Skip to main content
SpringerLink
Log in

Ruptured human Achilles tendon has elevated metabolic activity up to 1 year after repair

  • Original Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

Following Achilles tendon rupture, running is often allowed after 6 months. However, tendon healing is slow and the metabolic status of the tendon at this point is unknown. The purpose of this study was to investigate tendon metabolism (glucose uptake) and vascularization at 3, 6 and 12 months after Achilles tendon rupture as measured using PET and power Doppler ultrasonography (PDUS).

Methods

The study group comprised 23 patients with surgically repaired Achilles tendon rupture who were investigated at 3 months (n = 7), 6 months (n = 7) and 12 months (n = 9) after surgery. The triceps surae complex was loaded over 20 min of slow treadmill walking while a radioactive tracer (18F-FDG) was administered prior to PET. Vascularization was measured in terms of PDUS flow activity, and patient-reported outcomes were scored using the Achilles tendon rupture score (ATRS) and sports assessment (VISA-A) questionnaire.

Results

Relative glucose uptake (18F-FDG) was higher in repaired tendons than in intact tendons at all time-points (6, 3 and 1.6 times higher at 3, 6 and 12 months, respectively; P ≤ 0.001), and was also higher in the tendon core than in the periphery at 3 and 6 months (P ≤ 0.02), but lower at 12 months (P = 0.06). Relative glucose uptake was negatively related to ATRS at 6 months after repair (r = −0.89, P ≤ 0.01). PDUS flow activity was higher in repaired tendons than in intact tendons at 3 and 6 months (P < 0.05 for both), but had normalized by 12 months.

Conclusion

These data demonstrate that the healing process as determined by metabolic activity and vascularization continues for 6 months after injury when large loads are typically allowed on the tendon. Indeed, metabolic activity remained elevated for more than 1 year after injury despite normalized vascularization. The robust negative correlation between tendon metabolism and patient-reported outcome suggests that a high metabolic activity 6 months after the injury may be related to a poor clinical healing outcome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Mortensen HM, Skov O, Jensen PE. Early motion of the ankle after operative treatment of a rupture of the Achilles tendon. A prospective, randomized clinical and radiographic study. J Bone Joint Surg Am. 1999;81:983–90.

    CAS  PubMed  Google Scholar 

  2. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact. 2006;6:181–90.

    CAS  PubMed  Google Scholar 

  3. Maffulli N, Tallon C, Wong J, Lim KP, Bleakney R. Early weightbearing and ankle mobilization after open repair of acute midsubstance tears of the Achilles tendon. Am J Sports Med. 2003;31:692–700.

    PubMed  Google Scholar 

  4. Hutchison AM, Topliss C, Beard D, Evans RM, Williams P. The treatment of a rupture of the Achilles tendon using a dedicated management programme. Bone Joint J. 2015;97-B:510–5. doi:10.1302/0301-620X.97B4.35314.

    Article  CAS  PubMed  Google Scholar 

  5. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc. 2001;9:233–8.

    Article  CAS  PubMed  Google Scholar 

  6. Teefey SA, Middleton WD, Bauer GS, Hildebolt CF, Yamaguchi K. Sonographic differences in the appearance of acute and chronic full-thickness rotator cuff tears. J Ultrasound Med. 2000;19:377–8. quiz 83.

    CAS  PubMed  Google Scholar 

  7. Karjalainen PT, Ahovuo J, Pihlajamaki HK, Soila K, Aronen HJ. Postoperative MR imaging and ultrasonography of surgically repaired Achilles tendon ruptures. Acta Radiol. 1996;37:639–46.

    Article  CAS  PubMed  Google Scholar 

  8. Moller M, Kalebo P, Tidebrant G, Movin T, Karlsson J. The ultrasonographic appearance of the ruptured Achilles tendon during healing: a longitudinal evaluation of surgical and nonsurgical treatment, with comparisons to MRI appearance. Knee Surg Sports Traumatol Arthrosc. 2002;10:49–56. doi:10.1007/s001670100245.

