Skip to main content
SpringerLink
Log in

Aging and the effects of a half marathon on Achilles tendon force–elongation relationship

European Journal of Applied Physiology volume 116, pages 2281–2292 (2016)Cite this article

Abstract

Purpose

We aimed to determine whether there are different changes in Achilles tendon (AT) mechanical properties in middle-aged, compared to younger runners that might indicate that tendon fatigue, induced by long-distance running, is age-dependent.

Methods

27 middle-aged (50–67 years) and 22 younger (21–29 years) participants ran a 21 km route at their own pace (mean and SD: old: 3.1 ± 0.3 m s−1; young: 3.6 ± 0.5 m s−1). We tested for changes in the AT force–elongation relationship using dynamometry and ultrasonography during isometric voluntary ankle plantarflexion ramp contractions, conducted 20–28 h pre-run, immediately pre-run, immediately post-run and 20–28 h post-run. Stride frequency and number were examined to estimate cyclic tensile loading characteristics of the tendon during running.

Results

Muscle strength decreased significantly (P < 0.05) in both groups immediately post-run (old: 17 %; young: 11 %) and recovered to baseline within 20–28 h post-run. AT stiffness did not change for the younger adults, whereas the middle-aged adults showed a significant (P < 0.05) decrease in AT stiffness (22 %). However, tendon stiffness recovered to baseline 20–28 h post-run. Middle-aged, compared to young adults, demonstrated significantly (P < 0.05) greater stride frequency and number, but no correlations with tendon fatigue changes were determined (R 2 ≤ 0.038).

Conclusions

The results suggest that the plasticity of the AT in response to short-term mechanical loading may be age dependent and that the AT length–tension properties of middle-aged runners may be more vulnerable to change following running compared to younger athletes. However, the observed AT changes in the middle-aged runners dissipated within 20–28 h post-run, suggesting that a tendon viscoelastic recovery mechanism may occur in vivo.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

1dayPre-Run:

20–28 h before the run

1dayPost-Run:

Within 20–28 h after the run

AT:

Achilles tendon

ANOVA:

Analysis of variance

CSA:

Cross-sectional area

GM:

Gastrocnemius medialis

imPre-Run:

Immediately before the run

imPost-Run:

Immediately after the run

MTU:

Muscle–tendon unit

MVC:

Maximal voluntary plantarflexion ramp contraction

SD:

Standard deviation

References

  • Arampatzis A, Stafilidis S, DeMonte G, Karamanidis K, Morey-Klapsing G, Brüggemann GP (2005) Strain and elongation of the human gastrocnemius tendon and aponeurosis during maximal plantarflexion effort. J Biomech 38:833–841

    Article  CAS  PubMed  Google Scholar 

  • Arampatzis A, Karamanidis K, Stafilidis S, Morey-Klapsing G, DeMonte G, Brüggemann GP (2006) Effect of different ankle-and knee-joint positions on gastrocnemius medialis fascicle length and EMG activity during isometric plantar flexion. J Biomech 39:1891–1902

    Article  PubMed  Google Scholar 

  • Beaumont PWR (1989) The failure of fibre composites: an overview. J Strain Anal Eng 24:189–205

    Article  Google Scholar 

  • Biewener AA, Roberts TJ (2000) Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc Sport Sci Rev 28:99–107

    CAS  PubMed  Google Scholar 

  • Bjornsson HC, Norlin R, Johansson K, Adolfsson LE (2011) The influence of age, delay of repair, and tendon involvement in acute rotator cuff tears: structural and clinical outcomes after repair of 42 shoulders. Acta Orthop 82:187–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Brunet ME, Cook SD, Brinker MR, Dickinson JA (1990) A survey of running injuries in 1505 competitive and recreational runners. J Sport Med Phys Fit 30:307–315

    CAS  Google Scholar 

  • Clement DB, Taunton JE, Smart GW (1984) Achilles tendinitis and peritendinitis: etiology and treatment. Am J Sport Med 12:179–184

    Article  CAS  Google Scholar 

  • Dahners LE, Banes AJ, Burridge KW (1986) The relationship of actin to ligament contraction. Clin Orthop Relat Res 210:246–251

    CAS  Google Scholar 

  • Farris DJ, Trewartha G, McGuigan MP (2012) The effects of a 30-min run on the mechanics of the human Achilles tendon. Eur J Appl Physiol 112:653–660

