Fibril Morphology and Tendon Mechanical Properties in Patellar Tendinopathy: Effects of Heavy Slow Resistance Training
Abstract
Background
Patellar tendinopathy is characterized by pathologic abnormalities. Heavy slow resistance training (HSR) is effective in the management of patellar tendinopathy, but the underlying functional mechanisms remain elusive.
Purpose
To investigate fibril morphology and mechanical properties in patellar tendinopathy and the effect of HSR on these properties.
Study Design
Cohort study; Level of evidence, 2.
Methods
Eight male patients with patellar tendinopathy completed 12 weeks of HSR. Nine healthy subjects served as controls. Assessments were conducted at baseline and at 12 weeks. Patients assessed symptoms/function and maximal tendon pain during activity. Tendon biopsy samples were analyzed for fibril density, volume fraction, and mean fibril area. Tendon mechanical properties were assessed using force and ultrasonography samplings.
Results
Patients improved in symptoms/function (P = .02) and maximal tendon pain during activity (P = .008). Stiffness and modulus of control and tendinopathy tendons were similar at baseline. Stiffness remained unaffected in control tendons (3487 ± 392 to 3157 ± 327 N/mm, P = .57) but declined in tendinopathic tendons at 12 weeks (3185 ± 187 to 2701 ± 201 N/mm, P = .04). At baseline, fibril volume fraction was equal, fibril density smaller (P = .03), and mean fibril area tended to be higher in tendinopathy versus controls (P = .07). Fibril morphology remained unchanged in controls but fibril density increased (70% ± 18%, P = .02) and fibril mean area decreased (—26% ± 21%, P = .04) in tendinopathic tendons after HSR.
Conclusion
Fibril morphology is abnormal in tendinopathy, but tendon mechanical properties are not. Clinical improvements after HSR were associated with changes in fibril morphology toward normal fibril density and mean fibril area. Heavy slow resistance training improved the clinical outcome of patellar tendinopathy, and these improvements were associated with normalization of fibril morphology, most likely due to a production of new fibrils.
Get full access to this article
View all access and purchase options for this article.
References
1. Arnoczky SP, Lavagnino M., Egerbacher M. The mechanobiological aetiopathogenesis of tendinopathy: is it the over-stimulation or the under-stimulation of tendon cells? Int J Exp Pathol. 2007;88:217–226.
2. Bank RA, TeKoppele JM, Oostingh G., Hazleman BL, Riley GP Lysylhydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis. 1999;58:35–41.
3. Battaglia TC, Clark RT, Chhabra A., Gaschen V., Hunziker EB, Mikic B. Ultrastructural determinants of murine Achilles tendon strength during healing. Connect Tissue Res. 2003;44:218–224.
4. Birch HL Tendon matrix composition and turnover in relation to functional requirements. Int J Exp Pathol. 2007;88:241–248.
5. Cook JL, Khan KM, Harcourt PR, Grant M., Young DA, Bonar SF A cross sectional study of 100 athletes with jumper's knee managed conservatively and surgically: the Victorian Institute of Sport Tendon Study Group. Br J Sports Med. 1997;31:332–336.
6. Craig AS, Birtles MJ, Conway JF, Parry DA An estimate of the mean length of collagen fibrils in rat tail-tendon as a function of age. Connect Tissue Res. 1989;19:51–62.
7. de Mos M., van El B., DeGroot J., et al. Achilles tendinosis: changes in biochemical composition and collagen turnover rate. Am J Sports Med. 2007; 35:1549–1556.
8. Devitt D., Koike Y., Doherty GP, et al. The ability of ultrasonography, magnetic resonance imaging and bone mineral densitometry to predict the strength of human Achilles’ tendons. Arch Phys Med Rehabil. 2009;90:756–760.
9. Frohm A., Saartok T., Halvorsen K., Renstrom P. Eccentric treatment for patellar tendinopathy: a prospective randomised short-term pilot study of two rehabilitation protocols. Br J Sports Med. 2007;41:e7.
