Knee Surg Sports Traumatol Arthrosc DOI 10.1007/s00167-014-3190-3
Ankle
Preventive lateral ligament tester (PLLT): a novel method to evaluate mechanical properties of lateral ankle joint ligaments in the intact ankle Raymond Best · Caroline Böhle · Frieder Mauch · Peter G. Brüggemann
Received: 8 January 2014 / Accepted: 14 July 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose To construct and evaluate an ankle arthrometer that registers inversion joint deflection at standardized inversion loads and that, moreover, allows conclusions about the mechanical strain of intact ankle joint ligaments at these loads. Methods Twelve healthy ankles and 12 lower limb cadaver specimens were tested in a self-developed measuring device monitoring passive ankle inversion movement (Inv-ROM) at standardized application of inversion loads of 5, 10 and 15 N. To adjust in vivo and in vitro conditions, the muscular inactivity of the evertor muscles was assured by EMG in vivo. Preliminary, test–retest and trial-to-trial reliabilities were tested in vivo. To detect lateral ligament strain, the cadaveric calcaneofibular ligament was instrumented with a buckle transducer. After post-test harvesting of the ligament with its bony attachments, previously obtained resistance strain gauge results were then transferred to tensile loads, mounting the specimens with their buckle transducers into a hydraulic material testing machine. Results ICC reliability considering the Inv-ROM and torsional stiffness varied between 0.80 and 0.90. Inv-ROM Raymond Best and Caroline Böhle have contributed equally to this work. R. Best (*) · F. Mauch Department of Orthopedic and Sports Trauma Surgery, Sportklinik Stuttgart GmbH, Taubenheimstrasse 8, 70372 Stuttgart, Germany e-mail: [email protected]; Best.Raymond@Sportklinik‑stuttgart.de C. Böhle · P. G. Brüggemann Department of Orthopedics and Biomechanics, German Sports University Cologne, Cologne, Germany
ranged from 15.3° (±7.3°) at 5 N to 28.3° (±7.6) at 15 N. The different tests revealed a CFL tensile load of 31.9 (±14.0) N at 5 N, 51.0 (±15.8) at 10 N and 75.4 (±21.3) N at 15 N inversion load. Conclusions A highly reliable arthrometer was constructed allowing not only the accurate detection of passive joint deflections at standardized inversion loads but also reveals some objective conclusions of the intact CFL properties in correlation with the individual inversion deflections. The detection of individual joint deflections at predefined loads in correlation with the knowledge of tensile ligament loads in the future could enable more individual preventive measures, e.g. in high-level athletes. Keywords Ankle ligament · Inversion injury · Injury prevention · Ligament strain
Introduction Ankle sprains with lesions of the anterolateral ligament structures are still one of the most frequent injuries in daily life, during recreational activities [19], and especially in professional sports [11, 16, 35]. Approximately, one inversion injury occurs in 10,000 people each day, e.g. accounting for 23,000 ankle injuries in the USA per day [30], whereat about 50 % of the injuries occur in sports. Treated inadequately, ankle sprains may result in chronic structural or functional instability as well as in chronic pain in up to 40 % of the cases [5, 31, 34, 36]. Consequently, especially in professional sports, continuous scientific research has been focusing not only on optimal diagnostic and treatment strategies in the case of injury, but also on functional and orthotic preventive measures [5, 6, 11, 15, 17, 22, 23, 31, 35].
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To appraise an injury risk for preventive reasons, beyond clinical evaluation, it requires an objective measurement tool to evaluate the ankle ligament’s mechanical properties. Manual stress tests have numerously been described to be insufficient due to a high inter-observer and intra-observer variability [10, 25, 26], as well as to inappropriate or false results in patients who relax to various degrees during such tests [4, 10, 14, 18]. Also, widely used radiograph stress tests or several laxity testers revealed a high variability [20, 21, 32] and unsatisfying reliability [11, 13] as they do not respect and thus register adulterant muscular activity of the evertor muscles. Anyway, the majority of laxity testers are constructed to evaluate acute or chronic instability respecting certain thresholds rather than for the preventive purpose to evaluate the intact ankle individually irrespective of generalized thresholds. So far, scientifically, little is known about such predominantly preventive evaluations, e.g. to estimate an athlete’s injury risk in order to take appropriate, individually adapted orthotic precautions. The objective of this study therefore was to develop a standardized measurement device that may reveal basic information about the mechanical properties of the intact ankle joint and especially of the intact lateral calcaneofibular ankle ligament (CFL) during inversion. Furthermore, this study confirmed the reliability of such a device using appropriate reliability tests. Last but not least, we intended to support the interpretation of the obtained in vivo results by measuring the calcaneofibular ligament strain in vitro performing cadaveric tests and using the same measuring device.
Knee Surg Sports Traumatol Arthrosc
ankle inversion movement at predefined and standardized loads exactly and individually. The measuring device has been described previously [5], where an analogue methodical set-up for another preventive objective was used. Basically, the device consists of a stable main frame with a moveable tilting platform (Fig. 1) on which a subject’s foot can be fixated accurately in a standardized manner (Fig 2). For testing, participants lay on their side in the best orthogonal posture with the foot and lower leg completely fixated in the apparatus. Here, the position of the complete lower extremity could be adjusted and fixed in each plane in a standardized way, allowing all subjects as well as the cadaveric specimen to be positioned in a similar manner (Fig. 3a, b). In particular, the height of the ankle in the coronal plane in relation to the axis of rotation of the apparatus could be adjusted exactly and individually (Fig. 4a). The force to the ankle joint could thus be applied as directly as possible and without the chance of evasive movements. In the case of cadaver tests, the cadaveric lower extremity
Materials and methods The study was designed as a comparative intra-test experimental and cadaveric study. First, the passive inversion ankle range of motion was tested in healthy subjects using a self-constructed novel inversion ankle arthrometer which allowed the application of clearly defined loads to an ankle joint fixated with standardized procedures. Muscular inactivity was assured by registering the activity of the evertor muscles during testing. After reliability testing of the apparatus, the same device and testing method was used in cadaveric lower limb specimens with dissected lateral ligaments to register the tensile strain on the calcaneofibular ligament under the same testing conditions as above using an additionally instrumented buckle transducer to the CFL.
Fig. 1 Schematic drawing of the measuring apparatus
Testing device A self-developed measuring device preventive lateral ligament tester (PLLT) was constructed to monitor passive
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Fig. 2 Fixated foot on the tilting platform
Knee Surg Sports Traumatol Arthrosc
Fig. 3 Fixated lower extremity in the measuring device a view from the top b lateral view
(harvested 12 cm above the knee joint) was similarly adjusted. Because the passive stabilizing effect of the complete trunk was missing, in addition to the straps, the calcaneus was transfixed to the tilting platform by a screw. To secure best possible passive ankle movement without any muscular influence activity during in vivo testing, the activity of the long peroneal muscles was monitored using surface electromyography (EMG). Surface electrodes were stuck to the shaved and cleaned skin with a distance of 2.2 cm parallel to the muscle fibres. At the beginning of each testing cycle, mechanical artefacts of the leads were excluded and the system was calibrated. Monitoring electrical muscular inactivity by amplified EMG signal was prerequisite for initiating each test as well for the complete period of measuring. In case of any registered muscular activity, the test was interrupted and repeated. After all preparations, the tilting platform was then unlocked to invert the foot and locked in neutral ankle position at the end of each test. The instrument settings remained the same for a complete measuring cycle. Three constant forces (F1 = 5 N, F2 = 10 N, and F3 = 15 N) were applied to a lever arm (length: 19.4 cm) on the tilting
Fig. 4 Schematic drawing of the adjusted ankle a relating to the axis of rotation of the measuring device b with the application of standardized loads
platform (Fig 4b). The resulting torque to the origin of the lever arm and consequently to the ankle joint was a product of the applied force acting rectangular to the lever arm and the length of the lever arm itself. Accordingly, the applied force of, for example, 5 N increased the torque to the ankle joint and thus the resulting tensile strength to the ligament in relation to the length of the lever arm. In our study, the lever arm inverted the ankle with an initial torque of nearly 1 [5 N × 0.2 m], 2 and 3 Newton metre, respectively, until achieving maximal deflection. An electric goniometer at the axis of the tilting platform detected the range of inversion motion (Inv-ROM) of the ankle. Values were registered in degree, rounded after one decimal. Inv-Rom as well as the ligament strain in cadaveric tests (see below) were registered over a period of 20 s (frequency 1,000 Hz) using Vicon Nexus software (VICON Motion Systems, Oxford, United Kingdom). Each testing cycle consisted of three repetitive measurements, each with
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one of the three forces. The mean value of three measurements was taken for further analysis. Reliability testing Before further cadaveric data collection, a reliability test with 12 healthy subjects (Ø age: 24.42 ± 2.75 years, Ø height: 177.67 ± 7.29 cm, Ø weight: 69.08 ± 7.03 kg) without any ankle complaints or clinical signs of ankle instability was conducted. The a priori calculated sample size (Point biserial model, Software G-Power 3.1) (ICC 0.70, effect size 0.84, α-error 0.05, power 0.90) revealed a minimum of eight subjects. Subjects with an ankle injury within the past 6 months were excluded. Test–retest reliability for inversion range of motion (degree) as well as torsional joint stiffness (Newton metre/degree) was tested with a 7-day interval. A trial-totrial reliability test was conducted between the single tests for each applied force (5, 10, 15 N). All tests were performed by the same investigator. The study was approved by the institutional review board of the University of Cologne, and all participants of the in vivo tests gave informed written consent.
Fig. 5 Dissected calcaneofibular ligament (CFL)
In vitro testing For the in vitro testing, twelve lower limb cadaver specimens, harvested 12 cm above the knee joint, were used from seven female and five male donors (Ø age: 76.5 ± 15.4 years). The a priori calculated sample size (Software G-Power 3.1) (Estimated increase of ligament strain 25 Newton/Newton metre, effect size 1.66, α-error 0.05, power 0.95) revealed a minimum of 6 specimen. During the testing series, 4 specimens were damaged or found to have abnormal or injured lateral ligament anatomy and thus excluded, leaving 8 (three males, five females) specimens for further investigation (Ø age: 75.0 ± 15.5 years). The specimens were stored at −20° C and thawed at room temperature for 12 h before testing. The specimens were first dissected, resecting the subfibular fat and exciding the peroneal retinaculum. To attain the CFL for further strain testing, the peroneal tendons were released (Fig. 5), which was consistent with the inactivated evertor muscles of the vivo tests. In this manner, the anterolateral ankle ligaments (ATFL, CFL) were dissected preserving as much soft tissue as possible. The specimens were then mounted to the testing apparatus as described above. In order to detect the ligament strain of the CFL, when applying the predefined loads, before each testing cycle, a self-constructed buckle transducer was applied to the CFL. This registered the ligament strain via resistance strain gauges at the different induced loads (Fig. 6) converting it to electric potential (mV, rounded after one decimal).
