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Published in: Sports Medicine - Open 1/2015

Open Access 01-12-2015 | Systematic Review

Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults

Authors: Sebastian Bohm, Falk Mersmann, Adamantios Arampatzis

Published in: Sports Medicine - Open | Issue 1/2015

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Abstract

Background

The present article systematically reviews recent literature on the in vivo adaptation of asymptomatic human tendons following increased chronic mechanical loading, and meta-analyzes the loading conditions, intervention outcomes, as well as methodological aspects.

Methods

The search was performed in the databases PubMed, Web of Knowledge, and Scopus as well as in the reference lists of the eligible articles. A study was included if it conducted (a) a longitudinal exercise intervention (≥8 weeks) on (b) healthy humans (18 to 50 years), (c) investigating the effects on mechanical (i.e., stiffness), material (i.e., Young’s modulus) and/or morphological properties (i.e., cross-sectional area (CSA)) of tendons in vivo, and was reported (d) in English language. Weighted average effect sizes (SMD, random-effects) and heterogeneity (Q and I 2 statistics) of the intervention-induced changes of tendon stiffness, Young’s modulus, and CSA were calculated. A subgroup analysis was conducted regarding the applied loading intensity, muscle contraction type, and intervention duration. Further, the methodological study quality and the risk of bias were assessed.

Results

The review process yielded 27 studies with 37 separate interventions on either the Achilles or patellar tendon (264 participants). SMD was 0.70 (confidence interval: 0.51, 0.88) for tendon stiffness (N=37), 0.69 (0.36, 1.03) for Young’s modulus (N=17), and 0.24 (0.07, 0.42) for CSA (N=33), with significant overall intervention effects (p<0.05). The heterogeneity analysis (stiffness: I 2 =30%; Young’s modulus: I 2 =57%; CSA: I 2 =21%) indicated that differences in the loading conditions may affect the adaptive responses. The subgroup analysis confirmed that stiffness adaptation significantly (p<0.05) depends on loading intensity (I 2 =0%), but not on muscle contraction type. Although not significantly different, SMD was higher for interventions with longer duration (≥12 weeks). The average score of 71±9% in methodological quality assessment indicated an appropriate quality of most studies.

Conclusions

The present meta-analysis provides elaborate statistical evidence that tendons are highly responsive to diverse loading regimens. However, the data strongly suggests that loading magnitude in particular plays a key role for tendon adaptation in contrast to muscle contraction type. Furthermore, intervention-induced changes in tendon stiffness seem to be more attributed to adaptations of the material rather than morphological properties.
Literature
3.
go back to reference McNeill AR. Tendon elasticity and muscle function. Comp Biochem Physiol A Mol Integr Physiol. 2002;133:1001–11.CrossRef McNeill AR. Tendon elasticity and muscle function. Comp Biochem Physiol A Mol Integr Physiol. 2002;133:1001–11.CrossRef
4.
go back to reference Alexander R. Energy-saving mechanisms in walking and running. J Exp Biol. 1991;160:55–69.PubMed Alexander R. Energy-saving mechanisms in walking and running. J Exp Biol. 1991;160:55–69.PubMed
5.
go back to reference Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa H, Maganaris CN. In vivo behaviour of human muscle tendon during walking. Proc R Soc B Biol Sci. 2001;268:229–33.CrossRef Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa H, Maganaris CN. In vivo behaviour of human muscle tendon during walking. Proc R Soc B Biol Sci. 2001;268:229–33.CrossRef
6.
go back to reference Ettema GJ, Huijing PA, van Ingen Schenau GJ, de Haan A. Effects of prestretch at the onset of stimulation on mechanical work output of rat medial gastrocnemius muscle-tendon complex. J Exp Biol. 1990;152:333–51.PubMed Ettema GJ, Huijing PA, van Ingen Schenau GJ, de Haan A. Effects of prestretch at the onset of stimulation on mechanical work output of rat medial gastrocnemius muscle-tendon complex. J Exp Biol. 1990;152:333–51.PubMed
7.
go back to reference Ettema GJ, van Soest AJ, Huijing PA. The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions. J Exp Biol. 1990;154:121–36.PubMed Ettema GJ, van Soest AJ, Huijing PA. The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions. J Exp Biol. 1990;154:121–36.PubMed
8.
go back to reference Kawakami Y, Muraoka T, Ito S, Kanehisa H, Fukunaga T. In vivo muscle fibre behaviour during counter-movement exercise in humans reveals a significant role for tendon elasticity. J Physiol Lond. 2002;540:635–46.CrossRefPubMedCentralPubMed Kawakami Y, Muraoka T, Ito S, Kanehisa H, Fukunaga T. In vivo muscle fibre behaviour during counter-movement exercise in humans reveals a significant role for tendon elasticity. J Physiol Lond. 2002;540:635–46.CrossRefPubMedCentralPubMed
9.
