Load magnitude affects patellar tendon mechanical properties but not collagen or collagen cross-linking after long-term strength training in older adults

Christian S Eriksen, Rene B Svensson, Anne T Gylling, Christian Couppé, S Peter Magnusson, Michael Kjaer, Christian S Eriksen, Rene B Svensson, Anne T Gylling, Christian Couppé, S Peter Magnusson, Michael Kjaer

Abstract

Background: Regular loading of tendons may counteract the negative effects of aging. However, the influence of strength training loading magnitude on tendon mechanical properties and its relation to matrix collagen content and collagen cross-linking is sparsely described in older adults. The purpose of the present study was to compare the effects of moderate or high load resistance training on tendon matrix and its mechanical properties.

Methods: Seventeen women and 19 men, age 62-70 years, were recruited and randomly allocated to 12 months of heavy load resistance training (HRT), moderate load resistance training (MRT) or control (CON). Pre- and post-intervention testing comprised isometric quadriceps strength test (IsoMVC), ultrasound based testing of in vivo patellar tendon (PT) mechanical properties, MRI-based measurement of PT cross-sectional area (CSA), PT biopsies for assessment of fibril morphology, collagen content, enzymatic cross-links, and tendon fluorescence as a measure of advanced glycation end-products (AGEs).

Results: Thirty three participants completed the intervention and were included in the data analysis. IsoMVC increased more after HRT (+ 21%) than MRT (+ 8%) and CON (+ 7%) (p < 0.05). Tendon stiffness (p < 0.05) and Young's modulus (p = 0.05) were also differently affected by training load with a reduction in CON and MRT but not in HRT. PT-CSA increased equally after both MRT and HRT. Collagen content, fibril morphology, enzymatic cross-links, and tendon fluorescence were unaffected by training.

Conclusion: Despite equal improvements in tendon size after moderate and heavy load resistance training, only heavy. load training seemed to maintain tendon mechanical properties in old age. The effect of load magnitude on tendon biomechanics was unrelated to changes of major load bearing matrix components in the tendon core. The study is a sub-study of the LISA study, which was registered at https://ichgcp.net/clinical-trials-registry/NCT02123641" title="See in ClinicalTrials.gov">NCT02123641) April 25th 2014.

Keywords: Aging.; Collagen cross-links.; Strength training.; Tendon biomechanics.

Conflict of interest statement

Ethics approval and consent to participate

The study complied with the Helsinki Declaration and all participants gave oral and written consent before enrollment. The study was registered at Consent for publication

Not applicable.

Competing interests

All authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Typical magnetic resonance images of the proximal patellar tendon from the same subject before (PRE) and after (POST) 12 months intervention. The two images are obtained at the same location
Fig. 2
Fig. 2
Isometric quadriceps (Q)-strength and vastus lateralis cross-sectional area (CSA) before (0 months) and after 12 months heavy resistance training (HRT), moderate load resistance training (MRT) or no training (CON). *Significant time x group interaction based on 2-way repeated measures ANOVA (p < 0.05) a: Significantly different from 0 months (p < 0.05). b: Significantly different from CON12 (p < 0.05), and c: Significantly different from MRT12 (p < 0.05) based on Tukey-Kramer post-hoc test
Fig. 3
Fig. 3
Illustration of average patellar tendon force/deformation (left) and stress/strain (right) curves before (PRE) and after (POST) 12 months heavy load resistance training (HRT), moderate load resistance training (MRT), or no training (CON)
Fig. 4
Fig. 4
Common force patellar tendon (PT) stiffness and Young’s modulus before (0 months) and after 12 months heavy resistance training (HRT), moderate load resistance training (MRT) or no training (CON). Bars represent mean ± SE. Significant time x group interaction denoted by **(p < 0.01) or *(p = 0.05) based on repeated measures 2-way ANOVA. A: Significantly different from 0 months (p < 0.05). B: Significantly different from CON12 (p < 0.05), C: Significantly different from MRT12 (p < 0.05) based on Tukey-Kramer post-hoc test
Fig. 5
Fig. 5
Changes in patellar tendon cross-sectional area (CSA) in three different regions (proximal, mid, distal) and in total after 12 months heavy resistance training (HRT), moderate load resistance training (MRT) or no training (CON). Bars represent mean ± SE. *Significant time x group interaction based on repeated measures ANOVA (pz0.05). ‡: Main effect of time (p < 0.05). a: Significant change from 0 to 12 months (p < 0.05), b: Significantly different from CON (p < 0.05), c: Significantly different from MRT (p < 0.05) based on Tukey-Kramer post-hoc test
Fig. 6
Fig. 6
Fluorescence of patellar tendon (PT) biopsies as a marker of non-enzymatic (AGE) cross-links before (0 months) and after 12 months intervention. ‡: Main effect of time (p < 0.05) based on repeated measures two-way ANOVA with baseline adjustment. AU = arbitrary units
Fig. 7
Fig. 7
Correlation between age and patellar tendon (PT) fluorescence using bot PRE and POST values as determined by Pearson’s correlation coefficient. Dotted lines are 95% confidence bands of the best fit

