Adaptive response of human tendon to paralysis

Abstract

To gain insight into the adaptive response of human tendon to paralysis, we compared the mechanical properties of the in vivo patellar tendon in six men who were spinal cord-injured (SCI) and eight agematched, able-bodied men. Measurements were taken by combining dynamometry, electrical stimulation, and ultrasonography. Tendon stiffness and Young's modulus, calculated from force-elongation and stress-strain curves, respectively, were lower by 77% (P Ͻ 0.01) and 59% (P Ͻ 0.05) in the SCI than able-bodied subjects. The cross-sectional area (CSA) of the tendon was 17% smaller (P Ͻ 0.05) in the SCI subjects, but there was no difference in tendon length between the two groups. Our results indicate that paralysis causes substantial deterioration of the structural and material properties of tendon. This needs to be taken into consideration in the design of electrical stimulation protocols for rehabilitation and experimental purposes, and when interpreting changes in the contractile speed of paralyzed muscle. Although tendons transmit contractile force to the skeleton, they do not behave as rigid bodies but extend under tension as dictated by their structural and material properties. 8,11,31,47 These properties are not static throughout the lifespan, but change according to alterations in the level of mechanical loading that the tendons habitually experience. 23,45,52 In the present study, we were concerned with the adaptations of human tendons to severe disuse caused by long-term paralysis. Most of our knowledge on the effects of disuse on tendon mechanical properties originates from animal studies and relatively short durations of experimental unloading, lasting 3-12 weeks. These studies show that even short-term disuse may reduce the stiffness and Young's modulus of tendon to between 9% and 88% of baseline values. 3,18,19,24,26,32,33,42,49,50 Identifying any biological basis behind this ϳ10-fold interstudy variation on the impact of disuse is complicated by factors such as differences in the level of mechanical unloading between experimental models, baseline differences in physiological loading between tendons in a given animal, differences in activity between animals, and differences in the duration of unloading in absolute and relative terms with respect to the animal's lifespan. These discrepancies make it difficult to assess the applicability of findings from in vitro animal work to in vivo human tendons. Recent advances in ultrasound scanning, however, have enabled the assessment in vivo of the effects of disuse on the mechanical properties of intact human tendon. 24,42 One such study showed that short-term unloading (20 days) as a result of bed-rest reduced the stiffness of human tendons by ϳ30%. 24 Longer durations of bed-rest (90 days) produced larger reductions of tendon stiffness and Young's modulus, reaching the level of ϳ60% of the baseline value. 42 This suggests that severe disuse as a result of several Abbreviations: ANOVA, analysis of variance; ASIA, American Spinal Injury Association; CSA, ...

Imaging Studies of the Mechanical and Architectural Characteristics of the Human Achilles Tendon in Normal, Unloaded and Rehabilitating Conditions

“…For these VE-PC MRI studies, the Young's modulus showed a 17% reduction for the Achilles tendon ( Figure 5, Shin et al 2008a) and 29% reduction for the distal aponeurosis (Kinugasa et al 2010) after 4-wk unloading. The extent of decline found in these studies is similar to that reported by Kubo et al (2002Kubo et al ( , 2004, who studied humans subjected to 20 days of bed rest (-28%), but it is much more moderate than the percent decline reported in studies of 90 days simulated microgravity (-58%, Reeves et al 2005) and paralysis (-59%, Maganaris et al 2006). This suggests that the extent of stiffness decrease may have a direct correlation to the duration of unloading.…”

“…Previously, the reduction in stiffness was reported mainly from ultrasound studies in humans (Kubo et al 2002(Kubo et al , 2004Maganaris et al 2006;Reeves et al 2005) as well as in some animal studies (Ameida-Silveira et al 2000;Woo et al 1982). Recently, the tendon mechanical properties were measured with the stress-strain relationship established from the VE-PC MRI studies.…”

The Achilles tendon is mechanosensitive in older adults: adaptations following 14 weeks versus 1.5 years of cyclic strain exercise

“…However, unlike in muscles, it has to be ensured that the exercise intervention implements tendon strains corresponding to high mechanical loading (intensities of at least 80-90% of MVC) to induce tendon adaptation (Arampatzis et al, 2007a;Grosset et al, 2014). Similar to adaptations to loading, a relatively fast deterioration in the tendon mechanical, material and morphological properties has been shown during bed rest and paralysis (Kubo et al, 2000;Maganaris et al, 2006;Reeves et al, 2005), as well as trainingdetraining studies (Kubo et al, 2012). Such fast adaptation caused by high loads and deterioration following disuse or detraining indicates that the homeostatic response to changes in mechanical loading is a relatively quick process, occurring within 12-14 weeks, in both younger and older adults.…”

Is human Achilles tendon deformation greater in regions where cross-sectional area is smaller?

“…Although likely to be an oversimplification, the use of a single 'reference' point is a necessary step in obtaining measurements to permit calculation of tendon stiffness and modulus, with many current variations on the in vivo approach. It also allows specific questions to be answered relating to the variations in tendon properties between different populations Karamanidis and Arampatzis, 2006;Maganaris et al, 2006), or changes in tendon properties as a result of interventions (Arampatzis et al, 2007;Kubo et al, 2002;Reeves et al, 2005;Wiesinger et al, 2015). However, the implicit assumption with this approach is that tendon elongations are homogeneous, or at least representative of the entire tendon, which may not always be the case.…”