The influence of physical activity during youth on structural and functional properties of the Achilles tendon.

Achilles tendinopathy is a highly prevalent sports injury. Animal studies show a growth response in tendons in response to loading in the immature phase but not after puberty maturation. The aim of this investigation was to examine the structural and material properties in long distance runners who were either physically active (HAY) or inactive (LAY) in young age. Twelve men in HAY group and eight men in LAY group participated. Structural, functional, and biochemical properties of Achilles tendon were estimated from magnetic resonance imaging, ultrasound video recordings, mechanical tests, and tendon biopsies, respectively. There was no difference between the groups with respect to tendon cross-sectional area or tendon free length. There was no difference between the groups with respect to maximal force or mechanical properties. The collagen content, enzymatic and nonenzymatic cross-link density did not differ between the groups, nor did collagen fibril density, diameter, and area. There was a correlation between age and pentosidine/collagen within the groups [(HAY: P < 0.05 and r(2) = 0.47) and (LAY: P < 0.05 and r(2) = 0.52)]. The data suggest that high or low activity during youth did not appreciably influence the mechanical, structural, or biochemical properties of the Achilles tendon in adult long distance runners.

Increased mast cell numbers in a calcaneal tendon overuse model.

Tendinopathy is often discovered late because the initial development of tendon pathology is asymptomatic. The aim of this study was to examine the potential role of mast cell involvement in early tendinopathy using a high-intensity uphill running (HIUR) exercise model. Twenty-four male Wistar rats were divided in two groups: running group (n = 12); sedentary control group (n = 12). The running-group was exposed to the HIUR exercise protocol for 7 weeks. The calcaneal tendons of both hind limbs were dissected. The right tendon was used for histologic analysis using Bonar score, immunohistochemistry, and second harmonic generation microscopy (SHGM). The left tendon was used for quantitative polymerase chain reaction (qPCR) analysis. An increased tendon cell density in the runners were observed compared to the controls (P = 0.05). Further, the intensity of immunostaining of protein kinase B, P = 0.03; 2.75 ± 0.54 vs 1.17 ± 0.53, was increased in the runners. The Bonar score (P = 0.05), and the number of mast cells (P = 0.02) were significantly higher in the runners compared to the controls. Furthermore, SHGM showed focal collagen disorganization in the runners, and reduced collagen density (P = 0.03). IL-3 mRNA levels were correlated with mast cell number in sedentary animals. The qPCR analysis showed no significant differences between the groups in the other analyzed targets. The current study demonstrates that 7-week HIUR causes structural changes in the calcaneal tendon, and further that these changes are associated with an increased mast cell density.

Differences in tendon properties in elite badminton players with or without patellar tendinopathy.

The aim of this study was to examine the structural and mechanical properties of the patellar tendon in elite male badminton players with and without patellar tendinopathy. Seven players with unilateral patellar tendinopathy (PT group) on the lead extremity (used for forward lunge) and nine players with no current or previous patellar tendinopathy (CT group) were included. Magnetic resonance imaging was used to assess distal patellar tendon dimensions. Patellar tendon mechanical properties were assessed using simultaneous tendon force and deformation measurements. Distal tendon cross-sectional area (CSA) normalized for body weight (mm(2) /kg(2/3) ) was lower in the PT group compared with the CT group on both the non-lead extremity (6.1 ± 0.3 vs 7.4 ± 0.2, P < 0.05) and the lead extremity (6.5 ± 0.6 vs 8.4 ± 0.3, P < 0.05). Distal tendon stress was higher in the PT group compared with the CT group for both the non-lead extremity (31 ± 1 vs 27 ± 1 MPa, P < 0.05) and the lead extremity (32 ± 3 vs 21 ± 3 MPa, P < 0.01). Conclusively, the PT group had smaller distal patellar tendon CSA on both the injured (lead extremity) and the uninjured side (non-lead extremity) compared with the CT group. Subsequently, the smaller CSA yielded a greater distal patellar tendon stress in the PT group. Therefore, a small tendon CSA may predispose to the development of tendinopathy.

The effects of immobilization on the mechanical properties of the patellar tendon in younger and older men.

BACKGROUND: It remains unknown if inactivity changes the mechanical properties of the human patellar tendon in younger and older healthy persons. The purpose was to examine the effects of short-term unilateral immobilization on the structural and mechanical properties of the patellar tendon in older men and younger men, in vivo. METHODS: Eight older men and eight younger men underwent 14 days of unilateral immobilization. All individuals were assessed on both sides before and after the intervention. MRI was used to assess whole patellar tendon dimensions. The mechanical properties of the patellar tendon were assessed using simultaneous force and ultrasonographic measurements during isometric ramp contractions. FINDINGS: In older men, tendon stiffness [Pre: mean 2949 (SD 799) vs. Post: mean 2366 (SD 774) N mm(-1), P<0.01] and Young's Modulus [Pre: mean 1.2 (SD 0.3) vs. Post: mean 1.0 (SD 0.3) GPa, P<0.05] declined with immobilization on the immobilized side. On the control side, tendon stiffness [Pre: mean 3340 (SD 1209) vs. Post: mean 2230 (SD 503), P<0.01] and Young's Modulus [Pre: mean 1.5 (SD 0.4) vs. Post: mean 0.9 (SD 0.3) GPa, P<0.05] also decreased with immobilization. In younger men, tendon stiffness [Pre: 3622 (SD 1760) vs. Post: mean 2910 (SD 1528) N mm(-1), P<0.01] and Young's Modulus [Pre: mean 1.7 (SD 1.1) vs. Post: mean 1.4 (SD 0.8) GPa, P<0.05] decreased only on the immobilized side. INTERPRETATION: Short-term immobilization led to impaired mechanical properties of the patellar tendon on the immobilized side in both younger men and older men, which can influence the function of the muscle-tendon complex.

Uphill running improves rat Achilles tendon tissue mechanical properties and alters gene expression without inducing pathological changes.

Overuse Achilles tendinopathy is a common and challenging problem in sports medicine. Little is known about the etiology of this disorder, and the development of a good animal model for overuse tendinopathy is essential for advancing insight into the disease mechanisms. Our aim was to test a previously proposed rat model for Achilles tendon overuse. Ten adult male Sprague-Dawley rats ran on a treadmill with 10° incline, 1 h/day, 5 days/wk (17-20 m/min) for 12 wk and were compared with 12 control rats. Histological, mechanical, and gene-expression changes were measured on the Achilles tendons after the intervention, and local tendon glucose-uptake was measured before and after the intervention with positron emission tomography. No differences were detected between runners and controls in tissue histology or in glucose uptake, indicating that tendon pathology was not induced. Greater tendon tissue modulus (P < 0.005) and failure stress/body weight (P < 0.02) in runners compared with controls further supported that tendons successfully adapted to uphill running. Several genes of interest were regulated after 12 wk of running. Expression of collagen III and insulin-like growth factor I was increased, while collagen I was unchanged, and decreases were seen in noncollagen matrix components (fibromodulin and biglycan), matrix degrading enzymes, transforming growth factor-ß1, and connective tissue growth factor. In conclusion, the tested model could not be validated as a model for Achilles tendinopathy, as the rats were able to adapt to 12 wk of uphill running without any signs of tendinopathy. Improved mechanical properties were observed, as well as changes in gene-expression that were distinctly different from what is seen in tendinopathy and in response to short-term tendon loading.

Mechanical properties of the human Achilles tendon, in vivo.

