Falk Mersmann

Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults

BackgroundThe present article systematically reviews recent literature on the in vivo adaptation of asymptomatic human tendons following increased chronic mechanical loading, and meta-analyzes the loading conditions, intervention outcomes, as well as methodological aspects.MethodsThe search was performed in the databases PubMed, Web of Knowledge, and Scopus as well as in the reference lists of the eligible articles. A study was included if it conducted (a) a longitudinal exercise intervention (≥8 weeks) on (b) healthy humans (18 to 50 years), (c) investigating the effects on mechanical (i.e., stiffness), material (i.e., Young’s modulus) and/or morphological properties (i.e., cross-sectional area (CSA)) of tendons in vivo, and was reported (d) in English language. Weighted average effect sizes (SMD, random-effects) and heterogeneity (Q and I2 statistics) of the intervention-induced changes of tendon stiffness, Young’s modulus, and CSA were calculated. A subgroup analysis was conducted regarding the applied loading intensity, muscle contraction type, and intervention duration. Further, the methodological study quality and the risk of bias were assessed.ResultsThe review process yielded 27 studies with 37 separate interventions on either the Achilles or patellar tendon (264 participants). SMD was 0.70 (confidence interval: 0.51, 0.88) for tendon stiffness (N=37), 0.69 (0.36, 1.03) for Young’s modulus (N=17), and 0.24 (0.07, 0.42) for CSA (N=33), with significant overall intervention effects (p<0.05). The heterogeneity analysis (stiffness: I2=30%; Young’s modulus: I2=57%; CSA: I2=21%) indicated that differences in the loading conditions may affect the adaptive responses. The subgroup analysis confirmed that stiffness adaptation significantly (p<0.05) depends on loading intensity (I2=0%), but not on muscle contraction type. Although not significantly different, SMD was higher for interventions with longer duration (≥12 weeks). The average score of 71±9% in methodological quality assessment indicated an appropriate quality of most studies.ConclusionsThe present meta-analysis provides elaborate statistical evidence that tendons are highly responsive to diverse loading regimens. However, the data strongly suggests that loading magnitude in particular plays a key role for tendon adaptation in contrast to muscle contraction type. Furthermore, intervention-induced changes in tendon stiffness seem to be more attributed to adaptations of the material rather than morphological properties.

Human Achilles Tendon Plasticity in Response to Cyclic Strain: Effect of Rate and Duration

High strain magnitude and low strain frequency are important stimuli for tendon adaptation. Increasing the rate and duration of the applied strain may enhance the adaptive responses. Therefore, our purpose was to investigate the effect of strain rate and duration on Achilles tendon adaptation. The study included two experimental groups (N=14 and N=12) and a control group (N=13). The participants of the experimental groups exercised according to a reference protocol (14 weeks, four times a week), featuring a high strain magnitude (~6.5%) and a low strain frequency (0.17 Hz, 3 s loading/3 s relaxation) on one leg and with either a higher strain rate (one-legged jumps) or a longer strain duration (12 s loading) on the other leg. The strain magnitude and loading volume were similar in all protocols. Before and after the interventions, the tendon stiffness, Youngs modulus and cross-sectional area were examined using magnetic resonance imaging, ultrasound and dynamometry. The reference and long strain duration protocols induced significantly increased (P<0.05) tendon stiffness (57% and 25%), cross-sectional area (4.2% and 5.3%) and Youngs modulus (51% and 17%). The increases in tendon stiffness and Youngs modulus were higher in the reference protocol. Although region-specific tendon hypertrophy was also detected after the high strain rate training, there was only a tendency of increased stiffness (P=0.08) and cross-sectional area (P=0.09). The control group did not show any changes (P=0.86). The results provide evidence that a high strain magnitude, an appropriate strain duration and repetitive loading are essential components for an efficient adaptive stimulus for tendons.

Evidence of imbalanced adaptation between muscle and tendon in adolescent athletes

Adolescence may be regarded as a critical phase of tissue plasticity in young growing athletes, as the adaptation process of muscle‐tendon unit is affected by both environmental mechanical stimuli and maturation. The present study investigated potential imbalances of knee extensor muscle strength and patellar tendon properties in adolescent compared with middle‐aged athletes featuring long‐term musculotendinous adaptations. Nineteen adolescent elite volleyball athletes [(A), 15.9 ± 0.6 years] and 18 middle‐aged competitively active former elite volleyball athletes [(MA), 46.9 ± 0.6 years] participated in magnetic resonance imaging and ultrasound‐dynamometry sessions to determine quadriceps femoris muscle strength, vastus lateralis morphology and patellar tendon mechanical and morphological properties. There was no significant age effect on the physiological cross‐sectional area of the vastus lateralis and maximum knee extension moment (P > 0.05) during voluntary isometric contractions. However, the patellar tendon cross‐sectional area was significantly smaller (A: 107.4 ± 27.5 mm2; MA: 121.7 ± 39.8 mm2) and the tendon stress during the maximal contractions was significantly higher in adolescent compared with the middle‐aged athletes (A: 50.0 ± 10.1 MPa; MA: 40.0 ± 9.5 MPa). These findings provide evidence of an imbalanced development of muscle strength and tendon mechanical and morphological properties in adolescent athletes, which may have implications for the risk of tendon overuse injuries.