References

    1. Bailey AJ, Paul RG, Knott L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. 1998;106:1–2):1–56. doi: 10.1016/S0047-6374(98)00119-5.
    1. Brownlee M. Advanced protein glycosylation in diabetes and aging. Annu Rev Med. 1995;46:223–234. doi: 10.1146/annurev.med.46.1.223.
    1. Avery NC, Bailey AJ. The effects of the Maillard reaction on the physical properties and cell interactions of collagen. Pathol Biol [Internet] 2006;54(7):387–395. doi: 10.1016/j.patbio.2006.07.005.
    1. Kubo K, Kanehisa H, Miyatani M, Tachi M, Fukunaga T. Effect of low-load resistance training on the tendon properties in middle-aged and elderly women. Acta Physiol Scand. 2003;178(1):25–32. doi: 10.1046/j.1365-201X.2003.01097.x.
    1. Bojsen-Møller J, Magnusson SP, Rasmussen LR, Kjaer M, Aagaard P. Muscle Perfomance during maximal isometric and dynamic contractions is influenced by the stiffness of the tendinous structures. J Appl Physiol. 2005;99(3):986–994. doi: 10.1152/japplphysiol.01305.2004.
    1. Onambele GL, Narici MV, Maganaris CN. Calf muscle-tendon properties and postural balance in old age Calf muscle-tendon properties and postural balance in old age. J Appl Physiol. 2006:2048–56.
    1. Smith RKW, Birch HL, Goodman S, Heinegård D, Goodship AE. The influence of ageing and exercise on tendon growth and degeneration - hypotheses for the initiation and prevention of strain-induced tendinopathies. Comp Biochem Physiol - Part A. 2002;133(4):1039–1050. doi: 10.1016/S1095-6433(02)00148-4.
    1. Couppé C, Svensson RB, Grosset JF, Kovanen V, Nielsen RH, Olsen MR, et al. Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue. Age (Omaha). 2014;36(4).
    1. Reeves ND, Maganaris CN, Narici M V. Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol [Internet]. 2003;548(Pt 3):971–81.
    1. Epro G, Mierau A, Doerner J, Luetkens JA, Scheef L, Kukuk GM, et al. The Achilles tendon is mechanosensitive in older adults: adaptations following 14 weeks versus 1.5 years of cyclic strain exercise. J Exp Biol [Internet] 2017;220(6):1008–1018. doi: 10.1242/jeb.146407.
    1. Grosset JF, Breen L, Stewart CE, Burgess KE, Onambélé GL. Influence of exercise intensity on training-induced tendon mechanical properties changes in older individuals. Age (Omaha). 2014;36(3):9657. doi: 10.1007/s11357-014-9657-9.
    1. Bohm S, Mersmann F, Arampatzis A. Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults. Sport Med - Open [Internet]. 2015;1(7). Available from: Missingcontent/1/1/7.
    1. Carroll CC, Dickinson JM, LeMoine JK, Haus JM, Weinheimer EM, Hollon CJ, et al. Influence of acetaminophen and ibuprofen on in vivo patellar tendon adaptations to knee extensor resistance exercise in older adults. J Appl Physiol. 2011;111(2):508–515. doi: 10.1152/japplphysiol.01348.2010.
    1. Massey GJ, Balshaw TG, Maden-Wilkinson TM, Folland JP. Tendinous tissue properties after short- and long-term functional overload: Differences between controls, 12 weeks and 4 years of resistance training. Acta Physiol [Internet]. 2018;(July 2017):e13019.
    1. Couppe C, Kongsgaard M, Aagaard P, Hansen P, Bojsen-Moller J, Kjaer M, et al. Habitual loading results in tendon hypertrophy and increased stiffness of the human patellar tendon. J Appl Physiol [Internet] 2008;105(3):805–810. doi: 10.1152/japplphysiol.90361.2008.
