The tendinopathic Achilles tendon does not remain iso-volumetric upon repeated loading: insights from 3D ultrasound

Abstract

Mid-portion Achilles tendinopathy (MAT) alters the normal three-dimensional (3D) morphology of the Achilles tendon (AT) at rest and under a single tensile load. However, how MAT changes the 3D morphology of the AT during repeated loading remains unclear. This study compared the AT longitudinal, transverse and volume strains during repeated loading of the tendinopathic AT with those of the contralateral tendon in people with unilateral MAT. Ten adults with unilateral MAT performed 10 successive 25 s submaximal (50%) voluntary isometric plantarflexion contractions with both legs. Freehand 3D ultrasound scans were recorded and used to measure whole AT, free AT and proximal AT longitudinal strains and free AT cross-sectional area (CSA) and volume strains. The free AT experienced higher longitudinal and CSA strain and reached steady state following a greater number of contractions (five contractions) in the tendinopathic AT compared with the contralateral tendon (three contractions). Further, free tendon CSA and volume strain were greater in the tendinopathic AT than in the contralateral tendon from the first contraction, whereas free AT longitudinal strain was not greater than that of the contralateral tendon until the fourth contraction. Volume loss from the tendon core therefore preceded the greater longitudinal strain in the tendinopathic AT. Overall, these findings suggest that the tendinopathic free AT experiences an exaggerated longitudinal and transverse strain response under repeated loading that is underpinned by an altered interaction between solid and fluid tendon matrix components. These alterations are indicative of accentuated poroelasticity and an altered local stress-strain environment within the tendinopathic free tendon matrix, which could affect tendon remodelling via mechanobiological pathways.

Three‐dimensional morphology and volume of the free Achilles tendon at rest and under load in people with unilateral mid‐portion Achilles tendinopathy

“…These findings provide the first in vivo data that describe free tendon morphological characteristics across all tendon regions in both tendinopathic and contralateral tendons. Our finding that the free tendon with MAT has a larger CSA and AP diameter throughout the entire tendon length at rest supports earlier studies that have shown an increase in the thickness and area of the mean whole free AT (Docking & Cook, ; Nuri et al., ) and a single site of free AT mid‐portion (Docking et al., ; Grigg et al., ; Tsehaie et al., ) as a result of pathological alterations in tendon structure and composition in individuals with MAT. The widespread alteration in tendon morphology of the tendinopathic tendon (i.e.…”

“…Ten patients with unilateral MAT were included in the present study. The inclusion criteria were as follows: male adults, 18–60 years of age with unilateral symptomatic MAT, minimal duration of symptoms of 3 months, and a Victorian Institute of Sports Assessment‐Achilles tendon (VISA‐A) of <80 points (Nuri et al., ). The definition of MAT was pain, discomfort, tenderness to palpation, and focal thickening of the AT evident in both longitudinal and transverse scans of two‐dimensional (2‐D) ultrasound (2‐DUS) in the tendon mid‐portion (2–7 cm proximal to the AT calcaneal insertion; Maffulli et al., ; Figure ).…”

“…Pathological alterations in the tendon structure and composition in MAT include disruption and disorganization of collagen bundles, an increase in the proportion of type III relative to type I collagen, hypercellularity, hypervascularity, a high content of glycosaminoglycan, and accumulation of free and bound water molecules (Åström & Rausing, ; Corps et al., ; de Mos et al., ; Pingel et al., ). Such micropathological changes in tendon structure and composition have been shown to alter tendon macromorphology (Docking & Cook, ; Docking, Rosengarten, Daffy, & Cook, ; Grigg, Wearing, & Smeathers, ; Nuri, Obst, Newsham‐West, & Barrett, ; Shalabi, Kristoffersen‐Wilberg, Svensson, Aspelin, & Movin, ; Tsehaie, Poot, Oei, Verhaar, & de Vos, ) and adversely affect Achilles tendon (AT) mechanical behaviour and material properties (Arya & Kulig, ; Chang & Kulig, ; Child et al., ; Nuri et al., ; Wang, Lin, Su, Shih, & Huang, ).…”

“…Achilles tendons with MAT have been reported to have a greater free tendon [i.e. soleus muscle–tendon junction (MTJ) to calcaneus] cross‐sectional area (CSA), anteroposterior (AP) diameter and volume relative to healthy control tendons at rest (Docking & Cook, ; Docking et al., ; Grigg et al., ; Nuri et al., ; Shalabi et al., ; Tsehaie et al., ). However, reports of tendon resting transverse morphology (i.e.…”

“…Furthermore, although the normal free AT is known to remain isovolumetric and experience a reduction in tendon CSA and mediolateral (ML) diameter, and an increase in AP diameter throughout the entire tendon length during tensile loading (Iwanuma et al., ; Nuri, Obst, Newsham‐West, & Barrett, ; Obst, Renault, Newsham‐West, & Barrett, , ), relatively little is currently known about how three‐dimensional (3‐D) tendon morphology during tensile loading is altered in MAT. Studies of the tendinopathic Achilles and patellar tendons have demonstrated an immediate decrease in AP diameter and water content after an acute bout of eccentric exercise (Grigg et al., ; Ho & Kulig, ; Wearing, Locke, Smeathers, & Hooper, ) and 1 h floor‐ball match (Fahlström & Alfredson, ), and an immediate reduction in tendon CSA and volume during repeated isometric loading (Nuri et al., ) and after long‐term eccentric exercise (Shalabi et al., ; Tsehaie et al., ). Such acute reductions in tendinopathic tendon CSA, AP diameter, water content and volume are suggested to be the result of load‐induced fluid exudation from the tendon core to the peri‐tendinous space and collagen fibre realignment (Grigg et al., ; Hannafin & Arnoczky, ; Helmer, Wellen, Grigg, & Sotak, ).…”