Effects of Increased Loading on In Vivo Tendon Properties: A Systematic Review

Abstract

Introduction: In vivo measurements have been used in the past two decades to investigate the effects of increased loading on tendon properties, yet the current understanding of tendon macroscopic changes to training is rather fragmented, limited to reports of tendon stiffening, supported by changes in material properties and/or tendon hypertrophy. The main aim of this review was to analyze the existing literature to gain further insights into tendon adaptations by extracting patterns of dose-response and time-course.

Methods: PubMed/Medline, SPORTDiscus, and Google Scholar databases were searched for studies examining the effect of training on material, mechanical, and morphological properties via longitudinal or cross-sectional designs.

Results: Thirty-five of 6440 peer-reviewed articles met the inclusion criteria. The key findings were i) the confirmation of a nearly systematic adaptation of tendon tissue to training, ii) the important variability in the observed changes in tendon properties between and within studies, and iii) the absence of a consistent incremental pattern regarding the dose-response or the time-course relation of tendon adaptation within the first months of training. However, long-term (years) training was associated with a larger tendon cross-sectional area, without any evidence of differences in material properties. Our analysis also highlighted several gaps in the existing literature, which may be addressed in future research.

Conclusions: In line with some cross-species observations about tendon design, tendon cross-sectional area allegedly constitutes the ultimate adjusting parameter to increased loading. We propose here a theoretical model placing tendon hypertrophy and adjustments in material properties as parts of the same adaptive continuum.

FIGURE 1

Effects of physical training on the properties of the PT (A) and AT (B) measured in vivo. Changes in material, mechanical, and morphological tendon properties in response to short-term training interventions (squares) and long-term comparison studies (circles). Changes in maximal voluntary contraction torque of the knee extensor and plantarflexor muscles are shown in the “MVC” column. Filled symbols indicate significant changes, and hollow crossed symbols indicate nonsignificant changes. Extracted values (see “Data extraction and analysis” section) are distinguished from readily available values with an asterisk. Black symbols refer to data obtained with a training type favoring high load transmission, without a need for storage and release of elastic energy in the tendon (i.e., resistive exercise). Gray symbols refer to data obtained with a training type requiring storage and release of elastic energy in the tendon (i.e., running and plyometrics). For clarity, references to nonsignificant changes in the PT (39,41,42,44,45,55,56,62,74) and AT (1,4,13,19,38,41,43,74) CSA were not included in the figure.

FIGURE 2

Standardized effect and risk of bias. Standardized effect and confidence intervals for changes in tendon stiffness in response to short-term training interventions (squares) and for differences in tendon stiffness between long-term athletes and controls (comparison studies, circles). Studies focusing on the PT and the AT are grouped above and below the horizontal dotted line, respectively. Filled symbols indicate significant changes, and hollow crossed symbols indicate nonsignificant changes. Black symbols refer to data obtained with a training type favoring high load transmission, without a need for storage and release of elastic energy in the tendon (i.e., resistive exercise). Gray symbols refer to data obtained with a training type requiring storage and release of elastic energy in the tendon (i.e., running and plyometrics). Miss, relevant data unavailable; n/a, not applicable (single group design and comparison studies); + Indicates met criteria; - indicates unmet criteria; * indicates only one active control group.

FIGURE 3

Dose–response relation of the effects of resistance training on the PT (A, B, and C) and AT (D, E, and F). Percent daily increases in tendon Young’s modulus (rhombus), stiffness (square), and CSA (circle) against training volume, intensity, and frequency, respectively, are shown. Black filled symbols denote data obtained after training involving muscle dynamic contractions, and gray filled symbols denote data obtained after training involving muscle isometric contractions. Hollow crossed symbols refer to nonsignificant changes.

FIGURE 4

Time-course of average changes in the Young’s modulus, stiffness, and CSA of the PT (A, B, and C) and AT (D, E, and F). Differences in tendon material, mechanical, and morphological properties after short-term training interventions (squares) and between long-term athletes and controls (comparison studies, circles) are shown. Filled symbols indicate significant changes, and hollow crossed symbols indicate nonsignificant changes. Extracted values (see “Data extraction and analysis” section) are distinguished from readily available values with an asterisk. Black symbols refer to data obtained with a training type favoring high load transmission, without a need for storage and release of elastic energy in the tendon (i.e., resistive exercise). Gray symbols refer to data obtained with a training type requiring storage and release of elastic energy in the tendon (i.e., running and plyometrics). Confidence intervals were included as error bars when sufficient information was available for their calculation (i.e., mean and SD of changes).

FIGURE 5

Body mass plotted against the Young’s modulus and CSA of the PT and AT. Data points were obtained from baseline characteristics of the subjects recruited in short-term intervention studies and the untrained control subjects of comparison studies. The linear regressions and their 95% confidence limits indicate that body-mass correlate with the CSA but not with the Young’s modulus.

FIGURE 6

Hypothetical model of adaptive mechanisms. A. This panel shows the theoretical connection between training-induced changes in tendon material properties and hypertrophy. White arrows denote an increase in molecule production or in a variable. Dashed arrows denote a causal link. Question marks denote an unproven link. B. This panel illustrates the concept with a unitless graph of the time course of changes that may occur during short- and long-term training at constant loading.