The intra-class correlation coefficients were 0.99 (p b 0.001) for the TL, 0.99 (p b 0.001) for the CSA, and 0.98 (p b 0.001) for the tendon elongation. It seems safe to say, therefore, that the measurements were reliable. Both groups (STPT and PC) showed a similar between-sides behavior, with smaller values on the injured side compared to the uninjured side for force (effect size = 0.823), stiffness (effect size = 0.578) (Fig. 2A), stress (effect size = 0.946) and Young's modulus (effect size = 0.857) (Fig. 2B), and larger values for CSA (effect size = 0.904). However, no between-group difference was found in any of the variables (Table 3), and therefore the two patient groups were combined into one ATR group. The CTR group was included in the study in order to assess possible changes in the uninjured side of the ATR group. There was no difference
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
J.M. Geremia et al. / Clinical Biomechanics xxx (2015) xxx–xxx
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force and stiffness were 21% (effect size = 1.379) and 20% (effect size = 1.081) (respectively) lower on the injured side than on the uninjured side. However, the corresponding tendon elongation was not different (Table 4). There was no difference in TL between the injured and uninjured sides. CSA on the injured side was 113% higher than on the uninjured side (effect size = −3.536). Fig. 3(B) shows the stress–strain relationship of the dominant and non-dominant sides of the CTR group and of the injured and uninjured sides of the ATR group. There was no difference in strain at maximum isometric force. Maximal stress and Young's modulus were lower by 60% (effect size = 3.457) and 58% (effect size = 2.321), respectively, in the injured compared to the uninjured side, with no difference between the CTR group sides and the uninjured side of the ATR group. 4. Discussion
Fig. 2. Achilles tendon force-elongation (A) and stress–strain (B) relationships in the plaster cast (PC) and short-term physical therapy (STPT) groups. Vertical and horizontal error bars are SE of the force and elongation data, respectively.
in any of the structural or mechanical properties between the sides of the CTR group and the uninjured side of the ATR group (Table 4), indicating that the changes in activity level following the injury and during the rehabilitation period had no long-term effect on the AT properties on the uninjured side. The force-elongation (Fig. 3A) and stress–strain (Fig. 3B) relationships of the injured AT differed from those of the uninjured AT. Maximal
The purpose of the study was to determine if early physical rehabilitation of surgically repaired Achilles tendon ruptures leads to different long-term structural and mechanical results than traditional postsurgical techniques. No difference was found in any of the variables between the patients who underwent the STPT program and patients subjected to PC immobilization, suggesting that the type of rehabilitation made no long-term (more than 24 month post-operative) difference. Considering that many surgeons do not favor an early rehabilitation program for fear of possible AT complications (e.g., re-rupture), the results of this study are reassuring: our early rehabilitation program (Table 1) is safe as no re-rupture was observed in our STPT group. In addition, our STPT program allowed for early weight bearing and permitted patients to remove the orthosis; this allowed them to move the ankle and the foot of the injured limb and perform their daily life activities, which improved comfort during the rehabilitation period. Previous studies (Kannus et al., 1997; McNair et al., 2013) have shown that the mechanical properties of ruptured tendons are affected; they are more compliant than healthy tendons. Early weight bearing has been suggested as a way to prevent tendons from becoming compliant and preserve ankle functionality. However, McNair et al. (2013) compared the isokinetic plantar flexor torque (240°/s) and tendon stiffness between two groups of subjects that followed either a weight bearing or a non-weight bearing rehabilitation protocol after AT surgical repair. The authors found no between-group differences in torque production and in tendon stiffness 6 months post-surgery. Affected sides presented smaller isokinetic torques and tendon stiffness (20% and 20–40% deficit, respectively) than the contralateral uninjured side. According to the authors, the decrease in tendon stiffness was associated with the decrease in plantar flexor muscles force. In our study, both groups presented a reduction in plantar flexor force, which appears to have contributed to the observed reduction in tendon stiffness. McNair et al. (2013) also suggest
Table 3 Achilles tendon structural and mechanical properties of the uninjured (U) and injured (I) sides in the plaster cast (PC) and short-term physical therapy (STPT) groups [mean (standard deviation)].
