Skip to main content
Top
Published in: European Journal of Applied Physiology 7/2012

01-07-2012 | Original Article

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

Authors: Keitaro Kubo, Toshihiro Ikebukuro, Akira Maki, Hideaki Yata, Naoya Tsunoda

Published in: European Journal of Applied Physiology | Issue 7/2012

Login to get access

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.
Literature
go back to reference 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 210:2743–2753PubMedCrossRef 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 210:2743–2753PubMedCrossRef
go back to reference 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 524:305–313PubMedCrossRef 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 524:305–313PubMedCrossRef
go back to reference 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 21:986–989PubMed 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 21:986–989PubMed
go back to reference 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 105:1907–1915PubMedCrossRef 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 105:1907–1915PubMedCrossRef
go back to reference 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) 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)
go back to reference 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 583:1079–1091PubMedCrossRef 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 583:1079–1091PubMedCrossRef
go back to reference 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 27:557–564CrossRef 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 27:557–564CrossRef
go back to reference Erickson SJ, Prost RW, Timins ME (1993) The “magic angle” effect: background physics and clinical relevance. Radiology 188:23–25PubMed Erickson SJ, Prost RW, Timins ME (1993) The “magic angle” effect: background physics and clinical relevance. Radiology 188:23–25PubMed
go back to reference 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 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
go back to reference 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 77:1046–1053CrossRef 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 77:1046–1053CrossRef
go back to reference 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 35:211–213CrossRef 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 35:211–213CrossRef
go back to reference 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 35:485–489CrossRef 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 35:485–489CrossRef
go back to reference 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 26:847–854CrossRef 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 26:847–854CrossRef
go back to reference 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 19:790–802PubMedCrossRef 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 19:790–802PubMedCrossRef
go back to reference Kubo K, Kawakami Y, Fukunaga T (1999) Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87:2090–2096PubMed Kubo K, Kawakami Y, Fukunaga T (1999) Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87:2090–2096PubMed
go back to reference 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 538:219–226PubMedCrossRef 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 538:219–226PubMedCrossRef
go back to reference 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 14:296–302PubMedCrossRef 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 14:296–302PubMedCrossRef
go back to reference 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 39:1801–1810CrossRef 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 39:1801–1810CrossRef
go back to reference 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 104:859–866PubMedCrossRef 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 104:859–866PubMedCrossRef
go back to reference 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 193:257–264CrossRef 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 193:257–264CrossRef
go back to reference 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 106:445–455PubMedCrossRef 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 106:445–455PubMedCrossRef
go back to reference 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 106:412–417PubMedCrossRef 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 106:412–417PubMedCrossRef
go back to reference 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 24:322–331PubMedCrossRef 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 24:322–331PubMedCrossRef
go back to reference 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) 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)
go back to reference 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 515:919–927PubMedCrossRef 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 515:919–927PubMedCrossRef
go back to reference 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 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
go back to reference Langberg H, Rosendal L, Kjaer M (2001) Training-induced changes in peritendinous type 1 collagen turnover determined by microdialysis in humans. J Physiol 534:297–302PubMedCrossRef Langberg H, Rosendal L, Kjaer M (2001) Training-induced changes in peritendinous type 1 collagen turnover determined by microdialysis in humans. J Physiol 534:297–302PubMedCrossRef
go back to reference Magnusson SP, Aagaard P, Rosager S, Poulsen PD, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531:277–288PubMedCrossRef Magnusson SP, Aagaard P, Rosager S, Poulsen PD, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531:277–288PubMedCrossRef
go back to reference 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 27:105–111PubMedCrossRef 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 27:105–111PubMedCrossRef
go back to reference 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 567:1021–1033PubMedCrossRef 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 567:1021–1033PubMedCrossRef
go back to reference 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 43:309–316CrossRef 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 43:309–316CrossRef
go back to reference 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 46:487–493CrossRef 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 46:487–493CrossRef
go back to reference Nosaka K, Clarkson PM (1996) Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exer 28:953–961CrossRef Nosaka K, Clarkson PM (1996) Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exer 28:953–961CrossRef
go back to reference Reimers CD, Fleckenstein JL, Witt TN, Muller-Felber W, Pongratz DE (1993a) Muscular ultrasound in idiopathic inflammatory myopathies of adults. J Neurol Sci 116:82–92PubMedCrossRef Reimers CD, Fleckenstein JL, Witt TN, Muller-Felber W, Pongratz DE (1993a) Muscular ultrasound in idiopathic inflammatory myopathies of adults. J Neurol Sci 116:82–92PubMedCrossRef
go back to reference Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE (1993b) Skeletal muscle sonography. A correlative study of echogenicity and morphology. J Ultrasound Med 12:73–77PubMed Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE (1993b) Skeletal muscle sonography. A correlative study of echogenicity and morphology. J Ultrasound Med 12:73–77PubMed
go back to reference 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 43:198–206PubMed 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 43:198–206PubMed
go back to reference 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 35:438–441CrossRef 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 35:438–441CrossRef
go back to reference van Holsbeeck M, Introcaso JH (1992) Musculoskeletal ultrasonography. Radiol Clin Am 30:907–925 van Holsbeeck M, Introcaso JH (1992) Musculoskeletal ultrasonography. Radiol Clin Am 30:907–925
go back to reference Virtanen P, Viitasalo JT, Vuori J, Vaananen K, Takala TES (1993) Effect of concentric exercise on serum muscle and collagen markers. J Appl Physiol 75:1272–1277PubMed Virtanen P, Viitasalo JT, Vuori J, Vaananen K, Takala TES (1993) Effect of concentric exercise on serum muscle and collagen markers. J Appl Physiol 75:1272–1277PubMed
go back to reference 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 113:625–632CrossRef 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 113:625–632CrossRef
go back to reference Yoon JH, Halper J (2005) Tendon proteoglycans: biochemistry and function. J Musculoskelet Neuronal Interact 5:22–34PubMed Yoon JH, Halper J (2005) Tendon proteoglycans: biochemistry and function. J Musculoskelet Neuronal Interact 5:22–34PubMed
Metadata
Title
Time course of changes in the human Achilles tendon properties and metabolism during training and detraining in vivo
Authors
Keitaro Kubo
Toshihiro Ikebukuro
Akira Maki
Hideaki Yata
Naoya Tsunoda
Publication date
01-07-2012
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 7/2012
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-011-2248-x

Other articles of this Issue 7/2012

European Journal of Applied Physiology 7/2012 Go to the issue