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Fig. 6 CFL instrumented with a buckle transducer
After a completed and successful testing cycle appropriate to the in vivo testing, the CFL was harvested with its bony attachments and mounted into a hydraulic material testing machine (Zwick Z2.5/TN1S; Zwick GmbH & Co KG, Ulm, Germany). The harvested bone blocks were fixated in a hollow cylinder (Ø 37 mm) using polymerizing plastic (Technovit 4,004; Heraeus Kulzer GmbH, Wehrheim, Germany). Additional transfixation was assured by three fixation screws in the cylinder. Due to the described fixation, a slipping of the bony blocks could be completely avoided. Furthermore, attention was paid to mount the ligament in its anatomical direction of tension ((Fig. 7). During the test, the ligament was continuously moistened with saline (NACL 0.9 %). To determine the ligament’s tensile force during the inversion tests, the buckle transducer was again applied to the ligament in analogous manner and position and then connected to a multimeter. The testing machine strained the ligament until the buckle transducer achieved the same voltage value corresponding to the precedent inversion tests. Using testXpert software version 10.0
Knee Surg Sports Traumatol Arthrosc Table 1 Intra-class correlation coefficients (ICC) for test–retest and trial-to-trial reliabilities considering ankle inversion range of motion Reliability
Testing condition
Inversion [°]
ICC
Test–Retest
t1 (5 N) versus t2 (5 N) t1 (10 N) versus t2 (10 N) t1 (15 N) versus t2 (15 N) Trial 1 (5 N) versus Trial 2 (5 N) Trial 1 (5 N) versus Trial 3 (5 N) Trial 2 (5 N) versus Trial 3 (5 N) Trial 1 (10 N) versus Trial 2 (10 N) Trial 1 (10 N) versus Trial 3 (10 N) Trial 2 (10 N) versus Trial 3 (10 N) Trial 1 (15 N) versus Trial 2 (15 N) Trial 1 (15 N) versus Trial 3 (15 N)
15.3 ± 7.3 versus 17.5 ± 8.4
0.81
21.0 ± 6.3 versus 23.4 ± 8.6
0.80
26.4 ± 6.4 versus 28.3 ± 7.6 15.3 ± 7.3 versus 15.1 ± 7.4 15.3 ± 7.3 versus 15.4 ± 7.5 15.1 ± 7.4 versus 15.4 ± 7.5 20.8 ± 6.5 versus 20.9 ± 6.2 20.8 ± 6.5 versus 21.5 ± 6.8 20.9 ± 6.2 versus 21.5 ± 6.8 25.8 ± 5.9 versus 26.4 ± 6.6 25.9 ± 5.9 versus 26.9 ± 6.9
0.89
26.4 ± 6.6 versus 26.9 ± 6.9
0.99
Trial to trial
Trial 2 (15 N) versus Trial 3 (15 N)
Fig. 7 Harvested CFL mounted in a hydraulic testing machine
0.97 0.91 0.98 0.97 0.93 0.99 0.98 0.96
Figures as means and ± SDs
(Zwick GmbH & Co KG, Ulm, Germany), the tensile force of the CFL was then registered. Values are given in Newton, rounded after one decimal. Consideration of the particular tensile force of the CFL is given in relation to the inversion angle as well as to the amount of external force. Statistical analysis To determine the trial-to-trial and test–retest reliabilities, the intra-class correlation coefficient (ICC) was calculated using IBM SPSS Statistics 21 Software (IBM Germany GmbH, Ehningen, Germany). The level of significance was set at p 0.80, ranging between 0.80 and 0.90. Trial-to-trial reliability for inversion range of motion and torsional joint stiffness
t1 test-point 1, t2 test-point 2, ICC intra-class correlation coefficient
varied between 0.91 and 0.99. Means and corresponding standard deviations for the single results, as well as the resulting ICCs, are shown in Tables 1 and 2. Cadaveric testing A total of 8 specimens were tested over a complete testing cycle. Mounted to the testing machine, the corresponding
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Table 3 Mean CFL tensile loads at the different applied loads Applied load (N)
CFL tensile force [N]
5 10
31.9 ± 14.0 51.0 ± 15.8
15
75.4 ± 21.3
Figures as means and ± SDs
registered force of the buckle transducer equalled a mean ligament tensile force of 31.9 (±14.0) N with an applied force of 5 N, a tension load of 51.0 (±15.8) N at 10 N and 75.4 (±21.3) at 15 N. Table 3 summarizes the corresponding tensile force of the CFL with the three different applied external forces of 5, 10 and 15 N to the lever arm, equalling an initial torque of 1, 2, or 3 Nm, respectively.
Discussion The most important finding of the present study was the construction, description and validation of a highly reliable and reproducible, non-radiographic ankle arthrometer to individually measure an uninfluenced passive inversion range of motion, as well as to evaluate the tensile strain of the uninjured calcaneofibular ligament and the torsional joint stiffness at predefined, standardized loads. Rather than differentiating between stable and unstable, the results show that the inversion degrees measured with the ankle arthrometer at predefined loads can individually be correlated with the tensile ligament strain of the intact CFL. Preventing ankle injuries in professional sports have been of increasing scientific interest over the past decades [5, 6, 11, 15, 17, 22, 31, 35]. To protect ligaments successfully and individually, achieving a clear understanding of basic knowledge about physiologic joint and ligament properties and loading seems inevitable. Particularly, because the inversion range of motion of ankle joints varies individually, it was not intended to determine a degree-depending threshold for a higher risk of ligament injury. In fact, it was rather aimed to measure a subject individual amount of joint deflection at predefined loads which can also be correlated with the strain of the CFL. In future investigations, this might help to limit an athlete (or patient) not to a certain, standardized amount of joint deflection, relying on a non-individualized threshold, but individually respecting his or her individual ankle range of motion. Reliability Our results revealed an excellent test–retest and trialto-trial reliabilities with an ICC between 0.80 and 0.99
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for the single test situations and with regard to data from recent publications [10–12, 20, 21]. For example, De Vries et al. [10] published an intra-tester reliability of 0.74 and an inter-tester reliability of 0.76 for the talar inversion test using a LigMaster Joint arthrometer in 30 participants. The dynamic anterior ankle tester (DAAT), as well as the quasi-static anterior ankle tester (QAAT) of Kerkhoffs et al. [18, 20, 21], in fact, was established for anterior talar displacement. Both were first appraised to have a high reliability between 0.70 and 0.90 in 24 healthy subjects and 14 patients 1 year after acute lateral ankle ligament injury [20, 21]. The DAAT could not prove its reliability of earlier studies in a subsequent clinical evaluation [10]. A recently presented arthrometer by Nauck et al. [25–27] to distinguish between stable and unstable talofibular ligaments revealed an “excellent” ICC of 0.80. Assessing stress radiographs using the widely used Telos stress device was found to reveal accurate inter- and intra-observer reliability, [24] though obtained results are known to be difficult to interpret due to high variability [13]. In addition, Docherty et al. [11] considered the comparison of different ankle testers as difficult, as different amounts of force or torque were applied in the respective methodological set-ups. Furthermore, they found the force application mechanisms of the different testers hard to standardize. Finally, these and other studies were limited by their inability to quantify muscle activity of subjects during the special tests [10, 11], influencing the