Abstract
The purpose of this study was to quantify isolated coupling mechanisms of calcaneal adduction/abduction and calcaneal eversion/inversion to proximal bones in vitro. The in vitro approach is necessary because in vivo both movements appear together, making it impossible to determine the extent of their individual contribution to overall ankle joint coupling. Eight fresh frozen foot‐leg specimens were tested. Data describing bone orientation and coupling mechanisms between segments were obtained using bone pin marker triads. The bone movement was described in a global coordinate system to examine the coupling between the calcaneus, talus and tibia. The strength of coupling was determined by means of the slope of a linear least squares fit to an angle–angle plot. The coupling coefficients in the present study indicate that not only calcaneal eversion/inversion (coupling coefficient: 0.68 ± 0.15) but to an even greater extent calcaneal adduction/abduction (coupling coefficient: 0.99 ± 0.10) was transferred into talus and tibial rotation, highlighting the relevance of calcaneal adduction for the overall ankle joint coupling. The results of this study present the possibility that controlling calcaneal adduction/abduction can affect talus and tibial rotation and therefore the possible genesis of overuse knee injuries.
Keywords: ankle joint, locomotion, movement coupling, overuse injury
Introduction
In running, the movement of the rear foot and the shank are coupled mechanically through two functional axes: the subtalar joint axis, describing motion between the talus and the calcaneus, and the talocrural joint axis, describing motion between the tibia and the talus. Due to the oblique orientation of these anatomical axes and the influence of other anatomical characteristics, rearfoot eversion affects tibial rotation (Hicks, 1953; Inman, 1976; McClay & Manal, 1997; Fischer et al. 2017b).
This coupling mechanism has been described in several publications (Stacoff et al. 2000; Arndt et al. 2004, 2007). Excessive internal tibial rotation may result in load redistribution at the knee joint and has been postulated as a causative factor of knee pain in runners (James et al. 1978; Clement et al. 1981; Tiberio, 1987; Bahlsen, 1988; Noehren et al. 2006, 2007; Hamill et al. 2008). Depending on interindividual mechanical coupling characteristics conditioned by, for example, joint congruency or stiffness of ligaments surrounding the joint, large variations in the movement transfer between specimens were detected in vitro (Hintermann et al. 1994). These results indicate that not only the amount of rearfoot eversion but also more importantly the mechanism of transfer of eversion into tibial rotation might be a key factor in the development of knee pain.
To understand underlying mechanisms in the aetiology of knee pain, calcaneus movement or, more specifically, coupling mechanisms at the subtalar and talocrural joints need to be determined accurately.
In vivo studies using intracortical pins have provided a description of foot bone kinematics during walking (Arndt et al. 2004; Lundgren et al. 2008) and slow running (Arndt et al. 2007). Nonetheless, Arndt et al. (2007) provide evidence that joint rotations between the calcaneus and talus occur not only as eversion/inversion in the frontal plane (range of motion, RoM: 8.9°) but also as adduction/abduction in the transverse plane (RoM: 5.9 degrees) and in the sagittal plan (RoM: 5.7°). Furthermore, in a biplanar X‐ray study describing the effect of footwear on three‐dimensional talocrural and subtalar joint motion during running, Peltz et al. (2014) found a significantly greater transverse range of motion at the talocrural joint in the barefoot condition compared with two shoe conditions.
Recent in vivo research using skin‐mounted markers suggests that rearfoot movement in the transverse plane (i.e. rearfoot adduction/abduction) must also be considered given a significant correlation between rearfoot adduction and tibial rotation in running (Fischer et al. 2017b). The partial correlation for rearfoot adduction and tibial rotation was even stronger than for rearfoot eversion. Similar results were found by means of a bone‐anchored marker approach to determine the actual bone movement of the calcaneus and the tibia and to describe the relation between both bones during running (Fischer et al. 2017a).
The oblique ankle joint axis implies that during running, both rearfoot frontal and transverse plane movement appear simultaneously. Nonetheless, the weak correlation between rearfoot adduction and rearfoot eversion (Fischer et al. 2017b) indicates a complex relationship of the two movements on tibial rotation, which might be governed by different anatomical factors.
To improve our understanding of such fundamental coupling mechanisms at the ankle joint it would be of interest to analyse the isolated effects of calcaneal adduction/abduction and eversion/inversion on tibial rotation.
The investigation of this mechanism in vivo is not possible, as the two movements do not occur independently of each other. The restriction of in vivo measurements could be overcome by an in vitro experiment, in which the initiation of calcaneal adduction/abduction and eversion/inversion can be induced separately. To the authors' best knowledge, this approach has not been utilized yet.
The purpose of this study was to analyse experimentally the isolated mechanical coupling of: (1) calcaneal adduction/abduction and (2) eversion/inversion on talus and tibial rotation in vitro.
Based on the results of Fischer et al. (2017b) it was hypothesized that the relationship of calcaneal adduction to internal tibial rotation would be stronger than that of calcaneal eversion to internal tibial rotation.
Methods
In the experimental set‐up used for this in vitro investigation an aluminium frame was mounted on an aluminium plate assembly and the frame held a vertical rod which allowed rotational movement of the tibia around its longitudinal axis. A ball bearing‐ mounted disc with three degrees of freedom was fixed on the plate, supporting the rearfoot area. A disposable wooden plate covered with sandpaper was used for positioning of the forefoot (Fig. 1).
Figure 1.
Experimental set‐up, consisting of an aluminium frame mounted on a plate. (A) Rod for vertical fixation of the tibia. (B) Wooden foot plate assembly for fixation of the forefoot using a Kevlar strap. (C) Ball bearing mounted disc to allow rotation of the calcaneus in all three planes of movement. (D) Metal rod horizontally screwed into the calcaneus. Inserted marker arrays used for data analysis (tibia, talus and calcaneus).
Specimen preparation
Eight fresh frozen foot‐leg specimens (mean age 61.9 years, three females, five males, Table 1) were prepared for measurement. The specimens were made available through the Institute of Anatomy of the University Hospital Cologne.The study was approved by the ethical committee of the German Sport University Cologne (report no. 030/2017, 21 January 2017). The shanks were amputated 10 cm underneath the tibial plateau and custom‐made bone pin marker triads were inserted by an experienced orthopaedic surgeon into five separate bones (tibia, calcaneus, talus, navicular and metatarsal I). For the purpose of this study only information concerning the tibia, calcaneus and talus were included in the data analysis. Bone pin positions were controlled using a fluoroscope (GE OEC Flurostar 7900, GE OEC Medical Systems GmbH, Wendelstein, Germany). Locations of the marker triads and angles of insertion were chosen to avoid the risk of triads touching each other during movement and to ensure good marker detection. For manual initiation of adduction/abduction as well as eversion/inversion of the calcaneus, a metal rod was horizontally screwed into the posterior aspect of the calcaneus and fixed with two counter screws (Fig. 1).
Table 1.
Specimen details
Age (years) | Sex (f/m) | Side (r/l) | |
---|---|---|---|
Specimen 1 | 62 | f | r |
Specimen 2 | 48 | f | l |
Specimen 3 | 48 | f | r |
Specimen 4 | 68 | m | r |
Specimen 5 | 59 | m | l |
Specimen 6 | 68 | m | r |
Specimen 7 | 70 | m | l |
Specimen 8 | 72 | m | l |
The specimen was placed on the foot plate. To allow movement of the calcaneus, the rearfoot was aligned on top of the disc. For vertical fixation the rod connected to the frame was driven into the medullary cavity of the tibia. The forefoot was fixed on the foot plate by means of a Kevlar strap. The longitudinal axis of the foot (line through the most posterior point of the calcaneus and the second foot ray) was aligned to the anterior‐posterior axes of the laboratory coordinate system with the shank in a vertical position.
Experiment
Two conditions were performed: in the first condition (condition 1) calcaneal adduction/abduction (add/abd) and in the second (condition 2) calcaneal eversion/inversion (ev/inv) were initiated manually by the metal rod horizontally screwed into the calcaneus. The rotations were performed up to a maximum RoM in the frontal and transverse planes separately. RoM was restricted by bony structure, ensuring that no damage would occur at the calcaneus. Measurements of both variables were conducted in a neutral position of the foot with 0° plantarflexion and without vertical loading. The resulting movement of the tibia, calcaneus and talus was recorded. Furthermore, the out of‐plane motion induced by the operator was captured. This means that for condition 1 the amount of frontal plane motion and for condition 2 the amount of transverse plane motion was determined. Between two and five cycles were performed per variable and included into data analysis. Marker triad motion was collected at 250 Hz using a 10 camera motion analysis system (Vicon MX40, Vicon Motion Systems, Oxford, UK).