    1. Heinemeier KM, Olesen JL, Haddad F, Langberg H, Kjaer M, Baldwin KM, et al. Expression of collagen and related growth factors in rat tendon and skeletal muscle in response to specific contraction types. J Physiol [Internet] 2007;582(Pt 3):1303–1316. doi: 10.1113/jphysiol.2007.127639.
    1. Langberg H, Skovgaard D, Petersen LJ, Bulow J, Kjaer M. Type I collagen synthesis and degradation in peritendinous tissue after exercise determined by microdialysis in humans. J Physiol [Internet]. 1999;521(1):299–306.
    1. Lenskjold A, Kongsgaard M, Larsen JO, Nielsen RH, Kovanen V, Aagaard P, et al. The influence of physical activity during youth on structural and functional properties of the Achilles tendon. Scand J Med Sci Sport. 2015;25(1):25–31. doi: 10.1111/sms.12143.
    1. Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M. Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb 14C. FASEB J. 2013;27(5):2074–2079. doi: 10.1096/fj.12-225599.
    1. Eyre DR, M a P, Gallop PM. Cross-linking in collagen and elastin. Annu Rev Biochem. 1984;53:717–748. doi: 10.1146/annurev.bi.53.070184.003441.
    1. Wood LK, Brooks SV. Ten weeks of treadmill running decreases stiffness and increases collagen turnover in tendons of old mice. J Orthop Res. 2016;34(2):346–353. doi: 10.1002/jor.22824.
    1. Bailey AJ. Molecular mechanisms of ageing in connective tissues. Mech Ageing Dev. 2001;122(7):735–755. doi: 10.1016/S0047-6374(01)00225-1.
    1. Bank RA. TeKoppele JM, Oostingh G, Hazleman BL, Riley GP. Lysylhydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis [Internet] 1999;58(1):35–41. doi: 10.1136/ard.58.1.35.
    1. Avery NC, Bailey AJ. Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sport. 2005;15(4):231–240. doi: 10.1111/j.1600-0838.2005.00464.x.
    1. Fessel G, Li Y, Diederich V, Guizar-Sicairos M, Schneider P, Sell DR, et al. Advanced glycation end-products reduce collagen molecular sliding to affect collagen fibril damage mechanisms but not stiffness. PLoS One. 2014;9(11).
    1. Sell DR, Monnier VM. Age-related association of tail tendon break time with tissue pentosidine in DBA/2 vs C57BL/6 mice: the effect of dietary restriction. J Gerontol A Biol Sci Med Sci. 1997;52(5):B277–B284. doi: 10.1093/gerona/52A.5.B277.
    1. Kongsgaard M, Kovanen V, Aagaard P, Doessing S, Hansen P, Laursen AH, et al. Corticosteroid injections, eccentric decline squat training and heavy slow resistance training in patellar tendinopathy. Scand J Med Sci Sport. 2009;19(6):790–802. doi: 10.1111/j.1600-0838.2009.00949.x.
    1. Reddy GK. Cross-linking in collagen by nonenzymatic glycation increases the matrix stiffness in rabbit Achilles tendon. Exp Diabesity Res. 2004;5(2):143–153. doi: 10.1080/15438600490277860.
    1. Naresh MD, Brodsky B. X-ray diffraction studies on human tendon show age-related changes in collagen packing. Biochim Biophys Acta [Internet] 1992;1122(2):161–166. doi: 10.1016/0167-4838(92)90319-9.
    1. Couppé C, Hansen P, Kongsgaard M, Kovanen V, Suetta C, Aagaard P, et al. Mechanical properties and collagen cross-linking of the patellar tendon in old and young men. J Appl Physiol 2009;107(June 2009):880–6.
    1. Eriksen CS, Garde E, Reislev NL, Wimmelmann CL, Bieler T, Ziegler AK, et al. Physical activity as intervention for age-related loss of muscle mass and function: protocol for a randomised controlled trial (the LISA study). BMJ Open [Internet]. 2016;6(12):e012951.
