Contractile forces are transmitted to the skeleton through tendons. Numerous in vitro studies have shown that although tendons are stiff enough to act as effective force transmitters, they exhibit a time-dependent behaviour (e.g. Bennett et al. 1986). However, relying exclusively on results from experiments on isolated specimens when seeking to interpret physiological function may be inappropriate because in vitro testing necessitates application of conditions that deviate largely from the physiological environment of tendon. For example, the clamps used in in vitro testing may allow specimen slippage and artifactual elongations. Moreover, in contrast to physiological conditions, a specimen under in vitro conditions is biologically inert and is often tested after preservation and storage, which may alter the properties of the material.

We recently developed a method for in vivo quantification of the load-elongation response of human tendon (Maganaris & Paul, 1999, 2000). In this method, tendon loads are generated by contraction of the in-series muscle, and the resultant tendon elongations are taken from ultrasound-based measurements of the displacement of an anatomical landmark in the tendon proximal end. To avoid displacements in the tendon bony attachment, the contractions are elicited isometrically. The muscle moments generated by contraction are quantified using dynamometry, reduced to tendon forces using information about moment arm lengths obtained from analysis of magnetic resonance images (MRIs), and then combined with the respective tendon elongations to obtain the tendon force-elongation relation. Reduction of the force-elongation relation to the dimensions of the tendon, obtained again from analysis of MRIs, yields the stressÐstrain relation of the tendon.

We applied the above principles to examine the mechanical behaviour of the highly stressed and spring-like acting human gastrocnemius (GS) tendon, and the less highly stressed human tibialis anterior (TA) tendon. Our results from measurements in six healthy volunteers showed that, at forces corresponding to the maximal isometric muscle force, either tendon has a Young’s modulus of ~1.2 GPa, which is in line with in vitro results (Bennett et al. 1986) and suggests that the material of tendon does not adapt to produce a stiffer or more compliant structure in response to differences in the physiological loading applied. The mechanical hysteresis of either tendon was found to be ~ 19 %, which is larger than the average value of ~10 % reported from in vitro tests (Bennett et al. 1986), indicating that in our in vivo method heat loss form sources other than the tendon occurs, e.g. in the myotendinous and osteotendinous junctions and due to surface friction between the tendon and its surrounding tissues. In the GS tendon, the heat loss levels found could implicate the development of hyperthermia due to the high and repeated loading applied, predisposing the tendon to mechanical failure.

A second series of experiments were carried out to quantify the extent to which in vivo tendons exhibit force relaxation, i.e. a decrease over time in the force required to produce a given elongation. The experiments were performed in the human GS tendons of six healthy volunteers performing repeated isometric plantarflexion contractions-relaxations. Our results showed that the plantarflexion moment required to produce tendon elongations of 7 and 11 mm (7 mm corresponds to the tendon elongation during slow walking, Fukunaga et al. 2001; 11 mm corresponded to 90 % of the maximal elongation in the experiments) decreases by ~17 % in five consecutive contractionÐrelaxation cycles, following a curvilinear pattern as a function of cycle number. The relaxation found is in line with experiments from previously unloaded, ‘unconditioned’ tendons (Haut & Powlison, 1990), indicating that ‘conditioning’ is a relevant property of tendon and not a clamping-induced artifact.

The relaxation of in vivo tendon would allow the in-series muscle to shorten more as a function of cycle number and therefore reduce its fascicular length and increase its pennation angle, a hypothesis tested in a separate experiment. Indeed, repeated plantarflexion contractions at 80 % of the maximal plantarflexion moment altered the fascicular length and pennation angle as predicted, following the force relaxation pattern of the in-series tendon. The total reduction in fascicular length was ~12 %, which according to the cross-bridge mechanism of contraction would reduce the force-generating potential of the muscle by ~5 % compared with the first contraction. The total increase in pennation angle was ~20 %, which according to a simple planimetric muscle-tendon model would decrease the maximal plantarflexion moment produced by ~10 % compared with the first contraction.

To conclude, our results indicate that in vivo tendons do not behave as rigid structures, but exhibit viscoelastic properties as those seen when testing in vitro material. These findings have functional implications for contractile force generation and joint movement.

All procedures accord with the Declaration of Helsinki.