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Documentation:FIB book/Injury Tolerance of the Achilles Tendon in Different Loading Conditions: Applications to High-Impact Sports

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Introduction

Dorsiflexion and plantar flexion.

Connecting muscles to bones, tendons act as “mechanical bridges” which move bones and joints through muscle actuation [1]. Mainly composed of collagen, the tendon is very elastic and is able to store and return 90-95% of the applied energy. As such, the achilles tendon (AT), connecting the calcaneus bone of the heel to the posterior leg muscles, plays a very important role in human movement [2][3]. During active tasks such as running or jumping, the AT facilitates the plantar flexion of the foot and the absorption of ground reaction forces upon landing. The loads on the AT, measuring between 70 to 110 MPa of peak stresses, are much larger than the 30 MPa that other tendons of the body experience on average [2][4]. Large levels of torque due to jumping, rapid acceleration and deceleration, and running in high-impact sports have caused the AT to make up 45% of all tendon rupture cases [4][5].

The late Kobe Bryant famously shooting free throws, after tearing his AT during an NBA game in 2013.

AT ruptures can prove detrimental to the career of professional athletes, with a common example being in the realm of basketball. Studies in the National Basketball Association (NBA) conclude that many players do not return to play after an AT rupture, or significantly regress in performance [3][6]. For example, the player efficiency rating (PER) is a paramount measure that quantifies a player’s efficiency and impact on the game, and many players faced statistically significant declines (p-value = 0.04) after their return [6].

Consequently, the AT has become a very popular tissue to analyze over the past 50 years [2], with many research groups contributing to characterizing injury tolerances of the AT under different biomechanical conditions. The purpose of this paper is to investigate and synthesize literature surrounding the peak forces that the AT can sustain before failure in both static and dynamic loading environments. This paper prioritizes studies relating to sports settings as it is a direct application of AT research. Research gaps are identified to motivate future work in this field.

Testing methodologies, keywords and terminology are defined in Table 1.

Table 1. Relevant terminology for AT experiments

Terminology Definitions Relevant Papers
“Stress” Measured quantity, given as the load over the cross-sectional area (CSA) of the AT. Because the CSA varies along the length, the smallest area is often taken to obtain peak stresses acting on the tissue (2). N.A.
“Strain” Measured quantity; given as a percentage of changed length over the original length. N.A.
“Strain Rate” Experimental quantity; given in units of (mm/s). The rate of deforming the AT sample. [7][8][9]
“Young’s Modulus” Measured material property that conveys the stiffness of the material. Given in the same units as stress. Quantifies the AT’s resistance to deformation. [7][9][10]
“Ultimate Tensile Stress” (UTS) Measured material property; the maximum stress experienced by the AT before failure. [7][10][11]
“Cyclic Loading” Loading property; loading the sample and releasing in a sinusoidal manner. The tendon in particular demonstrates “hysteresis”, where there is lag in returning to a relaxed state. The accumulation of cyclic loading degenerates the tissue mechanics, causing rupture in different cases. [7]
“Creep” Loading property; holding the sample under load for a constant period of time. [7]
“Ex-vivo” Testing outside the body; in this context broadly refers to cadaveric testing. By testing on cadavers, destructive testing can be conducted, obtaining both quasi-static and dynamic loads for AT failure. [7][10][11][12]
“In-vivo” Testing within the living organism; in this context refers to live human testing. Because injury can not be applied during motor function, even on animal models, the testing is limited to analyzing video data of coincidental injury occurrence. Strain, joint angles, and body weight were all corroborated to achieve AT forces for rupture. [8][9][13][14][15][16][17]

A number of hardware devices are often implemented in AT studies to extract force and tensile metrics. Table 2 below summarizes some of the commonly used instrumentation that is used to measure forces and strains on the AT, which will be further discussed in this paper

Table 2. Instrumentation commonly used to obtain metrics

Instrument Application Relevant Papers
Force transducer In-vivo measurement of non-destructive loading [14]
Tensile tester Ex-vivo rupture testing of cadaver tendons [7][18]
Force plate Ex-vivo measurement of tendon force curve [8][13][19][20]
Markerless Capture Video analysis of joint kinematics, rupture mechanisms [15][21]