reliability as well as the results of the tested ankle arthrometer. By monitoring the muscle activity of the tested subjects and standardizing the position of the ankle and the applied force, we were able to eliminate all of the above-mentioned limitations, explaining the good reliability results. Cadaveric testing Several methods of cadaveric ligament strain testing have been published so far, amongst which mounting harvested ligaments in hydraulic testing machines [1], instrumenting ligaments with directly applied strain gauges [9, 30] or using buckle transducers [3] are the most common. However, to date, direct or at least transferred force measurements in intact ankles are not available. Furthermore, transferring obtained in vitro data to an equivalent in vivo test apparatus in order to derive conclusions for the intact ankle for preventive instead of diagnostic purpose has been scientifically unconsidered until now. The ankle arthrometer allows the detection of a passive ankle inversion angle produced by standardized forces and with monitored, inactivated evertor muscles. Subsequently, the ankle inversion angles can be correlated with an assumed tensile force of the intact CFL. For example, the amount of passive inversion angle at an applied force of
Knee Surg Sports Traumatol Arthrosc
15 N (initial torque of 3 Nm) reveals not only the particular joint deflection and joint stiffness but also the ligament tensile load of approximately 70 N at this deflection. A clear advantage of the described method is that—compared to other studies—the experimental set-up respects the high variability of ankle joint deflection as well as the widely varying loads to failure of ankle ligaments from one ankle to another [1, 3]. Several ligament strain test set-ups worked with predefined ankle positions [9, 28], instead of considering the variability of ankle deflection. Applying standardized torques to the ankle which causes a certain, individual degree of deflection, reversely allows more individual load correlations. The length and strain of the lateral ankle ligaments depend on the position of the foot, with respect to the degree of inversion–eversion, plantarflexion and dorsiflexion [3, 28], and not least to a little amount of 2.5 % on subjects axial loading [3, 8]. However, the registered tensile forces of the current study are consistent with the results of Bahr et al. [3], who also registered ligament forces using buckle transducers in cadaveric specimens. Differing between an axially loaded (375 Newton) and an unloaded situation as well as between different positions of the foot, they revealed a CFL ligament force of 60–70 N when applying 3.4 Nm torque to the cadaveric ankle [3]. Beyond this, they registered the highest strain of the CFL in either 20° plantarflexion or 10° dorsiflexion with simultaneous compressive loading, even though these maximum loads did not exceed a mean of 109 N, about one-third of the failure load of the respected ligament [1, 3]. In ten human ankle specimens, Colville et al. [9] applied a 3-Nm inversion torque after instrumenting the ligaments with strain gauges. They found the highest ligament strain of the LFC when inverting the ankle by increasing amounts when simultaneously dorsiflexed. Their study group did not transfer their results to an in vivo tester, nor did they determine quantitative tensile forces of particular ligaments. Measuring the ligament’s force with an indirect method, Nigg et al. [28] measured a CFL force of 46.3 N at maximal inversion and dorsiflexion in three cadaveric specimens. Their comparably low loads might be due to the fact that they moved the ankle in 36 different positions but did not apply an additional load to the ankle. Some limitations of this study have to be specified. Compared to an injury situation, the applied loads to the ankle in our study were comparably low and it might be doubted whether adequate ligament strain was created. Congruently, Tohyama et al. [33] also demonstrated in their cadaveric tests that lower loads rather than higher loads caused ankle translations [33]. Furthermore, investigating ankle ligaments especially at low loads, Butler et al. [7] examined ligament properties within a physiologic range. Bahr et al. [3] also applied a torque of only 3.5 Nm to
achieve their strain curves. Furthermore, a video analysis of Nauck et al. [27] confirmed that the ankle joint is already in a slightly deflected position at low loads. Furthermore, the soft tissue and ligament properties of the cadaveric tests may not be directly transferred to an in vivo situation, though previous studies confirmed that freezing has little or no effects on biomechanical properties of ligaments [1, 29]. However, the passive soft tissue slack (peroneal tendons even when unstrained, subcutaneous soft tissue skin etc.) needs to be considered, since there is a complex synergistic relationship between all soft tissue stabilizers in the intact ankle [3, 27]. However, instrumenting any measuring device to the CFL requires dissection of the subfibular soft tissue and the peroneal tendons making this limitation unavoidable. At least by monitoring the inactivated evertor muscle during in vivo testing, both test conditions could be adjusted as similar as possible. Not least, the simultaneous strain and property testing of the anterior talofibular ligament (ATFL) was not done but would have been interesting. It was intended to do so in the beginning, but preliminary tests revealed that neither the anatomical position of the ATF ligament nor its mean length and width would allow an appropriate, completely exposed and small buckle transducer to be instrumented without risking an impingement. Ozeki et al. [30] al. also claimed limitations with regard to using buckle transducers due to the ankle ligament’s anatomical prerequisites. This is in contrast to Bahr et al. who instrumented the ATFL as well as the CFL. However, their transducers have shown acceptable accuracy in the past [2]. Finally, in addition to an intra-observer reliability, a inter-observer reliability would have been desirable, assuring the measuring devices applicability at different facilities and with different investigators. Nonetheless, the present results might help to understand more about physiologic ligament loading in correlation with individual joint movements in intact ankles. Subsequently, in all day practice, in the future, this might support to reduce a subject-specific injury risk by applying individually adaptable protections.
Conclusion The PLLT is a highly reliable measuring device which allows some objective conclusions of intact ankle ligament properties and thus of ankle joint stability at predefined standardized loads without any muscular hindrance. Determining objectively individual joint deflections paired with the knowledge of ligament strain especially in professional sports, might help to quantify an athlete’s injury risk in more detail and consequently find appropriate, individually adapted, prevention measures, adequate to prevent
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injury and loose enough to avoid the perception of being hindered. Further studies are required to obtain more information in different ankle flexion positions, as well as about the talofibular ligament or even the deltoid ligament. The authors declare that they have no conflict of interest.