    Article  PubMed  Google Scholar 

  • Farris DJ, Trewartha G, McGuigan MP, Lichtwark GA (2013) Differential strain patterns of the human Achilles tendon determined in vivo with freehand three-dimensional ultrasound imaging. J Exp Biol 216:594–600

    Article  PubMed  Google Scholar 

  • Fung DT, Wang VM, Andarawis-Puri N et al (2010) Early response to tendon fatigue damage accumulation in a novel in vivo model. J Biomech 43:274–279

    Article  PubMed  Google Scholar 

  • Gardner K, Lavagnino M, Egerbacher M, Arnoczky SP (2012) Reestablishment of cytoskeletal tensional homeostasis in lax tendons occurs through an actin mediated cellular contraction of the extracellular matrix. J Orthop Res 30:1695–1701

    Article  CAS  PubMed  Google Scholar 

  • Huttunen TT, Kannus P, Rolf C, Felländer-Tsai L, Mattila VM (2014) Acute achilles tendon ruptures incidence of injury and surgery in Sweden between 2001 and 2012. Am J Sports Med 42:2419–2423

    Article  Google Scholar 

  • Jozsa L, Kvist M, Bálint BJ et al (1989) The role of recreational sport activity in Achilles tendon rupture. A clinical, pathoanatomical, and sociological study of 292 cases. Am J Sports Med 17:338–343

    Article  CAS  PubMed  Google Scholar 

  • Karamanidis K, Arampatzis A (2005) Mechanical and morphological properties of different muscle–tendon units in the lower extremity and running mechanics: effect of aging and physical activity. J Exp Biol 208:3907–3923

    Article  PubMed  Google Scholar 

  • Karamanidis K, Stafilidis S, DeMonte G, Morey-Klapsing G, Brüggemann GP, Arampatzis A (2005) Inevitable joint angular rotation affects muscle architecture during isometric contraction. J Electromyogr Kines 15:608–616

    Article  Google Scholar 

  • Kaux JF, Forthomme B, Le Goff C, Crieland JM, Croisier JL (2011) Current opinions on tendinopathy. J Sports Sci Med 10:238–253

    PubMed  PubMed Central  Google Scholar 

  • Ker RF, Bennett MB, Bibby SR, Kester RC, Alexander RM (1987) The spring in the arch of the human foot. Nature 325:147–149

    Article  CAS  PubMed  Google Scholar 

  • Ker RF, Wang XT, Pike AV (2000) Fatigue quality of mammalian tendons. J Exp Biol 203:1317–1327

    CAS  PubMed  Google Scholar 

  • Kvist M (1994) Achilles tendon injuries in athletes. Sports Med 18:173–201

    Article  CAS  PubMed  Google Scholar 

  • Lavagnino M, Gardner K, Arnoczky SP (2013) Age-related changes in the cellular, mechanical, and contractile properties of rat tail tendons. Connect Tissue Res 54:70–75

    Article  PubMed  Google Scholar 

  • Lavagnino M, Bedi A, Walsh CP, Enselman ERS, Sheibani-Rad S, Arnoczky SP (2014) Tendon contraction after cyclic elongation is an age-dependent phenomenon in vitro and in vivo comparisons. Am J Sport Med 42:1471–1477

    Article  Google Scholar 

  • Lichtwark GA, Bougoulias K, Wilson AM (2007) Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J Biomech 40:157–164

    Article  CAS  PubMed  Google Scholar 

  • Lichtwark GA, Cresswell AG, Newsham-West RJ (2013) Effects of running on human Achilles tendon length–tension properties in the free and gastrocnemius components. J Exp Biol 216:4388–4394

    Article  PubMed  Google Scholar 

  • Mademli L, Arampatzis A (2008) Mechanical and morphological properties of the triceps surae muscle–tendon unit in old and young adults and their interaction with a submaximal fatiguing contraction. J Electromyogr Kines 18:89–98

    Article  Google Scholar 

  • Mademli L, Arampatzis A, Walsh M (2006) Effect of muscle fatigue on the compliance of the gastrocnemius medialis tendon and aponeurosis. J Biomech 39:426–434

    Article  PubMed  Google Scholar 

  • Maganaris CN (2003) Tendon conditioning: artefact or property? Proc Biol Sci 270(Suppl 1):S39–S42