Ex-Vivo Analysis of AT Loading

Typical methodologies of testing

One of the methodologies for testing the failure limits of the AT is ex-vivo cadaveric testing, which involves isolating the AT from a cadaver and experimentally loading it in a laboratory setting. In particular, previous studies have employed this methodology by loading AT samples into a servo-hydraulic testing machine, while incorporating a 30-degree angle with the calcaneus to simulate anatomical foot positioning [11]. The samples are fixated by a PMMA/aluminum fixture. Additionally, some experimental setups also involved gluing glass beads at 1-1.5 cm intervals along the AT length to aid in video analysis [10]. AT strain is often computed using Digital Image Correlation (DIC), which involves the use of cameras to capture consecutive images of the AT, and then analyzing it in specialized software [12]. This allows the study of local deformations and stress fields within the AT [11]. As opposed to constant-strain loading, creep-relaxation experiments have also been performed until failure to analyze the viscoelastic properties of the AT. In one example, cyclic tests at 1 Hz were performed to apply sinusoidal loading between 10 and 80 MPa [10]. For the creep testing, the AT sample was held constant at 35, 40, 45, 50, 55, 60, 65, 70, and 76 MPa until failure occurred [7]. For these experiments, ultrasound imaging is used to measure the CSA of each tendon, and clamps that are cooled with liquid nitrogen are used to fixate the tendons in place [7][22]. In order to maintain tissue properties, the experiments take place at 35℃ [7].

Failure Thresholds of the Achilles Tendon (Quasi-static loads)

One of the studies that utilized the servo-hydraulic press measured the ultimate tensile strength (UTS) of n=20 different AT samples from cadavers under a loading rate of 1.33 mm/s [10]. The UTS across the sample ranged from 360-1965 N, with an average of 1189 N [10]. It was reported that there was no correlation between the UTS and CSA of the AT [10]. Furthermore, the authors measured the elastic moduli of the AT samples, denoting a range of 159-1154 N/mm2 [10].

A more recent study that utilized the servo-hydraulic press preconditioned the AT samples with 10 cycles of pre-load to 2% strain [11]. After that, the samples were subjected to a displacement-controlled tensile strain of 5 mm/s until total rupture of the tendon [11]. The authors reported that failures occurred in the mid-substance portion of the AT, at an average load of 5649.1 ± 565.5 N (n=5) [11]. Interestingly, 5 other AT samples had tendons that did not reach failure, due to calcaneus avulsions (heel bone fractures) [11]. Furthermore, DIC strain data showed that high strains applied to the AT are initially absorbed by the proximal region of the tendon, which may explain the high frequency of mid-substance injuries [11]. Compared to the older results from Louis-Ugbo et. al [10], the more recent studies seem to point toward a much higher UTS, but this could be explained given that the authors included the distal third of the soleus and gastrocnemius muscles in the AT samples (see Figure 1). Furthermore, it’s worth noting that higher loading rates seem to result in an increased tendon strength, which is consistent with small viscoelastic effects in-vivo, as reported by Rosario et al. [23]

AT Failure Thresholds in Cyclic Loading

As previously mentioned, creep relaxation testing has also been performed in the literature, which consists of applying a constant load over time (at a low strain rate), which is helpful when attempting to measure viscoelastic properties of the AT, as well as certain stretched positions often seen in high-impact sports like basketball, tennis, and soccer [9]. With respect to the AT, this is computed by the ratio of the Young’s modulus before and after the loading. When 43 ATs were subject to cyclic loads of varying frequencies, and then held constant until tendon rupture, the results showed that the initial strain that often causes most ruptures occurs at stresses of 30-40 MPa [7]. However, this data contained a lot of variability due to age and sex confounds [7]. Given that high-impact sports such as basketball, badminton, and running consist of cyclic loading on the AT, this research may provide further insights into injury mechanisms and possible preventative techniques that could be adopted.