Structural Properties Tendon length (mm) CSA (mm2) Mechanical properties Force (N) Elongation (mm) Stiffness (N/mm) Stress (MPa) Strain (%) Young's modulus (MPa)
PC (U) (n = 9)
PC (I) (n = 9)
STPT (U) (n = 9)
STPT (I) (n = 9)
Group effect, p value
Side effect, p value
Group vs. side, p value
240.33 (12.69) 63.49 (11.75)
243.23 (13.18) 138.22 (20.59)⁎
236.87 (6.06) 61.67 (2.37)
243.51 (18.01) 128.09 (32.64)⁎
0.787 0.395
0.079 b0.001
0.730 0.275
2884.07 (349.36) 14.75 (3.97) 231.53 (51.85) 47.38 (11.38) 5.92 (1.68) 994.24 (358.23)
2342.24 (484.48)⁎ 14.29 (3.45) 200.39 (30.70)⁎ 17.38 (3.11)⁎ 5.68 (1.56) 403.32 (88.81)⁎
3293.87 (626.56) 16.34 (4.00) 227.69 (49.93) 53.85 (10.69) 6.86 (1.56) 848.85 (260.57)
2555.51 (214.72)⁎ 15.37 (4.18) 165.58 (32.89)⁎ 22.77 (6.19)⁎ 6.45 (2.11) 369.74 (95.63)⁎
0.089 0.469 0.165 0.123 0.326 0.306
b0.001 0.630 0.011 b0.001 0.622 b0.001
0.468 0.800 0.369 0.844 0.838 0.374
CSA = cross-sectional area. ⁎ Difference between injured and uninjured sides within groups.
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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Table 4 Achilles tendon structural and mechanical properties of the dominant (D) and non-dominant (Non-D) sides in the control group (CTR), uninjured (UN), and injured (IN) sides in the Achilles tendon rupture group (ATR) [mean (standard deviation)].
Structural Properties Tendon length (mm) CSA (mm2) Mechanical properties Force (N) Elongation (mm) Stiffness (N/mm) Stress (MPa) Strain (%) Young's modulus (MPa)
CTR (D) (n = 9)
CTR (Non-D) (n = 9)
ATR (UN) (n = 18)
ATR (IN) (n = 18)
Two-Way ANOVA CTR vs. ATR p value
One-Way ANOVA D vs. Non-D vs. UN p value
Specific test UN vs. IN p value
235.05 (6.49) 58.73 (6.86)
235.19 (15.70) 61.62 (8.80)
238.60 (9.72) 62.58 (8.28)
243.37 (14.71) 133.16 (26.98)⁎
0.267 n.a.
n.a. 0.512
n.a. b0.001
3117.84 (604.58) 15.21 (2.58) 210.73 (49.40) 53.54 (10.58) 6.58 (1.04) 885.18 (214.31)
3060.86 (380.12) 16.11 (4.84) 220.41 (38.01) 50.05 (6.34) 6.86 (1.92) 762.23 (169.59)
3088.97 (535.38) 15.54 (3.95) 229.61 (49.42) 50.62 (11.22) 6.39 (1.64) 921.55 (312.95)
2448.88 (379.73)⁎ 14.83 (3.76) 182.99 (35.69)⁎ 20.08 (5.50)⁎ 6.07 (1.84) 386.53 (91.18)⁎
n.a. 0.674 n.a. n.a. 0.865 n.a.
0.973 n.a. 0.612 0.720 n.a 0.337
0.001 n.a. 0.03 b0.001 n.a. b0.001
CSA = cross-sectional area. Specific test = t-test or Mann–Whitney U test. n.a., not applicable. ⁎ Difference between UN and IN sides.
that strength-training programs focused on muscle hypertrophy would be valuable to improve tendon stiffness. However, as our rehabilitation programs (STPT, PC) focused on ROM gain rather than on muscle strengthening exercises, apparently they did not promote sufficient overload in the healing tendons of both groups to produce the desired long-term AT structural and mechanical adaptations for complete recovery.
Fig. 3. Achilles tendon force-elongation (A) and stress–strain (B) relationships in the control (CTR) and Achilles tendon rupture (ATR) groups. Vertical and horizontal error bars are SE of the stress and strain data, respectively.
The results of this study show that approximately 2 years and 6 months after surgical repair the AT material properties had still not fully recovered. Maffulli et al. (2003a) evaluated the isometric plantar flexor strength in patients with a complete AT rupture that were subjected to different rehabilitation protocols (immobilization and accelerated). Twenty-one months after surgical repair, these authors found a significant muscle strength deficit in the injured side of both groups compared to the uninjured side. Maffulli et al. (2003b) and Bressel and McNair (2001) emphasize that the observed reduction in force production might be associated with the different lifestyle adopted by the subjects after the injury, as some of them apparently avoided systematic physical activity fearing new ruptures or complications. Although we did not evaluate the subjects' lifestyle in our study, our results show a lack of recovery in the structural and functional properties of the plantar flexor group in the injured side, which has important clinical implications. The CTR group was included in the study in order to assess possible changes in the uninjured side of the ATR group. Overall, the uninjured side of the ATR group appeared similar to the dominant and nondominant sides of the CTR group; any changes in activity level that might have occurred after the injury on the injured side had no longterm effects on the uninjured tendon. This suggests that lifestyle did not change, that the changes in AT properties of the injured limb were directly related to the injury itself, and that the changes in properties on the injured side have something to do with structural changes in the tendon. The second question that we addressed was whether the forceelongation and the stress–strain relationships of the injured tendon differed from those of the uninjured tendon. Tendon elongation and tendon strain at MVC were similar at the injured and uninjured sides in the ATR group. However, similar elongation and strain were reached at lower tendon force and tendon stress on the injured side than on the uninjured side, evidencing that injured tendons are more compliant than uninjured tendons. The fact that both stiffness and Young's modulus were smaller on the injured side than on the uninjured side further supports the idea that tendon material is more compliant on the injured side, in contrast to previous findings that did not take into consideration the AT structural parameters to determine these mechanical properties (Bressel and McNair, 2001). The greater tendon compliance on the injured side, which may come with a higher risk of tendon re-rupture, seems to be in line with histological findings reported in the literature. It has been shown that the main content of uninjured tendons is type I collagen, while repaired tendons contain a greater proportion of type III collagen (Maffulli et al., 2000). Type I collagen is characterized by a higher tensile strength (Maffulli and Almekinders, 2007), which promotes the ability
Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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to support larger loads, while type III collagen has a lower tensile strength. Kannus et al. (1997) reported that injured tendons might not reach an optimum orientation of collagen fibers, at least not during short-term rehabilitation protocols. It is unclear what happens in the long-term, due to the lack of literature on well-defined long-term rehabilitation protocols aimed at promoting favorable structural and mechanical changes during tendon healing. We also think that new insights are necessary in the field of tendon rehabilitation to optimize the return to a healthy condition. There are two aspects to this: (1) we want the best outcome possible in terms of tendinous tissue itself, and (2) we want to reach this best outcome as quickly as possible by optimization of the rehabilitation program. The ideal protocol assures early return to function, patient comfort, and return of tendon structure and mechanical properties to normal values. The STPT program used here seems suitable to achieve the first and second goals, but not the third. When tendon force is normalized by CSA, large differences are found between injured and uninjured sides in the ATR group (Fig. 3B). Tendon thickening after AT surgical repair is a common finding. Our results showed that CSA was 113% larger on the injured side than on the uninjured side. Changes in tendon thickness seem to be present several months post-surgical repair, and our results agree with those of other studies (Maffulli et al., 2003a; Möller et al., 2002), indicating that the healed tendon is structurally different. Our methods to obtain the force-elongation and stress–strain curves of the AT have some limitations. According to previous studies, the moment arm does not remain constant during MVCs (Maganaris et al., 1998), and rotations in the joints can occur (Magnusson et al., 2001). Nevertheless, our values were similar to values obtained in studies in which error-reduction techniques were used (Arya and Kulig, 2010; Kubo et al., 2012; Magnusson et al., 2001; Stenroth et al., 2012; Waugh et al., 2012). The non-invasive method for assessing the mechanical properties of human tendon by real-time ultrasound scanning has often been used and the results obtained vary greatly (Maganaris et al., 2008). According to Maganaris et al. (2008), this variation is probably caused by inter-study methodological differences, which demonstrates the importance of a careful comparison of different studies. Interestingly, we did not find the characteristic toe region in the forceelongation and stress–strain curves. According to Maffulli and Almekinders (2007), this region is associated with forces that reduce the resting crimp angle of collagen fibers without causing further fiber stretching. The seated position we adopted with full knee extension can generate initial forces on the AT (Stenroth et al., 2012), which could have pre-stretched the collagen fibers. Evaluators were not blinded to the patients' allocation into the groups. Although few studies (Möller et al., 2002; Rosso et al., 2013) had their evaluators blinded to the patients' allocation into the groups, this is a limitation that can influence the study's internal validity. However, we do not believe that this limitation influenced the clinical relevance of our study. Most studies in the field fail to clearly describe the rehabilitation program used and do not report the mechanical properties of the sutured AT post-surgery. By showing that these properties are still different from a normal or a healthy tendon even more than 2 years after surgery, our study contributes to the existing knowledge in the area of tendon structural and mechanical properties. 5. Conclusion Early physical rehabilitation did not lead to long-term AT structural and mechanical differences when compared to traditional postsurgical techniques. However, more than 2 years after surgical repair the previously injured tendons are still structurally and mechanically different from healthy tendons. Our early rehabilitation protocol did not lead to deleterious effects on the sutured tendons and can be safely used for post-surgery treatment. Finally, further study is necessary to design long-term rehabilitation protocols that make injured tendons return to a healthy condition.
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Acknowledgments The authors would like to acknowledge Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Programa Ciências Sem Fronteiras (CSF) e Financiadora de Estudos e Projetos (FINEP) from Brazil for financial support, and Valdirene Gambarra da Silva for technical help during patient recruitment.
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Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
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Please cite this article as: Geremia, J.M., et al., The structural and mechanical properties of the Achilles tendon 2 years after surgical repair, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.03.005