    Article  PubMed  PubMed Central  Google Scholar 

  • Maganaris CN, Baltzopoulos V, Sargeant AJ (1998) Changes in Achilles tendon moment arm from rest to maximum isometric plantarflexion: in vivo observations in man. J Physiol 510:977–985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCamley J, Donati M, Grimpampi E, Mazza C (2012) An enhanced estimate of initial contact and final contact instants of time using lower trunk inertial sensor data. Gait Posture 36:316–318

    Article  PubMed  Google Scholar 

  • Noyes FR, Grood ES (1976) The strength of the anterior cruciate ligament in humans and Rhesus monkeys. J Bone Joint Surg 58:1074–1082

    Article  CAS  PubMed  Google Scholar 

  • Obst SJ, Newsham-West R, Barrett RS (2016) Changes in Achilles tendon mechanical properties following eccentric heel drop exercise are specific to the free tendon. Scand J Med Sci Spor 26:421–431

    Article  CAS  Google Scholar 

  • Peltonen J, Cronin NJ, Avela J, Finni T (2010) In vivo mechanical response of human Achilles tendon to a single bout of hopping exercise. J Exp Biol 213:1259–1265

    Article  PubMed  Google Scholar 

  • Peltonen J, Cronin NJ, Stenroth L, Finni T, Avela J (2012) Achilles tendon stiffness is unchanged 1 h after a marathon. J Exp Biol 215:3665–3671

    Article  PubMed  Google Scholar 

  • Reeves ND, Maganaris CN, Ferretti G, Narici MV (2005) Influence of 90-day simulated microgravity on human tendon mechanical properties and the effect of resistive countermeasures. J Appl Physiol 98:2278–2286

    Article  CAS  PubMed  Google Scholar 

  • Stenroth L, Peltonen J, Cronin NJ, Sipilä S, Finni T (2012) Age-related differences in Achilles tendon properties and triceps surae muscle architecture in vivo. J Appl Physiol 113:1537–1544

    Article  PubMed  Google Scholar 

  • Tkaczuk H (1968) Tensile properties of human lumbar longitudinal ligaments. Acta Orthop Scand 39(sup115):1–69

    Article  Google Scholar 

  • Viidik A (1982) Age-related changes in connective tissues. In: Viidik A (ed) Lectures on gerontology. Academic Press, London, pp 173–211

    Google Scholar 

  • Wang XT, Ker RF, Alexander RM (1995) Fatigue rupture of wallaby tail tendons. J Exp Biol 198:847–852

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The Bundesinstitut für Sportwissenschaft (BISp), the Olympiastützpunkt Rheinland and the Forschungsservicestelle of the German Sport University Cologne (Hochschulinterne Forschungsförderung) provided the funding for this study. In addition, we would like to thank Dr. Falk Schade for his support throughout this research project.

Author information

Authors and Affiliations

  1. Institute of Movement and Sport Gerontology, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933, Cologne, Germany

    Thijs Maria Anne Ackermans, Gaspar Epro, Christopher McCrum & Kiros Karamanidis

  2. Department of Human Movement Science, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University Medical Centre+, Universiteitssingel 60, 6229 ER, Maastricht, The Netherlands

    Thijs Maria Anne Ackermans, Christopher McCrum, Maarten Robert Drost & Kenneth Meijer

  3. Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933, Cologne, Germany

    Gaspar Epro

  4. Fresenius University of Applied Sciences, Media School, Im Mediapark 4C, 50670, Cologne, Germany

    Kai Daniel Oberländer

  5. Department of Molecular and Cellular Sport Medicine, Institute of Cardiovascular Research and Sport Medicine, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933, Cologne, Germany

    Frank Suhr

Authors
  1. Thijs Maria Anne Ackermans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gaspar Epro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher McCrum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kai Daniel Oberländer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Frank Suhr
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maarten Robert Drost
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kenneth Meijer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kiros Karamanidis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kiros Karamanidis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Olivier Seynnes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 146 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ackermans, T.M.A., Epro, G., McCrum, C. et al. Aging and the effects of a half marathon on Achilles tendon force–elongation relationship. Eur J Appl Physiol 116, 2281–2292 (2016). https://doi.org/10.1007/s00421-016-3482-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-016-3482-z

Keywords

search

Navigation