go back to reference Lichtwark GA, Bougoulias K, Wilson AM. Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J Biomech. 2007;40:157–64.CrossRefPubMed Lichtwark GA, Bougoulias K, Wilson AM. Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J Biomech. 2007;40:157–64.CrossRefPubMed
10.
go back to reference Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008;18:980–9.CrossRefPubMed Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008;18:980–9.CrossRefPubMed
11.
go back to reference Kubo K, Ikebukuro T, Yata H, Tomita M, Okada M. Morphological and mechanical properties of muscle and tendon in highly trained sprinters. J Appl Biomech. 2011;27:336–44.PubMed Kubo K, Ikebukuro T, Yata H, Tomita M, Okada M. Morphological and mechanical properties of muscle and tendon in highly trained sprinters. J Appl Biomech. 2011;27:336–44.PubMed
12.
go back to reference Stafilidis S, Arampatzis A. Muscle – tendon unit mechanical and morphological properties and sprint performance. J Sports Sci. 2007;25:1035–46.CrossRefPubMed Stafilidis S, Arampatzis A. Muscle – tendon unit mechanical and morphological properties and sprint performance. J Sports Sci. 2007;25:1035–46.CrossRefPubMed
13.
go back to reference Ishikawa M, Niemela E, Komi PV. Interaction between fascicle and tendinous tissues in short-contact stretch-shortening cycle exercise with varying eccentric intensities. J Appl Physiol. 2005;99:217–23.CrossRefPubMed Ishikawa M, Niemela E, Komi PV. Interaction between fascicle and tendinous tissues in short-contact stretch-shortening cycle exercise with varying eccentric intensities. J Appl Physiol. 2005;99:217–23.CrossRefPubMed
14.
go back to reference Lichtwark GA, Wilson AM. In vivo mechanical properties of the human Achilles tendon during one-legged hopping. J Exp Biol. 2005;208:4715–25.CrossRefPubMed Lichtwark GA, Wilson AM. In vivo mechanical properties of the human Achilles tendon during one-legged hopping. J Exp Biol. 2005;208:4715–25.CrossRefPubMed
15.
go back to reference Albracht K, Arampatzis A. Exercise-induced changes in triceps surae tendon stiffness and muscle strength affect running economy in humans. Eur J Appl Physiol. 2013;113:1605–15.CrossRefPubMed Albracht K, Arampatzis A. Exercise-induced changes in triceps surae tendon stiffness and muscle strength affect running economy in humans. Eur J Appl Physiol. 2013;113:1605–15.CrossRefPubMed
16.
go back to reference Arampatzis A, De Monte G, Karamanidis K, Morey-Klapsing G, Stafilidis S, Brueggemann G-P. Influence of the muscle-tendon unit’s mechanical and morphological properties on running economy. J Exp Biol. 2006;209:3345–57.CrossRefPubMed Arampatzis A, De Monte G, Karamanidis K, Morey-Klapsing G, Stafilidis S, Brueggemann G-P. Influence of the muscle-tendon unit’s mechanical and morphological properties on running economy. J Exp Biol. 2006;209:3345–57.CrossRefPubMed
17.
go back to reference Fletcher JR, Esau SP, MacIntosh BR. Changes in tendon stiffness and running economy in highly trained distance runners. Eur J Appl Physiol. 2010;110:1037–46.CrossRefPubMed Fletcher JR, Esau SP, MacIntosh BR. Changes in tendon stiffness and running economy in highly trained distance runners. Eur J Appl Physiol. 2010;110:1037–46.CrossRefPubMed
18.
go back to reference Galloway MT, Lalley AL, Shearn JT. The role of mechanical loading in tendon development, maintenance, injury, and repair. J Bone Joint Surg. 2013;95:1620–8.CrossRefPubMedCentralPubMed Galloway MT, Lalley AL, Shearn JT. The role of mechanical loading in tendon development, maintenance, injury, and repair. J Bone Joint Surg. 2013;95:1620–8.CrossRefPubMedCentralPubMed
19.
go back to reference Heinemeier KM, Kjaer M. In vivo investigation of tendon responses to mechanical loading. J Musculoskelet Neuronal Interact. 2011;11:115–23.PubMed Heinemeier KM, Kjaer M. In vivo investigation of tendon responses to mechanical loading. J Musculoskelet Neuronal Interact. 2011;11:115–23.PubMed
20.
go back to reference Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004;84:649–98.CrossRefPubMed Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004;84:649–98.CrossRefPubMed
21.
go back to reference Lavagnino M, Arnoczky SP. In vitro alterations in cytoskeletal tensional homeostasis control gene expression in tendon cells. J Orthop Res. 2005;23:1211–8.CrossRefPubMed Lavagnino M, Arnoczky SP. In vitro alterations in cytoskeletal tensional homeostasis control gene expression in tendon cells. J Orthop Res. 2005;23:1211–8.CrossRefPubMed
23.
go back to reference Arampatzis A, Karamanidis K, Morey-Klapsing G, De Monte G, Stafilidis S. Mechanical properties of the triceps surae tendon and aponeurosis in relation to intensity of sport activity. J Biomech. 2007;40:1946–52.CrossRefPubMed Arampatzis A, Karamanidis K, Morey-Klapsing G, De Monte G, Stafilidis S. Mechanical properties of the triceps surae tendon and aponeurosis in relation to intensity of sport activity. J Biomech. 2007;40:1946–52.CrossRefPubMed
24.
go back to reference Kongsgaard M, Reitelseder S, Pedersen TG, Holm L, Aagaard P, Kjaer M. Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol. 2007;191:111–21.CrossRef Kongsgaard M, Reitelseder S, Pedersen TG, Holm L, Aagaard P, Kjaer M. Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol. 2007;191:111–21.CrossRef
25.
go back to reference Kubo K, Kanehisa H, Fukunaga T. Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo. J Physiol. 2002;538:219–26.CrossRefPubMedCentralPubMed Kubo K, Kanehisa H, Fukunaga T. Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo. J Physiol. 2002;538:219–26.CrossRefPubMedCentralPubMed
26.
go back to reference Reeves ND, Maganaris CN, Narici MV. Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol Lond. 2003;548:971–81.CrossRefPubMedCentralPubMed Reeves ND, Maganaris CN, Narici MV. Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol Lond. 2003;548:971–81.CrossRefPubMedCentralPubMed
27.
go back to reference LaCroix AS, Duenwald-Kuehl SE, Lakes RS, Vanderby Jr R. Relationship between tendon stiffness and failure: a metaanalysis. J Appl Physiol (Bethesda Md: 1985). 2013;115:43–51.CrossRef LaCroix AS, Duenwald-Kuehl SE, Lakes RS, Vanderby Jr R. Relationship between tendon stiffness and failure: a metaanalysis. J Appl Physiol (Bethesda Md: 1985). 2013;115:43–51.CrossRef
28.
go back to reference Arampatzis A, Peper A, Bierbaum S, Albracht K. Plasticity of human Achilles tendon mechanical and morphological properties in response to cyclic strain. J Biomech. 2010;43:3073–9.CrossRefPubMed Arampatzis A, Peper A, Bierbaum S, Albracht K. Plasticity of human Achilles tendon mechanical and morphological properties in response to cyclic strain. J Biomech. 2010;43:3073–9.CrossRefPubMed
29.
go back to reference 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;210:2743–53.CrossRefPubMed 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;210:2743–53.CrossRefPubMed
30.
go back to reference Seynnes OR, Erskine RM, Maganaris CN, Longo S, Simoneau EM, Grosset JF. 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 (Bethesda, Md: 1985). 2009;107:523–30.CrossRef Seynnes OR, Erskine RM, Maganaris CN, Longo S, Simoneau EM, Grosset JF. 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 (Bethesda, Md: 1985). 2009;107:523–30.CrossRef
31.
go back to reference Bohm S, Mersmann F, Tettke M, Kraft M, Arampatzis A. Human Achilles tendon plasticity in response to cyclic strain: effect of rate and duration. J. Exp. Biol. 2014. doi:10.1242/jeb.112268. Bohm S, Mersmann F, Tettke M, Kraft M, Arampatzis A. Human Achilles tendon plasticity in response to cyclic strain: effect of rate and duration. J. Exp. Biol. 2014. doi:10.1242/jeb.112268.
32.
go back to reference Kjaer M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm L. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports. 2009;19:500–10.CrossRefPubMed Kjaer M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm L. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports. 2009;19:500–10.CrossRefPubMed
33.
go back to reference Miller BF, Olesen JL, Hansen M, Døssing S, Crameri RM, Welling RJ. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol. 2005;567:1021–33.CrossRefPubMedCentralPubMed Miller BF, Olesen JL, Hansen M, Døssing S, Crameri RM, Welling RJ. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol. 2005;567:1021–33.CrossRefPubMedCentralPubMed
34.
