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Biomechanical evaluation in runners with Achilles tendinopathy

Abstract

OBJECTIVES:

To evaluate the clinical characteristics, ground reaction force (GRF), and function of the plantar muscles and dorsiflexors of the ankle in runners with and without Achilles tendinopathy (AT) and in non-runners.

METHODS:

Seventy-two participants (42 men, 30 women; mean age: 37.3±9.9 years) were enrolled in this cross-sectional study and divided into three groups: AT group (ATG, n=24), healthy runners’ group (HRG, n=24), and non-runners’ group (NRG, n=24). Both ankles were evaluated in each group. The American Orthopedic Foot and Ankle Society (AOFAS) Ankle-Hindfoot Scale was used for clinical and functional evaluation. GRF was evaluated using force plates and muscle strength was evaluated using an isokinetic dynamometer.

RESULTS:

The AOFAS scores were lower in the ATG. The strike impulse was higher in the ATG than in the HRG and NRG. However, GRF was similar among the groups. The ATG exhibited lower total work at 120°/s speed than the HRG. The peak torque in concentric dorsiflexion was lower in the NRG than in the ATG and HRG. The peak torque and total work in concentric plantar flexion were lower in the NRG than in the ATG. The peak torque and total work in eccentric plantar flexion were lower in the NRG than in the ATG and HRG.

CONCLUSION:

Runners with AT showed higher strike impulse, lower muscle strength of the plantar flexors, and higher clinical and functional damage.

Tendinopathy; Achilles Tendon; Running; Ground Reaction Force; Biomechanical Phenomena; Muscle Strength


INTRODUCTION

Achilles tendinopathy (AT) is one of the most common overuse injuries in elite and recreational distance runners (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
,22. Silbernagel KG, Gustavsson A, Thomeé R, Karlsson J. Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc. 2006;14(11):1207-17. https://doi.org/10.1007/s00167-006-0150-6
https://doi.org/10.1007/s00167-006-0150-...
). Multiple factors (33. Longo UG, Rittweger J, Garau G, Radonic B, Gutwasser C, Gilliver SF, et al. No influence of age, gender, weight, height, and impact profile in achilles tendinopathy in masters track and field athletes. Am J Sports Med. 2009;37(7):1400-5. https://doi.org/10.1177/0363546509332250
https://doi.org/10.1177/0363546509332250...

4. Maffulli N, Kader D. Tendinopathy of tendo achillis. J Bone Joint Surg Br. 2002;84(1):1-8. https://doi.org/10.1302/0301-620X.84B1.0840001
https://doi.org/10.1302/0301-620X.84B1.0...

5. Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clin Sports Med. 2003;22(4):675-92. https://doi.org/10.1016/S0278-5919(03)00004-8
https://doi.org/10.1016/S0278-5919(03)00...

6. Munteanu SE, Barton CJ. Lower limb biomechanics during running in individuals with achilles tendinopathy: a systematic review. J Foot Ankle Res. 2011;4:15. https://doi.org/10.1186/1757-1146-4-15
https://doi.org/10.1186/1757-1146-4-15...
-77. Reule CA, Alt WW, Lohrer H, Hochwald H. Spatial orientation of the subtalar joint axis is different in subjects with and without Achilles tendon disorders. Br J Sports Med. 2011;45(13):1029-34. https://doi.org/10.1136/bjsm.2010.080119
https://doi.org/10.1136/bjsm.2010.080119...
) are related to AT including intrinsic factors such as poor vascularization, overweight, aging, male sex, height (44. Maffulli N, Kader D. Tendinopathy of tendo achillis. J Bone Joint Surg Br. 2002;84(1):1-8. https://doi.org/10.1302/0301-620X.84B1.0840001
https://doi.org/10.1302/0301-620X.84B1.0...
,55. Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clin Sports Med. 2003;22(4):675-92. https://doi.org/10.1016/S0278-5919(03)00004-8
https://doi.org/10.1016/S0278-5919(03)00...
,77. Reule CA, Alt WW, Lohrer H, Hochwald H. Spatial orientation of the subtalar joint axis is different in subjects with and without Achilles tendon disorders. Br J Sports Med. 2011;45(13):1029-34. https://doi.org/10.1136/bjsm.2010.080119
https://doi.org/10.1136/bjsm.2010.080119...
,88. Lorimer AV, Hume PA. Achilles tendon injury risk factors associated with running. Sports Med. 2014;44(10):1459-72. https://doi.org/10.1007/s40279-014-0209-3
https://doi.org/10.1007/s40279-014-0209-...
), lower limb misalignment, dysfunction and weakness of plantar flexors (33. Longo UG, Rittweger J, Garau G, Radonic B, Gutwasser C, Gilliver SF, et al. No influence of age, gender, weight, height, and impact profile in achilles tendinopathy in masters track and field athletes. Am J Sports Med. 2009;37(7):1400-5. https://doi.org/10.1177/0363546509332250
https://doi.org/10.1177/0363546509332250...

4. Maffulli N, Kader D. Tendinopathy of tendo achillis. J Bone Joint Surg Br. 2002;84(1):1-8. https://doi.org/10.1302/0301-620X.84B1.0840001
https://doi.org/10.1302/0301-620X.84B1.0...
-55. Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clin Sports Med. 2003;22(4):675-92. https://doi.org/10.1016/S0278-5919(03)00004-8
https://doi.org/10.1016/S0278-5919(03)00...
,99. Alfredson H, Lorentzon R. Chronic Achilles tendinosis: recommendations for treatment and prevention. Sports Med. 2000;29(2):135-46. https://doi.org/10.2165/00007256-200029020-00005
https://doi.org/10.2165/00007256-2000290...

10. Carcia CR, Martin RL, Houck J, Wukich DK; Orthopaedic Section of the American Physical Therapy Association. Achilles pain, stiffness, and muscle power deficits: achilles tendinitis. J Orthop Sports Phys Ther. 2010;40(9):A1-26. https://doi.org/10.2519/jospt.2010.0305
https://doi.org/10.2519/jospt.2010.0305...

11. Maffulli N, Via AG, Oliva F. Chronic Achilles Tendon Disorders: Tendinopathy and Chronic Rupture. Clin Sports Med. 2015;34(4):607-24. https://doi.org/10.1016/j.csm.2015.06.010
https://doi.org/10.1016/j.csm.2015.06.01...

12. Mahieu NN, Witvrouw E, Stevens V, Van Tiggelen D, Roget P. Intrinsic risk factors for the development of achilles tendon overuse injury: a prospective study. Am J Sports Med. 2006;34(2):226-35. https://doi.org/10.1177/0363546505279918
https://doi.org/10.1177/0363546505279918...

13. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
-1414. Zafar MS, Mahmood A, Maffulli N. Basic science and clinical aspects of achilles tendinopathy. Sports Med Arthrosc Rev. 2009;17(3):190-7. https://doi.org/10.1097/JSA.0b013e3181b37eb7
https://doi.org/10.1097/JSA.0b013e3181b3...
), decreased flexibility, excessive pronation, cavus feet, and lateral instability of the ankle (33. Longo UG, Rittweger J, Garau G, Radonic B, Gutwasser C, Gilliver SF, et al. No influence of age, gender, weight, height, and impact profile in achilles tendinopathy in masters track and field athletes. Am J Sports Med. 2009;37(7):1400-5. https://doi.org/10.1177/0363546509332250
https://doi.org/10.1177/0363546509332250...
,44. Maffulli N, Kader D. Tendinopathy of tendo achillis. J Bone Joint Surg Br. 2002;84(1):1-8. https://doi.org/10.1302/0301-620X.84B1.0840001
https://doi.org/10.1302/0301-620X.84B1.0...
,1010. Carcia CR, Martin RL, Houck J, Wukich DK; Orthopaedic Section of the American Physical Therapy Association. Achilles pain, stiffness, and muscle power deficits: achilles tendinitis. J Orthop Sports Phys Ther. 2010;40(9):A1-26. https://doi.org/10.2519/jospt.2010.0305
https://doi.org/10.2519/jospt.2010.0305...
,1111. Maffulli N, Via AG, Oliva F. Chronic Achilles Tendon Disorders: Tendinopathy and Chronic Rupture. Clin Sports Med. 2015;34(4):607-24. https://doi.org/10.1016/j.csm.2015.06.010
https://doi.org/10.1016/j.csm.2015.06.01...
,1414. Zafar MS, Mahmood A, Maffulli N. Basic science and clinical aspects of achilles tendinopathy. Sports Med Arthrosc Rev. 2009;17(3):190-7. https://doi.org/10.1097/JSA.0b013e3181b37eb7
https://doi.org/10.1097/JSA.0b013e3181b3...

15. Kannus P. Etiology and pathophysiology of chronic tendon disorders in sports. Scand J Med Sci Sports. 1997;7(2):78-85. https://doi.org/10.1111/j.1600-0838.1997.tb00123.x
https://doi.org/10.1111/j.1600-0838.1997...
-1616. Van Ginckel A, Thijs Y, Hesar NG, Mahieu N, De Clercq D, Roosen P, et al. Intrinsic gait-related risk factors for Achilles tendinopathy in novice runners: a prospective study. Gait Posture. 2009;29(3):387-91. https://doi.org/10.1016/j.gaitpost.2008.10.058
https://doi.org/10.1016/j.gaitpost.2008....
) and extrinsic factors such as old and bad conditions of running shoes, hard surface, conditions related to environment and equipment (88. Lorimer AV, Hume PA. Achilles tendon injury risk factors associated with running. Sports Med. 2014;44(10):1459-72. https://doi.org/10.1007/s40279-014-0209-3
https://doi.org/10.1007/s40279-014-0209-...
,99. Alfredson H, Lorentzon R. Chronic Achilles tendinosis: recommendations for treatment and prevention. Sports Med. 2000;29(2):135-46. https://doi.org/10.2165/00007256-200029020-00005
https://doi.org/10.2165/00007256-2000290...
,1111. Maffulli N, Via AG, Oliva F. Chronic Achilles Tendon Disorders: Tendinopathy and Chronic Rupture. Clin Sports Med. 2015;34(4):607-24. https://doi.org/10.1016/j.csm.2015.06.010
https://doi.org/10.1016/j.csm.2015.06.01...
,1414. Zafar MS, Mahmood A, Maffulli N. Basic science and clinical aspects of achilles tendinopathy. Sports Med Arthrosc Rev. 2009;17(3):190-7. https://doi.org/10.1097/JSA.0b013e3181b37eb7
https://doi.org/10.1097/JSA.0b013e3181b3...
), and training mistakes including those involving the distance, intensity, running rhythm, technique, and fatigue (55. Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clin Sports Med. 2003;22(4):675-92. https://doi.org/10.1016/S0278-5919(03)00004-8
https://doi.org/10.1016/S0278-5919(03)00...
,88. Lorimer AV, Hume PA. Achilles tendon injury risk factors associated with running. Sports Med. 2014;44(10):1459-72. https://doi.org/10.1007/s40279-014-0209-3
https://doi.org/10.1007/s40279-014-0209-...
,99. Alfredson H, Lorentzon R. Chronic Achilles tendinosis: recommendations for treatment and prevention. Sports Med. 2000;29(2):135-46. https://doi.org/10.2165/00007256-200029020-00005
https://doi.org/10.2165/00007256-2000290...
).

AT affects runners, but it is not clear how this condition changes the running technique.Among the spatiotemporal variables, runners with AT may exhibit similar (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
) or slower gait speed, shorter stride length, and shorter step length compared to those without AT (1717. Kim S, Yu J. Changes of gait parameters and lower limb dynamics in recreational runners with achilles tendinopathy. J Sports Sci Med. 2015;14(2):284-9.). Ogbonmwan et al. (1818. Ogbonmwan I, Kumar BD, Paton B. New lower-limb gait biomechanical characteristics in individuals with Achilles tendinopathy: A systematic review update. Gait Posture. 2018;62:146-56. https://doi.org/10.1016/j.gaitpost.2018.03.010
https://doi.org/10.1016/j.gaitpost.2018....
) suggested that reduced spatiotemporal gait variables constitute a protective and compensatory mechanism. Among the kinetic variables, Azevedo et al. (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
) and McCrory et al. (1313. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
) did not find differences in the vertical ground reaction force (vGRF) between healthy runners and runners with AT. Runners with a higher foot impact are at an increased risk of developing lower limb overuse injuries (1919. Hreljac A. Impact and overuse injuries in runners. Med Sci Sports Exerc. 2004;36(5):845-9. https://doi.org/10.1249/01.MSS.0000126803.66636.DD
https://doi.org/10.1249/01.MSS.000012680...
,2020. Robbins SE, Hanna AM. Running-related injury prevention through barefoot adaptations. Med Sci Sports Exerc. 1987;19(2):148-56. https://doi.org/10.1249/00005768-198704000-00014
https://doi.org/10.1249/00005768-1987040...
). Although vGRF indicates the body impact during running, runners with AT do not have a higher vGRF than healthy runners (1313. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
). McRoys et al. (1313. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
) suggested that peak torque in plantar flexion, touchdown angle, and years of running were the strongest discriminators between runners with Achilles tendinitis and runners who had no history of overuse injury. It is unclear whether healthy runners and runners with AT exhibit any kinetic differences during running.

Doubts still exist regarding the effect of mechanical factors on the etiopathogenesis and evolution of Achilles tendon injuries in runners (66. Munteanu SE, Barton CJ. Lower limb biomechanics during running in individuals with achilles tendinopathy: a systematic review. J Foot Ankle Res. 2011;4:15. https://doi.org/10.1186/1757-1146-4-15
https://doi.org/10.1186/1757-1146-4-15...
). Runners with Achilles tendon injuries experience functional loss in sports performance not only due to decrease of strength. Functional losses and changes in the plantar flexor muscles are associated with alterations in ground reaction force (GRF), especially during foot strikes. It is unclear whether runners with AT exhibit a different foot strike pattern compared to healthy runners? Thus, our objective was to evaluate the clinical characteristics, kinetic variables, and the strength of ankle plantar flexors and dorsiflexors in runners with and without AT and in non-runners. Our first hypothesis was that runners with AT would exhibit lower muscle strength than runners without AT. The second hypothesis was that runners with AT would show a different foot strike pattern than the others. We expected that runners with AT would exhibit altered plantar flexor muscles, affecting their foot strike pattern during running.

METHODS

Study location and ethical issues

This cross-sectional study was conducted at the Motion Study Laboratory of the Department of Orthopedics and Traumatology, University of São Paulo. Ethical approval was granted by the Ethics Committee of the University of São Paulo (number 0422/11).

Sample Size

The sample size calculation was based on a previous study (1313. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
). An isokinetic variable (peak torque of the plantar flexors) was used to find a difference of 4.3 Nm between the AT group and the healthy runners’ group (HRG). The power of the test was set at 90% (sampling power) with a 5% (two-tailed alpha) level of significance. To meet these conditions, at least 24 subjects were required in each group.

Subjects

Seventy-two adults (42 men and 30 women) were divided into three groups. The AT group (ATG, n=24) comprised of competitive (professional/elite athletes or those who participated in international competitions) and recreational (individuals running in a nonprofessional or amateur context) runners (2121. Alentorn-Geli E, Samuelsson K, Musahl V, Green CL, Bhandari M, Karlsson J. The Association of Recreational and Competitive Running With Hip and Knee Osteoarthritis: A Systematic Review and Meta-analysis. J Orthop Sports Phys Ther. 2017;47(6):373-90. https://doi.org/10.2519/jospt.2017.7137
https://doi.org/10.2519/jospt.2017.7137...
) who had been running at least 20 km/week for 1 year and had suffered an injury within 5 years before the evaluation. The HRG, (n=24) comprised of recreational and competitive runners who had been running at least 20 km/week for 1 year and had not suffered any injury (requiring medical care or stoppage of running) in the last 2 years. The non-runners’ group (NRG, n=24) comprised of non-athletes who did not practice any regular sports or physical activities (less than three times/week). All participants were evaluated using ankle magnetic resonance imaging (MRI). They were also evaluated by an orthopedic physician (foot diseases specialist) who performed a clinical evaluation to diagnose and classify the tendon injury and to verify the absence of other injuries that could constitute the exclusion criteria. The inclusion criteria were as follows: (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
) age between 25 and 50 years and (22. Silbernagel KG, Gustavsson A, Thomeé R, Karlsson J. Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc. 2006;14(11):1207-17. https://doi.org/10.1007/s00167-006-0150-6
https://doi.org/10.1007/s00167-006-0150-...
) absence of neurological, cardiovascular, or cardiorespiratory impairment and/or any mental disturbances or disorders. The specific inclusion criteria for the ATG were: (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
) no use of medications in the last 60 days, (22. Silbernagel KG, Gustavsson A, Thomeé R, Karlsson J. Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc. 2006;14(11):1207-17. https://doi.org/10.1007/s00167-006-0150-6
https://doi.org/10.1007/s00167-006-0150-...
) presence of Achilles tendinopathy (inflammatory process) or tendinosis (degenerative process) with no calcaneal tendon rupture on MRI, and (33. Longo UG, Rittweger J, Garau G, Radonic B, Gutwasser C, Gilliver SF, et al. No influence of age, gender, weight, height, and impact profile in achilles tendinopathy in masters track and field athletes. Am J Sports Med. 2009;37(7):1400-5. https://doi.org/10.1177/0363546509332250
https://doi.org/10.1177/0363546509332250...
) absence of previous lower-limb surgery. The exclusion criteria were the presence of pain or inability to complete any of the tests.

Procedures

Participants answered a questionnaire about their personal training protocols. They were submitted to a clinical evaluation to analyze their AT. For clinical and functional evaluation, the American Orthopedic Foot and Ankle Society (AOFAS) Ankle-Hindfoot Scale was used followed by evaluation using ankle MRI. The AOFAS scale includes nine items that can be divided into three subscales (pain, function, and alignment). The pain subscale consists of one item with a maximum score of 40 points, which indicates no pain. The function subscale consists of seven items with a maximum score of 50 points, which indicates full function. The alignment subscale consists of one item with a maximum score of 10 points, which indicates good alignment. The maximum score is 100 points, indicating no symptoms or impairment (2222. Lins C, Ninomya AF, Bittar CK, de Carvalho AE Jr, Cliquet A Jr. Kinetic and kinematic evaluation of the ankle joint after achilles tendon reconstruction with free semitendinosus tendon graft: preliminary results. Artif Organs. 2013;37(3):291-7. https://doi.org/10.1111/j.1525-1594.2012.01559.x
https://doi.org/10.1111/j.1525-1594.2012...
).

GRF was measured using two plates (1 kHz sampling frequency, ORC6, AMTI, MA, USA). The participants ran (at 3.0 to 4.0 m/s) on a 10-m sidewalk where these two force plates were mounted right in the center. They performed 10 trials: five for familiarization and five for records. GRF was low-pass filtered with fourth-order Butterworth filter at 100 Hz and normalized by body weight. The maximum vGRF (Fmax), strike impulse (GRF integral during the first 50 ms of contact), and total impulse (GRF integral during the full stance phase). MATLAB scripts (MATLAB 2015; MathWorks, CA, USA) version (8.5) were processed and used to calculate the GRF variables (2323. Baur H, Müller S, Hirschmüller A, Cassel M, Weber J, Mayer F. Comparison in lower leg neuromuscular activity between runners with unilateral mid-portion Achilles tendinopathy and healthy individuals. J Electromyogr Kinesiol. 2011;21(3):499-505. https://doi.org/10.1016/j.jelekin.2010.11.010
https://doi.org/10.1016/j.jelekin.2010.1...
).

Isokinetic dynamometry was performed using the Biodex® Multi-Joint System 3 (Biodex Medical; Shirley, NY, USA). The isokinetic dynamometer was calibrated for 30 minutes before starting the tests. The participants underwent this measurement after the running test. Thus, they were already warm. For concentric evaluation of dorsiflexion and concentric and eccentric evaluation of plantar flexion of the ankle joint, the participants were positioned such that they remained seated with the hips in 90° flexion. The biological axis of motion of the ankle joint was aligned with the mechanical axis of the dynamometer and the knee was held at 30° flexion. The rigid plate allowed a 20° range of plantar flexion from the neutral position of the ankle. The participants were held in this position by two thoracic belts, one pelvic belt, Velcro straps on the distal portion of the thigh, and Velcro straps on the metatarsal area in the dorsal region of the foot (2424. Luna NM, Alonso AC, Brech GC, Mochizuki L, Nakano EY, Greve JM. Isokinetic analysis of ankle and ground reaction forces in runners and triathletes. Clinics (Sao Paulo). 2012;67(9):1023-8. https://doi.org/10.6061/clinics/2012(09)07
https://doi.org/10.6061/clinics/2012(09)...
).

All tests were bilateral and standardized and the right lower limb was evaluated first. The subjects performed three submaximal repetitions to familiarize themselves with the equipment, followed by a 60-second rest interval. For data collection, a set of four repetitions at a velocity of 60°/s and another set of 20 repetitions at 120°/s were completed in the concentric-concentric (con-con) mode for both plantar flexion and dorsiflexion and in the concentric-eccentric (con-ecc) mode for plantar flexion. Constant standardized verbal encouragement was provided during the tests to promote maximum effort during contractions (2525. Möller M, Lind K, Styf J, Karlsson J. The reliability of isokinetic testing of the ankle joint and a heel-raise test for endurance. Knee Surg Sports Traumatol Arthrosc. 2005;13(1):60-71. https://doi.org/10.1007/s00167-003-0441-0
https://doi.org/10.1007/s00167-003-0441-...
). The isokinetic variables included the maximum peak torque corrected for body weight (PT/BW) value in % and total work (J).

Statistical analysis

Shapiro-Wilk test was used to test the normal distribution of the variables. Student’s t-test (parametric distribution) and Mann-Whitney U test (non-parametric distribution) were used to compare the variables between sides. Among the 24 individuals from the ATG, 17 had unilateral injuries and 7 had bilateral injuries. For individuals with unilateral injury, ankles with and without injury were compared. For individuals with bilateral injury, the dominant and the non-dominant sides were compared.

Whenever both the sides exhibited similar results for kinetic and isokinetic variables, only the data from the injured side were analyzed (31 ankles). Since the dominant and the non-dominant sides in the HRG and NRG exhibited similar kinetic and isokinetic results, their results were grouped together with each group containing 48 ankles.

Analysis of variance was used to compare the kinetic and isokinetic variables among the ATG, HRG, and NRG. Bonferroni post-hoc test was used for within-group comparisons. SPSS for Windows, version 15.0 (SPSS Inc., Chicago, IL, USA) was used for the analyses and p<0.05 was considered statistically significant.

RESULTS

Table 1 shows the comparison of baseline characteristics (mean values, standard deviations, and results for testing the hypothesis of equality) among the groups.

Table 1
Baseline characteristics of the groups.

Sixteen (67%) runners from the ATG continued training with the same intensity, but presented lower competition performance. Four (16.5%) runners maintained the same training and competition performance and 4 (16.5%) runners showed poor performance during training and competition. Twenty (83%) runners from the ATG experienced pain while running, but they continued running. Two (8%) runners did not experience any pain during running, but experienced it after running. Two (8%) runners stopped running due to pain.

The ATG exhibited lower AOFAS score than the HRG and NRG (Figure 1).

Figure 1
Mean (standard deviation) of American Orthopedic Foot and Ankle Society scale scores in the Achilles tendinopathy group, healthy runners’ group, and non-runners’ group.

The vGRF peak was similar among the ATG, HRG, and NRG. The ATG exhibited a higher impulse in the first 50 ms of contact than the HRG and NRG. The total impulse was similar among the three groups (Table 2).

Table 2
Test results for the hypothesis of equality of the means of kinetic variables.

The isokinetic variables at 60°/s are listed in Table 3. In the con-con mode, there were no difference in the total work of plantar flexors among the groups. The peak torque in the HRG was higher than that in the NRG. In the con-ecc mode, concentric total work of the plantar flexors was higher in the ATG than in the NRG. The eccentric total work in the NRG was lower than that in the ATG and HRG.

Table 3
Test results for the hypothesis of equality of the means of isokinetic variables at 60°/sec.

The isokinetic variables at 120°/s are listed in Table 4. In the con-con mode, the total work of the plantar flexors in the ATG was lower than that in the HRG. The dorsiflexor peak torque in the NRG was lower than that in the ATG and HRG. In the con-ecc mode, the plantar flexor peak torque and total work were higher in the ATG than in the NRG. The eccentric peak torque and total work in the NRG were lower than those in the ATG and HRG.

Table 4
Test results for the hypothesis of equality of the means of isokinetic variables at 120°/sec.

DISCUSSION

In the present study, we compared the results of kinetic analysis (GRF) and muscle strength analysis (isokinetic dynamometer) among runners with AT, runners without AT, and the non-runner control group. Runners in the ATG exhibited the lowest AOFAS score and the highest strike impulse. They also experienced pain, functional loss, and loss of biomechanical alignment. Although most of the injured runners continued running, many of them ran with pain and decreased performance. Worse performance and pain may be associated with lower muscle resistance and fatigue. This in turn causes impairment of long-term resistance, which is essential for distance runners. We observed that healthy runners had stronger dorsiflexor muscles than non-runners.

The maximal vGRF was similar among the ATG, HRG, and NRG. This peak occurred during the propulsion phase and the participants ran at the same speed. Other authors have not found differences in vGRF between runners with and without AT (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
,1313. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
). However, GRF increased in runners with tibial stress fractures (2626. Milner CE, Ferber R, Pollard CD, Hamill J, Davis IS. Biomechanical factors associated with tibial stress fracture in female runners. Med Sci Sports Exerc. 2006;38(2):323-8. https://doi.org/10.1249/01.mss.0000183477.75808.92
https://doi.org/10.1249/01.mss.000018347...
) and plantar fasciitis (2727. Chang R, Rodrigues PA, Van Emmerik RE, Hamill J. Multi-segment foot kinematics and ground reaction forces during gait of individuals with plantar fasciitis. J Biomech. 2014;47(11):2571-7. https://doi.org/10.1016/j.jbiomech.2014.06.003
https://doi.org/10.1016/j.jbiomech.2014....
). The total impulse was similar among the three groups, as all participants were running at the same speed. McCrory et al. (1313. McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
https://doi.org/10.1097/00005768-1999100...
) and Azevedo et al. (11. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
https://doi.org/10.1136/bjsm.2008.053421...
) reported similar total impulses between runners with and without AT. These authors did not evaluate the strike impulse.

AT may change the foot strike pattern during running. The ATG exhibited a higher strike impulse than the HRG and NRG. This result supports our hypothesis that runners with AT would exhibit a different foot strike pattern than the other groups. Wyndow et al. (2828. Wyndow N, Cowan SM, Wrigley TV, Crossley KM. Triceps surae activation is altered in male runners with Achilles tendinopathy. J Electromyogr Kinesiol. 2013;23(1):166-72. https://doi.org/10.1016/j.jelekin.2012.08.010
https://doi.org/10.1016/j.jelekin.2012.0...
) found alterations in sural triceps muscle activity in runners with AT, which may impair impact absorption during foot strike. It is possible that plantar flexor eccentric training may improve pain and performance. In military recruits (1212. Mahieu NN, Witvrouw E, Stevens V, Van Tiggelen D, Roget P. Intrinsic risk factors for the development of achilles tendon overuse injury: a prospective study. Am J Sports Med. 2006;34(2):226-35. https://doi.org/10.1177/0363546505279918
https://doi.org/10.1177/0363546505279918...
), AT leads to a decrease in the force of the plantar flexor muscles. Runners with and without AT had stronger dorsiflexor muscles than the controls. Gymnasts and soccer players also have higher dorsiflexion peak torque, as their sports activities demand high ankle stability (2929. So CH, Siu TO, Chan KM, Chin MK, Li CT. Isokinetic profile of dorsiflexors and plantar flexors of the ankle - A comparative study of élite versus untrained subjects. Br J Sports Med. 1994;28(1):25-30. https://doi.org/10.1136/bjsm.28.1.25
https://doi.org/10.1136/bjsm.28.1.25...
).

Runners with AT have higher concentric and eccentric total work of the plantar flexors than non-runners. Runners are more physically trained than non-runners due to the higher eccentric activity during running, especially in downhill areas (3030. Fourchet F, Millet GP, Tomazin K, Guex K, Nosaka K, Edouard P, et al. Effects of a 5-h hilly running on ankle plantar and dorsal flexor force and fatigability. Eur J Appl Physiol. 2012;112(7):2645-52. https://doi.org/10.1007/s00421-011-2220-9
https://doi.org/10.1007/s00421-011-2220-...
). Haglund-Åkerlind and Eriksson (3131. Haglund-Akerlind Y, Eriksson E. Range of motion, muscle torque and training habits in runners with and without Achilles tendon problems. Knee Surg Sports Traumatol Arthrosc. 1993;1(3-4):195-9. https://doi.org/10.1007/BF01560205
https://doi.org/10.1007/BF01560205...
) found lower eccentric torque at 30°/s, 60°/s, and 120°/s in runners with AT than in runners without injury. Silbernagel et al. (22. Silbernagel KG, Gustavsson A, Thomeé R, Karlsson J. Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc. 2006;14(11):1207-17. https://doi.org/10.1007/s00167-006-0150-6
https://doi.org/10.1007/s00167-006-0150-...
) observed lower functional capacity in subjects with AT during jumping and strength tests. The Achilles tendon injury did not decrease the muscle performance in the ATG, which was the same as that in the HRG.

Muscle power and resistance are essential for performance in sports and for prevention of injury (22. Silbernagel KG, Gustavsson A, Thomeé R, Karlsson J. Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc. 2006;14(11):1207-17. https://doi.org/10.1007/s00167-006-0150-6
https://doi.org/10.1007/s00167-006-0150-...
). The plantar flexors exhibited lower total work in the ATG than in the HRG at a speed of 120°/s, corroborating the results reported by O’Neill et al. (3232. O’Neill S, Barry S, Watson P. Plantarflexor strength and endurance deficits associated with mid-portion Achilles tendinopathy: The role of soleus. Phys Ther Sport. 2019;37:69-76. https://doi.org/10.1016/j.ptsp.2019.03.002
https://doi.org/10.1016/j.ptsp.2019.03.0...
). These data show that endurance and fatigue can contribute to injury. Achilles tendon injury may result in decreased contractile capacity of the musculotendinous unit and increased susceptibility to muscle fatigue (1010. Carcia CR, Martin RL, Houck J, Wukich DK; Orthopaedic Section of the American Physical Therapy Association. Achilles pain, stiffness, and muscle power deficits: achilles tendinitis. J Orthop Sports Phys Ther. 2010;40(9):A1-26. https://doi.org/10.2519/jospt.2010.0305
https://doi.org/10.2519/jospt.2010.0305...
) with loss of performance over the time course of muscle activity.

Concentric and eccentric peak torque of the plantar flexors was higher in the ATG than in the NRG. The ATG and HRG exhibited similar eccentric torques. Hence, the injury might not have compromised the eccentric action. In contrast, decreased isokinetic plantar flexor strength is a risk factor for AT (3333. van der Vlist AC, Breda SJ, Oei EHG, Verhaar JAN, de Vos RJ. Clinical risk factors for Achilles tendinopathy: a systematic review. Br J Sports Med. 2019;53(21):1352-61. https://doi.org/10.1136/bjsports-2018-099991
https://doi.org/10.1136/bjsports-2018-09...
). This result is contrary to our hypothesis that runners with AT would exhibit lower muscle strength than runners without AT. Although multiple extrinsic factors are related to the injury (shoes, surface, environment, equipment, and training mistakes), it is widely known that trained athletes who perform strength training are stronger and faster than resistance athletes and non-trained individuals. Moreover, long-term low-intensity muscle training can modify the muscle profile and help in the treatment and prevention of injury (3434. Bogdanis GC. Effects of physical activity and inactivity on muscle fatigue. Front Physiol. 2012;3:142. https://doi.org/10.3389/fphys.2012.00142
https://doi.org/10.3389/fphys.2012.00142...
).

The interventions aimed at strength training have been reasonably effective in improving pain and disability in individuals with AT (3535. McAuliffe S, Tabuena A, McCreesh K, O’Keeffe M, Hurley J, Comyns T, et al. Altered Strength Profile in Achilles Tendinopathy: A Systematic Review and Meta-Analysis. J Athl Train. 2019;54(8):889-900. https://doi.org/10.4085/1062-6050-43-18
https://doi.org/10.4085/1062-6050-43-18...
). In this context, the observed data regarding GRF, force, and muscle resistance can help in improving rehabilitation programs for people with AT, in injury prevention, and in training preparation for competitions based on these specific variables. A better understanding of kinetic and isokinetic force biomechanics discussed in this study would help the professionals involved in studying the factors related to running and their relationship with AT. This in turn would promote better performance, functionality, and quality of life in clinical practice.

Haglund-Åkerlind and Eriksson (3131. Haglund-Akerlind Y, Eriksson E. Range of motion, muscle torque and training habits in runners with and without Achilles tendon problems. Knee Surg Sports Traumatol Arthrosc. 1993;1(3-4):195-9. https://doi.org/10.1007/BF01560205
https://doi.org/10.1007/BF01560205...
) observed lower eccentric torque values in runners with AT. Eccentric exercises to treat AT are still controversial, but they decrease pain and improve function (1010. Carcia CR, Martin RL, Houck J, Wukich DK; Orthopaedic Section of the American Physical Therapy Association. Achilles pain, stiffness, and muscle power deficits: achilles tendinitis. J Orthop Sports Phys Ther. 2010;40(9):A1-26. https://doi.org/10.2519/jospt.2010.0305
https://doi.org/10.2519/jospt.2010.0305...
,1111. Maffulli N, Via AG, Oliva F. Chronic Achilles Tendon Disorders: Tendinopathy and Chronic Rupture. Clin Sports Med. 2015;34(4):607-24. https://doi.org/10.1016/j.csm.2015.06.010
https://doi.org/10.1016/j.csm.2015.06.01...
,1717. Kim S, Yu J. Changes of gait parameters and lower limb dynamics in recreational runners with achilles tendinopathy. J Sports Sci Med. 2015;14(2):284-9.,2323. Baur H, Müller S, Hirschmüller A, Cassel M, Weber J, Mayer F. Comparison in lower leg neuromuscular activity between runners with unilateral mid-portion Achilles tendinopathy and healthy individuals. J Electromyogr Kinesiol. 2011;21(3):499-505. https://doi.org/10.1016/j.jelekin.2010.11.010
https://doi.org/10.1016/j.jelekin.2010.1...
). AT is associated with different biomechanical and functional alterations including tendinopathy-induced muscle weakness and imbalance that modifies the landing pattern.

The comparison of the muscle and running kinetic conditions among the three groups revealed the low morbidity of the injury. There were many differences between the NRG and the two runner groups. The slow evolution of calcaneal tendon injury with progressive loss of function allowed the maintenance of running practice and contributed to the homogenization of the runner groups in this study. This characteristic of a calcaneal tendon injury might be considered a limitation of the present study, as it would require a larger sample size to obtain significant data. Another limitation was the difficulty in collecting running-related data in a laboratory environment, which can inhibit the execution of natural gestures involved in sports.

However, some clinical implications need to be considered. In the present study, the ATG exhibited increased initial impulse and loss of muscle endurance. These functional changes may be related to the development of tendinopathy. If not corrected, the injury could worsen or result in disability. In runners, assessments of muscle condition (performance and balance) and GRF are essential for maintaining biomechanically safe and functional gestures. Difficulties in assessing running as well as multiple factors related to a calcaneal tendon injury and its insidious evolution contribute to controversies regarding the etiopathogenesis, biomechanical aspects, prevention, and treatment of AT, highlighting the need for further studies. The follow-up of the groups of lifelong runners with successive assessments can help clarify these controversies. We observed a difference in the mean age between the NRG and ATG, which was an allocation problem for the participants.

CONCLUSION

Runners with AT exhibited higher strike impulse, lower plantar flexor strength (resistance), and higher clinical and functional damage. The association between higher strike impulse and lower resistance could be a predisposing and maintaining factor for Achilles tendon injury. Runners with AT have altered plantar flexor muscles and such conditions alter their foot strike pattern during running.

ACKNOWLEDGMENTS

The authors gratefully acknowledge the financial support provided by Fundação de Amparo è Pesquisa do Estado de São Paulo (11/52026-8) and Nathalie Ferrari Bechara Andere (Master scholarship). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001. We would also like to thank the Anima Institute.

REFERENCES

  • 1
    Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwellnus MP. Biomechanical variables associated with Achilles tendinopathy in runners. Br J Sports Med. 2009;43(4):288-92. https://doi.org/10.1136/bjsm.2008.053421
    » https://doi.org/10.1136/bjsm.2008.053421
  • 2
    Silbernagel KG, Gustavsson A, Thomeé R, Karlsson J. Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc. 2006;14(11):1207-17. https://doi.org/10.1007/s00167-006-0150-6
    » https://doi.org/10.1007/s00167-006-0150-6
  • 3
    Longo UG, Rittweger J, Garau G, Radonic B, Gutwasser C, Gilliver SF, et al. No influence of age, gender, weight, height, and impact profile in achilles tendinopathy in masters track and field athletes. Am J Sports Med. 2009;37(7):1400-5. https://doi.org/10.1177/0363546509332250
    » https://doi.org/10.1177/0363546509332250
  • 4
    Maffulli N, Kader D. Tendinopathy of tendo achillis. J Bone Joint Surg Br. 2002;84(1):1-8. https://doi.org/10.1302/0301-620X.84B1.0840001
    » https://doi.org/10.1302/0301-620X.84B1.0840001
  • 5
    Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clin Sports Med. 2003;22(4):675-92. https://doi.org/10.1016/S0278-5919(03)00004-8
    » https://doi.org/10.1016/S0278-5919(03)00004-8
  • 6
    Munteanu SE, Barton CJ. Lower limb biomechanics during running in individuals with achilles tendinopathy: a systematic review. J Foot Ankle Res. 2011;4:15. https://doi.org/10.1186/1757-1146-4-15
    » https://doi.org/10.1186/1757-1146-4-15
  • 7
    Reule CA, Alt WW, Lohrer H, Hochwald H. Spatial orientation of the subtalar joint axis is different in subjects with and without Achilles tendon disorders. Br J Sports Med. 2011;45(13):1029-34. https://doi.org/10.1136/bjsm.2010.080119
    » https://doi.org/10.1136/bjsm.2010.080119
  • 8
    Lorimer AV, Hume PA. Achilles tendon injury risk factors associated with running. Sports Med. 2014;44(10):1459-72. https://doi.org/10.1007/s40279-014-0209-3
    » https://doi.org/10.1007/s40279-014-0209-3
  • 9
    Alfredson H, Lorentzon R. Chronic Achilles tendinosis: recommendations for treatment and prevention. Sports Med. 2000;29(2):135-46. https://doi.org/10.2165/00007256-200029020-00005
    » https://doi.org/10.2165/00007256-200029020-00005
  • 10
    Carcia CR, Martin RL, Houck J, Wukich DK; Orthopaedic Section of the American Physical Therapy Association. Achilles pain, stiffness, and muscle power deficits: achilles tendinitis. J Orthop Sports Phys Ther. 2010;40(9):A1-26. https://doi.org/10.2519/jospt.2010.0305
    » https://doi.org/10.2519/jospt.2010.0305
  • 11
    Maffulli N, Via AG, Oliva F. Chronic Achilles Tendon Disorders: Tendinopathy and Chronic Rupture. Clin Sports Med. 2015;34(4):607-24. https://doi.org/10.1016/j.csm.2015.06.010
    » https://doi.org/10.1016/j.csm.2015.06.010
  • 12
    Mahieu NN, Witvrouw E, Stevens V, Van Tiggelen D, Roget P. Intrinsic risk factors for the development of achilles tendon overuse injury: a prospective study. Am J Sports Med. 2006;34(2):226-35. https://doi.org/10.1177/0363546505279918
    » https://doi.org/10.1177/0363546505279918
  • 13
    McCrory JL, Martin DF, Lowery RB, Cannon DW, Curl WW, Read HM Jr, et al. Etiologic factors associated with Achilles tendinitis in runners. Med Sci Sports Exerc. 1999;31(10):1374-81. https://doi.org/10.1097/00005768-199910000-00003
    » https://doi.org/10.1097/00005768-199910000-00003
  • 14
    Zafar MS, Mahmood A, Maffulli N. Basic science and clinical aspects of achilles tendinopathy. Sports Med Arthrosc Rev. 2009;17(3):190-7. https://doi.org/10.1097/JSA.0b013e3181b37eb7
    » https://doi.org/10.1097/JSA.0b013e3181b37eb7
  • 15
    Kannus P. Etiology and pathophysiology of chronic tendon disorders in sports. Scand J Med Sci Sports. 1997;7(2):78-85. https://doi.org/10.1111/j.1600-0838.1997.tb00123.x
    » https://doi.org/10.1111/j.1600-0838.1997.tb00123.x
  • 16
    Van Ginckel A, Thijs Y, Hesar NG, Mahieu N, De Clercq D, Roosen P, et al. Intrinsic gait-related risk factors for Achilles tendinopathy in novice runners: a prospective study. Gait Posture. 2009;29(3):387-91. https://doi.org/10.1016/j.gaitpost.2008.10.058
    » https://doi.org/10.1016/j.gaitpost.2008.10.058
  • 17
    Kim S, Yu J. Changes of gait parameters and lower limb dynamics in recreational runners with achilles tendinopathy. J Sports Sci Med. 2015;14(2):284-9.
  • 18
    Ogbonmwan I, Kumar BD, Paton B. New lower-limb gait biomechanical characteristics in individuals with Achilles tendinopathy: A systematic review update. Gait Posture. 2018;62:146-56. https://doi.org/10.1016/j.gaitpost.2018.03.010
    » https://doi.org/10.1016/j.gaitpost.2018.03.010
  • 19
    Hreljac A. Impact and overuse injuries in runners. Med Sci Sports Exerc. 2004;36(5):845-9. https://doi.org/10.1249/01.MSS.0000126803.66636.DD
    » https://doi.org/10.1249/01.MSS.0000126803.66636.DD
  • 20
    Robbins SE, Hanna AM. Running-related injury prevention through barefoot adaptations. Med Sci Sports Exerc. 1987;19(2):148-56. https://doi.org/10.1249/00005768-198704000-00014
    » https://doi.org/10.1249/00005768-198704000-00014
  • 21
    Alentorn-Geli E, Samuelsson K, Musahl V, Green CL, Bhandari M, Karlsson J. The Association of Recreational and Competitive Running With Hip and Knee Osteoarthritis: A Systematic Review and Meta-analysis. J Orthop Sports Phys Ther. 2017;47(6):373-90. https://doi.org/10.2519/jospt.2017.7137
    » https://doi.org/10.2519/jospt.2017.7137
  • 22
    Lins C, Ninomya AF, Bittar CK, de Carvalho AE Jr, Cliquet A Jr. Kinetic and kinematic evaluation of the ankle joint after achilles tendon reconstruction with free semitendinosus tendon graft: preliminary results. Artif Organs. 2013;37(3):291-7. https://doi.org/10.1111/j.1525-1594.2012.01559.x
    » https://doi.org/10.1111/j.1525-1594.2012.01559.x
  • 23
    Baur H, Müller S, Hirschmüller A, Cassel M, Weber J, Mayer F. Comparison in lower leg neuromuscular activity between runners with unilateral mid-portion Achilles tendinopathy and healthy individuals. J Electromyogr Kinesiol. 2011;21(3):499-505. https://doi.org/10.1016/j.jelekin.2010.11.010
    » https://doi.org/10.1016/j.jelekin.2010.11.010
  • 24
    Luna NM, Alonso AC, Brech GC, Mochizuki L, Nakano EY, Greve JM. Isokinetic analysis of ankle and ground reaction forces in runners and triathletes. Clinics (Sao Paulo). 2012;67(9):1023-8. https://doi.org/10.6061/clinics/2012(09)07
    » https://doi.org/10.6061/clinics/2012(09)07
  • 25
    Möller M, Lind K, Styf J, Karlsson J. The reliability of isokinetic testing of the ankle joint and a heel-raise test for endurance. Knee Surg Sports Traumatol Arthrosc. 2005;13(1):60-71. https://doi.org/10.1007/s00167-003-0441-0
    » https://doi.org/10.1007/s00167-003-0441-0
  • 26
    Milner CE, Ferber R, Pollard CD, Hamill J, Davis IS. Biomechanical factors associated with tibial stress fracture in female runners. Med Sci Sports Exerc. 2006;38(2):323-8. https://doi.org/10.1249/01.mss.0000183477.75808.92
    » https://doi.org/10.1249/01.mss.0000183477.75808.92
  • 27
    Chang R, Rodrigues PA, Van Emmerik RE, Hamill J. Multi-segment foot kinematics and ground reaction forces during gait of individuals with plantar fasciitis. J Biomech. 2014;47(11):2571-7. https://doi.org/10.1016/j.jbiomech.2014.06.003
    » https://doi.org/10.1016/j.jbiomech.2014.06.003
  • 28
    Wyndow N, Cowan SM, Wrigley TV, Crossley KM. Triceps surae activation is altered in male runners with Achilles tendinopathy. J Electromyogr Kinesiol. 2013;23(1):166-72. https://doi.org/10.1016/j.jelekin.2012.08.010
    » https://doi.org/10.1016/j.jelekin.2012.08.010
  • 29
    So CH, Siu TO, Chan KM, Chin MK, Li CT. Isokinetic profile of dorsiflexors and plantar flexors of the ankle - A comparative study of élite versus untrained subjects. Br J Sports Med. 1994;28(1):25-30. https://doi.org/10.1136/bjsm.28.1.25
    » https://doi.org/10.1136/bjsm.28.1.25
  • 30
    Fourchet F, Millet GP, Tomazin K, Guex K, Nosaka K, Edouard P, et al. Effects of a 5-h hilly running on ankle plantar and dorsal flexor force and fatigability. Eur J Appl Physiol. 2012;112(7):2645-52. https://doi.org/10.1007/s00421-011-2220-9
    » https://doi.org/10.1007/s00421-011-2220-9
  • 31
    Haglund-Akerlind Y, Eriksson E. Range of motion, muscle torque and training habits in runners with and without Achilles tendon problems. Knee Surg Sports Traumatol Arthrosc. 1993;1(3-4):195-9. https://doi.org/10.1007/BF01560205
    » https://doi.org/10.1007/BF01560205
  • 32
    O’Neill S, Barry S, Watson P. Plantarflexor strength and endurance deficits associated with mid-portion Achilles tendinopathy: The role of soleus. Phys Ther Sport. 2019;37:69-76. https://doi.org/10.1016/j.ptsp.2019.03.002
    » https://doi.org/10.1016/j.ptsp.2019.03.002
  • 33
    van der Vlist AC, Breda SJ, Oei EHG, Verhaar JAN, de Vos RJ. Clinical risk factors for Achilles tendinopathy: a systematic review. Br J Sports Med. 2019;53(21):1352-61. https://doi.org/10.1136/bjsports-2018-099991
    » https://doi.org/10.1136/bjsports-2018-099991
  • 34
    Bogdanis GC. Effects of physical activity and inactivity on muscle fatigue. Front Physiol. 2012;3:142. https://doi.org/10.3389/fphys.2012.00142
    » https://doi.org/10.3389/fphys.2012.00142
  • 35
    McAuliffe S, Tabuena A, McCreesh K, O’Keeffe M, Hurley J, Comyns T, et al. Altered Strength Profile in Achilles Tendinopathy: A Systematic Review and Meta-Analysis. J Athl Train. 2019;54(8):889-900. https://doi.org/10.4085/1062-6050-43-18
    » https://doi.org/10.4085/1062-6050-43-18
  • Errata

    CLINICS (Sao Paulo). 2021;76:e2803err
    Erratum for: doi: https://doi.org/10.6061/clinics/2021/e2803, published in 2021.
    In the article Biomechanical evaluation in runners with Achilles tendinopathy
    Replace “Alexandre Leme Godoy” and “Andere NFB, Godoy AL, Mochizuki L, Rodrigues MB, Fernandes TD, Soares-Júnior JM, et al. Biomechanical evaluation in runners with Achilles tendinopathy. Clinics (Sao Paulo). 2021;76:e2803” for:
    “Alexandre Leme Godoy-Santos” and “Andere NFB, Godoy-Santos AL, Mochizuki L, Rodrigues MB, Fernandes TD, Soares-Júnior JM, et al. Biomechanical evaluation in runners with Achilles tendinopathy. Clinics (Sao Paulo). 2021;76:e2803”
    and Page 5 – AUTHOR CONTRIBUTIONS
    where it reads “Godoy AL” replace for “Godoy-Santos AL”

Publication Dates

  • Publication in this collection
    27 May 2021
  • Date of issue
    2021

History

  • Received
    25 Jan 2021
  • Accepted
    22 Apr 2021
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