Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 10/2016

01-09-2016 | Original Article

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

Authors: Pernilla Eliasson, Christian Couppé, Markus Lonsdale, René B. Svensson, Christian Neergaard, Michael Kjær, Lars Friberg, S. Peter Magnusson

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 10/2016

Login to get access

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.
Literature
1.
go back to reference 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.PubMed 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.PubMed
2.
go back to reference Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact. 2006;6:181–90.PubMed Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact. 2006;6:181–90.PubMed
3.
go back to reference 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 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
5.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
6.
go back to reference 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.PubMed 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.PubMed
7.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
8.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
9.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
14.
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
21.
go back to reference 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.CrossRef 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.CrossRef
23.
go back to reference 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.CrossRef 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.CrossRef
24.
27.
go back to reference 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.PubMed 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.PubMed
Metadata
Title
Ruptured human Achilles tendon has elevated metabolic activity up to 1 year after repair
Authors
Pernilla Eliasson
Christian Couppé
Markus Lonsdale
René B. Svensson
Christian Neergaard
Michael Kjær
Lars Friberg
S. Peter Magnusson
Publication date
01-09-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 10/2016
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-016-3379-4

Other articles of this Issue 10/2016

European Journal of Nuclear Medicine and Molecular Imaging 10/2016 Go to the issue