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Ankle
Preventive lateral ligament tester (PLLT): a novel method to evaluate mechanical properties of lateral ankle joint ligaments in the intact ankle Raymond Best · Caroline Böhle · Frieder Mauch · Peter G. Brüggemann
Received: 8 January 2014 / Accepted: 14 July 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose To construct and evaluate an ankle arthrometer that registers inversion joint deflection at standardized inversion loads and that, moreover, allows conclusions about the mechanical strain of intact ankle joint ligaments at these loads. Methods Twelve healthy ankles and 12 lower limb cadaver specimens were tested in a self-developed measuring device monitoring passive ankle inversion movement (Inv-ROM) at standardized application of inversion loads of 5, 10 and 15 N. To adjust in vivo and in vitro conditions, the muscular inactivity of the evertor muscles was assured by EMG in vivo. Preliminary, test–retest and trial-to-trial reliabilities were tested in vivo. To detect lateral ligament strain, the cadaveric calcaneofibular ligament was instrumented with a buckle transducer. After post-test harvesting of the ligament with its bony attachments, previously obtained resistance strain gauge results were then transferred to tensile loads, mounting the specimens with their buckle transducers into a hydraulic material testing machine. Results ICC reliability considering the Inv-ROM and torsional stiffness varied between 0.80 and 0.90. Inv-ROM Raymond Best and Caroline Böhle have contributed equally to this work. R. Best (*) · F. Mauch Department of Orthopedic and Sports Trauma Surgery, Sportklinik Stuttgart GmbH, Taubenheimstrasse 8, 70372 Stuttgart, Germany e-mail: [email protected]; Best.Raymond@Sportklinik‑stuttgart.de C. Böhle · P. G. Brüggemann Department of Orthopedics and Biomechanics, German Sports University Cologne, Cologne, Germany
ranged from 15.3° (±7.3°) at 5 N to 28.3° (±7.6) at 15 N. The different tests revealed a CFL tensile load of 31.9 (±14.0) N at 5 N, 51.0 (±15.8) at 10 N and 75.4 (±21.3) N at 15 N inversion load. Conclusions A highly reliable arthrometer was constructed allowing not only the accurate detection of passive joint deflections at standardized inversion loads but also reveals some objective conclusions of the intact CFL properties in correlation with the individual inversion deflections. The detection of individual joint deflections at predefined loads in correlation with the knowledge of tensile ligament loads in the future could enable more individual preventive measures, e.g. in high-level athletes. Keywords Ankle ligament · Inversion injury · Injury prevention · Ligament strain
Introduction Ankle sprains with lesions of the anterolateral ligament structures are still one of the most frequent injuries in daily life, during recreational activities [19], and especially in professional sports [11, 16, 35]. Approximately, one inversion injury occurs in 10,000 people each day, e.g. accounting for 23,000 ankle injuries in the USA per day [30], whereat about 50 % of the injuries occur in sports. Treated inadequately, ankle sprains may result in chronic structural or functional instability as well as in chronic pain in up to 40 % of the cases [5, 31, 34, 36]. Consequently, especially in professional sports, continuous scientific research has been focusing not only on optimal diagnostic and treatment strategies in the case of injury, but also on functional and orthotic preventive measures [5, 6, 11, 15, 17, 22, 23, 31, 35].
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To appraise an injury risk for preventive reasons, beyond clinical evaluation, it requires an objective measurement tool to evaluate the ankle ligament’s mechanical properties. Manual stress tests have numerously been described to be insufficient due to a high inter-observer and intra-observer variability [10, 25, 26], as well as to inappropriate or false results in patients who relax to various degrees during such tests [4, 10, 14, 18]. Also, widely used radiograph stress tests or several laxity testers revealed a high variability [20, 21, 32] and unsatisfying reliability [11, 13] as they do not respect and thus register adulterant muscular activity of the evertor muscles. Anyway, the majority of laxity testers are constructed to evaluate acute or chronic instability respecting certain thresholds rather than for the preventive purpose to evaluate the intact ankle individually irrespective of generalized thresholds. So far, scientifically, little is known about such predominantly preventive evaluations, e.g. to estimate an athlete’s injury risk in order to take appropriate, individually adapted orthotic precautions. The objective of this study therefore was to develop a standardized measurement device that may reveal basic information about the mechanical properties of the intact ankle joint and especially of the intact lateral calcaneofibular ankle ligament (CFL) during inversion. Furthermore, this study confirmed the reliability of such a device using appropriate reliability tests. Last but not least, we intended to support the interpretation of the obtained in vivo results by measuring the calcaneofibular ligament strain in vitro performing cadaveric tests and using the same measuring device.
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ankle inversion movement at predefined and standardized loads exactly and individually. The measuring device has been described previously [5], where an analogue methodical set-up for another preventive objective was used. Basically, the device consists of a stable main frame with a moveable tilting platform (Fig. 1) on which a subject’s foot can be fixated accurately in a standardized manner (Fig 2). For testing, participants lay on their side in the best orthogonal posture with the foot and lower leg completely fixated in the apparatus. Here, the position of the complete lower extremity could be adjusted and fixed in each plane in a standardized way, allowing all subjects as well as the cadaveric specimen to be positioned in a similar manner (Fig. 3a, b). In particular, the height of the ankle in the coronal plane in relation to the axis of rotation of the apparatus could be adjusted exactly and individually (Fig. 4a). The force to the ankle joint could thus be applied as directly as possible and without the chance of evasive movements. In the case of cadaver tests, the cadaveric lower extremity
Materials and methods The study was designed as a comparative intra-test experimental and cadaveric study. First, the passive inversion ankle range of motion was tested in healthy subjects using a self-constructed novel inversion ankle arthrometer which allowed the application of clearly defined loads to an ankle joint fixated with standardized procedures. Muscular inactivity was assured by registering the activity of the evertor muscles during testing. After reliability testing of the apparatus, the same device and testing method was used in cadaveric lower limb specimens with dissected lateral ligaments to register the tensile strain on the calcaneofibular ligament under the same testing conditions as above using an additionally instrumented buckle transducer to the CFL.