BACKGROUND: Ultrasonography has been widely applied for in vivo measurements of tendon mechanical properties. Assessments of human Achilles tendon mechanical properties have received great interest. Achilles tendon injuries predominantly occur in the tendon region between the Achilles-soleus myotendinous junction and Achilles-calcaneus osteotendinous junction i.e. in the free Achilles tendon. However, there has been no adequate ultrasound based method for quantifying the mechanical properties of the free human Achilles tendon. This study aimed to: 1) examine the mechanical properties of the free human Achilles tendon in vivo by the use of ultrasonography and 2) assess the between-day reproducibility of these measurements. METHODS: Ten male subjects had the Achilles tendon moment arm length, Achilles tendon cross sectional area and free Achilles tendon length determined. All subjects performed isometric plantarflexion ramp contractions to assess between-day reproducibility on two separate days. Simultaneous ultrasonography based measurements of Achilles-soleus myotendinous junction and Achilles-calcaneus osteotendinous junction displacement together with Achilles tendon force estimates yielded free Achilles tendon mechanical properties. FINDINGS: Free Achilles tendon maximal force, deformation and stiffness were 1924 (SD 229) N, 2.2 (SD 0.6) mm and 2622 (SD 534) N/mm on day 1. For between-day reproducibility there were no significant differences between days for free Achilles tendon mechanical properties. The between-day correlation coefficient and typical error percent were 0.81 and 5.3% for maximal Achilles tendon force, 0.85 and 11.8% for maximal Achilles tendon deformation and 0.84 and 8.8% for Achilles tendon stiffness respectively. Last, osteotendinous junction proximal displacement on average contributed with 71 (SD 12) % of proximal myotendinous junction displacement. INTERPRETATION: This study, for the first time, presents an ultrasonography based in vivo method for measurement of free AT mechanical properties. The method is applicable for evaluation of free human Achilles tendon mechanical properties in relation to training, injury and rehabilitation.

Corticosteroid injections, eccentric decline squat training and heavy slow resistance training in patellar tendinopathy.

A randomized-controlled single-blind trial was conducted to investigate the clinical, structural and functional effects of peritendinous corticosteroid injections (CORT), eccentric decline squat training (ECC) and heavy slow resistance training (HSR) in patellar tendinopathy. Thirty-nine male patients were randomized to CORT, ECC or HSR for 12 weeks. We assessed function and symptoms (VISA-p questionnaire), tendon pain during activity (VAS), treatment satisfaction, tendon swelling, tendon vascularization, tendon mechanical properties and collagen crosslink properties. Assessments were made at 0 weeks, 12 weeks and at follow-up (half-year). All groups improved in VISA-p and VAS from 0 to 12 weeks (P<0.05). VISA-p and VAS improvements were maintained at follow-up in ECC and HSR but deteriorated in CORT (P<0.05). In CORT and HSR, tendon swelling decreased (-13+/-9% and -12+/-13%, P<0.05) and so did vascularization (-52+/-49% and -45+/-23%, P<0.01) at 12 weeks. Tendon mechanical properties were similar in healthy and injured tendons and were unaffected by treatment. HSR yielded an elevated collagen network turnover. At the half-year follow-up, treatment satisfaction differed between groups, with HSR being most satisfied. Conclusively, CORT has good short-term but poor long-term clinical effects, in patellar tendinopathy. HSR has good short- and long-term clinical effects accompanied by pathology improvement and increased collagen turnover.

From mechanical loading to collagen synthesis, structural changes and function in human tendon.

The adaptive response of connective tissue to loading requires increased synthesis and turnover of matrix proteins, with special emphasis on collagen. Collagen formation and degradation in the tendon increases with both acute and chronic loading, and data suggest that a gender difference exists, in that females respond less than males with regard to an increase in collagen formation after exercise. It is suggested that estrogen may contribute toward a diminished collagen synthesis response in females. Conversely, the stimulation of collagen synthesis by other growth factors can be shown in both animal and human models where insulin-like growth factor 1 (IGF-I) and transforming growth factor-beta-1 (TGF-beta-1) expression increases to accompany or precede an increase in procollagen expression and collagen synthesis. In humans, it can be demonstrated that an increase in the interstitial concentration of TGF-beta, PGE2, IGF-I plus its binding proteins and interleukin-6 takes place after exercise. The increase in IGF-I expression in tendon includes the isoform that has so far been thought only to exist in skeletal muscle (mechano growth factor). The increase in IGF-I and procollagen expression showed a similar response whether the tendon was stimulated by concentric, isometric or eccentric muscle contraction, suggesting that strain rather that stress/torque determines the collagen-synthesis stimulating response seen with exercise. The adaptation time to chronic loading is longer in tendon tissue compared with contractile elements of skeletal muscle or the heart, and only with very prolonged loading are significant changes in gross dimensions of the tendon observed, suggesting that habitual loading is associated with a robust change in the size and mechanical properties of human tendons. An intimate interplay between mechanical signalling and biochemical changes in the matrix is needed in tendon, such that chemical changes can be converted into adaptations in the morphology, structure and material properties.

Mechanical properties and collagen cross-linking of the patellar tendon in old and young men.

Age-related loss in muscle mass and strength impairs daily life function in the elderly. However, it remains unknown whether tendon properties also deteriorate with age. Cross-linking of collagen molecules provides structural integrity to the tendon fibrils and has been shown to change with age in animals but has never been examined in humans in vivo. In this study, we examined the mechanical properties and pyridinoline and pentosidine cross-link and collagen concentrations of the patellar tendon in vivo in old (OM) and young men (YM). Seven OM (67 +/- 3 years, 86 +/- 10 kg) and 10 YM (27 +/- 2 years, 81 +/- 8 kg) with a similar physical activity level (OM 5 +/- 6 h/wk, YM 5 +/- 2 h/wk) were examined. MRI was used to assess whole tendon dimensions. Tendon mechanical properties were assessed with the use of simultaneous force and ultrasonographic measurements during ramped isometric contractions. Percutaneous tendon biopsies were taken and analyzed for hydroxylysyl pyridinoline (HP), lysyl pyridinoline (LP), pentosidine, and collagen concentrations. We found no significant differences in the dimensions or mechanical properties of the tendon between OM and YM. Collagen concentrations were lower in OM than in YM (0.49 +/- 0.27 vs. 0.73 +/- 0.14 mg/mg dry wt; P < 0.05). HP concentrations were higher in OM than in YM (898 +/- 172 vs. 645 +/- 183 mmol/mol; P < 0.05). LP concentrations were higher in OM than in YM (49 +/- 38 vs. 16 +/- 8 mmol/mol; P < 0.01), and pentosidine concentrations were higher in OM than in YM (73 +/- 13 vs. 11 +/- 2 mmol/mol; P < 0.01). These cross-sectional data raise the possibility that age may not appreciably influence the dimensions or mechanical properties of the human patellar tendon in vivo. Collagen concentration was reduced, whereas both enzymatic and nonenzymatic cross-linking of concentration was elevated in OM vs. in YM, which may be a mechanism to maintain the mechanical properties of tendon with aging.

Habitual loading results in tendon hypertrophy and increased stiffness of the human patellar tendon.

The purpose of this study was to examine patellar tendon (PT) size and mechanical properties in subjects with a side-to-side strength difference of > or =15% due to sport-induced loading. Seven elite fencers and badminton players were included. Cross-sectional area (CSA) of the PT obtained from MRI and ultrasonography-based measurement of tibial and patellar movement together with PT force during isometric contractions were used to estimate mechanical properties of the PT bilaterally. We found that distal tendon and PT, but not mid-tendon, CSA were greater on the lead extremity compared with the nonlead extremity (distal: 139 +/- 11 vs. 116 +/- 7 mm(2); mid-tendon: 85 +/- 5 vs. 77 +/- 3 mm(2); proximal: 106 +/- 7 vs. 83 +/- 4 mm(2); P < 0.05). Distal tendon CSA was greater than proximal and mid-tendon CSA on both the lead and nonlead extremity (P < 0.05). For a given common force, stress was lower on the lead extremity (52.9 +/- 4.8 MPa) compared with the nonlead extremity (66.0 +/- 8.0 MPa; P < 0.05). PT stiffness was also higher in the lead extremity (4,766 +/- 716 N/mm) compared with the nonlead extremity (3,494 +/- 446 N/mm) (P < 0.05), whereas the modulus did not differ (lead 2.27 +/- 0.27 GPa vs. nonlead 2.16 +/- 0.28 GPa) at a common force. These data show that a habitual loading is associated with a significant increase in PT size and mechanical properties.

Effect of habitual exercise on the structural and mechanical properties of human tendon, in vivo, in men and women.

We examined whether long-term habitual training (a) was associated with differences in structural and mechanical properties in tendon in women and (b) yielded different tendon properties in men and women. Ten male runners, 10 female runners and 10 female non-runners were tested. Tendon cross-sectional area (CSA) and length of the patellar and Achilles tendon were determined with MRI. Ultrasonography-based measurement of tendon elongation and force during isometric contractions provided mechanical properties. Distal patellar and Achilles tendon CSAs were greater than the proximal part in all three groups (P<0.05). Weight-normalized Achilles tendon CSA were similar in trained (2.78+/-0.17 mm(2)/kg(3/4)) and untrained women (2.60+/-0.13 mm(2)/kg(3/4)), while that in trained men (3.77+/-0.27 mm(2)/kg(3/4)) was greater compared with trained women (P<0.01). Patellar tendon CSA were comparable in trained and untrained women, while that in trained men was greater compared with trained women (P<0.01). Patellar tendon stiffness was greater in male runners (3528+/-773 N/mm) compared with female runners (2069+/-666 N/mm) and non-runners (2477+/-381 N/mm), (P<0.01), but patellar tendon deformation, stress, strain and modulus were similar. These data indirectly suggest that the ability of Achilles and patellar tendons to adapt in response to habitual loading such as running is attenuated in women.

Region specific patellar tendon hypertrophy in humans following resistance training.

AIM: To examine if cross-sectional area (CSA) differs along the length of the human patellar tendon (PT), and if there is PT hypertrophy in response to resistance training. METHODS: Twelve healthy young men underwent baseline and post-training assessments. Maximal isometric knee extension strength (MVC) was determined unilaterally in both legs. PT CSA was measured at the proximal-, mid- and distal PT level and quadriceps muscle CSA was measured at mid-thigh level using magnetic resonance imaging. Mechanical properties of the patellar tendons were determined using ultrasonography. Subsequently, subjects performed 12 weeks of heavy resistance knee extension training with one leg (Heavy-leg), and light resistance knee extension training with the other leg (Light-leg). RESULTS: The MVC increased for heavy-leg (15 +/- 4%, P < 0.05), but not for light-leg (6 +/- 4%). Quadriceps CSA increased in heavy-legs (6 +/- 1%, P < 0.05) while unchanged in light-legs. Proximal PT CSA (104 +/- 4 mm(2)) was smaller than the mid-tendon CSA (118 +/- 3 mm(2)), which again was smaller than distal tendon CSA (127 +/- 2 mm(2), P < 0.05). Light-leg PT CSA increased by 7 +/- 3% (P < 0.05) at the proximal tendon level, but was otherwise unchanged. Heavy-leg PT CSA increased at the proximal and distal tendon levels by 6 +/- 3% and 4 +/- 2% respectively (P < 0.05), but was unchanged at the mid tendon level. PT stiffness increased in heavy-legs (P < 0.05) but was unchanged in light-legs. Modulus remained unchanged in both legs. CONCLUSIONS: To our knowledge, this study is the first to report tendon hypertrophy following resistance training. Further, the data show that the human PT CSA varies along the length of the tendon.

Enhanced satellite cell proliferation with resistance training in elderly men and women.

In addition to the well-documented loss of muscle mass and strength associated with aging, there is evidence for the attenuating effects of aging on the number of satellite cells in human skeletal muscle. The aim of this study was to investigate the response of satellite cells in elderly men and women to 12 weeks of resistance training. Biopsies were collected from the m. vastus lateralis of 13 healthy elderly men and 16 healthy elderly women (mean age 76+/-SD 3 years) before and after the training period. Satellite cells were visualized by immunohistochemical staining of muscle cross-sections with a monoclonal antibody against neural cell adhesion molecule (NCAM) and counterstaining with Mayer's hematoxylin. Compared with the pre-training values, there was a significant increase (P<0.05) in the number of NCAM-positively stained cells per fiber post-training in males (from 0.11+/-0.03 to 0.15+/-0.06; mean+/-SD) and females (from 0.11+/-0.04 to 0.13+/-0.05). These results suggest that 12 weeks of resistance training is effective in enhancing the satellite cell pool in skeletal muscle in the elderly.

Decline eccentric squats increases patellar tendon loading compared to standard eccentric squats.

BACKGROUND: Recent studies have shown excellent clinical results using eccentric squat training on a 25 degrees decline board to treat patellar tendinopathy. It remains unknown why therapeutic management of patellar tendinopathy using decline eccentric squats offer superior clinical efficacy compared to standard horizontal eccentric squats. This study aimed to compare electromyography activity, patellar tendon strain and joint angle kinematics during standard and decline eccentric squats. METHODS: Thirteen subjects performed unilateral eccentric squats on flat-and a 25 degrees decline surface. During the squats, electromyography activity was obtained in eight representative muscles. Also, ankle, knee and hip joint goniometry was obtained. Additionally, patellar tendon strain was measured in vivo using ultrasonography as subjects maintained a unilateral isometric 90 degrees knee angle squat position on either flat or 25 degrees decline surface. FINDINGS: Patellar tendon strain was significantly greater (P<0.05) during the squat position on the decline surface compared to the standard surface. The stop angles of the ankle and hip joints were significantly smaller during the decline compared to the standard squats (P<0.001, P<0.05). Normalized mean electromyography amplitudes of the knee extensor muscles were significantly greater during the decline compared to the standard squats (P<0.05). Hamstring and calf muscle mean electromyography did not differ, respectively, between standard and decline squats. INTERPRETATION: The use of a 25 degrees decline board increases the load and the strain of the patellar tendon during unilateral eccentric squats. This finding likely explains previous reports of superior clinical efficacy of decline eccentric squats in the rehabilitative management of patellar tendinopathy.

Structural Achilles tendon properties in athletes subjected to different exercise modes and in Achilles tendon rupture patients.

The prevalence of Achilles tendon (AT) injury is high in various sports, and AT rupture patients have been reported to have a 200-fold risk of sustaining a contralateral rupture. Tendon adaptation to different exercise modes is not fully understood. The present study investigated the structural properties of the AT in male elite athletes that subject their AT to different exercise modes as well as in Achilles rupture patients. Magnetic resonance imaging of the foot and leg, anthropometric measurements, and maximal isometric plantar flexion force were obtained in 6 male AT rupture patients and 25 male elite athletes (kayak/control group n = 9, volleyball n = 8 and endurance running n = 8). AT cross-sectional area (CSA) was normalized to body mass. Runners had a larger normalized AT CSA along the entire length of the tendon compared with the control group (P < 0.05). The volleyball subjects had a larger normalized CSA compared with the control group (P < 0.05) in the area of thinnest tendon CSA. No structural differences of the AT were found in the rupture subjects compared with the control group. Rupture subjects did not subject their AT to greater force or stress during a maximal voluntary isometric plantar flexion than the other groups. The CSA of the triceps surae musculature was the strongest predictor of AT CSA (r(s) = 0.569, P < 0.001). This study is the first to show larger CSA in tendons that are subjected to intermittent high loads. AT rupture patients did not display differences in structural or loading properties of the tendons.

Heavy resistance training increases muscle size, strength and physical function in elderly male COPD-patients--a pilot study.

This study investigated the effects of heavy resistance training in elderly males with chronic obstructive pulmonary disease (COPD). 18 Home-dwelling male patients (age range: 65-80 years), with a mean forced expiratory volume in the first second (FEV1) of 46 +/- 3.4% of predicted value, were recruited. Baseline and post-training assessments included: Cross-sectional area (CSA) of quadriceps assessed by MRI, isometric and isokinetic knee extension strength, isometric trunk strength, leg extension power, normal and maximal gait-speed on a 30 m track, stair climbing time, number of chair stands in 30 s, lung function (FEV1) and self-reported health. Subjects were randomized to a resistance training group (RE, n = 9) or a control group conducting breathing exercises (CON, n = 9). RE performed heavy progressive resistance training twice a week for 12 weeks. 6 RE and 7 CON completed the study. In RE the following improved (P < 0.05): Quadriceps CSA: 4%, isometric knee extension strength: 14%, isokinetic knee extension strength at 60 degrees /s.: 18%, leg extension power: 19%, maximal gait speed: 14%, stair climbing time: 17%, isometric trunk flexion: 5% and self-reported health. In CON no changes were found. In conclusion, 12 weeks of heavy resistance training twice a week resulted in significant improvements in muscle size, knee extension strength, leg extension power, functional performance and self-reported health in elderly male COPD patients.