go back to reference Wang JH-C, Guo Q, Li B. Tendon biomechanics and mechanobiology—a minireview of basic concepts and recent advancements. J Hand Ther. 2012;25:133–41.CrossRefPubMedCentralPubMed Wang JH-C, Guo Q, Li B. Tendon biomechanics and mechanobiology—a minireview of basic concepts and recent advancements. J Hand Ther. 2012;25:133–41.CrossRefPubMedCentralPubMed
35.
go back to reference Magnan B, Bondi M, Pierantoni S, Samaila E. The pathogenesis of Achilles tendinopathy: a systematic review. Foot Ankle Surg. 2014;20:154–9.CrossRefPubMed Magnan B, Bondi M, Pierantoni S, Samaila E. The pathogenesis of Achilles tendinopathy: a systematic review. Foot Ankle Surg. 2014;20:154–9.CrossRefPubMed
36.
go back to reference Arampatzis A, Karamanidis K, Mademli L, Albracht K. Plasticity of the human tendon to short- and long-term mechanical loading. Exerc Sport Sci Rev. 2009;37:66–72.CrossRefPubMed Arampatzis A, Karamanidis K, Mademli L, Albracht K. Plasticity of the human tendon to short- and long-term mechanical loading. Exerc Sport Sci Rev. 2009;37:66–72.CrossRefPubMed
37.
go back to reference Kubo K, Kanehisa H, Ito M, Fukunaga T. Effects of isometric training on the elasticity of human tendon structures in vivo. J Appl Physiol. 2001;91:26–32.PubMed Kubo K, Kanehisa H, Ito M, Fukunaga T. Effects of isometric training on the elasticity of human tendon structures in vivo. J Appl Physiol. 2001;91:26–32.PubMed
38.
go back to reference Foure A, Nordez A, Cornu C. Effects of plyometric training on plantar flexor mechanical properties. Comput Methods Biomech Biomed Engin. 2010;13:57–9.CrossRef Foure A, Nordez A, Cornu C. Effects of plyometric training on plantar flexor mechanical properties. Comput Methods Biomech Biomed Engin. 2010;13:57–9.CrossRef
39.
go back to reference Houghton LA, Dawson BT, Rubenson J. Effects of plyometric training on Achilles tendon properties and shuttle running during a simulated cricket batting innings. J Strength Cond Res. 2013;27:1036–46.CrossRefPubMed Houghton LA, Dawson BT, Rubenson J. Effects of plyometric training on Achilles tendon properties and shuttle running during a simulated cricket batting innings. J Strength Cond Res. 2013;27:1036–46.CrossRefPubMed
40.
go back to reference Kubo K, Ohgo K, Takeishi R, Yoshinaga K, Tsunoda N, Kanehisa H. Effects of isometric training at different knee angles on the muscle-tendon complex in vivo. Scand J Med Sci Sports. 2006;16:159–67.CrossRefPubMed Kubo K, Ohgo K, Takeishi R, Yoshinaga K, Tsunoda N, Kanehisa H. Effects of isometric training at different knee angles on the muscle-tendon complex in vivo. Scand J Med Sci Sports. 2006;16:159–67.CrossRefPubMed
41.
go back to reference Malliaras P, Kamal B, Nowell A, Farley T, Dhamu H, Simpson V. Patellar tendon adaptation in relation to load-intensity and contraction type. J Biomech. 2013;46:1893–9.CrossRefPubMed Malliaras P, Kamal B, Nowell A, Farley T, Dhamu H, Simpson V. Patellar tendon adaptation in relation to load-intensity and contraction type. J Biomech. 2013;46:1893–9.CrossRefPubMed
42.
go back to reference Kubo K, Kanehisa H, Fukunaga T. Effects of different duration isometric contractions on tendon elasticity in human quadriceps muscles. J Physiol. 2001;536:649–55.CrossRefPubMedCentralPubMed Kubo K, Kanehisa H, Fukunaga T. Effects of different duration isometric contractions on tendon elasticity in human quadriceps muscles. J Physiol. 2001;536:649–55.CrossRefPubMedCentralPubMed
43.
go back to reference Foure A, Nordez A, Cornu C. Effects of eccentric training on mechanical properties of the plantar flexor muscle-tendon complex. J Appl Physiol. 2013;114:523–37.CrossRefPubMed Foure A, Nordez A, Cornu C. Effects of eccentric training on mechanical properties of the plantar flexor muscle-tendon complex. J Appl Physiol. 2013;114:523–37.CrossRefPubMed
44.
go back to reference Urlando A, Hawkins D. Achilles tendon adaptation during strength training in young adults. Med Sci Sports Exerc. 2007;39:1147–52.CrossRefPubMed Urlando A, Hawkins D. Achilles tendon adaptation during strength training in young adults. Med Sci Sports Exerc. 2007;39:1147–52.CrossRefPubMed
45.
go back to reference Ekizos A, Papatzika F, Charcharis G, Bohm S, Mersmann F, Arampatzis A. Ultrasound does not provide reliable results for the measurement of the patellar tendon cross sectional area. J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol. 2013;23:1278–82.CrossRef Ekizos A, Papatzika F, Charcharis G, Bohm S, Mersmann F, Arampatzis A. Ultrasound does not provide reliable results for the measurement of the patellar tendon cross sectional area. J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol. 2013;23:1278–82.CrossRef
46.
go back to reference Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.​cochrane-handbook.​org.