Analysis
Marker coordinates were filtred using a recursive fourth order digital Butterworth low‐pass filter (cut‐off frequency, 5 Hz). A mathematical optimization of marker triad coordinates was performed for each marker triad to comply better with rigid body assumptions (Soderkvist & Wedin, 1993). In the neutral position, local bone coordinate systems of each segment were derived by applying the laboratory coordinate system.
In the dynamic trials, the orientation of the local coordinate systems was determined by tracking the technical marker triad‐based coordinate systems and with knowledge about the rotational offset between the local and technical coordinate system from the reference measurement (Cappozzo et al. 2005). Bone orientation angles were calculated using the Cardan angle convention. The sequence of rotation was flexion‐extension, adduction‐abduction, internal‐external rotation (Zatsiorsky, 1998). Global frontal and transverse plane RoM were calculated for each cycle and then averaged for each specimen.
Angle‐angle plots of the relative motion between segments (calcaneus to tibia, calcaneus to talus and talus to tibia) in different planes of motion were plotted and the slope of a linear least squares fit was used to determine the respective coupling coefficients (CC). Coupling coefficients were compared by means of a dependent sample t‐test. Effect sizes (Cohen's d) were calculated between different CCs.
Results
Both calcaneal add/abd and calcaneal ev/inv were coupled to talus and tibial rotation (tibial rot), with CCs ranging from 0.30 to 1.15 (Table 2, Figs 2 and 3). By qualitatively analysing the repeatability of the induced movement, the relation of the relative motions of two bones followed a linear trend and appeared to be repeatable (Figs 2–4). A significantly stronger coupling to tibial and talus rotation for the initiation of calcaneal add/abd than for calcaneal ev/inv could be detected (P = 0.004; d = 1.729 and P = 0.002; d = 1.923, respectively, Fig. 5). Only one specimen (specimen 1) exhibited lower CCs for calcaneal add/abd than for calcaneal ev/inv on tibial and talus rotation (Table 2, Figs 2 and 3).
Table 2.
Individual CCs and their respective means and standard deviations (mean, SD) describing the coupling of calcaneal add/abd and ev/inv to talus and tibial rotation. In condition 1, calcaneal add/abd was initiated; in condition 2 calcaneal ev/inv was initiated. Furthermore, the out‐of‐plane motion was described as percentage of the RoM of the respective initiated movement in conditions 1 and 2
Condition 1: Initiation of calcaneal abd/add | Eversion out‐of‐plane motion (%) | |||
---|---|---|---|---|
Coupling coefficient Calcaneal abd/add‐tibial rot | Coupling coefficient Calcaneal abd/add‐talus rot | Coupling coefficient Talus rot‐tibial rot | ||
Specimen 1 | 0.90 | 0.89 | 1.01 | 23.9 |
Specimen 2 | 0.99 | 0.96 | 1.03 | 25.6 |
Specimen 3 | 0.96 | 1.00 | 0.96 | 25.1 |
Specimen 4 | 0.98 | 0.95 | 1.03 | 17.5 |
Specimen 5 | 1.15 | 1.11 | 1.03 | 12.7 |
Specimen 6 | 0.87 | 0.89 | 0.97 | 18.8 |
Specimen 7 | 0.94 | 0.95 | 0.98 | 19.9 |
Specimen 8 | 1.10 | 1.07 | 1.03 | 23.9 |
Mean | 0.99 | 0.98 | 1.01 | 20.9 |
SD | 0.10 | 0.08 | 0.03 | 4.5 |
Condition 2: Initiation of calcaneal ev/inv | Adduction out‐of‐plane motion (%) | |||
---|---|---|---|---|
Coupling coefficient Calcaneal ev/inv‐tibial rotation |
Coupling coefficient Calcaneal ev/inv‐talus rot |
Coupling Coefficient Talus rot‐tibial rot |
||
Specimen 1 | 0.95 | 0.93 | 1.02 | 23.7 |
Specimen 2 | 0.55 | 0.30 | 1.67 | 19.2 |
Specimen 3 | 0.63 | 0.38 | 1.52 | 14.8 |
Specimen 4 | 0.50 | 0.51 | 1.00 | 25.9 |
Specimen 5 | 0.75 | 0.61 | 1.17 | 21.7 |
Specimen 6 | 0.75 | 0.47 | 1.39 | 17.6 |
Specimen 7 | 0.75 | 0.74 | 0.99 | 30.4 |
Specimen 8 | 0.58 | 0.32 | 1.43 | 17.2 |
Mean | 0.68 | 0.53 | 1.27 | 21.3 |
SD | 0.15 | 0.22 | 0.26 | 5.2 |
Figure 2.
