Method and strain rate dependence of Achilles tendon stiffness

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Abstract

Tendon stiffness is calculated by dividing changes in tendon force by tendon elongation. For this purpose, participants are commonly asked to perform a maximal muscle contraction (“active” method). Alternatively tendon elongation can be achieved by means of a passive joint rotation (“passive” method). The purpose of this study was to compare Achilles tendon stiffness obtained from both methods across different tendon strain rates. Twenty adults performed a series of ramped maximum isometric plantarflexions of different durations. Passive ankle rotations of different angular velocities were also performed. Achilles tendon stiffness was obtained from a combination of motion analysis, isokinetic dynamometry and ultrasonography and compared across methods at three strain rates. At all strain rates, tendon stiffness obtained from the active method was 6% greater compared to the passive method. In spite of this systematic bias, there was good agreement between the methods. Intraclass correlation coefficients were greater than 0.98, and more than 95% of data points fell into the 95% confidence intervals. This agreement will be acceptable in many research contexts. We also found a linear increase in tendon stiffness with increasing strain rate, which must be taken into consideration when interpreting or reporting tendon stiffness.

Introduction

Muscle and tendon stiffness are important parameters when performing daily motor activities or sporting movements (Hof et al., 2002, Fukunaga et al., 2001). The stiffness of the body’s elastic tissues governs the storage and release of elastic potential energy, and humans take advantage of this to maximise movement efficiency (Lichtwark and Wilson, 2008, Maganaris and Paul, 1999). Within this context, tendon stiffness has been widely studied in athletic (Kubo et al., 2001, McNair and Stanley, 1996) and clinical populations (Vaz et al., 2006, Tardieu et al., 1982). The findings of such studies have led to an enhanced understanding of how tendon stiffness influences force production (Reeves, 2006) as well as how tendon stiffness adapts to changes in loading (Kubo et al., 2010, Seynnes et al., 2009).

Tendon stiffness is calculated by dividing the estimated tendon force by the tendon’s elongation (Kubo et al., 2002, Maganaris and Paul, 1999). For this purpose, participants are commonly asked to perform a maximal isometric contraction to shorten the muscle and thereby elongate the tendon (“active method”) (Kubo et al., 2002). An alternative method is to record tendon force and elongation from a passive stretch, applied by an isokinetic rotation (“passive method”) (Morse et al., 2008).

The choice of method is often driven by the specific purpose of an experiment and by the population of interest. For example, in clinical populations where patients with neuromuscular or musculoskeletal disorders may be unable to perform a maximal voluntary contraction (MVC) reliably (Tedroff et al., 2008), it may be more appropriate to use the passive method. The primary advantage of this method is that it allows for both tendon stiffness and muscle stiffness to be estimated (Morse et al., 2008). The disadvantage with this method is that that tendon stiffness can only be calculated at relatively low levels of force. The force-stiffness relationship has been shown to be non-linear (Rigby et al., 1959), as at lower tendon stiffness values the un-crimping of collagen fibrils causes significant tendon elongation. As a result, tendon stiffness is greater at high compared to low force levels (Mizuno et al., 2011).

A further variable, which may affect the comparability between stiffness obtained from the two methods, is the tendon’s strain rate. Tendons exhibit viscoelastic behaviour in response to stretch, meaning that tendon stiffness increases with an increased strain rate (Le Veau, 1992, Pearson et al., 2007). Thus, strain rate needs to be taken into consideration when comparing different methods of obtaining tendon stiffness.

A range of methods, which are likely to result in different strain rates have been used in the literature to obtain tendon stiffness, including the passive method (Mizuno et al., 2011, Morse et al., 2008), and several variations of the active method (e.g., fast MVC manoeuvres - Kay and Blazevich, 2009, Muraoka et al., 2005 or slow, ramped MVC’s - Waugh et al., 2012, Peltonen et al., 2010, Kubo et al., 2002). Such differences in strain rates could potentially explain the relatively large range of tendon stiffness values reported across these studies. Thus, it is important to understand whether the passive and active methods are comparable to interpret findings from the literature appropriately and to compare results from studies employing different methodologies. Such an understanding would also enable researchers to make more informed decisions about the most appropriate method to use within a specific research context. Therefore the purpose of this study was to compare tendon stiffness obtained from the active and passive methods across different strain rates.

Section snippets

Participants

With institutional ethical approval, 20 healthy adults participated in this study (11 male, 9 female; age 24 ± 4 years; stature 1.78 ± 0.09 m; mass 74.9 ± 13.0 kg). All participants were recreationally physically active and free from known neuromuscular or musculoskeletal problems. Written consent was obtained from all participants prior to participation.

Procedure

Participants attended the laboratory on one occasion. They were seated in the isokinetic dynamometer (Biodex Medical Systems, New York, USA), which was

Results

Results from the ANOVA revealed that the method-by-strain rate interaction was non-significant (F1, 19 = 1.04, p = 0.51). Further, there was a significant main effect for method (F1, 19 = 55.39, p < 0.01). A follow up paired samples t-test revealed that stiffness values obtained from the active method were significantly greater compared to the passive method at all strain rates (t59 = 17.29, p < 0.001). The Pearson’s correlation coefficients describing the relationship of tendon stiffness obtained from

Discussion

The purpose of this study was to investigate the agreement between Achilles tendon stiffness obtained from the active and passive methods across different tendon strain rates. We found that (1) the active method produced greater stiffness values than the passive method across all strain rates, (2) in spite of this difference, agreement existed between the two methods across all strain rates, and (3) tendon stiffness increased linearly across strain rates for both methods.

Tendon stiffness is

Acknowledgements

This study was supported by Engineering and Physical Sciences Research Council [United Kingdom] Grant EP/E013007/1.

Nicola Theis is a researcher at Brunel University in London, UK. She completed her undergraduate degree in Sport Science and her Master of Science degree in Human Performance. Her current research focus is investigating muscle tendon mechanics in typically developing children and those with neuromuscular disorders.

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    Nicola Theis is a researcher at Brunel University in London, UK. She completed her undergraduate degree in Sport Science and her Master of Science degree in Human Performance. Her current research focus is investigating muscle tendon mechanics in typically developing children and those with neuromuscular disorders.

    Dr Amir A. Mohagheghi completed his PhD at the University of Otago. Currently, he is a Lecturer in the Centre for Sports Medicine and Human Performance at Brunel University, London, UK. His recent research activity is focused on the mechanisms underlying movement disability in both adults and children.

    Dr Thomas Korff received his PhD in biomechanics from the University of Texas at Austin in 2005. Currently, he is a Senior Lecturer in the Centre for Sports Medicine and Human Performance at Brunel University, London, UK. His main research focus is the use of biomechanical techniques with the goal of understanding the mechanical determinants of typical and atypical child motor development.

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