10. Gundersen HJ, Bendtsen TF, Korbo L., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS. 1988;96:379–394.
11. Hannafin JA, Arnoczky SP, Hoonjan A., Torzilli PA Effect of stress deprivation and cyclic tensile loading on the material and morphologic properties of canine flexor digitorum profundus tendon: an in vitro study. J Orthop Res. 1995;13:907–914.
12. Hansen M., Kongsgaard M., Holm L., et al. Effect of estrogen on tendon collagen synthesis, tendon structural characteristics, and biomechanical properties in postmenopausal women. J Appl Physiol. 2008;106:1385–1393.
13. Hansen P., Bojsen-Moller J., Aagaard P., Kjaer M., Magnusson SP Mechanical properties of the human patellar tendon, in vivo. Clin Biomech. 2006;21:54–58.
14. Jozsa L., Kvist M., Balint BJ, et al. The role of recreational sport activity in Achilles tendon rupture: a clinical, pathoanatomical, and sociological study of 292 cases. Am J Sports Med. 1989;17:338–343.
15. Kadler KE, Holmes DF, Trotter JA, Chapman JA Collagen fibril formation. Biochem J. 1996; 316(pt 1):1–11.
16. Kannus P., Jozsa L. Histopathological changes preceding spontaneous rupture of a tendon: a controlled study of 891 patients. J Bone Joint Surg Am. 1991;73:1507–1525.
17. Kongsgaard M., Aagaard P., Kjaer M., Magnusson SP Structural Achilles tendon properties in athletes subjected to different exercise modes and in Achilles tendon rupture patients. J Appl Physiol. 2005;99:1965–1971.
18. Kongsgaard M., Kovanen V., Aagaard P., et al. Corticosteroid injections, eccentric decline squat training and heavy slow resistance training in patellar tendinopathy. Scand J Med Sci Sports. 2009; epub.
19. Kongsgaard M., Reitelseder S., Pedersen TG, et al. Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol. 2007;191:111–121.
20. Lake SP, Miller KS, Elliott DM, Soslowsky LJ Effect of fiber distribution and realignment on the nonlinear and inhomogeneous mechanical properties of human supraspinatus tendon under longitudinal tensile Loading. J Orthop Res. Epub ahead of print June 19, 2009.
21. Lavagnino M., Arnoczky SP, Frank K., Tian T. Collagen fibril diameter distribution does not reflect changes in the mechanical properties of in vitro stress-deprived tendons. J Biomech. 2005;38:69–75.
22. Maffulli N., Ewen SW, Waterston SW, Reaper J., Barrass V. Tenocytes from ruptured and tendinopathic achilles tendons produce greater quantities of type III collagen than tenocytes from normal achilles tendons: an in vitro model of human tendon healing. Am J Sports Med. 2000;28:499–505.
23. Maffulli N., Khan KM, Puddu G. Overuse tendon conditions: time to change a confusing terminology. Arthroscopy. 1998; 14:840–843.
24. Maffulli N., Testa V., Capasso G., et al. Similar histopathological picture in males with Achilles and patellar tendinopathy. Med Sci Sports Exerc. 2004;36:1470–1475.
25. Magnusson SP, Qvortrup K., Larsen JO, et al. Collagen fibril size and crimp morphology in ruptured and intact Achilles tendons. Matrix Biol. 2002;21:369–377.
26. Michna H. Morphometric analysis of loading-induced changes in collagen-fibril populations in young tendons. Cell Tissue Res. 1984; 236:465–470.
27. Ohberg L., Lorentzon R., Alfredson H. Eccentric training in patients with chronic Achilles tendinosis: normalised tendon structure and decreased thickness at follow up. Br J Sports Med. 2004; 38:8–11.
28. 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;9:233–238.
29. Parry DA The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys Chem. 1988;29:195–209.
30. Parry DA, Barnes GR, Craig AS A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc R Soc Lond B Biol Sci. 1978;203:305–321.