47.
go back to reference Deeks JJ, Higgins JPT, Altman DG (editors). Chapter 9: Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org. Deeks JJ, Higgins JPT, Altman DG (editors). Chapter 9: Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011. Available from www.​cochrane-handbook.​org.
48.
go back to reference Cooper H. Research synthesis and meta-analysis: a step-by-step approach. 4th ed. Thousand Oaks: Sage Publications, Inc; 2010. Cooper H. Research synthesis and meta-analysis: a step-by-step approach. 4th ed. Thousand Oaks: Sage Publications, Inc; 2010.
49.
go back to reference Deeks JJ, Altman DG, Bradburn MJ. Statistical methods for examining heterogeneity and combining results from several studies in meta-analysis. In: Egger M, Smith GD, Altman DG, editors. Systematic reviews in healthcare. BMJ Publishing Group; Chichester: UK, 2001. p. 285–312. Deeks JJ, Altman DG, Bradburn MJ. Statistical methods for examining heterogeneity and combining results from several studies in meta-analysis. In: Egger M, Smith GD, Altman DG, editors. Systematic reviews in healthcare. BMJ Publishing Group; Chichester: UK, 2001. p. 285–312.
51.
go back to reference The Cochrane Collaboration. Review Manager (RevMan). Copenhagen: The Nordic Cochrane Centre; 2012. The Cochrane Collaboration. Review Manager (RevMan). Copenhagen: The Nordic Cochrane Centre; 2012.
52.
go back to reference Kubo K, Tabata T, Ikebukuro T, Igarashi K, Tsunoda N. A longitudinal assessment of running economy and tendon properties in long-distance runners. J Strength Cond Res Natl Strength Cond Assoc. 2010;24:1724–31.CrossRef Kubo K, Tabata T, Ikebukuro T, Igarashi K, Tsunoda N. A longitudinal assessment of running economy and tendon properties in long-distance runners. J Strength Cond Res Natl Strength Cond Assoc. 2010;24:1724–31.CrossRef
53.
go back to reference Milgrom Y, Milgrom C, Altaras T, Globus O, Zeltzer E, Finestone AS. Achilles tendons hypertrophy in response to high loading training. Foot Ankle Int. 2014. doi:10.1177/1071100714550651. Milgrom Y, Milgrom C, Altaras T, Globus O, Zeltzer E, Finestone AS. Achilles tendons hypertrophy in response to high loading training. Foot Ankle Int. 2014. doi:10.1177/1071100714550651.
54.
go back to reference Bloomquist K, Langberg H, Karlsen S, Madsgaard S, Boesen M, Raastad T. Effect of range of motion in heavy load squatting on muscle and tendon adaptations. Eur J Appl Physiol. 2013;113:2133–42.CrossRefPubMed Bloomquist K, Langberg H, Karlsen S, Madsgaard S, Boesen M, Raastad T. Effect of range of motion in heavy load squatting on muscle and tendon adaptations. Eur J Appl Physiol. 2013;113:2133–42.CrossRefPubMed
55.
go back to reference Farup J, Rahbek SK, Vendelbo MH, Matzon A, Hindhede J, Bejder A. Whey protein hydrolysate augments tendon and muscle hypertrophy independent of resistance exercise contraction mode. Scand J Med Sci Sports. 2014;24:788–98.CrossRefPubMed Farup J, Rahbek SK, Vendelbo MH, Matzon A, Hindhede J, Bejder A. Whey protein hydrolysate augments tendon and muscle hypertrophy independent of resistance exercise contraction mode. Scand J Med Sci Sports. 2014;24:788–98.CrossRefPubMed
56.
go back to reference Foure A, Nordez A, Cornu C. Plyometric training effects on Achilles tendon stiffness and dissipative properties. J Appl Physiol. 2010;109:849–54.CrossRefPubMed Foure A, Nordez A, Cornu C. Plyometric training effects on Achilles tendon stiffness and dissipative properties. J Appl Physiol. 2010;109:849–54.CrossRefPubMed
57.