    1. Volper BD, Huynh RT, Arthur KA, Noone J, Gordon BD, Zacherle EW, et al. Influence of acute and chronic streptozotocin-induced diabetes on the rat tendon extracellular matrix and mechanical properties. Am J Physiol Regul Integr Comp Physiol. 2015;309(9):R1135–R1143. doi: 10.1152/ajpregu.00189.2015.
    1. Couppé C, Svensson RB, Kongsgaard M, Kovanen V, Grosset J-F, Snorgaard O, et al. Human Achilles tendon glycation and function in diabetes. J Appl Physiol [Internet]. 2016;120(2):130–137. Available from: 10.1152/japplphysiol.00547.2015
    1. Beason DP, Hsu JE, Marshall SM, McDaniel AL, Temel RE, Abboud JA, et al. Hypercholesterolemia increases supraspinatus tendon stiffness and elastic modulus across multiple species. J Shoulder Elb Surg [Internet]. 2013;22(5):681–686. Available from: 10.1016/j.jse.2012.07.008
    1. Hansen M, Couppe C, Hansen CSE, Skovgaard D, Kovanen V, Larsen JO, et al. Impact of oral contraceptive use and menstrual phases on patellar tendon morphology, biochemical composition, and biomechanical properties in female athletes. J Appl Physiol [Internet]. 2013;114(8):998–1008.
    1. Dahlgren G, Carlsson D, Moorhead A, Häger-Ross C, McDonough SM. Test-retest reliability of step counts with the ActivPAL device in common daily activities. Gait Posture. 2010;32(3):386–390. doi: 10.1016/j.gaitpost.2010.06.022.
    1. Hansen P, Bojsen-Moller J, Aagaard P, Kjaer M, Magnusson SP. Mechanical properties of the human patellar tendon, in vivo. Clin Biomech. 2006;21(1):54–58. doi: 10.1016/j.clinbiomech.2005.07.008.
    1. Magnusson SP, Hansen P, Aagaard P, Brønd J, Dyhre-Poulsen P, Bojsen-Moller J, et al. Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. Acta Physiol Scand. 2003;177(2):185–195. doi: 10.1046/j.1365-201X.2003.01048.x.
    1. Visser JJ, Hoogkamer JE, Bobbert MF, Huijing PA. Length and moment arm of human leg muscles as a function of knee and hip-joint angles. Eur J Appl Physiol. 1990;61(5–6):453–460. doi: 10.1007/BF00236067.
    1. Couppé C, Svensson RB, Sødring-Elbrønd V, Hansen P, Kjær M, Magnusson SP. Accuracy of MRI technique in measuring tendon cross-sectional area. Clin Physiol Funct Imaging. 2014;34(3):237–241. doi: 10.1111/cpf.12086.
    1. Boesen AP, Dideriksen K, Couppé C, Magnusson SP, Schjerling P, Boesen M, et al. Tendon and skeletal muscle matrix gene expression and functional responses to immobilisation and rehabilitation in young males: effect of growth hormone administration. J Physiol 2013;591.23(591):6039–6052.
    1. Shalabi A, Kristoffersen-Wiberg M, Aspelin P, Movin T. Immediate achilles tendon response after strength training evaluated by MRI. Med Sci Sports Exerc. 2004;36(11):1841–1846. doi: 10.1249/01.MSS.0000145450.75035.61.
    1. Kongsgaard M, Qvortrup K, Larsen J, Aagaard P, Doessing S, Hansen P, et al. Fibril morphology and tendon mechanical properties in patellar tendinopathy: effects of heavy slow resistance training. Am J Sports Med. 2010;38(4):749–756. doi: 10.1177/0363546509350915.
    1. Yeung CYC, Gossan N, Lu Y, Hughes A, Hensman JJ, Bayer ML, et al. Gremlin-2 is a BMP antagonist that is regulated by the circadian clock. Sci Rep. 2014;4:1–8.
    1. Heinemeier KM, Lorentzen MP, Jensen JK, Schjerling P, Seynnes O, Narici M V, et alLocal trauma in human patellar tendon leads to widespread changes in the tendon gene expression. J Appl Physiol [Internet]. 2016;120:1000–10.
