Time course of changes in the human Achilles tendon properties and metabolism during training and detraining in vivo

Abstract

The purpose of this study was to investigate the time course of changes in human tendon properties and metabolism during resistance training and detraining. Nine men (21–27 years) completed 3 months of isometric plantar flexion training and another 3 months of detraining. At the beginning and on every 1 month of training and detraining periods, the stiffness, blood circulation (blood volume and oxygen saturation), serum procollagen type 1 C-peptide (P1P; reflects synthesis of type 1 collagen), echointensity (reflects collagen content), and MRI signal intensity (reflects collagen structure) of the Achilles tendon were measured. Tendon stiffness did not change until 2 months of training, and the increase (50.3%) reached statistical significance at the end of the training period. After 1 month of detraining, tendon stiffness had already decreased to pre-training level. Blood circulation in the tendon did not change during the experimental period. P1P increased significantly after 2 months of training. Echointensity increased significantly by 9.1% after 2 months of training, and remained high throughout the experiment. MRI signal intensity increased by 24.2% after 2 months and by 21.4% after 3 months of training, but decreased to the pre-training level during the detraining period. These results suggested that the collagen synthesis, content, and structure of human tendons changed at the 2-month point of training period. During detraining, the sudden decrease in tendon stiffness might be related to changes in the structure of collagen fibers within the tendon.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Arampatzis A, Karamanidis K, Albracht K (2007) Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. J Exp Biol 210:2743–2753

    PubMed  Article  Google Scholar 

  2. Boushel R, Langberg H, Green S, Skovgaard D, Bulow J, Kjaer M (2000) Blood flow and oxygenation in peritendinous tissue and calf muscle during dynamic exercise in humans. J Physiol 524:305–313

    PubMed  Article  CAS  Google Scholar 

  3. Burgess KE, Connick MJ, Graham-Smith P, Pearson SJ (2007) Plyometric vs. isometric training influences on tendon properties and muscle output. J Strength Cond Res 21:986–989

    PubMed  Google Scholar 

  4. Carroll CC, Dickinson JM, Haus JM, Lee GA, Hollon CJ, Aagaard P, Magnusson SP, Trappe TA (2008) Influence of aging on the in vivo properties of human patellar tendon. J Appl Physiol 105:1907–1915

    PubMed  Article  CAS  Google Scholar 

  5. Carroll CC, Dickinson JM, LeMoine JK, Haus JM, Weinheimer EM, Hollon CJ, Aagaard P, Magnusson SP, Trappe TA (2011) Influence of acetaminophen and ibuprofen on in vivo patellar tendon adaptations to knee extensor resistance exercise in older adults. J Appl Physiol (in press)

  6. de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV (2007) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079–1091

    PubMed  Article  Google Scholar 

  7. Du J, Pak BC, Znamirowski R, Statum S, Takahashi A, Chung C, Bydder GM (2009) Magic angle effect in magnetic resonance imaging of the Achilles tendon and enthesis. Mag Reson Imag 27:557–564

    Article  Google Scholar 

  8. Erickson SJ, Prost RW, Timins ME (1993) The “magic angle” effect: background physics and clinical relevance. Radiology 188:23–25

    PubMed  CAS  Google Scholar 

  9. Greive DW, Pheasant S, Cavagna, PR (1978) Prediction of gastrocnemius length from knee and ankle joint posture. In: Asmussen E, Jorgensen K (eds) Biomechanics VI-A, International series in biomechanics. University Park Press, Baltimore, pp 405–412

  10. Garnero P, Delmas PD (1993) Assessment of the serum levels of bone alkaline phosphatase with a new immunoradiometric assay in patients with metabolic bone disease. J Clil Endocrinol Met 77:1046–1053

    Article  CAS  Google Scholar 

  11. Jackson BF, Smith RKW, Price JS (2003) A molecular markers of type 1 collagen metabolism reflects changes in connective tissue remodeling associated with injury to the equine superficial digital flexor tendon. Equine Ver J 35:211–213

    Article  CAS  Google Scholar 

  12. Kashima S (2003) Spectroscopic measurement of blood volume and its oxygenation in a small volume of tissue using red laser lights and differential calculation between two point detections. Optics Laser Technol 35:485–489

    Article  CAS  Google Scholar 

  13. Klein MB, Pham H, Yalamanchi N, Chang J (2001) Flexor tendon wound healing in vitro: the effects of lactate on tendon cell proliferation and collagen production. J Hand Surg 26:847–854

    Article  CAS  Google Scholar 

  14. Kongsgaard M, Kovanen V, Aagaard P, Doessing S, Hansen P, Laursen AH, Kaldau NC, Kjaer M, Magnusson SP (2009) Corticosteroid injections, eccentric decline squat training and heavy slow resistance training in patellar tendinopathy. Scand J Med Sci Sports 19:790–802

    PubMed  Article  CAS  Google Scholar 

  15. Kubo K, Kawakami Y, Fukunaga T (1999) Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87:2090–2096

    PubMed  CAS  Google Scholar 

  16. Kubo K, Kanehisa H, Fukunaga T (2002) Effects of resistance and stretching training programs on the viscoelastic properties of tendon structures in vivo. J Physiol 538:219–226

    PubMed  Article  CAS  Google Scholar 

  17. Kubo K, Akima H, Ushiyama J, Tabata I, Fukuoka H, Kanehisa H, Fukunaga T (2004) Effects of resistance training during bed rest on the viscoelastic properties of tendon structures in lower limb. Scand J Med Sci Sports 14:296–302

    PubMed  Article  Google Scholar 

  18. Kubo K, Morimoto M, Komuro T, Yata H, Tsunoda N, Kanehisa H, Fukunaga T (2007) Effects of plyometric and weight training on muscle-tendon complex and jump performance. Med Sci Sports Exer 39:1801–1810

    Article  Google Scholar 

  19. Kubo K, Ikebukuro T, Tsunoda N, Kanehisa H (2008a) Changes in oxygen consumption of human muscle and tendon following repeat muscle contractions. Eur J Appl Physiol 104:859–866

    PubMed  Article  CAS  Google Scholar 

  20. Kubo K, Ikebukuro T, Tsunoda N, Kanehisa H (2008b) Noninvasive measures of blood volume and oxygen saturation of human Achilles tendon by red laser lights. Acta Physiol 193:257–264

    Article  CAS  Google Scholar 

  21. Kubo K, Ikebukuro T, Yaeshima K, Kanehisa H (2009a) Effects of different duration contractions on elasticity, blood volume, and oxygen saturation of human tendon in vivo. Eur J Appl Physiol 106:445–455

    PubMed  Article  CAS  Google Scholar 

  22. Kubo K, Ikebukuro T, Yaeshima K, Yata H, Tsunoda N, Kanehisa H (2009b) Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. J Appl Physiol 106:412–417

    PubMed  Article  Google Scholar 

  23. Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H (2010) Time course of changes in muscle and tendon properties during strength training and detraining. J Strength Cond Res 24:322–331

    PubMed  Article  Google Scholar 

  24. Kubo K, Yuki K, Ikebukuro T (2011) Changes in bone alkaline phosphatase and procollagen type-1 C-peptide after static and dynamic exercises. Res Quart Exer Sport (in press)

  25. Langberg H, Skovgaard D, Karamouzis M, Bulow J, Kjaer M (1999) Metabolism and inflammatory mediators in the peritendinous space measured by microdialysis during intermittent isometric exercise in humans. J Physiol 515:919–927

    PubMed  Article  CAS  Google Scholar 

  26. Langberg H, Skovgaard D, Asp S, Kjaer M (2000) Time pattern of exercise-induced changes in type 1 collagen turnover after prolonged endurance exercise in humans. Calcif Tissue Int 67:41–44

    Google Scholar 

  27. Langberg H, Rosendal L, Kjaer M (2001) Training-induced changes in peritendinous type 1 collagen turnover determined by microdialysis in humans. J Physiol 534:297–302

    PubMed  Article  CAS  Google Scholar 

  28. Magnusson SP, Aagaard P, Rosager S, Poulsen PD, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531:277–288

    PubMed  Article  CAS  Google Scholar 

  29. Maimoun L, Manetta J, Couret I, Dupuy AM, Mariano-Goulart D, Micallef JP, Peruchon E, Rossi M (2006) The intensity level of physical exercise and the bone metabolism response. Int J Sports Med 27:105–111

    PubMed  Article  CAS  Google Scholar 

  30. Miller BF, Olesen JL, Hansen M, Dossing S, Crameri RM, Welling RJ, Langeberg H, Flyvbjerg A, Kjaer M, Babraj JA, Smith K, Rennie MJ (2005) Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol 567:1021–1033

    PubMed  Article  CAS  Google Scholar 

  31. Nagy A, Dyson S (2011) Anatomical, magnetic resonance imaging and histological findings in the accessory ligament of the deep digital flexor tendon of forelimbs in nonlame horses. Equine Ver J 43:309–316

    Article  CAS  Google Scholar 

  32. Nieminen MT, Rieppo J, Toyras J, Hakumaki JM, Silvennoinen J, Hyttinen MM, Helminen HJ, Jurvelin JS (2001) T2 relaxation reveals spatial collagen architecture in articular cartilage: a comparative quantitative MRI and polarized light microscopic study. Mag Reson Med 46:487–493

    Article  CAS  Google Scholar 

  33. Nosaka K, Clarkson PM (1996) Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exer 28:953–961

    Article  CAS  Google Scholar 

  34. Reimers CD, Fleckenstein JL, Witt TN, Muller-Felber W, Pongratz DE (1993a) Muscular ultrasound in idiopathic inflammatory myopathies of adults. J Neurol Sci 116:82–92

    PubMed  Article  CAS  Google Scholar 

  35. Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE (1993b) Skeletal muscle sonography. A correlative study of echogenicity and morphology. J Ultrasound Med 12:73–77

    PubMed  CAS  Google Scholar 

  36. Risteli L, Risteli J (1993) Biochemical markers of bone metabolism. Ann Med 25:385–393

    PubMed  Article  CAS  Google Scholar 

  37. Shalabi A, Kristoffersen-Wiberg M, Papadogiannakis N, Aspelin P, Movin T (2002) Dynamic contrast-enhanced MR imaging and histopathology in chronic Achilles tendinosis. A longitudinal MR study of 15 patients. Acta Radiol 43:198–206

    PubMed  CAS  Google Scholar 

  38. Soyama N, Kuratsu J, Ushio Y (1995) Correlation between magnetic resonance images and histology in meningiomas: T2-weighted images indicate collagen contents in tissue. Neurol Med Chir 35:438–441

    Article  CAS  Google Scholar 

  39. van Holsbeeck M, Introcaso JH (1992) Musculoskeletal ultrasonography. Radiol Clin Am 30:907–925

    Google Scholar 

  40. Virtanen P, Viitasalo JT, Vuori J, Vaananen K, Takala TES (1993) Effect of concentric exercise on serum muscle and collagen markers. J Appl Physiol 75:1272–1277

    PubMed  CAS  Google Scholar 

  41. Yalamanchi N, Klein MB, Pham HM, Longaker MT, Chang J (2004) Flexor tendon wound healing in vitro: lactate up-regulation of TGF-ß expression and functional activity. Plastic Reconstr Surg 113:625–632

    Article  Google Scholar 

  42. Yoon JH, Halper J (2005) Tendon proteoglycans: biochemistry and function. J Musculoskelet Neuronal Interact 5:22–34

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a Grant-in-Aid for Young Scientists (A) (21680047 to K. Kubo) from Japan Society for the Promotion of Science and Yamaha Motor Foundation for Sports. The authors thank the staff of Kouikai Clinic for their technical assistance with MRI measurements. The authors also thank Mr. Yuki K and Mr. Sato H (Kishimoto Clinical Laboratory Group) for their conscientious work on the analyses of serum biochemical markers.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Keitaro Kubo.

Additional information

Communicated by Toshio Moritani.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kubo, K., Ikebukuro, T., Maki, A. et al. Time course of changes in the human Achilles tendon properties and metabolism during training and detraining in vivo. Eur J Appl Physiol 112, 2679–2691 (2012). https://doi.org/10.1007/s00421-011-2248-x

Download citation

Keywords

  • Plantar flexor
  • Tendon stiffness
  • Collagen synthesis
  • Structure