    Article  PubMed  Google Scholar 

  9. Rominger MB, Bachmann G, Schulte S, Zedler A. Value of ultrasound and magnetic resonance imaging in the control of the postoperative progress after Achilles tendon rupture. Rofo. 1998;168:27–35. doi:10.1055/s-2007-1015178.

    Article  CAS  PubMed  Google Scholar 

  10. Rubin JM, Bude RO, Carson PL, Bree RL, Adler RS. Power Doppler US: a potentially useful alternative to mean frequency-based color Doppler US. Radiology. 1994;190:853–6. doi:10.1148/radiology.190.3.8115639.

    Article  CAS  PubMed  Google Scholar 

  11. Fealy S, Adler RS, Drakos MC, Kelly AM, Allen AA, Cordasco FA, et al. Patterns of vascular and anatomical response after rotator cuff repair. Am J Sports Med. 2006;34:120–7. doi:10.1177/0363546505280212.

    Article  PubMed  Google Scholar 

  12. Mittra E, Quon A. Positron emission tomography/computed tomography: the current technology and applications. Radiol Clin N Am. 2009;47:147–60. doi:10.1016/j.rcl.2008.10.005.

    Article  PubMed  Google Scholar 

  13. Hannukainen J, Kalliokoski KK, Nuutila P, Fujimoto T, Kemppainen J, Viljanen T, et al. In vivo measurements of glucose uptake in human Achilles tendon during different exercise intensities. Int J Sports Med. 2005;26:727–31. doi:10.1055/s-2005-837458.

    Article  CAS  PubMed  Google Scholar 

  14. Kalliokoski KK, Bojsen-Moller J, Seppanen M, Johansson J, Kjaer M, Teras M, et al. Contraction-induced [18F]-fluoro-deoxy-glucose uptake can be measured in human calf muscle using high-resolution PET. Clin Physiol Funct Imaging. 2007;27:239–41. doi:10.1111/j.1475-097X.2007.00744.x.

    Article  PubMed  Google Scholar 

  15. Bojsen-Moller J, Kalliokoski KK, Seppanen M, Kjaer M, Magnusson SP. Low-intensity tensile loading increases intratendinous glucose uptake in the Achilles tendon. J Appl Physiol. 2006;101:196–201. doi:10.1152/japplphysiol.00004.2006.

    Article  CAS  PubMed  Google Scholar 

  16. Boellaard R, O’Doherty MJ, Weber WA, Mottaghy FM, Lonsdale MN, Stroobants SG, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37:181–200. doi:10.1007/s00259-009-1297-4.

    Article  PubMed  Google Scholar 

  17. Karjalainen PT, Aronen HJ, Pihlajamaki HK, Soila K, Paavonen T, Bostman OM. Magnetic resonance imaging during healing of surgically repaired Achilles tendon ruptures. Am J Sports Med. 1997;25:164–71.

    Article  CAS  PubMed  Google Scholar 

  18. Rupp S, Tempelhof S, Fritsch E. Ultrasound of the Achilles tendon after surgical repair: morphology and function. Br J Radiol. 1995;68:454–8. doi:10.1259/0007-1285-68-809-454.

    Article  CAS  PubMed  Google Scholar 

  19. Schepull T, Aspenberg P. Early controlled tension improves the material properties of healing human Achilles tendons after ruptures: a randomized trial. Am J Sports Med. 2013;41:2550–7. doi:10.1177/0363546513501785.

    Article  PubMed  Google Scholar 

  20. Schepull T, Aspenberg P. Healing of human Achilles tendon ruptures: radiodensity reflects mechanical properties. Knee Surg Sports Traumatol Arthrosc. 2015;23:884–9. doi:10.1007/s00167-013-2720-8.

    Article  PubMed  Google Scholar 

  21. Sasaki K, Yamamoto N, Kiyosawa T, Sekido M. The role of collagen arrangement change during tendon healing demonstrated by scanning electron microscopy. J Electron Microsc. 2012;61:327–34. doi:10.1093/jmicro/dfs057.