In-Vivo Analyses of AT Loading

Video Analysis and Kinematics

Injury biomechanics of AT rupture in sports is commonly characterized using video. Videos can capture unrestricted movement in natural sports environments. For instance, video analysis of AT rupture in soccer revealed that 94% of injuries were non-contact [16]. These videos also demonstrate that the knee is in extension in 97% of cases, with 92% of ruptures occurring during the knee flexion-extension transition. Video analysis can also locate the moment rupture occurs, which 60% of the time is through a running stance [17][20]. This can be explained by the function of the gastrocnemius as a shock absorber, since the AT facilitates the flow of energy into this muscle. Sudden knee extension and unexpected ankle eversion causes rapid loading in the AT [20]. The elevated mechanical energy in the tendon ruptures it if it cannot be dissipated in time.

Video analysis visualizes the loading conditions that can lead to AT rupture. Videos in controlled environments can quantify ankle and joint angles under different loading phases. Sudden knee extension is usually accompanied by high dorsiflexion at the start of a stance. This heightens the energy barrier that must be overcome for plantar flexion [20]. When coupled with hyperpronation, the AT is stretched beyond normal loading conditions [21]. Hyperpronation misaligns the tendon with the loading direction of the gastrocnemius. Ultimately, these two loading conditions greatly increase the risk of rupture, though the risk is not quantified [20][21]. These findings from video analysis propose loading mechanisms that result in AT rupture.

Peak Forces under Normal Loading

In-vivo loading of the AT during landing phase, described by body weight.

ATFs under normal conditions are characterized using anatomical models and external force data. The AT moment arm can be determined from MRI and ultrasound using the center of rotation and tendon as reference locations. An example equation for the AT moment arm as a function of ankle plantar flexion angle (θ) is shown below (Equation 1).

ATmoment arm=0.591+0.08297θ0.00026062θ2


Equation 1. AT moment arm as a function of ankle plantar flexion angle [16]

Peak ATF forces vary with loading conditions. During walking, the peak ATF is approximately 2.5 times body weight (BW) [20]. This force rises to 6-8 times BW in jumping and running. This equates to roughly 5000 to 6000 N for most athletes [17]. The peak ATF is found near 60% of the phase, which is consistent with video analysis of actual AT rupture during running [13][21]. Figure 3 depicts the typical AT force over landing phases from jumping. This figure was developed based on a culmination of figures from studies on landing normal locomotive forces [8][19][20].

Peak ATFs can be correlated with ground reaction forces (GRFs), anatomical angles, and rate of loading. The greatest contributors are GRFs, where a one BW increase in GRF can result in up to 3.2 BW increase in ATF [19]. Larger hip flexion angles can also reduce peak ATFs due to the dissipation of energy throughout the lower limbs. Another predictor of peak ATFs is the rate of loading which is pronounced in high-intensity activities like running. Increased loading rates create higher peak ATFs due to the AT’s viscoelastic nature [17].

Rupture Mechanisms in Dynamic Loading

ATFs vary with landing mechanisms. One study found that ATFs were higher when athletes landed with stiff legs (2500 N) compared to their natural landing mechanism (2000 N) [8]. This finding is explained by the function of the gastrocnemius as a shock absorber. In stiff-legged landings, the ground reaction forces are conducted from the AT to the plantar flexor. Flat-footed landings result in the least ATF as the reaction force is mostly conducted through the bones. An analysis of the force-time curve also reveals that the natural landing mechanism distributes a lower ATF over a longer period of time. This finding suggests that peak forces are the primary contributor to achilles tendon ruptures. This theory agrees with the most commonly reported mechanism for achilles tendon rupture [24]. The stiff-legged landing mechanism mimics an athlete pushing off with an extended knee and plantar-flexed ankle. This mechanism poses the greatest risk for rupture as it exposes the achilles tendon to the highest peak forces.

In most rupture mechanisms, the AT is acting eccentrically. While most muscles contract to perform a function, the AT is an energy absorber in running and landing mechanisms [15]. The tendon resists excessive dorsiflexion by plantar flexing. The AT experiences peak stresses of 70 MPa during maximal eccentric plantar flexion [4]. This counterforce causes the AT to be the most common tendon to rupture spontaneously.