Individual angle – angle plots for condition 1 (initiation of calcaneal add/abd, blue lines) and condition 2 (initiation of calcaneal ev/inv, red lines) and talus rotation. CCs for both conditions are represented in the bottom right‐hand corner of each plot. The out‐of‐plane motion induced by the operator was recorded. For condition 1 (blue slope) the amount of frontal plane motion (blue lines) and for condition 2 (red slope) the amount of transverse plane motion (red lines) are presented.
Figure 3.
Individual angle – angle plots for condition 1 (initiation of calcaneal add/abd, blue lines) and condition 2 (initiation of calcaneal ev/inv, red lines) and tibial rotation. CCs for both conditions are represented in the bottom right‐hand corner of each plot. The out‐of‐plane motion induced by the operator was recorded. For condition 1 (blue slope) the amount of frontal plane motion (blue lines) and for condition 2 (red slope) the amount of transverse plane motion (red lines) are presented.
Figure 4.
Individual angle – angle plots for talus rotation and tibial rotation while initiating condition 1 (initiation of calcaneal add/abd, blue lines) and condition 2 (initiation of calcaneal ev/inv, red lines). CCs for both conditions are represented in the bottom right hand corner of each plot. The out‐of‐plane motion induced by the operator was recorded. For condition 1 (blue slope) the amount of frontal plane motion (blue lines) and for condition 2 (red slope) the amount of transverse plane motion (red lines) are presented.
Figure 5.
Box plot representation of individual CCs for (A) condition 1 (initiation of calcaneal adduction/abduction; blue dots) and condition 2 (initiation of calcaneal eversion/inversion, red dots) on talus rotation; (B) talus rotation on tibial rotation for condition 1 and condition 2; (C) condition 1 and condition 2 on tibial rotation. Mean CCs of both conditions were compared by means of a dependent sampled t‐test and effect sizes (Cohen's d) were calculated between different CCs.
Overall, the strongest motion coupling in both conditions was found between talus and tibial rotation, with larger CCs for the initiation of calcaneal ev/inv compared with the initiation of calcaneal add/abd (Condition 1, CC 1.01; Condition 2, CC 1.27, respectively; Table 2, Fig. 4).
Comparing the out‐of‐plane motion during both conditions, no difference was found (P = 0.900; Cohen's d = 0.054, Fig. 6).
Figure 6.
Box plot representation of individual out‐of‐plane motions, displayed as percentage of the RoM of the respective initiated movement. For condition 1 (initiation of calcaneal adduction/abduction) the amount of frontal plane motion (blue dots) and for condition 2 (initiation of calcaneal eversion/inversion) the amount of transverse plane motion (red dots) are represented. Mean CCs for both conditions were compared by means of a dependent sampled t‐test and effect sizes (Cohen's d) were calculated between different CCs.
Discussion
The purpose of this study was to quantify experimentally isolated coupling mechanisms of calcaneal add/abd and calcaneal ev/inv to proximal segments in vitro. Data describing inter‐bone motion and coupling mechanisms between segments were obtained using bone pins. This method permitted the precise measurement of actual bone kinematics, including the talus, which is hidden from the outside view. The advantage of an in vitro compared with an in vivo experimental design is the possibility of the isolated initiation of either calcaneal add/abd or calcaneal ev/inv, which allows investigation of their independent mechanical coupling to the tibia. In vivo, both movements appear together, making the estimation of the strength of coupling by means of a least square fit to angle‐angle plots impossible. This is because tibial rotation, the dependent variable, is affected by both calcaneal add/abd and calcaneal ev/inv. However, the extent of their contribution is unknown.
The coupling coefficient of calcaneal eversion into internal tibial rotation has previously been investigated using bone pins during running (Stacoff et al. 2000) as well in vitro measurement set‐ups (Hintermann et al. 1994), while ignoring the influence of calcaneal adduction. This coupling mechanism has been associated with anterior knee pain in runners (Tiberio, 1987). The CCs provided by Hintermann et al. (1994) for the unloaded situation are on average comparable to values collected in the current experiment. For the unloaded condition and in 0° plantarflexion, Hintermann et al. (1994) found a transfer coefficient for eversion of 0.46 and for inversion 0.74. In comparison, for the same conditions we found a coupling coefficient of 0.68, using the whole range from eversion to inversion. The major differences between both studies may be the initiation of movement. Hintermann et al. (1994) fixed the foot on a foot plate assembly by screws and cement on the calcaneus and initiated a rotation of the foot plate. Thus, the natural movement of the calcaneus relative to the forefoot in the transverse plane might have been restricted.
