Influence of preconditioning on morphological and mechanical properties of human Achilles tendon in vivo

Over the past quarter century, numerous studies have been reported on the mechanical properties of human tendons. In these previous studies (Lichtwark et al., 2013, Magnusson et al., 2003, Peltonen et al., 2012, Reeves et al., 2003), the contractions were repeated before the measurements so that the measured variables were not affected by preconditioning, e.g., “Measurements were taken after four pre-conditioning contractions to ensure reproducibility of the measurements (Reeves et al., 2003)”. However, the findings (e.g., Rigby, 1964) cited in these previous studies (human studies) were obtained by a large number of tensile tests using extracted tendons from animals and human cadavers, which are quite different from measurements of human tendon properties in vivo. Therefore, it is necessary to verify the effect of repeating contractions in advance (preconditioning) in the protocol employed in measuring human tendon properties in vivo (i.e., repeated contractions with breaks between trials).

In vivo studies on human tendons, as well as in vitro studies, have shown the phenomenon of tendon creep (i.e., increased tendon strain) with repeated contractions (Hawkins et al., 2009, Kubo et al., 2001, Kubo et al., 2005, Kubo et al., 2009, Merza et al., 2022, Nuri et al., 2017, Nuri et al., 2018). On the other hand, it has been reported that tendon elongation does not change with repeated ballistic contractions (Kubo et al., 2001, Kubo et al., 2009, Mademli et al., 2006, Mademli et al., 2008), repetitive jumps (Kubo et al., 2005, Peltonen et al., 2010), and endurance running (Farris et al., 2012, Lichtwark et al., 2013, Peltonen et al., 2012). The reasons for the discrepancies in the findings of these previous studies are unknown, but may include differences in the number of repetitions, intensity, and contraction modes. In particular, most previous studies have found no change in the tendon elongation and strain after repeated ballistic contractions. To the best of our knowledge, however, three earlier studies showed that tendon elongation increased “during” repetitive contractions (Hawkins et al., 2009, Maganaris, 2003, Maganaris et al., 2002). On the other hand, in most studies cited above, tendon properties were evaluated before and after, rather than during, the fatigue task. Considering these findings, we need to examine changes in tendon properties “during” the fatigue task since tendon properties may have recovered immediately after the fatigue task was completed to the start of the measurement.

On the other hand, changes in hysteresis of human tendons due to repeated muscle contractions have yet to be studied. In a few in vitro studies (De Zee et al., 2000, Rigby, 1964; Schatzmann et al., 1998), preconditioning has reduced tendon hysteresis. Tendon hysteresis is theoretically related to the amount of reused elastic energy during the concentric phase of stretch–shortening cycle exercises. Indeed, several previous studies reported that tendon hysteresis was closely related to performance during stretch–shortening cycle exercises (Kubo et al., 2005, Wang et al., 2012) and that tendon hysteresis of athletes was lower than that of the general population (Wiesinger et al., 2017). Furthermore, plyometric training increased jump performance and decreased tendon hysteresis (Foure et al., 2010; Kubo et al., 2021). Therefore, when considering the effect of preconditioning on tendon properties as a warm-up, changes in tendon hysteresis, as well as creep (increase in strain), should be examined.

According to the findings of in vitro studies, the preconditioning-induced creep phenomenon (increased strain) in tendons is thought to be caused by changes in collagen fiber arrangement and decreased water content in the tendon (Hannafin and Arnczloy, 1994; Miller et al., 2012; Quinn and Winkelstein, 2011). Our previous studies have demonstrated that water content and collagen fiber arrangement in human tendons can be estimated from information about the echogenicity of ultrasonic images of tendons (Ishigaki et al., 2016; Ishigaki and Kubo, 2018; Kubo, 2018). Thus, applying this technique would reveal the mechanism of tendon preconditioning in humans in vivo if an increase in tendon elongation (creep) and a change in tendon hysteresis are observed during repeated muscle contractions.

The purposes of this study were 1) to verify whether the effect of muscle contractions before measurement (i.e., preconditioning) was observed in the measured variables (elongation and hysteresis) during the measurement of the human tendon mechanical properties in vivo (i.e., repeated contractions with breaks between trials) and 2) to determine the changes in tendon properties and their mechanisms due to repeated muscle contraction (fatigue task and/or preconditioning). On the basis of the points made in the previous paragraphs, we hypothesized that 1) the tendon properties measured during measurements did not change over several measurement trials, and 2) an increase in tendon elongation and a decrease in tendon hysteresis were observed during, not after, repeated muscle contractions, and these changes would be associated with a decrease in water content and changes in collagen fiber arrangement in the tendon.

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