The magnitude and character of resistance-training-induced increase in tendon stiffness at old age is gender specific

Abstract

Human tendon mechanical properties are modified with loading. Moreover, there are indications that the training response in the tendon is gender specific. The aim of the current study was to examine whether in vivo patella tendon stiffness (K) differentially alters with training in older males compared with females. We also aimed to identify which endocrine pathway underlies the responses. Maximal knee extensor forces were also monitored to determine the training effect on muscle function. Fourteen healthy, habitually active older persons (seven males aged 74.0 ± 1.2 years (mean±SEM) and seven females aged 76.7 ± 1.2 years) were tested at baseline and after 12 weeks of weekly, progressive resistance training. With training, percentage increase in quadriceps maximum voluntary isometric force (MVC) was similar in males (2,469.6 ± 168.0 to 3,097.3 ± 261.9 N; +25.3 ± 6.1% (p < 0.01)) and females (1,728.8 ± 136.3 to 2,166.5 ± 135.8 N; +30.4 ± 15.1% (p < 0.05)), respectively. K increased more in males (338.0 ± 26.6 to 616.9 ± 58.7 N/mm; 79.8 ± 4.2% (p < 0.001)) compared to females (338.9 ± 31.0 to 373.2 ± 25.8 N/mm; +13.0 ± 3.7% (p < 0.001)). Interestingly, a pattern was found whereby below ~40% MVC, the females showed their greatest degree of K changes, whereas the males showed their greatest degree of K change above this relative force level. This gender contrast was also true at a standardised force level (1,200 N), with 5.8 ± 0.4% vs. 82.5 ± 1.8% increments in the females (i.e. value change from 380.3 ± 14.1 to 402.4 ± 13.3 N/mm) and the males (i.e. value change from 317.8 ± 13.8 to 580.2 ± 30.9 N/mm), respectively (p < 0.001). While circulating levels of both IGF-I and IL-6 did not alter with training, IGFBP-3 showed a significant training effect (19.1 ± 4.8%, p < 0.001) and only in the male sub-group (p = 0.038). We show here that with training, in vivo older females' tendon is less dramatically modulated than that of males'. We also show that the relative forces, at which the greatest adaptations are exhibited, differ by gender, with a suggestion of endocrine adaptations in males only. We thus propose that both training and rehabilitation regimens should consider gender-specific tendon responsiveness, at least in older persons.

Fig. 1

Force–elongation relationships in an aged population by gender and phase of a training intervention. It is notable that even though the maximal muscle strength is greater in the older males (triangles) than their female counterparts (circles) at baseline, the tendon properties (at comparable force levels) are in fact very similar. With training, the relative strength increments are similar but the shapes of the tendon force–elongation curves are dissimilar. Horizontal dashed line standardised force level (1,200 N) at which the tendons were compared. Data are means±SEM

Fig. 2

The characteristic of tendon adaptation by force level is gender dependent in terms both of a magnitude, b the characteristic force region. In a, we see that where stiffness changes are expressed relative to baseline values (i.e., K change in % or %K change), both genders show increments in stiffness with training, though the absolute magnitude of increment is greater in the males compared to the females across all the levels of forces. In other words the values of %K changes are higher in males compared with females. In b where the %K changes are further normalised for the mean %K change within each gender (in order to highlight how, within each gender, %K changes (at discreet force levels) compared with the average of the whole range of tendon stiffness values changes (mean K at 0–100% MVC)), there is a pattern emerging whereby the female tendon exhibits the greatest average change at low forces (<40% MVC; i.e. a decrease, followed by a stabilisation, of the magnitude of stiffness increment as loading increases), in contrast to males showing a high response pattern at high forces (>40% MVC; i.e. an increase, followed by a stabilisation, of the magnitude of stiffness increment as loading increases). a and b both represent data from group changes