go back to reference Foure A, Nordez A, McNair P, Cornu C. Effects of plyometric training on both active and passive parts of the plantarflexors series elastic component stiffness of muscle-tendon complex. Eur J Appl Physiol. 2011;111:539–48.CrossRefPubMed Foure A, Nordez A, McNair P, Cornu C. Effects of plyometric training on both active and passive parts of the plantarflexors series elastic component stiffness of muscle-tendon complex. Eur J Appl Physiol. 2011;111:539–48.CrossRefPubMed
58.
go back to reference Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H. Effects of training on muscle and tendon in knee extensors and plantar flexors in vivo. J Appl Biomech. 2010;26:316–23.PubMed Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H. Effects of training on muscle and tendon in knee extensors and plantar flexors in vivo. J Appl Biomech. 2010;26:316–23.PubMed
59.
go back to reference Kubo K, Morimoto M, Komuro T, Yata H, Tsunoda N, Kanehisa H. Effects of plyometric and weight training on muscle-tendon complex and jump performance. Med Sci Sports Exerc. 2007;39:1801–10.CrossRefPubMed Kubo K, Morimoto M, Komuro T, Yata H, Tsunoda N, Kanehisa H. Effects of plyometric and weight training on muscle-tendon complex and jump performance. Med Sci Sports Exerc. 2007;39:1801–10.CrossRefPubMed
60.
go back to reference Kubo K, Ikebukuro T, Yaeshima K, Yata H, Tsunoda N, Kanehisa H. Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. J Appl Physiol (Bethesda Md: 1985). 2009;106:412–7.CrossRef Kubo K, Ikebukuro T, Yaeshima K, Yata H, Tsunoda N, Kanehisa H. Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. J Appl Physiol (Bethesda Md: 1985). 2009;106:412–7.CrossRef
61.
go back to reference Carroll CC, Dickinson JM, LeMoine JK, Haus JM, Weinheimer EM, Hollon CJ. Influence of acetaminophen and ibuprofen on in vivo patellar tendon adaptations to knee extensor resistance exercise in older adults. J Appl Physiol (Bethesda Md: 1985). 2011;111:508–15.CrossRefPubMedCentral Carroll CC, Dickinson JM, LeMoine JK, Haus JM, Weinheimer EM, Hollon CJ. Influence of acetaminophen and ibuprofen on in vivo patellar tendon adaptations to knee extensor resistance exercise in older adults. J Appl Physiol (Bethesda Md: 1985). 2011;111:508–15.CrossRefPubMedCentral
62.
go back to reference Hansen P, Aagaard P, Kjaer M, Larsson B, Magnusson SP. Effect of habitual running on human Achilles tendon load-deformation properties and cross-sectional area. J Appl Physiol. 2003;95:2375–80.CrossRefPubMed Hansen P, Aagaard P, Kjaer M, Larsson B, Magnusson SP. Effect of habitual running on human Achilles tendon load-deformation properties and cross-sectional area. J Appl Physiol. 2003;95:2375–80.CrossRefPubMed
63.
go back to reference 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;178:25–32.CrossRefPubMed 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;178:25–32.CrossRefPubMed
64.
go back to reference Cohen J. Statistical power analysis for the behavioral sciences. Psychology Press; Hillsdale, New Jersey: US, 1988. Cohen J. Statistical power analysis for the behavioral sciences. Psychology Press; Hillsdale, New Jersey: US, 1988.
65.
go back to reference Arnoczky SP, Tian T, Lavagnino M, Gardner K. Ex vivo static tensile loading inhibits MMP-1 expression in rat tail tendon cells through a cytoskeletally based mechanotransduction mechanism. J Orthop Res Off Publ Orthop Res Soc. 2004;22:328–33.CrossRef Arnoczky SP, Tian T, Lavagnino M, Gardner K. Ex vivo static tensile loading inhibits MMP-1 expression in rat tail tendon cells through a cytoskeletally based mechanotransduction mechanism. J Orthop Res Off Publ Orthop Res Soc. 2004;22:328–33.CrossRef
66.
go back to reference 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;44:181–7.CrossRefPubMed 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;44:181–7.CrossRefPubMed
67.
go back to reference Hansen KA, Weiss JA, Barton JK. Recruitment of tendon crimp with applied tensile strain. J Biomech Eng Trans Asme. 2002;124:72–7.CrossRef Hansen KA, Weiss JA, Barton JK. Recruitment of tendon crimp with applied tensile strain. J Biomech Eng Trans Asme. 2002;124:72–7.CrossRef
68.
go back to reference Schatzmann L, Brunner P, Stäubli HU. Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg Sports Traumatol Arthrosc Off J ESSKA. 1998;6 Suppl 1:S56–61.CrossRef Schatzmann L, Brunner P, Stäubli HU. Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg Sports Traumatol Arthrosc Off J ESSKA. 1998;6 Suppl 1:S56–61.CrossRef
69.
go back to reference Arnoczky SP, Tian T, Lavagnino M, Gardner K, Schuler P, Morse P. Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude, and cytosolic calcium. J Orthop Res Off Publ Orthop Res Soc. 2002;20:947–52.CrossRef Arnoczky SP, Tian T, Lavagnino M, Gardner K, Schuler P, Morse P. Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude, and cytosolic calcium. J Orthop Res Off Publ Orthop Res Soc. 2002;20:947–52.CrossRef
70.
go back to reference Lavagnino M, Arnoczky SP, Kepich E, Caballero O, Haut RC. A finite element model predicts the mechanotransduction response of tendon cells to cyclic tensile loading. Biomech Model Mechanobiol. 2008;7:405–16.CrossRefPubMed Lavagnino M, Arnoczky SP, Kepich E, Caballero O, Haut RC. A finite element model predicts the mechanotransduction response of tendon cells to cyclic tensile loading. Biomech Model Mechanobiol. 2008;7:405–16.CrossRefPubMed
71.
go back to reference Fouré A, Nordez A, Guette M, Cornu C. Effects of plyometric training on passive stiffness of gastrocnemii and the musculo-articular complex of the ankle joint. Scand J Med Sci Sports. 2009;19:811–8.CrossRefPubMed Fouré A, Nordez A, Guette M, Cornu C. Effects of plyometric training on passive stiffness of gastrocnemii and the musculo-articular complex of the ankle joint. Scand J Med Sci Sports. 2009;19:811–8.CrossRefPubMed
72.
go back to reference Kubo K, Ikebukuro T, Maki A, Yata H, Tsunoda N. Time course of changes in the human Achilles tendon properties and metabolism during training and detraining in vivo. Eur J Appl Physiol. 2012;112:2679–91.CrossRefPubMed Kubo K, Ikebukuro T, Maki A, Yata H, Tsunoda N. Time course of changes in the human Achilles tendon properties and metabolism during training and detraining in vivo. Eur J Appl Physiol. 2012;112:2679–91.CrossRefPubMed
73.
go back to reference Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H. Time course of changes in muscle and tendon properties during strength training and detraining. J Strength Cond Res. 2010;24:322–31.CrossRefPubMed Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H. Time course of changes in muscle and tendon properties during strength training and detraining. J Strength Cond Res. 2010;24:322–31.CrossRefPubMed
74.
go back to reference de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV. Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol. 2007;583:1079–91.CrossRefPubMedCentralPubMed de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV. Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol. 2007;583:1079–91.CrossRefPubMedCentralPubMed
75.
go back to reference Mersmann F, Bohm S, Schroll A, Boeth H, Duda G, Arampatzis A. Evidence of imbalanced adaptation between muscle and tendon in adolescent athletes. Scand J Med Sci Sports. 2014;24:e283–9.CrossRef Mersmann F, Bohm S, Schroll A, Boeth H, Duda G, Arampatzis A. Evidence of imbalanced adaptation between muscle and tendon in adolescent athletes. Scand J Med Sci Sports. 2014;24:e283–9.CrossRef
76.
go back to reference Couppé C, Svensson RB, Sødring-Elbrønd V, Hansen P, Kjaer M, Magnusson SP. Accuracy of MRI technique in measuring tendon cross-sectional area. Clin Physiol Funct Imaging. 2014;34:237–41.CrossRefPubMed Couppé C, Svensson RB, Sødring-Elbrønd V, Hansen P, Kjaer M, Magnusson SP. Accuracy of MRI technique in measuring tendon cross-sectional area. Clin Physiol Funct Imaging. 2014;34:237–41.CrossRefPubMed
77.
go back to reference Noble JA. Ultrasound image segmentation and tissue characterization. Proc Inst Mech Eng Part H-J Eng Med. 2010;224:307–16.CrossRef Noble JA. Ultrasound image segmentation and tissue characterization. Proc Inst Mech Eng Part H-J Eng Med. 2010;224:307–16.CrossRef
78.
go back to reference Van Schie HTM, de Vos RJ, de Jonge S, Bakker EM, Heijboer MP, Verhaar JA. Ultrasonographic tissue characterisation of human Achilles tendons: quantification of tendon structure through a novel non-invasive approach. Br J Sports Med. 2010;44:1153–9.CrossRefPubMed Van Schie HTM, de Vos RJ, de Jonge S, Bakker EM, Heijboer MP, Verhaar JA. Ultrasonographic tissue characterisation of human Achilles tendons: quantification of tendon structure through a novel non-invasive approach. Br J Sports Med. 2010;44:1153–9.CrossRefPubMed
79.
