AbstractBackground

Calcaneal fractures result in severe functional impairments and walking restrictions. Postoperative evaluation mainly focusses on the restoration of calcaneal anatomy while ankle plantar flexor insufficiency remains largely neglected. This study aims to investigate biomechanical and morphologic adaptions of elastic and contractile components of the gastrocnemius medialis after unilateral calcaneal fracture.

Methods

20 Patients (BMI: 27.6 ± 3.1 kgm−2, Age: 50 ± 12 years) were measured using gait analysis and portable ultrasound over a follow-up of three, six and twelve months after surgery. Data comparison was performed using 20 matched healthy controls (BMI: 26.2 ± 2.9 kgm−2, Age: 48 ± 11 years). Static and dynamic behavior of the gastrocnemius muscle tendon unit, muscle fascicle and the serial-elastic element as well ankle joint kinematics and kinetics were analyzed.

Findings

Within patients, a significant (p < 0.05) increase in fascicle length (by 67%) during single support and a decrease of serial elastic element shortening (by 20%) during push off was found between three and twelve months follow-up comparisons. Patients showed differences for fascicle lengthening and pennation angle increase during single support after three and six months compared to healthy controls. A smaller shortening of the serial-elastic element (by 29%) and muscle-tendon unit (by 16%) persisted even for the twelve month comparisons.

Interpretation

Patients with calcaneal fracture showed an incomplete restoration of the medial gastrocnemius dynamic morphological behavior. While muscle fascicle contraction almost recovered, the serial elastic component still showed restrictions regarding its shortening behavior. Limited foot mobility and plantarflexor strength as well as lowered responsiveness of elastic tissues to mechanical loading are regarded as key mechanisms.