    Article  Google Scholar 

  22. Gumucio JP, Phan AC, Ruehlmann DG, Noah AC, Mendias CL. Synergist ablation induces rapid tendon growth through the synthesis of a neotendon matrix. J Appl Physiol. 2014;117:1287–91. doi:10.1152/japplphysiol.00720.2014.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S. Muscle synergism during isometric plantarflexion in Achilles tendon rupture patients and in normal subjects revealed by velocity-encoded cine phase-contrast MRI. Clin Biomech. 2006;21:67–74. doi:10.1016/j.clinbiomech.2005.08.007.

    Article  Google Scholar 

  24. Suydam SM, Buchanan TS, Manal K, Silbernagel KG. Compensatory muscle activation caused by tendon lengthening post-Achilles tendon rupture. Knee Surg Sports Traumatol Arthrosc. 2015;23:868–74. doi:10.1007/s00167-013-2512-1.

    Article  PubMed  Google Scholar 

  25. Weinberg EP, Adams MJ, Hollenberg GM. Color Doppler sonography of patellar tendinosis. AJR Am J Roentgenol. 1998;171:743–4. doi:10.2214/ajr.171.3.9725308.

    Article  CAS  PubMed  Google Scholar 

  26. Gisslen K, Alfredson H. Neovascularisation and pain in jumper’s knee: a prospective clinical and sonographic study in elite junior volleyball players. Br J Sports Med. 2005;39:423–8. doi:10.1136/bjsm.2004.013342. discussion 423−8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Peltoniemi P, Lonnroth P, Laine H, Oikonen V, Tolvanen T, Gronroos T, et al. Lumped constant for [(18)F] fluorodeoxyglucose in skeletal muscles of obese and nonobese humans. Am J Physiol Endocrinol Metab. 2000;279:E1122–30.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank specialist technologist Eva Brødsgaard for excellent help with the PET procedures.

Author information

Author notes

    Authors and Affiliations

    1. Institute of Sports Medicine Copenhagen, Department of Ortopaedic Surgery, Bispebjerg Hospital, University Hospital of Copenhagen, Bldg. 8, Bispebjerg Bakke 23, DK-2400, Copenhagen NV, Denmark

      Pernilla Eliasson, Christian Couppé, René B. Svensson, Michael Kjær & S. Peter Magnusson

    2. Center for Healthy Aging, Faculty of Health Sciences, University of Copenhagen, Copenhagen, Denmark

      Christian Couppé, René B. Svensson, Michael Kjær & S. Peter Magnusson

    3. Department of Clinical Physiology and Nuclear Medicine, Bispebjerg Hospital, University Hospital of Copenhagen, Copenhagen, Denmark

      Markus Lonsdale & Lars Friberg

    4. Metropol, School of Physiotherapy, Copenhagen, Denmark

      Christian Neergaard

    5. Musculoskeletal Rehabilitation Research Unit, Bispebjerg Hospital, University Hospital of Copenhagen, Copenhagen, Denmark

      Christian Couppé & S. Peter Magnusson

    Authors
    1. Pernilla Eliasson
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Christian Couppé
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Markus Lonsdale
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. René B. Svensson
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Christian Neergaard
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Michael Kjær
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Lars Friberg
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. S. Peter Magnusson
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Pernilla Eliasson.

    Ethics declarations

    Conflict of interest

    The authors have no conflict of interest.

    Funding

    This study was supported by the Center of Healthy Aging, Danish Association of Rheumatism, IOC Sports Medicine Copenhagen, the Danish Medical Research Council and the Swedish Society for Medical Research.

    Ethical approval

    The study was approved by the local ethics committee for experimental procedures (H-3-2012-060) and was performed according to the principles of the Declaration of Helsinki.

    Informed consent

    Informed consent was obtained from the patients.

    Additional information

    Pernilla Eliasson and Christian Couppé contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Eliasson, P., Couppé, C., Lonsdale, M. et al. Ruptured human Achilles tendon has elevated metabolic activity up to 1 year after repair. Eur J Nucl Med Mol Imaging 43, 1868–1877 (2016). https://doi.org/10.1007/s00259-016-3379-4

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00259-016-3379-4

    Keywords

    Search

    Navigation