go back to reference Kongsgaard M, Nielsen CH, Hegnsvad S, Aagaard P, Magnusson SP. Mechanical properties of the human Achilles tendon, in vivo. Clin Biomech. 2011;26:772–7.CrossRef Kongsgaard M, Nielsen CH, Hegnsvad S, Aagaard P, Magnusson SP. Mechanical properties of the human Achilles tendon, in vivo. Clin Biomech. 2011;26:772–7.CrossRef
80.
go back to reference Arampatzis A, Morey-Klapsing G, Karamanidis K, DeMonte G, Stafilidis S, Brüggemann G-P. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech. 2005;38:885–92.CrossRefPubMed Arampatzis A, Morey-Klapsing G, Karamanidis K, DeMonte G, Stafilidis S, Brüggemann G-P. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech. 2005;38:885–92.CrossRefPubMed
81.
go back to reference Arampatzis A, Karamanidis K, De Monte G, Stafilidis S, Morey-Klapsing G, Brüggemann G-P. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomech (Bristol, Avon). 2004;19:277–83.CrossRef Arampatzis A, Karamanidis K, De Monte G, Stafilidis S, Morey-Klapsing G, Brüggemann G-P. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomech (Bristol, Avon). 2004;19:277–83.CrossRef
82.
go back to reference Arampatzis A, Stafilidis S, DeMonte G, Karamanidis K, Morey-Klapsing G, Brüggemann GP. Strain and elongation of the human gastrocnemius tendon and aponeurosis during maximal plantarflexion effort. J Biomech. 2005;38:833–41.CrossRefPubMed Arampatzis A, Stafilidis S, DeMonte G, Karamanidis K, Morey-Klapsing G, Brüggemann GP. Strain and elongation of the human gastrocnemius tendon and aponeurosis during maximal plantarflexion effort. J Biomech. 2005;38:833–41.CrossRefPubMed
83.
go back to reference Mademli L, Arampatzis A, Morey-Klapsing G, Brüggemann G-P. Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J Electromyogr Kinesiol. 2004;14:591–7.CrossRefPubMed Mademli L, Arampatzis A, Morey-Klapsing G, Brüggemann G-P. Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J Electromyogr Kinesiol. 2004;14:591–7.CrossRefPubMed
84.
go back to reference Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M. Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol. 2001;531:277–88.CrossRefPubMedCentralPubMed Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M. Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol. 2001;531:277–88.CrossRefPubMedCentralPubMed
85.
go back to reference Arampatzis A, Monte GD, Karamanidis K. Effect of joint rotation correction when measuring elongation of the gastrocnemius medialis tendon and aponeurosis. J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol. 2008;18:503–8.CrossRef Arampatzis A, Monte GD, Karamanidis K. Effect of joint rotation correction when measuring elongation of the gastrocnemius medialis tendon and aponeurosis. J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol. 2008;18:503–8.CrossRef
86.
go back to reference Schulze F, Mersmann F, Bohm S, Arampatzis A. A wide number of trials is required to achieve acceptable reliability for measurement patellar tendon elongation in vivo. Gait Posture. 2012;35:334–8.CrossRefPubMed Schulze F, Mersmann F, Bohm S, Arampatzis A. A wide number of trials is required to achieve acceptable reliability for measurement patellar tendon elongation in vivo. Gait Posture. 2012;35:334–8.CrossRefPubMed
87.
go back to reference Kubo K, Yata H, Kanehisa H, Fukunaga T. Effects of isometric squat training on the tendon stiffness and jump performance. Eur J Appl Physiol. 2006;96:305–14.CrossRefPubMed Kubo K, Yata H, Kanehisa H, Fukunaga T. Effects of isometric squat training on the tendon stiffness and jump performance. Eur J Appl Physiol. 2006;96:305–14.CrossRefPubMed
88.
go back to reference Kubo K, Komuro T, Ishiguro N, Tsunoda N, Sato Y, Ishii N. Effects of low-load resistance training with vascular occlusion on the mechanical properties of muscle and tendon. J Appl Biomech. 2006;22:112–9.PubMed Kubo K, Komuro T, Ishiguro N, Tsunoda N, Sato Y, Ishii N. Effects of low-load resistance training with vascular occlusion on the mechanical properties of muscle and tendon. J Appl Biomech. 2006;22:112–9.PubMed
Metadata
Title
Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults
Authors
Sebastian Bohm
Falk Mersmann
Adamantios Arampatzis
Publication date
01-12-2015
Publisher
Springer International Publishing
Published in
Sports Medicine - Open / Issue 1/2015
Print ISSN: 2199-1170
Electronic ISSN: 2198-9761
DOI
https://doi.org/10.1186/s40798-015-0009-9

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