Asymmetry of Achilles tendon mechanical and morphological properties between both legs

Although symmetry of Achilles tendon (AT) properties between legs is commonly assumed in research and clinical settings, different loading profiles of both legs in daily life (i.e., foot dominance) may affect the tendon properties in a side‐depended manner. Therefore, AT properties were examined with regard to symmetry between legs. Thirty‐six male healthy adults (28 ± 4 years), who were physically active but not involved in sports featuring dissimilar leg load participated. Mechanical and morphological AT properties of the non‐dominant and dominant leg were measured by means of ultrasound, magnetic resonance imaging and dynamometry. The AT of the dominant leg featured a significant higher Youngs modulus and length (P < 0.05) but a tendency toward lower maximum strain (P = 0.068) compared with the non‐dominant leg. The tendon cross‐sectional area and stiffness were not significantly different between sides. The absolute asymmetry index of the investigated parameters ranged from 3% to 31% indicating poor AT side symmetry. These findings provide evidence of distinct differences of AT properties between both legs in a population without any sport‐specific side‐depended leg loading. The observed asymmetry may be a result of different loading profiles of both legs during daily activities (i.e., foot dominance) and challenges the general assumption of symmetrical AT properties between legs.

Ultrasound does not provide reliable results for the measurement of the patellar tendon cross sectional area

PURPOSE This study examined the reliability of patellar tendon cross sectional area (CSA) measurement using brightness mode ultrasonography. METHODS The patellar tendon CSA of fourteen participants was examined on two different days and at three different positions (proximal, median and distal). Five trials per day were conducted in each position, replacing the ultrasound probe on every trial. The images were examined by three different and equally experienced observers. We compared the mean of the five trials in each position to examine the day, observer and position effect. Further, Bland and Altman plots, root mean square (RMS) differences and intraclass correlation coefficients (ICC) were calculated. RESULTS There was a significant (p < 0.05) day, observer and position effect on the CSA, while the average ICC was 0.592. The Bland and Altman plots showed that differences between conditions or groups, should be in average lower than 37% or higher than 55% of the patellar tendon CSA to be important for clinical or intervention studies. CONCLUSION Our findings show low reliability of the method, which resulted from the low clarity and unclear visibility of tissue boundaries in the ultrasound images. Therefore, the measurement of the CSA of the patellar tendon using ultrasound does not provide accurate and reliable results.

Insufficient accuracy of the ultrasound-based determination of Achilles tendon cross-sectional area.

The accurate assessment of the Achilles tendon cross-sectional area (CSA) is a crucial prerequisite to investigate tendon adaptation and to calculate the tendon Young׳s modulus. Besides magnetic resonance imaging (MRI), ultrasonography emerged as an alternative imaging technique. The purpose of the present study was to assess the objectivity and reliability of the ultrasound-based methodology and its validity with respect to the established MRI-based assessment. The Achilles tendon CSA from 17 healthy males was assessed by ultrasonography at the proximal, medial and distal position five times each on two separate days and three observers segmented the CSAs. For the validation, MRI-based CSA measurements were provided accordingly. The analysis of the ultrasound-based method revealed significant observer and day effects (p<0.05), despite high intra-class correlation coefficients for the three observers (>0.93) and both days (>0.89), respectively. The mean typical percentage error of both days was 7.1%. Comparing both methods, ultrasonography underestimated (19%) the CSA values obtained by MRI (p<0.05). Although the correlation coefficients of both methods were high in all three positions (>0.88), the respective absolute difference of in average 12mm2 and limits of agreement of up to +28mm2 and -2mm2 (~37% of the mean CSA) evidence considerable inconsistency. Besides the dependency of the CSA determination from the observer, the ultrasound method is not sensitive enough to detect physiological changes in tendon morphology of the magnitude that is reported by intervention studies. Furthermore, the validity analysis revealed a lack of agreement between both methods. Therefore, the ultrasound-based methodology cannot be recommended for an accurate Achilles tendon CSA determination in vivo.