Discussion

Overall, this review described the failure thresholds and injury mechanisms of the AT in both ex-vivo and in-vivo environments. In spite of differences in study methodologies, such as variations in specimen preparation, there was still an established range of UTS values reporting 360 to 1965 N [10][11]. These estimates have been improved by more recent work employing DICs and servo-hydraulic testing [12], which identified mid-substance ruptures as the most frequent failure mode, subsequently reporting higher failure loads of approximately 5649 N [11]. Dynamic loading experiments also showed that rupture thresholds are strain-rate and cyclic-loading dependent, attaining initial strains of 30-40 MPa prior to failure [7]. Through force transducer and video recordings, in-vivo experiments have also supported these ex-vivo findings by associating AT ruptures with certain movement patterns, such as abrupt dorsiflexion with knee extension [20]. The AT faces peak forces of 6-10 times BW during high-impact activities [17][20], conveying its susceptibility to overload in sports.

Problems and Controversies with Current Methods

In general, there are several difficulties with studying the forces on the AT, which has resulted in a limited amount of ex-vivo research being performed on AT specimens. One of these difficulties is the limited supply of fresh human achilles specimens, which is currently the best way to obtain anatomically-accurate loading reactions [11]. While AT ruptures most frequently occur in young, active populations, the majority of the cadaveric specimens are from older individuals. Nagelli’s research group utilized cadavers with a mean age of 42 [11], while Louis-Ugbo’s studies collected cadavers ranging from age 57-93 [10]. These age differences introduce potential age biases, challenging the relevance and applicability of these studies in a high-impact, sports environment. Our understanding of AT failure mechanics in relevant populations is limited by these inherent factors of ex-vivo studies.

Furthermore, there can be difficulties with securely fixing the AT in an anatomically accurate position, which limits the clinical validation of these current studies [11]. In the selected papers for analysis, there is also some inconsistency regarding which structures are kept on the AT during cadaver dissection, as some studies kept components of the posterior muscles (gastrocnemius and soleus) attached to the AT before testing. This seemed to correspond to a large discrepancy in UTS values, making it quite difficult to truly narrow down on a consistent injury threshold of the AT [10][11][18]. In the present research, it is evident that there is a large variation in UTS values across cohorts of samples [10][11], which could point towards the possibility of many confounding variables affecting the UTS values, such as surrounding muscle strengths, prior lower limb fractures, and reduced plantar flexor strength [25].

Future Work

Most research on rupture mechanics quantifies ATFs in ideal loading environments, but competitive sports often produce complex loading conditions [19]. ATFs are also estimated using anatomical models from GRFs, while video analyses estimate forces based on angles and anatomical features [15][21]. These estimates are minimally accurate, demonstrating the gaps in direct in-vivo measurements of AT rupture forces. While some approaches use accelerometers to supplement the GRF data, these sensors have the potential to introduce variability due to motion artifacts [8]. Further development of force approximation techniques will enable more direct quantification of GRFs in natural sport environments. For example, new technologies like biplanar fluoroscopy can improve AT force quantification, particularly during landing or a gait cycle [26]. This technology can potentially be integrated with GRF and electromyography (EMG) to quantify ATFs with loading phases and muscle activation. This information can also be used to validate computational models, expanding the tools available to study AT loading mechanisms.

Material properties of the AT also need to be addressed through future experimentation, as existing properties are determined under quasi-static loading conditions. While ATFs do vary with strain rates, quantifying ATFs by varying loading rates is more representative of real-world conditions [8]. These tests will measure ATFs beyond peak forces in complex loading conditions, which will allow rupture prediction based on impact duration and loading rate. This information can be used to aid athletes in altering movement patterns to avoid rapid loading.

There is also little research that predicts an athlete’s risk to AT rupture based on fatigue and training stress. Epidemiological studies identify pre-existing factors but do not address activity-related changes in AT health. By quantifying the fatigue state of the AT, these values could motivate the development of training programs that reduce the risk of rupture. Future work can also investigate the efficacy of conditioning programs that train the AT, as they are more susceptible to rupture under untrained loading conditions. The various approaches presented can help prevent and minimize the risk of AT rupture.

References

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