    1. Boesen AP, Dideriksen K, Couppe C, Magnusson SP, Schjerling P, Boesen M, et al. Effect of growth hormone on aging connective tissue in muscle and tendon: gene expression, morphology, and function following immobilization and rehabilitation. J Appl Physiol [Internet]. 2014;116(2):192–203.
    1. Svensson RB, Smith ST, Moyer PJ, Magnusson SP. Acta Biomater Effects of maturation and advanced glycation on tensile mechanics of collagen fibrils from rat tail and Achilles tendons. Acta Biomater [Internet]. 2018. Available from: 10.1016/j.actbio.2018.02.005.
    1. Monnier VM, Vishwanath V, KE F, CA E, P D RRK. Relation between complications of type I diabetes mellitus and collagen-linked fluorescence. N Engl J Med. 1986;314(7):403–408. doi: 10.1056/NEJM198602133140702.
    1. GraphPad Software I ©2017. Grubb’s test [Internet]. [cited 2017 Oct 11]. Available from:
    1. Peterson MD, Rhea MR, Sen A, Gordon PM. Resistance exercise for muscular strength in older adults: a meta-analysis. Ageing Res Rev [Internet] 2010;9(3):226–237. Available from: 10.1016/j.arr.2010.03.004
    1. Onambele-Pearson GL, Pearson SJ. The magnitude and character of resistance-training-induced increase in tendon stiffness at old age is gender specific. Age (Omaha) 2012;34(2):427–438. doi: 10.1007/s11357-011-9248-y.
    1. Seynnes OR, Erskine RM, Maganaris CN, Longo S, Simoneau EM, Grosset JF, et al. Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol. 2009;107(2):523–530. doi: 10.1152/japplphysiol.00213.2009.
    1. Malliaras P, Kamal B, Nowell A, Farley T, Dhamu H, Simpson V, et al. Patellar tendon adaptation in relation to load-intensity and contraction type. J Biomech. 2013;46(11):1893–1899. doi: 10.1016/j.jbiomech.2013.04.022.
    1. Arampatzis A, Karamanidis K, Albracht K. Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. J Exp Biol 2007;210(Pt 15):2743–2753.
    1. Lavagnino M, Arnoczky SP, Tian T, Vaupel Z. Effect of amplitude and frequency of cyclic tensile strain on the inhibition of MMP-1 mRNA expression in tendon cells: an in vitro study. Connect Tissue Res. 2003;44(3–4):181–187. doi: 10.1080/03008200390215881.
    1. Voigt M, Bojsen-Møller F, Simonsen EB, Dyhre-Poulsen P. The influence of tendon youngs modulus, dimensions and instantaneous moment arms on the efficiency of human movement. J Biomech. 1995;28(3):281–291. doi: 10.1016/0021-9290(94)00071-B.
    1. Holm L, van Hall G, Rose AJ, Miller BF, Doessing S, E a R, et al. Contraction intensity and feeding affect collagen and myofibrillar protein synthesis rates differently in human skeletal muscle. Am J Physiol Endocrinol Metab. 2010;298(23):E257–E269. doi: 10.1152/ajpendo.00609.2009.
    1. Standley RA, Harber MP, Lee JD, Konopka AR, Trappe SW, Trappe TA. Influence of aerobic cycle exercise training on patellar tendon cross-sectional area in older women. Scand J Med Sci Sport. 2013;23(3):367–373. doi: 10.1111/j.1600-0838.2011.01396.x.
    1. Kongsgaard M, Reitelseder S, Pedersen TG, Holm L, Aagaard P, Kjaer M, et al. Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol. 2007;191(2):111–121. doi: 10.1111/j.1748-1716.2007.01714.x.
    1. Lemoine JK, Lee JD, Trappe TA. Impact of sex and chronic resistance training on human patellar tendon dry mass, collagen content, and collagen cross-linking. Am J Physiol Regul Integr Comp Physiol [Internet]. 2009;296(1):R119–24.
    1. Herchenhan A, Uhlenbrock F, Eliasson P, Weis M, Eyre D, Kadler KE, et al. Lysyl oxidase activity is required for ordered collagen fibrillogenesis by tendon cells. J Biol Chem. 2015;290(26):16440–16450. doi: 10.1074/jbc.M115.641670.
    1. Hansen P, Haraldsson BT, Aagaard P, Kovanen V, Avery NC, Qvortrup K, et al. Lower strength of the human posterior patellar tendon seems unrelated to mature collagen cross-linking and fibril morphology. J Appl Physiol. 2010;108(1):47–52. doi: 10.1152/japplphysiol.00944.2009.
    1. Thorpe CT, Stark RJF, Goodship AE, Birch HL. Mechanical properties of the equine superficial digital flexor tendon relate to specific collagen cross-link levels. Equine Vet J. 2010;42(SUPPL. 38):538–543. doi: 10.1111/j.2042-3306.2010.00175.x.
    1. Dubowitz N, Xue W, Long Q, Ownby JG, Olson DE, Barb D, et al. Aging is associated with increased HbA1c levels, independently of glucose levels and insulin resistance, and also with decreased HbA1c diagnostic specificity. Diabet Med [Internet]. 2014;31(8):927–935.
    1. Li Y, Fessel G, Georgiadis M, Snedeker JG. Advanced glycation end-products diminish tendon collagen fiber sliding. Matrix Biol. 2013;32(3–4):169–177. doi: 10.1016/j.matbio.2013.01.003.
    1. Eriksen C, Svensson RB, Scheijen J, Hag A. MF, Schalkwijk C, Praet SFE, et al. Systemic stiffening of mouse tail tendon is related to dietary advanced glycation end products but not high-fat diet or cholesterol. J Appl Physiol [Internet]. 2014;117(8):840–7.
    1. Svensson RB, Mulder H, Kovanen V, Magnusson SP. Fracture mechanics of collagen fibrils: influence of natural cross-links. Biophys J [Internet] 2013;104(11):2476–2484. doi: 10.1016/j.bpj.2013.04.033.
    1. Uzel SGM, Buehler MJ. Molecular structure, mechanical behavior and failure mechanism of the C-terminal cross-link domain in type I collagen. J Mech Behav Biomed Mater [Internet] 2011;4(2):153–161. Available from: 10.1016/j.jmbbm.2010.07.003
    1. Gautieri A, Passini FS, Silván U, Guizar-Sicairos M, Carimati G, Volpi P, et al. Advanced glycation end-products: Mechanics of aged collagen from molecule to tissue. Matrix Biol [Internet]. 2017;59:95–108. Available from: 10.1016/j.matbio.2016.09.001
    1. Magnusson SP, Hansen M, Langberg H, Miller B, Haraldsson B, Westh EK, Koskinen S, Aagaard P, Kjaer M. The adaptability of tendon to loading differs in men and women. Int J Exp Pathol. 2007;88:237–240. doi: 10.1111/j.1365-2613.2007.00551.x.
    1. Westh E, Kongsgaard M, Bojsen-Moller J, Aagaard P, Hansen M, Kjaer M, et al. Effect of habitual exercise on the structural and mechanical properties of human tendon, in vivo, in men and women. Scand J Med Sci Sport. 2008;18(1):23–30. doi: 10.1111/j.1600-0838.2007.00638.x.
    1. Burgess KE, Pearson SJ, Breen L, Onambélé GNL. Tendon structural and mechanical properties do not differ between genders in a healthy community-dwelling elderly population. J Orthop Res. 2009;27(6):820–825. doi: 10.1002/jor.20811.
    1. Kösters A, Wiesinger HP, Bojsen-Møller J, Müller E, Seynnes O. Influence of loading rate on patellar tendon mechanical properties in vivo. Clin Biomech. 2014;29:323–329. doi: 10.1016/j.clinbiomech.2013.12.010.
    1. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Bojsen- Møller F, Dyhre-Poulsen P. Antagonist muscle coactivation during isokinetic knee extension. Scand J Med Sci Sport. 2000;10:58–67. doi: 10.1034/j.1600-0838.2000.010002058.x.

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa