Abstract
Purpose
Differential displacement between tendon layers has been shown to occur within the healthy Achilles tendon, and changes of this mechanism have been proposed to result in shear forces, which potentially could lead to tendinopathy. The magnitude of displacement between the tendon layers in tendinopathy is unknown. The purpose of this study was to investigate Achilles tendon layer displacement in individuals suffering from unilateral tendinopathy compared with the asymptomatic contralateral side.
Methods
Ten participants (9 men and 1 woman 45 ± 10 years, BMI: 28 ± 5) with unilateral Achilles tendinopathy were included. Intra-tendinous motion was assessed using ultrasonography during dynamic unilateral heel rises in standing and seated position. Speckle displacement was determined using a cross-correlation algorithm, in four independent rows, representing superficial and deep tendon layers.
Results
The most superficial layer displaced less than the deepest in all condition, except standing for the tendinopathic leg. There was a strong tendency (p = 0.054) for the displacement difference being reduced in the tendinopathic tendon (Tendinopathic side: 0.52 ± 0.16 mm vs. asymptomatic contralateral side: 1.02 ± 0.18 mm).
Conclusion
These novel data suggest that the presence of tendinopathy diminishes intra-tendinous sliding in the Achilles tendon.
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Abbreviations
- AGE:
-
Advanced glycation end-products
- BMI:
-
Body mass index
- MVC:
-
Maximal voluntary contractions
- NRS:
-
Numeric rating scale
- ROI:
-
Region of interest
- ROM:
-
Range of motion
- SAF:
-
Skin autofluorescence
References
Abate M, Salini V (2018) Mid-portion Achilles tendinopathy in runners with metabolic disorders. Eur J Orthop Surg Traumatol. https://doi.org/10.1007/s00590-018-2336-2
Arndt A, Bengtsson AS, Peolsson M, Thorstensson A, Movin T (2012) Non-uniform displacement within the Achilles tendon during passive ankle joint motion. Knee Surg Sports Traumatol Arthrosc 20:1868–1874. https://doi.org/10.1007/s00167-011-1801-9
Arnoczky SP, Lavagnino M, Egerbacher M (2007) The mechanobiological aetiopathogenesis of tendinopathy: Is it the over-stimulation or the under-stimulation of tendon cells? IntJ ExpPathol 88:217–226
Bashford GR, Tomsen N, Arya S, Burnfield JM, Kulig K (2008) Tendinopathy discrimination by use of spatial frequency parameters in ultrasound B-mode images. IEEE Trans Med Imaging 27:608–615. https://doi.org/10.1109/TMI.2007.912389
Beyer R, Agergaard A, Magnusson S, Svensson R (2018) Speckle tracking in healthy and surgically repaired human Achilles tendons at different knee angles—a validation using implanted tantalum beads. Trans Sports Med 1:79–88
Bogaerts S, De Brito CC, De Groef A, Suetens P, Peers K (2018) Non-uniformity in pre-insertional Achilles tendon is not influenced by changing knee angle during isometric contractions. Scand J Med Sci Sports 28:2322–2329. https://doi.org/10.1111/sms.13230
Bojsen-Moller J, Hansen P, Aagaard P, Svantesson U, Kjaer M (1985) Magnusson SP (2004) Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. J Appl Physiol 97:1908–1914. https://doi.org/10.1152/japplphysiol.00084.2004
Couppe C et al (2014) Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue. Age (Dordr) 36:9665. https://doi.org/10.1007/s11357-014-9665-9
Cresswell AG, Loscher WN, Thorstensson A (1995) Influence of gastrocnemius muscle length on triceps surae torque development and electromyographic activity in man. Exp Brain Res 105:283–290
de Jonge S et al (2011) Incidence of midportion Achilles tendinopathy in the general population. Br J Sports Med 45:1026–1028. https://doi.org/10.1136/bjsports-2011-090342
de Mos M et al (2007) Achilles tendinosis: changes in biochemical composition and collagen turnover rate. Am J Sports Med 35:1549–1556
Edama M et al (2015) The twisted structure of the human Achilles tendon. Scand J Med Sci Sports 25:e497–503. https://doi.org/10.1111/sms.12342
Eliasson P et al (2016) Ruptured human Achilles tendon has elevated metabolic activity up to 1 year after repair. Eur J Nucl Med Mol Imaging. https://doi.org/10.1007/s00259-016-3379-4
Eriksen C et al (2014) Systemic stiffening of mouse tail tendon is related to dietary advanced glycation end products but not high-fat diet or cholesterol. J Appl Physiol 117:840–847. https://doi.org/10.1152/japplphysiol.00584.2014
Ferreira-Valente MA, Pais-Ribeiro JL, Jensen MP (2011) Validity of four pain intensity rating scales. Pain 152:2399–2404. https://doi.org/10.1016/j.pain.2011.07.005
Fessel G et al (2014) Advanced glycation end-products reduce collagen molecular sliding to affect collagen fibril damage mechanisms but not stiffness. PLoS ONE 9:e110948. https://doi.org/10.1371/journal.pone.0110948
Finni T, Bernabei M, Baan GC, Noort W, Tijs C, Maas H (2018) Non-uniform displacement and strain between the soleus and gastrocnemius subtendons of rat Achilles tendon. Scand J Med Sci Sports 28:1009–1017. https://doi.org/10.1111/sms.13001
Franz JR, Thelen DG (2016) Imaging and simulation of Achilles tendon dynamics: Implications for walking performance in the elderly. J Biomech 49:1403–1410. https://doi.org/10.1016/j.jbiomech.2016.04.032
Fredberg U, Bolvig L, Andersen NT, Stengaard-Pedersen K (2008) Ultrasonography in evaluation of Achilles and patella tendon thickness. Ultraschall Med 29:60–65. https://doi.org/10.1055/s-2007-963027
Froberg A, Cisse AS, Larsson M, Martensson M, Peolsson M, Movin T, Arndt A (2016) Altered patterns of displacement within the Achilles tendon following surgical repair. Knee Surg Sports Traumatol Arthrosc. https://doi.org/10.1007/s00167-016-4394-5
Fukashiro S, Komi PV, Jarvinen M, Miyashita M (1995) vivo Achilles tendon loading during jumping in humans. Eur J Appl Physiol Occup Physiol 71:453–458
Gaida JE, Ashe MC, Bass SL, Cook JL (2009) Is adiposity an under-recognized risk factor for tendinopathy? A systematic review. Arthritis Rheum 61:840–849
Gautieri A et al (2016) Advanced glycation end-products: mechanics of aged collagen from molecule to tissue. Matrix Biol. https://doi.org/10.1016/j.matbio.2016.09.001
Grasa J, Calvo B, Delgado-Andrade C, Navarro MP (2013) Variations in tendon stiffness due to diets with different glycotoxins affect mechanical properties in the muscle-tendon unit. Ann Biomed Eng 41:488–496. https://doi.org/10.1007/s10439-012-0674-5
Haraldsson BT et al (2008) Lateral force transmission between human tendon fascicles. Matrix Biol 27:86–95
Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M (2013) Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb (14). C FASEB J 27:2074–2079. https://doi.org/10.1096/fj.12-225599
Heinemeier KM, Schjerling P, Ohlenschlaeger TF, Eismark C, Olsen J, Kjaer M (2018) Carbon-14 bomb pulse dating shows that tendinopathy is preceded by years of abnormally high collagen turnover. FASEB J. 32:4763–4775. https://doi.org/10.1096/fj.201701569R
Kennedy PM, Cresswell AG (2001) The effect of muscle length on motor-unit recruitment during isometric plantar flexion in humans. Exp Brain Res 137:58–64
Khan KM, Forster BB, Robinson J, Cheong Y, Louis L, Maclean L, Taunton JE (2003) Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A 2 year prospective study. Br J Sports Med 37:149–153
Koenig MJ, Torp-Pedersen S, Holmich P, Terslev L, Nielsen MB, Boesen M, Bliddal H (2007) Ultrasound Doppler of the Achilles tendon before and after injection of an ultrasound contrast agent–findings in asymptomatic subjects. Ultraschall Med. 28:52–56. https://doi.org/10.1055/s-2006-926715
Komi PV, Fukashiro S, Jarvinen M (1992) Biomechanical loading of Achilles tendon during normal locomotion. Clin Sports Med 11:521–531
Kongsgaard M, Nielsen CH, Hegnsvad S, Aagaard P, Magnusson SP (2011) Mechanical properties of the human Achilles tendon, in vivo. Clin Biomech (Bristol, Avon) 26:772–777. https://doi.org/10.1016/j.clinbiomech.2011.02.011
Korstanje JW, Selles RW, Stam HJ, Hovius SE, Bosch JG (2010) Development and validation of ultrasound speckle tracking to quantify tendon displacement. J Biomech 43:1373–1379. https://doi.org/10.1016/j.jbiomech.2010.01.001
Kujala UM, Sarna S, Kaprio J (2005) Cumulative incidence of achilles tendon rupture and tendinopathy in male former elite athletes. Clin J Sport Med 15:133–135
Li Y, Fessel G, Georgiadis M, Snedeker JG (2013) Advanced glycation end-products diminish tendon collagen fiber sliding. Matrix Biol 32:169–177. https://doi.org/10.1016/j.matbio.2013.01.003
Longo UG, Ronga M, Maffulli N (2009) Achilles tendinopathy. Sports Med Arthrosc Rev 17:112–126. https://doi.org/10.1097/JSA.0b013e3181a3d625
Magnan B, Bondi M, Pierantoni S, Samaila E (2014) The pathogenesis of Achilles tendinopathy: a systematic review. Foot Ankle Surg 20:154–159. https://doi.org/10.1016/j.fas.2014.02.010
Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531:277–288
Magnusson SP, Langberg H, Kjaer M (2010) The pathogenesis of tendinopathy: balancing the response to loading. Nat Rev Rheumatol 6:262–268
Meerwaldt R et al (2004) Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 47:1324–1330. https://doi.org/10.1007/s00125-004-1451-2
Monnier VM, Mustata GT, Biemel KL, Reihl O, Lederer MO, Zhenyu D, Sell DR (2005) Cross-linking of the extracellular matrix by the maillard reaction in aging and diabetes: an update on "a puzzle nearing resolution". Ann N Y Acad Sci 1043:533–544. https://doi.org/10.1196/annals.1333.061
Ohberg L, Lorentzon R, Alfredson H (2001) Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc 9:233–238
O'Neill S, Barry S, Watson P (2019) Plantarflexor strength and endurance deficits associated with mid-portion Achilles tendinopathy: the role of soleus. Phys Ther Sport 37:69–76. https://doi.org/10.1016/j.ptsp.2019.03.002
Pingel J et al (2014) 3-D ultrastructure and collagen composition of healthy and overloaded human tendon: evidence of tenocyte and matrix buckling. J Anat 224:548–555. https://doi.org/10.1111/joa.12164
Scott A, Zwerver J, Grewal N, de Sa A, Alktebi T, Granville DJ, Hart DA (2015) Lipids, adiposity and tendinopathy: is there a mechanistic link? Critical review. Br J Sports Med 49:984–988. https://doi.org/10.1136/bjsports-2014-093989
Silbernagel KG, Gustavsson A, Thomee R, Karlsson J (2006) Evaluation of lower leg function in patients with Achilles tendinopathy. Knee Surg Sports Traumatol Arthrosc 14:1207–1217. https://doi.org/10.1007/s00167-006-0150-6
Skovgaard D et al (2017) An advanced glycation endproduct (AGE)-rich diet promotes accumulation of AGEs in Achilles tendon. Physiol Rep. https://doi.org/10.14814/phy2.13215
Slane LC, Thelen DG (2014) Non-uniform displacements within the Achilles tendon observed during passive and eccentric loading. J Biomech 47:2831–2835. https://doi.org/10.1016/j.jbiomech.2014.07.032
Slane LC, Thelen DG (2015) Achilles tendon displacement patterns during passive stretch and eccentric loading are altered in middle-aged adults. Med Eng Phys 37:712–716. https://doi.org/10.1016/j.medengphy.2015.04.004
Stenroth L, Thelen D, Franz J (2019) Biplanar ultrasound investigation of in vivo Achilles tendon displacement non-uniformity Transl. Sports Med 2:73–81. https://doi.org/10.1002/tsm2.61
Szaro P, Witkowski G, Smigielski R, Krajewski P, Ciszek B (2009) Fascicles of the adult human Achilles tendon—an anatomical study. Ann Anat 191:586–593. https://doi.org/10.1016/j.aanat.2009.07.006
Thorpe CT, Streeter I, Pinchbeck GL, Goodship AE, Clegg PD, Birch HL (2010) Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging. J Biol Chem 285:15674–15681. https://doi.org/10.1074/jbc.M109.077503
Thorpe CT, Udeze CP, Birch HL, Clegg PD, Screen HR (2012) Specialization of tendon mechanical properties results from interfascicular differences. J R Soc Interface 9:3108–3117. https://doi.org/10.1098/rsif.2012.0362
Thorpe CT, Udeze CP, Birch HL, Clegg PD, Screen HR (2013) Capacity for sliding between tendon fascicles decreases with ageing in injury prone equine tendons: a possible mechanism for age-related tendinopathy? Eur Cell Mater 25:48–60
Thorpe CT, Peffers MJ, Simpson D, Halliwell E, Screen HR, Clegg PD (2016) Anatomical heterogeneity of tendon: fascicular and interfascicular tendon compartments have distinct proteomic composition. Sci Rep 6:20455. https://doi.org/10.1038/srep20455
Verzijl N et al (2000) Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275:39027–39031
Acknowledgements
We would like to thank Sarah Gaston, PT for her excellent assistance during recruitment and testing. We would also like to thank Center for Healthy Aging, University of Copenhagen, and the Danish medical research council.
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CC conceived of the study, participated in its design and coordination, interpretation of the data and drafted the manuscript; COJ and EK participated in the design and coordination of the study and performed the measurement; RBS participated in the design of the study, interpretation of the data and performed the statistical analysis; SPM conceived of the study, and participated in its design and coordination, interpretation of the data and helped to draft the manuscript. All authors read and approved the final manuscript.
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Communicated by Olivier Seynnes.
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Couppé, C., Svensson, R.B., Josefsen, C.O. et al. Ultrasound speckle tracking of Achilles tendon in individuals with unilateral tendinopathy: a pilot study. Eur J Appl Physiol 120, 579–589 (2020). https://doi.org/10.1007/s00421-020-04317-5
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DOI: https://doi.org/10.1007/s00421-020-04317-5