Fig. 1 Schematic drawing of the measuring apparatus
Testing device A self-developed measuring device preventive lateral ligament tester (PLLT) was constructed to monitor passive
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Fig. 2 Fixated foot on the tilting platform
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Fig. 3 Fixated lower extremity in the measuring device a view from the top b lateral view
(harvested 12 cm above the knee joint) was similarly adjusted. Because the passive stabilizing effect of the complete trunk was missing, in addition to the straps, the calcaneus was transfixed to the tilting platform by a screw. To secure best possible passive ankle movement without any muscular influence activity during in vivo testing, the activity of the long peroneal muscles was monitored using surface electromyography (EMG). Surface electrodes were stuck to the shaved and cleaned skin with a distance of 2.2 cm parallel to the muscle fibres. At the beginning of each testing cycle, mechanical artefacts of the leads were excluded and the system was calibrated. Monitoring electrical muscular inactivity by amplified EMG signal was prerequisite for initiating each test as well for the complete period of measuring. In case of any registered muscular activity, the test was interrupted and repeated. After all preparations, the tilting platform was then unlocked to invert the foot and locked in neutral ankle position at the end of each test. The instrument settings remained the same for a complete measuring cycle. Three constant forces (F1 = 5 N, F2 = 10 N, and F3 = 15 N) were applied to a lever arm (length: 19.4 cm) on the tilting
Fig. 4 Schematic drawing of the adjusted ankle a relating to the axis of rotation of the measuring device b with the application of standardized loads
platform (Fig 4b). The resulting torque to the origin of the lever arm and consequently to the ankle joint was a product of the applied force acting rectangular to the lever arm and the length of the lever arm itself. Accordingly, the applied force of, for example, 5 N increased the torque to the ankle joint and thus the resulting tensile strength to the ligament in relation to the length of the lever arm. In our study, the lever arm inverted the ankle with an initial torque of nearly 1 [5 N × 0.2 m], 2 and 3 Newton metre, respectively, until achieving maximal deflection. An electric goniometer at the axis of the tilting platform detected the range of inversion motion (Inv-ROM) of the ankle. Values were registered in degree, rounded after one decimal. Inv-Rom as well as the ligament strain in cadaveric tests (see below) were registered over a period of 20 s (frequency 1,000 Hz) using Vicon Nexus software (VICON Motion Systems, Oxford, United Kingdom). Each testing cycle consisted of three repetitive measurements, each with
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one of the three forces. The mean value of three measurements was taken for further analysis. Reliability testing Before further cadaveric data collection, a reliability test with 12 healthy subjects (Ø age: 24.42 ± 2.75 years, Ø height: 177.67 ± 7.29 cm, Ø weight: 69.08 ± 7.03 kg) without any ankle complaints or clinical signs of ankle instability was conducted. The a priori calculated sample size (Point biserial model, Software G-Power 3.1) (ICC 0.70, effect size 0.84, α-error 0.05, power 0.90) revealed a minimum of eight subjects. Subjects with an ankle injury within the past 6 months were excluded. Test–retest reliability for inversion range of motion (degree) as well as torsional joint stiffness (Newton metre/degree) was tested with a 7-day interval. A trial-totrial reliability test was conducted between the single tests for each applied force (5, 10, 15 N). All tests were performed by the same investigator. The study was approved by the institutional review board of the University of Cologne, and all participants of the in vivo tests gave informed written consent.
Fig. 5 Dissected calcaneofibular ligament (CFL)
In vitro testing For the in vitro testing, twelve lower limb cadaver specimens, harvested 12 cm above the knee joint, were used from seven female and five male donors (Ø age: 76.5 ± 15.4 years). The a priori calculated sample size (Software G-Power 3.1) (Estimated increase of ligament strain 25 Newton/Newton metre, effect size 1.66, α-error 0.05, power 0.95) revealed a minimum of 6 specimen. During the testing series, 4 specimens were damaged or found to have abnormal or injured lateral ligament anatomy and thus excluded, leaving 8 (three males, five females) specimens for further investigation (Ø age: 75.0 ± 15.5 years). The specimens were stored at −20° C and thawed at room temperature for 12 h before testing. The specimens were first dissected, resecting the subfibular fat and exciding the peroneal retinaculum. To attain the CFL for further strain testing, the peroneal tendons were released (Fig. 5), which was consistent with the inactivated evertor muscles of the vivo tests. In this manner, the anterolateral ankle ligaments (ATFL, CFL) were dissected preserving as much soft tissue as possible. The specimens were then mounted to the testing apparatus as described above. In order to detect the ligament strain of the CFL, when applying the predefined loads, before each testing cycle, a self-constructed buckle transducer was applied to the CFL. This registered the ligament strain via resistance strain gauges at the different induced loads (Fig. 6) converting it to electric potential (mV, rounded after one decimal).
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Fig. 6 CFL instrumented with a buckle transducer
After a completed and successful testing cycle appropriate to the in vivo testing, the CFL was harvested with its bony attachments and mounted into a hydraulic material testing machine (Zwick Z2.5/TN1S; Zwick GmbH & Co KG, Ulm, Germany). The harvested bone blocks were fixated in a hollow cylinder (Ø 37 mm) using polymerizing plastic (Technovit 4,004; Heraeus Kulzer GmbH, Wehrheim, Germany). Additional transfixation was assured by three fixation screws in the cylinder. Due to the described fixation, a slipping of the bony blocks could be completely avoided. Furthermore, attention was paid to mount the ligament in its anatomical direction of tension ((Fig. 7). During the test, the ligament was continuously moistened with saline (NACL 0.9 %). To determine the ligament’s tensile force during the inversion tests, the buckle transducer was again applied to the ligament in analogous manner and position and then connected to a multimeter. The testing machine strained the ligament until the buckle transducer achieved the same voltage value corresponding to the precedent inversion tests. Using testXpert software version 10.0
Knee Surg Sports Traumatol Arthrosc Table 1 Intra-class correlation coefficients (ICC) for test–retest and trial-to-trial reliabilities considering ankle inversion range of motion Reliability
Testing condition
Inversion [°]
ICC
Test–Retest
t1 (5 N) versus t2 (5 N) t1 (10 N) versus t2 (10 N) t1 (15 N) versus t2 (15 N) Trial 1 (5 N) versus Trial 2 (5 N) Trial 1 (5 N) versus Trial 3 (5 N) Trial 2 (5 N) versus Trial 3 (5 N) Trial 1 (10 N) versus Trial 2 (10 N) Trial 1 (10 N) versus Trial 3 (10 N) Trial 2 (10 N) versus Trial 3 (10 N) Trial 1 (15 N) versus Trial 2 (15 N) Trial 1 (15 N) versus Trial 3 (15 N)
15.3 ± 7.3 versus 17.5 ± 8.4
0.81
21.0 ± 6.3 versus 23.4 ± 8.6
0.80
26.4 ± 6.4 versus 28.3 ± 7.6 15.3 ± 7.3 versus 15.1 ± 7.4 15.3 ± 7.3 versus 15.4 ± 7.5 15.1 ± 7.4 versus 15.4 ± 7.5 20.8 ± 6.5 versus 20.9 ± 6.2 20.8 ± 6.5 versus 21.5 ± 6.8 20.9 ± 6.2 versus 21.5 ± 6.8 25.8 ± 5.9 versus 26.4 ± 6.6 25.9 ± 5.9 versus 26.9 ± 6.9
0.89
26.4 ± 6.6 versus 26.9 ± 6.9
0.99
Trial to trial
Trial 2 (15 N) versus Trial 3 (15 N)
Fig. 7 Harvested CFL mounted in a hydraulic testing machine
0.97 0.91 0.98 0.97 0.93 0.99 0.98 0.96
Figures as means and ± SDs
(Zwick GmbH & Co KG, Ulm, Germany), the tensile force of the CFL was then registered. Values are given in Newton, rounded after one decimal. Consideration of the particular tensile force of the CFL is given in relation to the inversion angle as well as to the amount of external force. Statistical analysis To determine the trial-to-trial and test–retest reliabilities, the intra-class correlation coefficient (ICC) was calculated using IBM SPSS Statistics 21 Software (IBM Germany GmbH, Ehningen, Germany). The level of significance was set at p 0.80, ranging between 0.80 and 0.90. Trial-to-trial reliability for inversion range of motion and torsional joint stiffness
t1 test-point 1, t2 test-point 2, ICC intra-class correlation coefficient
varied between 0.91 and 0.99. Means and corresponding standard deviations for the single results, as well as the resulting ICCs, are shown in Tables 1 and 2. Cadaveric testing A total of 8 specimens were tested over a complete testing cycle. Mounted to the testing machine, the corresponding
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Table 3 Mean CFL tensile loads at the different applied loads Applied load (N)
CFL tensile force [N]
5 10
31.9 ± 14.0 51.0 ± 15.8
15
75.4 ± 21.3
Figures as means and ± SDs
registered force of the buckle transducer equalled a mean ligament tensile force of 31.9 (±14.0) N with an applied force of 5 N, a tension load of 51.0 (±15.8) N at 10 N and 75.4 (±21.3) at 15 N. Table 3 summarizes the corresponding tensile force of the CFL with the three different applied external forces of 5, 10 and 15 N to the lever arm, equalling an initial torque of 1, 2, or 3 Nm, respectively.
Discussion The most important finding of the present study was the construction, description and validation of a highly reliable and reproducible, non-radiographic ankle arthrometer to individually measure an uninfluenced passive inversion range of motion, as well as to evaluate the tensile strain of the uninjured calcaneofibular ligament and the torsional joint stiffness at predefined, standardized loads. Rather than differentiating between stable and unstable, the results show that the inversion degrees measured with the ankle arthrometer at predefined loads can individually be correlated with the tensile ligament strain of the intact CFL. Preventing ankle injuries in professional sports have been of increasing scientific interest over the past decades [5, 6, 11, 15, 17, 22, 31, 35]. To protect ligaments successfully and individually, achieving a clear understanding of basic knowledge about physiologic joint and ligament properties and loading seems inevitable. Particularly, because the inversion range of motion of ankle joints varies individually, it was not intended to determine a degree-depending threshold for a higher risk of ligament injury. In fact, it was rather aimed to measure a subject individual amount of joint deflection at predefined loads which can also be correlated with the strain of the CFL. In future investigations, this might help to limit an athlete (or patient) not to a certain, standardized amount of joint deflection, relying on a non-individualized threshold, but individually respecting his or her individual ankle range of motion. Reliability Our results revealed an excellent test–retest and trialto-trial reliabilities with an ICC between 0.80 and 0.99
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for the single test situations and with regard to data from recent publications [10–12, 20, 21]. For example, De Vries et al. [10] published an intra-tester reliability of 0.74 and an inter-tester reliability of 0.76 for the talar inversion test using a LigMaster Joint arthrometer in 30 participants. The dynamic anterior ankle tester (DAAT), as well as the quasi-static anterior ankle tester (QAAT) of Kerkhoffs et al. [18, 20, 21], in fact, was established for anterior talar displacement. Both were first appraised to have a high reliability between 0.70 and 0.90 in 24 healthy subjects and 14 patients 1 year after acute lateral ankle ligament injury [20, 21]. The DAAT could not prove its reliability of earlier studies in a subsequent clinical evaluation [10]. A recently presented arthrometer by Nauck et al. [25–27] to distinguish between stable and unstable talofibular ligaments revealed an “excellent” ICC of 0.80. Assessing stress radiographs using the widely used Telos stress device was found to reveal accurate inter- and intra-observer reliability, [24] though obtained results are known to be difficult to interpret due to high variability [13]. In addition, Docherty et al. [11] considered the comparison of different ankle testers as difficult, as different amounts of force or torque were applied in the respective methodological set-ups. Furthermore, they found the force application mechanisms of the different testers hard to standardize. Finally, these and other studies were limited by their inability to quantify muscle activity of subjects during the special tests [10, 11], influencing the reliability as well as the results of the tested ankle arthrometer. By monitoring the muscle activity of the tested subjects and standardizing the position of the ankle and the applied force, we were able to eliminate all of the above-mentioned limitations, explaining the good reliability results. Cadaveric testing Several methods of cadaveric ligament strain testing have been published so far, amongst which mounting harvested ligaments in hydraulic testing machines [1], instrumenting ligaments with directly applied strain gauges [9, 30] or using buckle transducers [3] are the most common. However, to date, direct or at least transferred force measurements in intact ankles are not available. Furthermore, transferring obtained in vitro data to an equivalent in vivo test apparatus in order to derive conclusions for the intact ankle for preventive instead of diagnostic purpose has been scientifically unconsidered until now. The ankle arthrometer allows the detection of a passive ankle inversion angle produced by standardized forces and with monitored, inactivated evertor muscles. Subsequently, the ankle inversion angles can be correlated with an assumed tensile force of the intact CFL. For example, the amount of passive inversion angle at an applied force of
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15 N (initial torque of 3 Nm) reveals not only the particular joint deflection and joint stiffness but also the ligament tensile load of approximately 70 N at this deflection. A clear advantage of the described method is that—compared to other studies—the experimental set-up respects the high variability of ankle joint deflection as well as the widely varying loads to failure of ankle ligaments from one ankle to another [1, 3]. Several ligament strain test set-ups worked with predefined ankle positions [9, 28], instead of considering the variability of ankle deflection. Applying standardized torques to the ankle which causes a certain, individual degree of deflection, reversely allows more individual load correlations. The length and strain of the lateral ankle ligaments depend on the position of the foot, with respect to the degree of inversion–eversion, plantarflexion and dorsiflexion [3, 28], and not least to a little amount of 2.5 % on subjects axial loading [3, 8]. However, the registered tensile forces of the current study are consistent with the results of Bahr et al. [3], who also registered ligament forces using buckle transducers in cadaveric specimens. Differing between an axially loaded (375 Newton) and an unloaded situation as well as between different positions of the foot, they revealed a CFL ligament force of 60–70 N when applying 3.4 Nm torque to the cadaveric ankle [3]. Beyond this, they registered the highest strain of the CFL in either 20° plantarflexion or 10° dorsiflexion with simultaneous compressive loading, even though these maximum loads did not exceed a mean of 109 N, about one-third of the failure load of the respected ligament [1, 3]. In ten human ankle specimens, Colville et al. [9] applied a 3-Nm inversion torque after instrumenting the ligaments with strain gauges. They found the highest ligament strain of the LFC when inverting the ankle by increasing amounts when simultaneously dorsiflexed. Their study group did not transfer their results to an in vivo tester, nor did they determine quantitative tensile forces of particular ligaments. Measuring the ligament’s force with an indirect method, Nigg et al. [28] measured a CFL force of 46.3 N at maximal inversion and dorsiflexion in three cadaveric specimens. Their comparably low loads might be due to the fact that they moved the ankle in 36 different positions but did not apply an additional load to the ankle. Some limitations of this study have to be specified. Compared to an injury situation, the applied loads to the ankle in our study were comparably low and it might be doubted whether adequate ligament strain was created. Congruently, Tohyama et al. [33] also demonstrated in their cadaveric tests that lower loads rather than higher loads caused ankle translations [33]. Furthermore, investigating ankle ligaments especially at low loads, Butler et al. [7] examined ligament properties within a physiologic range. Bahr et al. [3] also applied a torque of only 3.5 Nm to
achieve their strain curves. Furthermore, a video analysis of Nauck et al. [27] confirmed that the ankle joint is already in a slightly deflected position at low loads. Furthermore, the soft tissue and ligament properties of the cadaveric tests may not be directly transferred to an in vivo situation, though previous studies confirmed that freezing has little or no effects on biomechanical properties of ligaments [1, 29]. However, the passive soft tissue slack (peroneal tendons even when unstrained, subcutaneous soft tissue skin etc.) needs to be considered, since there is a complex synergistic relationship between all soft tissue stabilizers in the intact ankle [3, 27]. However, instrumenting any measuring device to the CFL requires dissection of the subfibular soft tissue and the peroneal tendons making this limitation unavoidable. At least by monitoring the inactivated evertor muscle during in vivo testing, both test conditions could be adjusted as similar as possible. Not least, the simultaneous strain and property testing of the anterior talofibular ligament (ATFL) was not done but would have been interesting. It was intended to do so in the beginning, but preliminary tests revealed that neither the anatomical position of the ATF ligament nor its mean length and width would allow an appropriate, completely exposed and small buckle transducer to be instrumented without risking an impingement. Ozeki et al. [30] al. also claimed limitations with regard to using buckle transducers due to the ankle ligament’s anatomical prerequisites. This is in contrast to Bahr et al. who instrumented the ATFL as well as the CFL. However, their transducers have shown acceptable accuracy in the past [2]. Finally, in addition to an intra-observer reliability, a inter-observer reliability would have been desirable, assuring the measuring devices applicability at different facilities and with different investigators. Nonetheless, the present results might help to understand more about physiologic ligament loading in correlation with individual joint movements in intact ankles. Subsequently, in all day practice, in the future, this might support to reduce a subject-specific injury risk by applying individually adaptable protections.
Conclusion The PLLT is a highly reliable measuring device which allows some objective conclusions of intact ankle ligament properties and thus of ankle joint stability at predefined standardized loads without any muscular hindrance. Determining objectively individual joint deflections paired with the knowledge of ligament strain especially in professional sports, might help to quantify an athlete’s injury risk in more detail and consequently find appropriate, individually adapted, prevention measures, adequate to prevent
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injury and loose enough to avoid the perception of being hindered. Further studies are required to obtain more information in different ankle flexion positions, as well as about the talofibular ligament or even the deltoid ligament. The authors declare that they have no conflict of interest.
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