A wide number of trials is required to achieve acceptable reliability for measurement patellar tendon elongation in vivo

The purpose of the current study was to examine the reproducibility of patellar tendon elongation measurements using brightness-mode ultrasonography (BMU) during isometric knee extension contractions. We hypothesized that the measurement of the patellar tendon elongation during only one maximal voluntary isometric knee extension contractions would not provide reliable results and that a wide number of trials is required to achieve acceptable reliability. Ten participants (eight male and two female) performed 10 isometric knee extension contractions on two separate days (5 trials on each day). Using a modified knee brace, the ultrasound probe was firmly adjusted in the sagittal plane overlying the patellar tendon. The registered ultrasound images were analyzed by three different but equally trained observers. The reproducibility was examined by the calculation of the within-day, between-day and overall coefficient of multiple correlations (wCMC, bCMC and oCMC). The Spearman-Brown prophecy formula was use to estimate the required trials to achieve the desired reliability. The wCMC, bCMC and oCMC were in average 0.824, 0.798 and 0.770, respectively, suggesting a rather moderate reproducibility of patellar tendon elongation measurements. For a high reliability (≥0.95) of tendon elongation measurements 5-6 trials are required. Finally, the results revealed an independence of the measurements from days and observers.

Muscle and tendon adaptation in adolescent athletes: A longitudinal study

There is evidence that a non‐uniform adaptation of muscle and tendon in young athletes results in increased tendon stress during mid‐adolescence. The present longitudinal study investigated the development of the morphological and mechanical properties of muscle and tendon of volleyball athletes in a time period of 2 years from mid‐adolescence to late adolescence. Eighteen elite volleyball athletes participated in magnetic resonance imaging and ultrasound‐dynamometry sessions to determine quadriceps femoris muscle strength, vastus lateralis, medialis and intermedius morphology, and patellar tendon mechanical and morphological properties in mid‐adolescence (16 ± 1 years) and late adolescence (18 ± 1 years). Muscle strength, anatomical cross‐sectional area (CSA), and volume showed significant (P < 0.05) but moderate increases of 13%, 6%, and 6%, respectively. The increase of patellar tendon CSA (P < 0.05) was substantially greater (27%) and went in line with increased stiffness (P < 0.05; 25%) and reduced stress (P < 0.05; 9%). During late adolescence, a pronounced hypertrophy of the patellar tendon led to a mechanical strengthening of the tendon in relation to the functional and morphological development of the muscle. These adaptive processes may compensate the unfavorable relation of muscle strength and tendon loading capacity in mid‐adolescence and might have implications on athletic performance and tendon injury risk.

Muscle shape consistency and muscle volume prediction of thigh muscles

The present study investigated the applicability of a muscle volume prediction method using only the muscle length (LM), the maximum anatomical cross‐sectional area (ACSAmax), and a muscle‐specific shape factor (p) on the quadriceps vastii. LM, ACSAmax, muscle volume, and p were obtained from magnetic resonance images of the vastus intermedius (VI), lateralis (VL), and medialis (VM) of female (n = 20) and male (n = 17) volleyball athletes. The average p was used to predict muscle volumes (Vp) using the equation Vp = p × ACSAmax × LM. Although there were significant differences in the muscle dimensions between male and female athletes, p was similar and on average 0.582, 0.658, 0.543 for the VI, VL, and VM, respectively. The position of ACSAmax showed low variability and was at 57%, 60%, and 81% of the thigh length for VI, VL, and VM. Further, there were no significant differences between measured and predicted muscle volumes with root mean square differences of 5–8%. These results suggest that the muscle shape of the quadriceps vastii is independent of muscle dimensions or sex and that the prediction method could be sensitive enough to detect changes in muscle volume related to degeneration, atrophy, or hypertrophy.

Athletic training affects the uniformity of muscle and tendon adaptation during adolescence.

With the double stimulus of mechanical loading and maturation acting on the muscle-tendon unit, adolescent athletes might be at increased risk of developing imbalances of muscle strength and tendon mechanical properties. This longitudinal study aims to provide detailed information on how athletic training affects the time course of muscle-tendon adaptation during adolescence. In 12 adolescent elite athletes (A) and 8 similar-aged controls (C), knee extensor muscle strength and patellar tendon mechanical properties were measured over 1 yr in 3-mo intervals. A linear mixed-effects model was used to analyze time-dependent changes and the residuals of the model to quantify fluctuations over time. The cosine similarity (CS) served as a measure of uniformity of the relative changes of tendon force and stiffness. Muscle strength and tendon stiffness increased significantly in both groups (P < 0.01). However, the fluctuations of muscle strength were greater [A, 17 ± 7 (SD) N·m; C, 6 ± 2 N·m; P < 0.05] and the uniformity of changes of tendon force and stiffness was lower in athletes (CS A, -0.02 ± 0.5; C, 0.5 ± 0.4; P < 0.05). Further, athletes demonstrated greater maximum tendon strain (A, 7.6 ± 1.7%; C, 5.5 ± 0.9%; P < 0.05) and strain fluctuations (A, 0.9 ± 0.4; C, 0.3 ± 0.1; P < 0.05). We conclude that athletic training in adolescence affects the uniformity of muscle and tendon adaptation, which increases the demand on the tendon with potential implications for tendon injury.