The CCs in the present study indicate that not only calcaneal ev/inv (0.68 ± 0.15) but to an even greater extent calcaneal add/abd (0.99 ± 0.10) was transferred into tibial rotation. Both conditions induced a rotation of the talus in the transverse plane which was transferred into tibial rotation. These results support our hypothesis that a stronger relationship of calcaneal add/abd than of calcaneal ev/inv to internal tibial rotation would occur, highlighting the relevance of calcaneal adduction.
A significant relationship between rearfoot adduction and tibial rotation has previously been described by Fischer et al. (2017b) in an in vivo study using a partial correlation analysis. However, this method does not allow determination of the strength of coupling by means of the slope of a linear least square fit to an angle‐angle plot, as both rearfoot add/abd and ev/inv appear together in vivo. Therefore, for the individual contribution of both individual movements on tibial rotation, the dependent variable is unknown. The in vitro approach used in this study overcame these problems, which exist in real world locomotion.
Even though the transfer of calcaneal add/abd into tibial rotation was stronger than for calcaneal ev/inv to tibial rotation, the strongest overall CCs were found between talus and tibial rotation, when initiating calcaneal ev/inv. This result can be explained by the contribution of coupling between individual joints to overall ankle joint coupling. The coupling from calcaneal add/abd to talus rotation was stronger than for calcaneal ev/inv; in contrast, talus rotation was coupled more strongly to tibial rotation when initiating calcaneal ev/inv vs. calcaneal add/abd. Additionally, in some cases the CCs found in this study exceeded the value of one. It can be concluded that movement coupling seems to be affected by multiple factors. The different influences of calcaneal add/abd and calcaneal ev/inv to CCs of individual joints can be attributed not only to joint surfaces but also to passive structures covering more than two bones, providing an explanation for the amplitudes of CCs found in this study.
In the present study a global bone orientation approach has been applied to examine the coupling of bone motion. Determining the relationship between segmental movements on the basis of joint angles precludes the possibility to detect relationships of segmental movement within the same plane of movement. If the proximal and the distal segments were to move in the same direction and amplitude at the same time, no changes in the joint angle between segments would be detected, making it impossible to estimate validly the linear coupling between these movements. The example described above represents a perfect coupling (CC 1.00); however, the slope of the regression line indicates no relationship between both movements. Therefore, to examine, for example the relationship between calcaneal add/abd and tibial rotation, two segments moving in the same plane of movement, an analysis of global segment orientation is necessary.
A limitation of the present in vitro method is the poor control of the manually initiated movements. Nonetheless, the out of‐plane motion (for condition 1 the amount of frontal plane motion and for condition 2 the amount of transverse plane motion) induced by the operator has been monitored and was shown to be of the same magnitude (Fig. 6). The manual initiation of movements was necessary to avoid the destruction of bony structures. Nonetheless, future studies should improve the standardization and control of this movement.
Another limitation is that in vitro loading conditions contrast strongly with natural loading conditions during running, due to the much higher vertical loading of the lower extremity in in vivo conditions and the absence of joint guidance through muscular activation. However, in a pilot study it was shown that under loaded conditions it is almost impossible manually to induce a relevant RoM as a basis for estimating a valid slope without damaging the bone and provoking a breaking out of the metal rod horizontally screwed into the posterior aspect of the calcaneus. Future efforts to determine the movement coupling at the ankle joint should include different loading conditions and means to induce relevant RoM without destroying the biological structures.
In conclusion, this study presented novel information describing the isolated coupling of calcaneal adduction/abduction as well as eversion/inversion on tibial rotation using an in vitro method for independent initiation of both conditions. Our results suggest that the effects of calcaneal add/abd may previously have been underestimated. These findings will contribute to the clarification of distal to proximal movement coupling at the ankle joint complex – a mechanism that has been related to overuse knee injuries in runners.
Acknowledgements
Study founded by the Institute of Biomechanics of the German Sport University.
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