31. Patterson-Kane JC, Firth EC, Parry DA, Wilson AM, Goodship AE Effects of training on collagen fibril populations in the suspensory ligament and deep digital flexor tendon of young thoroughbreds. Am J Vet Res. 1998;59:64–68.
32. Patterson-Kane JC, Wilson AM, Firth EC, Parry DA, Goodship AE Comparison of collagen fibril populations in the superficial digital flexor tendons of exercised and nonexercised thoroughbreds. Equine Vet J. 1997;29:121–125.
33. Provenzano PP, Vanderby R. Jr. Collagen fibril morphology and organization: Implications for force transmission in ligament and tendon. Matrix Biol. 2006;25:71–84.
34. Purdam CR, Jonsson P., Alfredson H., Lorentzon R., Cook JL, Khan KM A pilot study of the eccentric decline squat in the management of painful chronic patellar tendinopathy. Br J Sports Med. 2004;38: 395–397.
35. Riley G. Chronic tendon pathology: molecular basis and therapeutic implications. Expert Rev Mol Med. 2005;7:1–25.
36. Riley GP, Harrall RL, Constant CR, Chard MD, Cawston TE, Hazleman BL Tendon degeneration and chronic shoulder pain: changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis. Ann Rheum Dis. 1994;53: 359–366.
37. Robinson PS, Lin TW, Reynolds PR, Derwin KA, Iozzo RV, Soslowsky LJ Strain-rate sensitive mechanical properties of tendon fascicles from mice with genetically engineered alterations in collagen and decorin. J Biomech Eng. 2004;126:252–257.
38. Svensson L., Aszodi A., Reinholt FP, Fassler R., Heinegard D., Oldberg A. Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J Biol Chem. 1999;274:9636–9647.
39. Svensson M., Movin T., Rostgard-Christensen L., Blomen E., Hultenby K., Kartus J. Ultrastructural collagen fibril alterations in the patellar tendon 6 years after harvesting its central third. Am J Sports Med. 2007;35:301–306.
40. Visentini PJ, Khan KM, Cook JL, Kiss ZS, Harcourt PR, Wark JD The VISA score: an index of severity of symptoms in patients with jumper's knee (patellar tendinosis). Victorian Institute of Sport Tendon Study Group. J Sci Med Sport. 1998;1:22–28.
41. Williams LN, Elder SH, Horstemeyer MF, Harbarger D. Variation of diameter distribution, number density, and area fraction of fibrils within five areas of the rabbit patellar tendon. Ann Anat. 2008;190:442–451.
42. Wong MW, Tang YN, Fu SC, Lee KM, Chan KM Triamcinolone suppresses human tenocyte cellular activity and collagen synthesis. Clin Orthop Relat Res. 2004;421:277–281.
Cite article
Cite article
Cite article
OR
Download to reference manager
If you have citation software installed, you can download article citation data to the citation manager of your choice
Information, rights and permissions
Information
Published In
Article first published online: February 12, 2010
Issue published: April 2010
Keywords
PubMed: 20154324
Authors
Metrics and citations
Metrics
Journals metrics
This article was published in The American Journal of Sports Medicine.
VIEW ALL JOURNAL METRICSArticle usage*
Total views and downloads: 4717
*Article usage tracking started in December 2016
Altmetric
See the impact this article is making through the number of times it’s been read, and the Altmetric Score.
Learn more about the Altmetric Scores
Articles citing this one
Receive email alerts when this article is cited
Web of Science: 152 view articles Opens in new tab
Crossref: 164
-
Effects of low-load blood flow restriction training in healthy adult t...
-
Maximal Lower Limb Strength in Patellar Tendinopathy: A Systematic Rev...
-
Effectiveness of non-surgical management in rotator cuff calcific tend...
-
Longitudinal Evidence for High-Level Patellar Tendon Strain as a Risk ...
-
Exercise therapy for tendinopathy: a mixed-methods evidence synthesis ...
