Mechanical, Material and Morphological Adaptations of Healthy Lower Limb Tendons to Mechanical Loading: A Systematic Review and Meta-Analysis

Abstract

Background: Exposure to increased mechanical loading during physical training can lead to increased tendon stiffness. However, the loading regimen that maximises tendon adaptation and the extent to which adaptation is driven by changes in tendon material properties or tendon geometry is not fully understood.

Objective: To determine (1) the effect of mechanical loading on tendon stiffness, modulus and cross-sectional area (CSA); (2) whether adaptations in stiffness are driven primarily by changes in CSA or modulus; (3) the effect of training type and associated loading parameters (relative intensity; localised strain, load duration, load volume and contraction mode) on stiffness, modulus or CSA; and (4) whether the magnitude of adaptation in tendon properties differs between age groups.

Methods: Five databases (PubMed, Scopus, CINAHL, SPORTDiscus, EMBASE) were searched for studies detailing load-induced adaptations in tendon morphological, material or mechanical properties. Standardised mean differences (SMDs) with 95% confidence intervals (CIs) were calculated and data were pooled using a random effects model to estimate variance. Meta regression was used to examine the moderating effects of changes in tendon CSA and modulus on tendon stiffness.

Results: Sixty-one articles met the inclusion criteria. The total number of participants in the included studies was 763. The Achilles tendon (33 studies) and the patella tendon (24 studies) were the most commonly studied regions. Resistance training was the main type of intervention (49 studies). Mechanical loading produced moderate increases in stiffness (standardised mean difference (SMD) 0.74; 95% confidence interval (CI) 0.62-0.86), large increases in modulus (SMD 0.82; 95% CI 0.58-1.07), and small increases in CSA (SMD 0.22; 95% CI 0.12-0.33). Meta-regression revealed that the main moderator of increased stiffness was modulus. Resistance training interventions induced greater increases in modulus than other training types (SMD 0.90; 95% CI 0.65-1.15) and higher strain resistance training protocols induced greater increases in modulus (SMD 0.82; 95% CI 0.44-1.20; p = 0.009) and stiffness (SMD 1.04; 95% CI 0.65-1.43; p = 0.007) than low-strain protocols. The magnitude of stiffness and modulus differences were greater in adult participants.

Conclusions: Mechanical loading leads to positive adaptation in lower limb tendon stiffness, modulus and CSA. Studies to date indicate that the main mechanism of increased tendon stiffness due to physical training is increased tendon modulus, and that resistance training performed at high compared to low localised tendon strains is associated with the greatest positive tendon adaptation. PROSPERO registration no.: CRD42019141299.

Fig. 1

PRISMA flow diagram

Fig. 2

Forest plot for the meta-analysis of all studies providing stiffness measures, showing standardised mean differences (SMD) and 95% confidence intervals (CI)

Fig. 3

Forest plot for the meta-analysis of all studies providing elastic modulus measures, showing standardised mean differences (SMD) and 95% confidence intervals (CI) of all studies

Fig. 4

Forest plot for the meta-analysis of all studies providing cross-sectional area measures, showing standardised mean differences (SMD) and 95% confidence intervals (CI) of all studies

Fig. 5

Bubble plot visualisation of meta-regression between the pre- and post-intervention percentage difference in stiffness increases versus a pre- and post-intervention percentage difference in modulus, and b pre- and post-intervention percentage difference in cross-sectional area (CSA). Only studies that concurrently measured stiffness, modulus and CSA were included in the meta-regression. The size of each bubble is proportional to the sample size of the included intervention groups. The black line represents the regression line of best fit. Grey-shaded area represents the 95% confidence intervals of the regression line

Fig. 6

Sub-groups of moderating factors of adaptation in stiffness, modulus and cross-sectional area (CSA), demonstrating standardised mean differences (SMD) and 95% confidence intervals (CI) for each factor. All comparisons beneath the dashed line contain resistance training-only groups. Comparisons beneath the dotted line contain high intensity, resistance training groups. Con:Ecc = concentric:eccentric action; low intensity =  < 70% of maximal voluntary contraction or one repetition maximum; high intensity =  ≥ 70% of maximal voluntary contraction or one repetition maximum, low strain =  ~ 3%; high strain =  ~ 5%; low volume =  ≤ 3100 arbitrary units, high volume =  > 3100 arbitrary units. *p < 0.05 for sub-group analysis