1. IntroductionFractures of the calcaneus can cause severe restrictions of dynamic foot function which often lead to large periods of working disability and considerable socioeconomic costs (; Biz et al., 2016Biz C. Barison E. Ruggieri P. Iacobellis C. Radiographic and functional outcomes after displaced intra-articular calcaneal fractures: a comparative cohort study among the traditional open technique (ORIF) and percutaneous surgical procedures (PS).; Sanders et al., 1993Sanders R. Fortin P. DiPasquale T. Walling A. Operative treatment in 120 displaced intraarticular calcaneal fractures: results using a prognostic computed tomography scan classification.). Although great efforts in the treatment of calcaneal fractures (CF) have been made, the functional outcome often remains unsatisfying with considerable restrictions of dynamic foot mobility and insufficiency of plantar flexor muscles (Bozkurt et al., 2004Bozkurt M. Kentel B.B. Yavuzer G. Oçgüder A. Heycan C. Tonuk E. Functional evaluation of intraarticular severely comminuted fractures of the calcaneus with gait analysis.; Hirschmüller et al., 2011Hirschmüller A. Konstantinidis L. Baur H. Müller S. Mehlhorn A. Kontermann J. Grosse U. Südkamp N.P. Helwig P. Do changes in dynamic plantar pressure distribution, strength capacity and postural control after intra-articular calcaneal fracture correlate with clinical and radiological outcome?.; Rosenbaum et al., 1996Rosenbaum D. Bauer G. Augat P. Claes L. Calcaneal fractures cause a lateral load shift in Chopart joint contact stress and plantar pressure pattern in vitro.). While clinicians primarily focus on anatomical restoration of the calcaneus using radiography, pathologic structural adaptions of the plantar flexors remain unconsidered. Even two years after a CF dynamic ankle plantar flexion power has not been completely recovered (Bozkurt et al., 2004Bozkurt M. Kentel B.B. Yavuzer G. Oçgüder A. Heycan C. Tonuk E. Functional evaluation of intraarticular severely comminuted fractures of the calcaneus with gait analysis.). This insufficiency and an altered mechanical behavior of the triceps surae play an important role in the healing process and regaining foot mobility.Immobilization is a major determinant for the development of musculoskeletal changes after trauma. However, there seems to be an inequality in the time ratio between tissue quality loss and regeneration. Restoration of muscle and tendon morphology is slow and it is unclear whether a normal state can be completely regained (Kannus et al., 1992Kannus P. Jozsa L. Renström P. Järvinen M. Kvist M. Lehto M. Oja P. Vuort I. The effects of training, immobilization and remobilization on musculoskeletal tissue: 2. Remobilization and prevention of immobilization atrophy.). Muscle atrophy is widely observed due to prolonged immobilization after surgical interventions. Patients with CF follow long immobilization periods including cast immobilization and non-weightbearing of up to twelve weeks after surgery (De Boer et al., 2015De Boer A.S. Van Lieshout E.M.M. Den Hartog D. Weerts B. Verhofstad M.H.J. Schepers T. Functional outcome and patient satisfaction after displaced intra-articular calcaneal fractures: a comparison among open, percutaneous, and nonoperative treatment.). This often results into high rates of calf muscle atrophy (reductions by up to 3 cm of calf circumference) that persist even one year after trauma, indicating that the restoration of musculoskeletal tissue remains decreased or might even tend to deteriorate (Follak and Merk, 2003The benefit of gait analysis in functional diagnostics in the rehabilitation of patients after operative treatment of calcaneal fractures.; Hirschmüller et al., 2011Hirschmüller A. Konstantinidis L. Baur H. Müller S. Mehlhorn A. Kontermann J. Grosse U. Südkamp N.P. Helwig P. Do changes in dynamic plantar pressure distribution, strength capacity and postural control after intra-articular calcaneal fracture correlate with clinical and radiological outcome?.; Kitaoka et al., 1994Kitaoka H.B. Schaap E.J. Chao E.Y.S. An K.N. Displaced intra-articular fractures of the calcaneus treated non- operatively. Clinical results and analysis of motion and ground-reaction and temporal forces.). Trauma and disuse could also have a significant effect on mechanical tendon properties. In this context, decreased stiffness of lower limb tendons and aponeuroses (up to 67%) as well as reduced tendon force (up to 36%) was found after several weeks of immobilization (Kannus et al., 1992Kannus P. Jozsa L. Renström P. Järvinen M. Kvist M. Lehto M. Oja P. Vuort I. The effects of training, immobilization and remobilization on musculoskeletal tissue: 2. Remobilization and prevention of immobilization atrophy.; Kubo et al., 2000Kubo K. Akima H. Kouzaki M. Ito M. Kawakami Y. Kanehisa H. Fukunaga T. Changes in the elastic properties of tendon structures following 20 days bed-rest in humans.). Reductions of tendon stiffness could result in a relevant decrease of muscle strength and the ability of muscle fascicles to transfer force to the tendon. However, the investigation of the dynamic behavior of muscle structural tissues after trauma is rare and practically nothing is known about potential biomechanical adaptions that occur due to muscular deficits after CF.Sonographic measurements of dynamic muscle structure behavior have demonstrated that an almost isometric contraction of fascicles during mid-stance and simultaneous stretch-shortening behavior of serial-elastic tissues are a main mechanism for generating an efficient power output during walking (Fukunaga et al., 2001Fukunaga T. Kubo K. Kawakami Y. Fukashiro S. Kanehisa H. Maganaris C.N. In vivo behaviour of human muscle tendon during walking.; Lichtwark and Wilson, 2006Lichtwark G.A. Wilson A.M. Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion.). Clinically, abnormal behavior of muscle structure will have a large impact on force potential, and decreased tissue quality might even lead to permanent muscle damage (Rader and Faulkner, 2006Recovery from contraction-induced injury is impaired in weight-bearing muscles of old male mice.). However, it is unclear if and to what extent the interaction between fascicles and elastic tissue during movement is altered and whether structural changes can be completely restored during the healing process after trauma.

The main research objective of this study is to provide information regarding dynamic structural adaptions of the gastrocnemius medialis as a main ankle plantar flexor, after CF. We want to know, how muscle fascicles and serial elastic components contribute to the limited function of the ankle plantar flexors during walking. We hypothesize that during a follow-up period of three, six and twelve months, a difference in static and dynamic muscle structure behavior of the gastrocnemius medialis in patients after unilateral CF is observed. We further hypothesize that patients with CF show an altered dynamic behavior of muscle-tendon components when compared to healthy controls.

4. Discussion

This study investigated the static and dynamic muscle structural behavior and morphological adaptions of the gastrocnemius medialis muscle after surgically treated unilateral CF. Our findings indicate that both, serial-elastic (tendons with aponeuroses) and contractile (muscle fascicles) components recovered in a different way. Twelve months after surgery, fascicles of the medial gastrocnemius showed an almost similar movement behavior compared to healthy controls, while elastic components still demonstrated some considerable differences. Regarding the identification of differences in static and dynamic muscle structure behavior during follow-up (first study hypothesis), only an incomplete recovery towards a physiologic muscle structural behavior could be observed in patients with CF. Regarding the detection of an altered muscle-tendon behavior when compared to healthy controls (second study hypothesis) and supported by strong effect sizes, we could confirm relevant muscle structural differences regarding changes of fascicle length, pennation angle, muscle tendon unit length and serial elastic element length. These differences mainly occurred during supportive and propulsive gait phases such as single support and push-off.

In patients with CF, muscle fascicles during single support showed an increase in fascicle length and a simultaneous decrease of pennation angle after three and six months. During locomotion gastrocnemius fascicles usually follow an almost isometric behavior in order to transfer mechanical energy to the tendon (Lichtwark et al., 2007Lichtwark G.A. Bougoulias K. Wilson A.M. Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running.). The observed non-isometric fascicle movement in our patients indicated a restricted and energetically inefficient function of the gastrocnemius muscle during locomotion. It might be assumed that an increased dorsiflexion of the ankle joint during single support which would induce a passive stretch on the muscle belly and fascicles might explain our findings (Kitaoka et al., 1994Kitaoka H.B. Schaap E.J. Chao E.Y.S. An K.N. Displaced intra-articular fractures of the calcaneus treated non- operatively. Clinical results and analysis of motion and ground-reaction and temporal forces.; van Hoeve et al., 2015van Hoeve S. de Vos K. Verbruggen J. Willems P. Meijer K. Poeze M. Gait analysis and functional outcome after calcaneal fracture.). However, in our study, maximum ankle dorsiflexion angles as well as ankle range of motion during single support were almost comparable with controls and showed no differences between follow-up measurements in our patients. Therefore, a compensatory ankle joint movement during locomotion may not entirely explain an increased fascicle lengthening during single support phase. In this context, the observed non-physiologic fascicle behavior might be more related to residual strength deficits of the plantar flexors that are frequently observed in patients with CF (Bozkurt et al., 2004Bozkurt M. Kentel B.B. Yavuzer G. Oçgüder A. Heycan C. Tonuk E. Functional evaluation of intraarticular severely comminuted fractures of the calcaneus with gait analysis.; Brand et al., 2019Brand A. Klöpfer-Krämer I. Böttger M. Kröger I. Gaul L. Wackerle H. Müßig J.A. Dietrich A. Gabel J. Augat P. Gait characteristics and functional outcomes during early follow-up are comparable in patients with calcaneal fractures treated by either the sinus tarsi or the extended lateral approach.). In our study, an indication of the decreased plantar flexor strength could be related to the severely diminished maximum ankle joint moments during the last third of stance phase especially three and six-months after surgery. It might be assumed that less resistance of the gastrocnemius fascicles to the tensile forces during single support resulted in an increased fascicle lengthening. This consequently decreases the amount of elastic energy storage and release in tendinous tissues (Fry et al., 2006Fry N.R. Perrot M. Morrissey M. Shortland A.P. Dynamic measurement of gastrocnemius tendon and belly length during heel-toe and toe-walking in normally developingchildren and adults.; Fukunaga et al., 2001Fukunaga T. Kubo K. Kawakami Y. Fukashiro S. Kanehisa H. Maganaris C.N. In vivo behaviour of human muscle tendon during walking.).Factors such as posttraumatic immobilization and its effect on fibre type composition (slow – to fast-twitch transformation) and mechanical properties (decrease in stiffness) could also explain the altered muscle structural behavior (Blazevich, 2006Effects of physical training and detraining, immobilisation, growth and aging on human fascicle geometry.). In this context, our patients followed a standard aftercare protocol of up to eight weeks of cast immobilization with partial weight bearing which could have induced structural remodeling of muscle morphology. This might be an explanation for the increased gastrocnemius fascicle stretch and less compliant elastic tissues that both would contribute to a loss of mechanical power that needs to be transferred to the foot during locomotion (Bozkurt et al., 2004Bozkurt M. Kentel B.B. Yavuzer G. Oçgüder A. Heycan C. Tonuk E. Functional evaluation of intraarticular severely comminuted fractures of the calcaneus with gait analysis.; Lichtwark et al., 2007Lichtwark G.A. Bougoulias K. Wilson A.M. Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running.). In our patients with CF, this effect could be also observed by the lowered serial elastic element elongation during single support and reduced shortening during push-off, which persisted even one year after surgery. Due to this reduced stretch, less recoil of the serial elastic element could be transferred to generate adequate dynamic ankle joint push-off power.From a biological perspective, de-tensioning also removes the constant mechanotransduction on elastic tissues such as tendons and aponeuroses and therefore might decrease the expression of collagen type I and inflammatory signaling markers which are important for the mechanical adaption to exercise (). In contrast to muscle fascicle behavior, the decreased serial elastic element lengthening and shortening behavior during walking even persisted after the twelve months when compared to healthy controls. This is supported by previous findings, that elastic tissues such as tendons generally show a different responsiveness to mechanical loading than muscle fascicles, and that a normal function may not be achieved within one year after surgery (M. D. de Boer et al., 2007de Boer M.D. Maganaris C.N. Seynnes O.R. Rennie M.J. Narici M.V. Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men.; Kubo et al., 2010Kubo K. Ikebukuro T. Yata H. Tsunoda N. Kanehisa H. Time course of changes in muscle and tendon properties during strength training and detraining.; ).To counteract these issues, training interventions that increase tendon stiffness and fascicle tensile stress resistance by applying higher loading intensities (> 70% of maximum voluntary contraction) at longer intervention duration (> twelve weeks) in the early rehabilitation phase might serve as a potential therapeutic strategy (Bohm et al., 2015Bohm S. Mersmann F. Arampatzis A. Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults.; Kubo et al., 2010Kubo K. Ikebukuro T. Yata H. Tsunoda N. Kanehisa H. Time course of changes in muscle and tendon properties during strength training and detraining.). In this context, interdisciplinary collaboration between orthopedic surgeons, sports technicians and physical therapists is essential to improve muscular recovery in patients with CF.Nonetheless, other confounding factors such as compensatory unloading of the ankle joint as well as an insufficient calcaneal restoration might contribute to long-lasting or even irreversible effects on elastic components during walking (Blazevich, 2006Effects of physical training and detraining, immobilisation, growth and aging on human fascicle geometry.; Kitaoka et al., 1994Kitaoka H.B. Schaap E.J. Chao E.Y.S. An K.N. Displaced intra-articular fractures of the calcaneus treated non- operatively. Clinical results and analysis of motion and ground-reaction and temporal forces.; ). In this context, radiographic parameters, such as Böhler's angle, Gissanes angle, talocalcaneal angle or absolute foot height revealed significant intra-individual differences between the injured (fractured) and uninjured side (Schepers et al., 2007Schepers T. Ginai A.Z. Mulder P.G.H. Patka P. Radiographic evaluation of calcaneal fractures: to measure or not to measure.). Future studies might focus on long-term investigations regarding the interaction between dynamic muscle function and restored bony anatomy of the calcaneus.As shown in our study, static measurements of muscle properties only partly reflected morphological adaptions of muscles and did not provide sufficient information about functional adaptions. Static fascicle length measures showed no differences within patients and when compared to healthy controls, while dynamic measures revealed meaningful differences in terms of isometric (healthy) and a non-isometric (CF) fascicle behavior. This generally supports the clinical importance of dynamic muscle structure analysis to evaluate morphological adaptions of muscles and tendons after trauma ().This study has some limitations. Morphologic analyses were only conducted for the medial gastrocnemius and therefore cannot reflect the biomechanical behavior of the entire plantar-flexor muscle group. Differences in the dynamic mechanical behavior between uniarticular (Soleus) and biarticular (Gastrocnemius) muscles were identified in previous studies (Cronin et al., 2013Cronin N.J. Avela J. Finni T. Peltonen J. Differences in contractile behaviour between the soleus and medial gastrocnemius muscles during human walking.; Ishikawa et al., 2005Ishikawa M. Komi P.V. Grey M.J. Lepola V. Bruggemann G.P. Muscle-tendon interaction and elastic energy usage in human walking.). This indicates that, during walking, single ankle plantar flexors might not be considered as unique synergists during gait especially in clinical populations and that additional information is needed to provide a complete understanding of their morphologic behavior. Using 2D ultrasound in dynamic muscle analysis limits the information on fascicle measures since tracked fascicles tend to rotate and change their curvature during contraction and may move outside of the 2D image plane (Bolsterlee et al., 2016Bolsterlee B. Gandevia S.C. Herbert R.D. Ultrasound imaging of the human medial gastrocnemius muscle: how to orient the transducer so that muscle fascicles lie in the image plane.; Muramatsu et al., 2002Muramatsu T. Muraoka T. Kawakami Y. Shibayamaand A. Fukunaga T. In vivo determination of fascicle curvature in contracting human skeletal muscles.). Although correct probe alignment reduces fascicle misestimations, interpretation of fascicle data is still limited. Muscle tendon unit estimation was only obtained using one static knee and ankle joint moment arm. Since changes in moment arm during gait were not considered, especially knee moment arms might be overestimated and would result in an altered gastrocnemius length (Yuen and Orendurff, 2006A comparison of gastrocnemius muscle-tendon unit length during gait using anatomic, cadaveric and MRI models.). Regarding elastic components we only analyzed combined tendon and aponeurosis movement of the medial gastrocnemius which cannot represent isolated tendon (Achilles tendon) behavior during walking. In this context, the Achilles tendon is a complex structure of different subtendons demonstrating inhomogeneous functional loading deformations and intertendon sliding during walking (Farris et al., 2013Farris D.J. Trewartha G. McGuigan M.P. Lichtwark G.A. Differential strain patterns of the human Achilles tendon determined in vivo with freehand three-dimensional ultrasound imaging.; Franz et al., 2015Franz J.R. Slane L.C. Rasske K. Thelen D.G. Non-uniform in vivo deformations of the human Achilles tendon during walking.). Future research regarding dynamic tendon analysis and posttraumatic adaption is needed to provide a complete understanding about the clinical rehabilitation process in patients with CF or other comparable foot and ankle pathologies.CRediT authorship contribution statement

Andreas Brand: Conceptualization, Project administration, Methodology, Investigation, Formal analysis, Funding acquisition, Writing – original draft, Writing – review & editing. Inga Kröger: Investigation, Formal analysis, Writing – review & editing. Isabella Klöpfer-Krämer: Investigation, Funding acquisition, Writing – review & editing. Hannes Wackerle: Investigation, Writing – review & editing. Janina Anna Müßig: Investigation, Writing – review & editing. Andrea Dietrich: Resources, Writing – review & editing. Moritz Böttger: Resources, Writing – review & editing. Leander Gaul: Resources, Writing – review & editing. Johannes Gabel: Supervision, Resources. Peter Augat: Supervision, Conceptualization, Methodology, Formal analysis, Funding acquisition, Writing – original draft, Writing – review & editing.