Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
BMC Geriatrics
Published in: BMC Geriatrics 1/2019

Open Access 01-12-2019 | Research article

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

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

Published in: BMC Geriatrics | Issue 1/2019

Login to get access

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 http://​clinicaltrials.​gov (NCT02123641) April 25th 2014.
Literature
1.
Bailey AJ, Paul RG, Knott L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. 1998;106:1–2):1–56.CrossRef
2.
Brownlee M. Advanced protein glycosylation in diabetes and aging. Annu Rev Med. 1995;46:223–34.CrossRef
3.
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):387–95.CrossRef
4.
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.CrossRef
5.
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):986–94.CrossRef
6.
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.
7.
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):1039–50.CrossRef
8.
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).
9.
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.
10.
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):1008–18.CrossRef
11.
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.CrossRef
12.
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.
13.
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):508–15.CrossRef
14.
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.
15.
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):805–10.CrossRef
16.
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):1303–16.CrossRef
17.
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.
18.
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.CrossRef
19.
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):2074–9.CrossRef
20.
Eyre DR, M a P, Gallop PM. Cross-linking in collagen and elastin. Annu Rev Biochem. 1984;53:717–48.CrossRef
21.
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):346–53.CrossRef
22.
Bailey AJ. Molecular mechanisms of ageing in connective tissues. Mech Ageing Dev. 2001;122(7):735–55.CrossRef
23.
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.CrossRef
24.
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):231–40.CrossRef
25.
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).
26.
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):B277–84.CrossRef
27.
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.CrossRef
28.
Reddy GK. Cross-linking in collagen by nonenzymatic glycation increases the matrix stiffness in rabbit Achilles tendon. Exp Diabesity Res. 2004;5(2):143–53.CrossRef
29.
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):161–6.CrossRef
30.
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.
31.
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.
32.
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):R1135–43.CrossRef
33.
34.
35.
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.
36.
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):386–90.CrossRef
37.
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):54–8.CrossRef
38.
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):185–95.CrossRef
39.
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):453–60.CrossRef
40.
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):237–41.CrossRef
41.
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.
42.
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):1841–6.CrossRef
43.
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):749–56.CrossRef
44.
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.
45.
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.
46.
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.
47.
48.
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):403–8.CrossRef
49.
50.
51.
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):427–38.CrossRef
52.
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):523–30.CrossRef
53.
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):1893–9.CrossRef
54.
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.
55.
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):181–7.CrossRef
56.
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):281–91.CrossRef
57.
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):E257–69.CrossRef
58.
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):367–73.CrossRef
59.
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):111–21.CrossRef
60.
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.
61.
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):16440–50.CrossRef
62.
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.CrossRef
63.
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):538–43.CrossRef
64.
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.
65.
Li Y, Fessel G, Georgiadis M, Snedeker JG. Advanced glycation end-products diminish tendon collagen fiber sliding. Matrix Biol. 2013;32(3–4):169–77.CrossRef
66.
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.
67.
68.
69.
70.
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;88:237–40.CrossRef
71.
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.CrossRef
72.
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):820–5.CrossRef
73.
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;29:323–9.CrossRef
74.
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.CrossRef
Metadata
Title
Load magnitude affects patellar tendon mechanical properties but not collagen or collagen cross-linking after long-term strength training in older adults
Authors
Christian S. Eriksen
Rene B. Svensson
Anne T. Gylling
Christian Couppé
S. Peter Magnusson
Michael Kjaer
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Geriatrics / Issue 1/2019
Electronic ISSN: 1471-2318
DOI
https://doi.org/10.1186/s12877-019-1043-0

Other articles of this Issue 1/2019

BMC Geriatrics 1/2019 Go to the issue

Research article

Cognitive function in Prefrail and frail community-dwelling older adults in China

Research article

A collective case study of the features of impactful dementia training for care home staff

Research article

Body weight, frailty, and chronic pain in older adults: a cross-sectional study

Research article

Transitioning of older Australian women into and through the long-term care system: a cohort study using linked data

Research article

Age-related deficits in bilateral motor synergies and force coordination

Research article

Blood pressure and hypertension prevalence among oldest-old in China for 16 year: based on CLHLS
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits