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

2009 ◽  
Vol 107 (3) ◽  
pp. 880-886 ◽  
Author(s):  
C. Couppé ◽  
P. Hansen ◽  
M. Kongsgaard ◽  
V. Kovanen ◽  
C. Suetta ◽  
...  

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.

2008 ◽  
Vol 105 (6) ◽  
pp. 1907-1915 ◽  
Author(s):  
C. C. Carroll ◽  
J. M. Dickinson ◽  
J. M. Haus ◽  
G. A. Lee ◽  
C. J. Hollon ◽  
...  

Tendons are important for optimal muscle force transfer to bone and play a key role in functional ability. Changes in tendon properties with aging could contribute to declines in physical function commonly associated with aging. We investigated the in vivo mechanical properties of the patellar tendon in 37 men and women [11 young (27 ± 1 yr) and 26 old (65 ± 1 yr)] using ultrasonography and magnetic resonance imaging (MRI). Patella displacement relative to the tibia was monitored with ultrasonography during ramped isometric contractions of the knee extensors, and MRI was used to determine tendon cross-sectional area (CSA) and signal intensity. At peak force, patellar tendon deformation, stress, and strain were 13 ( P = 0.05), 19, and 12% less in old compared with young ( P < 0.05). Additionally, deformation, stiffness, stress, CSA, and length were 18, 35, 41, 28, and 11% greater ( P < 0.05), respectively, in men compared with women. After normalization of mechanical properties to a common force, no age differences were apparent; however, stress and strain were 26 and 22% higher, respectively, in women compared with men ( P < 0.05). CSA and signal intensity decreased 12 and 24%, respectively, with aging ( P < 0.05) in the midregion of the tendon. These data suggest that differences in patellar tendon in vivo mechanical properties with aging are more related to force output rather than an age effect. In contrast, the decrease in signal intensity indirectly suggests that the internal milieu of the tendon is altered with aging; however, the physiological and functional consequence of this finding requires further study.


2012 ◽  
Vol 112 (3) ◽  
pp. 419-426 ◽  
Author(s):  
René B. Svensson ◽  
Philip Hansen ◽  
Tue Hassenkam ◽  
Bjarki T. Haraldsson ◽  
Per Aagaard ◽  
...  

Tendons are strong hierarchical structures, but how tensile forces are transmitted between different levels remains incompletely understood. Collagen fibrils are thought to be primary determinants of whole tendon properties, and therefore we hypothesized that the whole human patellar tendon and its distinct collagen fibrils would display similar mechanical properties. Human patellar tendons ( n = 5) were mechanically tested in vivo by ultrasonography. Biopsies were obtained from each tendon, and individual collagen fibrils were dissected and tested mechanically by atomic force microscopy. The Young's modulus was 2.0 ± 0.5 GPa, and the toe region reached 3.3 ± 1.9% strain in whole patellar tendons. Based on dry cross-sectional area, the Young's modulus of isolated collagen fibrils was 2.8 ± 0.3 GPa, and the toe region reached 0.86 ± 0.08% strain. The measured fibril modulus was insufficient to account for the modulus of the tendon in vivo when fibril content in the tendon was accounted for. Thus, our original hypothesis was not supported, although the in vitro fibril modulus corresponded well with reported in vitro tendon values. This correspondence together with the fibril modulus not being greater than that of tendon supports that fibrillar rather than interfibrillar properties govern the subfailure tendon response, making the fibrillar level a meaningful target of intervention. The lower modulus found in vitro suggests a possible adverse effect of removing the tissue from its natural environment. In addition to the primary work comparing the two hierarchical levels, we also verified the existence of viscoelastic behavior in isolated human collagen fibrils.


2018 ◽  
Vol 125 (1) ◽  
pp. 205-214 ◽  
Author(s):  
Christian Skou Eriksen ◽  
Cecilie Henkel ◽  
Rene B. Svensson ◽  
Anne-Sofie Agergaard ◽  
Christian Couppé ◽  
...  

Aging negatively affects collagen-rich tissue, like tendons, but in vivo tendon mechanical properties and the influence of physical activity after the 8th decade of life remain to be determined. This study aimed to compare in vivo patellar tendon mechanical properties in moderately old (old) and very old adults and the effect of short-term resistance training. Twenty old (9 women, 11 men, >65 yr) and 30 very old (11 women, 19 men, >83 yr) adults were randomly allocated to heavy resistance training (HRT) or no training (CON) and underwent testing of in vivo patellar tendon (PT) mechanical properties and PT dimensions before and after a 3-mo intervention. Previous measurements of muscle properties, blood parameters, and physical activity level were included in the analysis. Data from 9 old HRT, 10 old CON, 14 very old CON, and 12 old HRT adults were analyzed. In addition to lower quadriceps muscle strength and cross-sectional area (CSA), we found lower PT stiffness and Young’s modulus ( P < 0.001) and a trend toward the lower mid-portion PT-CSA ( P = 0.09) in very old compared with old subjects. Daily step count was also lower in very old subjects ( P < 0.001). Resistance training improved muscle strength and cross-sectional area equally in old and very old subjects ( P < 0.05) but did not affect PT mechanical properties or dimension. We conclude that PT material properties are reduced in very old age, and this may likely be explained by reduced physical activity. Three months of resistance training however, could not alter PT mechanical properties in very old individuals. NEW & NOTEWORTHY This research is the first to quantify in vivo tendon mechanical properties in a group of very old adults in their eighties. Patellar tendon stiffness was lower in very old (87 yr on average) compared with moderately old (68 yr on average) individuals. Reduced physical activity with aging may explain some of the loss in tendon stiffness, but regular heavy resistance training for 3 mo was not sufficient to change tendon mechanical properties.


2008 ◽  
Vol 130 (2) ◽  
Author(s):  
K. L. Goh ◽  
D. F. Holmes ◽  
H.-Y. Lu ◽  
S. Richardson ◽  
K. E. Kadler ◽  
...  

Connective tissues are biological composites comprising of collagen fibrils embedded in (and reinforcing) the hydrated proteoglycan-rich (PG) gel within the extracellular matrices (ECMs). Age-related changes to the mechanical properties of tissues are often associated with changes to the structure of the ECM, namely, fibril diameter. However, quantitative attempts to correlate fibril diameter to mechanical properties have yielded inconclusive evidence. Here, we described a novel approach that was based on the rule of mixtures for fiber composites to evaluate the dependence of age-related changes in tendon tensile strength (σ) and stiffness (E) on the collagen fibril cross-sectional area fraction (ρ), which is related to the fibril volume fraction. Tail tendons from C57BL6 mice from age groups 1.6–35.3months old were stretched to failure to determine σ and E. Parallel measurements of ρ as a function of age were made using transmission electron microscopy. Mathematical models (rule of mixtures) of fibrils reinforcing a PG gel in tendons were used to investigate the influence of ρ on ageing changes in σ and E. The magnitudes of σ, E, and ρ increased rapidly from 1.6monthsto4.0months (P-values <0.05) before reaching a constant (age independent) from 4.0monthsto29.0months (P-values >0.05); this trend continued for E and ρ (P-values >0.05) from 29.0monthsto35.3months, but not for σ, which decreased gradually (P-values <0.05). Linear regression analysis revealed that age-related changes in σ and E correlated positively to ρ (P-values <0.05). Collagen fibril cross-sectional area fraction ρ is a significant predictor of ageing changes in σ and E in the tail tendons of C57BL6 mice.


2008 ◽  
Vol 105 (3) ◽  
pp. 805-810 ◽  
Author(s):  
C. Couppé ◽  
M. Kongsgaard ◽  
P. Aagaard ◽  
P. Hansen ◽  
J. Bojsen-Moller ◽  
...  

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 ≥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 mm2; mid-tendon: 85 ± 5 vs. 77 ± 3 mm2; proximal: 106 ± 7 vs. 83 ± 4 mm2; 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.


2016 ◽  
Vol 116 (10) ◽  
pp. 1921-1929 ◽  
Author(s):  
Luis M. Alegre ◽  
Michael Hasler ◽  
Sebastian Wenger ◽  
Werner Nachbauer ◽  
Robert Csapo

2003 ◽  
Vol 125 (6) ◽  
pp. 893-901 ◽  
Author(s):  
Ei Yamamoto ◽  
Susumu Tokura ◽  
Kozaburo Hayashi

Effects of cyclic stress on the mechanical properties of collagen fascicles were studied by in vitro tissue culture experiments. Collagen fascicles (approximately 300 μm in diameter) obtained from the rabbit patellar tendon were applied cyclic load at 4 Hz for one hour per day during culture period for one or two weeks, and then their mechanical properties were determined using a micro-tensile tester. There was a statistically significant correlation between tensile strength and applied peak stress in the range of 0 to 5 MPa, and the relation was expressed by a quadratic function. The maximum strength (19.4 MPa) was obtained at the applied peak stress of 1.8 MPa. The tensile strength of fascicles were within a range of control values, if they were cultured under peak stresses between 1.1 and 2.6 MPa. Similar results were also observed in the tangent modulus, which was maintained at control level under applied peak stresses between 0.9 and 2.8 MPa. The stress of 0.9 to 1.1 MPa is equivalent to approximately 40% of the in vivo peak stress which is developed in the intact rabbit patellar tendon by running, whereas that of 2.6 to 2.8 MPa corresponds to approximately 120% of the in vivo peak stress. Therefore, the fascicles cultured under applied peak stresses of lower than 40% and higher than 120% of the in vivo peak stress do not keep the original strength and modulus. These results indicate that the mechanical properties of cultured collagen fascicles strongly depend upon the magnitude of the stress applied during culture, which are similar to our previous results observed in stress-shielded and overstressed patellar tendons in vivo.


2013 ◽  
Vol 114 (8) ◽  
pp. 998-1008 ◽  
Author(s):  
Mette Hansen ◽  
Christian Couppe ◽  
Christina S. E. Hansen ◽  
Dorthe Skovgaard ◽  
Vuokko Kovanen ◽  
...  

Sex differences exist with regards to ligament and tendon injuries. Lower collagen synthesis has been observed in exercising women vs. men, and in users of oral contraceptives (OC) vs. nonusers, but it is unknown if OC will influence tendon biomechanics of women undergoing regular training. Thirty female athletes (handball players, 18–30 yr) were recruited: 15 long-term users of OC (7.0 ± 0.6 yr) and 15 nonusers (>5 yr). Synchronized values of patellar tendon elongation (obtained by ultrasonography) and tendon force were sampled during ramped isometric knee extensor maximum voluntary contraction to estimate mechanical tendon properties. Furthermore, tendon cross-sectional area and length were measured from MRI images, and tendon biopsies were obtained for analysis of tendon fibril characteristics and collagen cross-linking. Overall, no difference in tendon biomechanical properties, tendon fibril characteristics, or collagen cross-linking was observed between the OC users and nonusers, or between the different phases of the menstrual cycle. In athletes, tendon cross-sectional area in the preferred jumping leg tended to be larger than that in the contralateral leg ( P = 0.09), and a greater absolute ( P = 0.01) and normalized tendon stiffness ( P = 0.02), as well as a lower strain ( P = 0.04), were observed in the jumping leg compared with the contralateral leg. The results indicate that long-term OC use or menstrual phases does not influence structure or mechanical properties of the patellar tendon in female team handball athletes.


2014 ◽  
Vol 307 (9) ◽  
pp. R1124-R1135 ◽  
Author(s):  
Anita D. Christie ◽  
Anne Tonson ◽  
Ryan G. Larsen ◽  
Jacob P. DeBlois ◽  
Jane A. Kent

We tested the hypothesis that older muscle has greater metabolic economy (ME) in vivo than young, in a manner dependent, in part, on contraction intensity. Twenty young (Y; 24 ± 1 yr, 10 women), 18 older healthy (O; 73 ± 2, 9 women) and 9 older individuals with mild-to-moderate mobility impairment (OI; 74 ± 1, 7 women) received stimulated twitches (2 Hz, 3 min) and performed nonfatiguing voluntary (20, 50, and 100% maximal; 12 s each) isometric dorsiflexion contractions. Torque-time integrals (TTI; Nm·s) were calculated and expressed relative to maximal fat-free muscle cross-sectional area (cm2), and torque variability during voluntary contractions was calculated as the coefficient of variation. Total ATP cost of contraction (mM) was determined from flux through the creatine kinase reaction, nonoxidative glycolysis and oxidative phosphorylation, and used to calculate ME (Nm·s·cm−2·mM ATP−1). While twitch torque relaxation was slower in O and OI compared with Y ( P ≤ 0.001), twitch TTI, ATP cost, and economy were similar across groups ( P ≥ 0.15), indicating comparable intrinsic muscle economy during electrically induced isometric contractions in vivo. During voluntary contractions, normalized TTI and total ATP cost did not differ significantly across groups ( P ≥ 0.20). However, ME was lower in OI than Y or O at 20% and 50% MVC ( P ≤ 0.02), and torque variability was greater in OI than Y or O at 20% MVC ( P ≤ 0.05). These results refute the hypothesis of greater muscle ME in old age, and provide support for lower ME in impaired older adults as a potential mechanism or consequence of age-related reductions in functional mobility.


2007 ◽  
Vol 22 (6) ◽  
pp. 712-717 ◽  
Author(s):  
Stephen J. Pearson ◽  
Katherine Burgess ◽  
Gladys N.L. Onambele

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