-
A New Test for Achilles Tendinopathy Based on Kager’s Fat Pad Clinical...
-
Exercise for rotator cuff tendinopathy: Proposed mechanisms of recover...
-
Overload in a Rat in Vivo Model of Synergist Ablation Induces Tendon M...
-
Achilles Tendon and Patellar Tendon Structure in Combat Soldiers Follo...
-
Blood Flow Restriction Training for Tendinopathy Rehabilitation: A Pot...
-
Rehabilitation Principles for Interventional Orthopedics and Orthobiol...
-
Gluteal Tendinopathy
-
Effects of Different Long-Term Exercise Modalities on Tissue Stiffness
-
Whole body vibration for chronic patellar tendinopathy: A randomized e...
-
Patellar Tendon Injury: A Bibliometric Analysis of the Most-Cited Arti...
-
Current understanding of the diagnosis and management of the tendinopa...
-
Effects of Heavy Slow Resistance Training Combined With Corticosteroid...
-
Fatigue Failure of Musculoskeletal Tissues
-
Decreasing patellar tendon stiffness during exercise therapy for patel...
-
Scleraxis and collagen I expression increase following pilot isometric...
-
Blood Flow Restriction Resistance Training in Tendon Rehabilitation: A...
-
The Influence of a 14-Week Infantry Commanders Courses on the Achilles...
-
Resistance Training Interventions for Lower Limb Tendinopathies: A Sco...
-
Novel interventions for recalcitrant patella tendinopathy: Results may...
-
Combined extracorporeal shockwave therapy and exercise for the treatme...
-
Neuromechanical changes in Achilles tendinopathy and the effects of ex...
-
Ultrasound-Guided Orthobiologics of the Foot and Ankle
-
Rehabilitation Principles for Interventional Orthopedics and Orthobiol...
-
Rehabilitation After Gluteus Medius and Minimus Treatment
-
Knee Extensor Mechanism Tendinopathy: Evaluation, Treatment, and Preve...
-
Tendinopathy
-
Pain-guided activity modification during treatment for patellar tendin...
-
The dispersion of viscoelastic properties of fascicle bundles within t...
-
No Difference in Clinical Effects When Comparing Alfredson Eccentric a...
-
Mechanical properties and UTE‐T2* in Patellar tendinopathy: The effect...
-
Autoregulation in Resistance Training for Lower Limb Tendinopathy: A P...
-
Maximum dorsiflexion increases Achilles tendon force during exercise f...
-
Substantial Achilles adaptation following strength training has no imp...
-
An indirect evaluation between corticosteroid injections and gluteal e...
-
Clinical Outcomes, Structure, and Function Improve With Both Heavy and...
-
Treating tendinopathies – are we searching for a needle in a haystack,...
-
Patellapeestendinose
-
The influence of a multidisciplinary intervention program on Achilles ...
-
Gesundes Gewebe kräftigen – Tendinopathien der unteren Extremität
-
Quantitative Analysis of Patellar Tendon After Total Knee Arthroplasty...
-
Immediate and Short-Term Effects of Short- and Long-Duration Isometric...
-
Association Between Clinical and Imaging Outcomes After Therapeutic Lo...
-
Mechanical and Material Tendon Properties in Patients With Proximal Pa...
-
Common Musculoskeletal Disorders in the Elderly: The Star Triad
-
Basic Muscle Physiology in Relation to Hamstring Injury and Repair
-
Rehabilitation of Tendinopathy in Basketball
-
Tendon Homeostasis: Overview
-
Musculoskeletal elastography
-
Early development of tendinopathy in humans: Sequence of pathological ...
-
Adaptation of Tendon Structure and Function in Tendinopathy With Exerc...
-
Changes on Tendon Stiffness and Clinical Outcomes in Athletes Are Asso...
-
Load magnitude affects patellar tendon mechanical properties but not c...
-
Exercise therapy in the treatment of tendinopathies of the lower limbs...
-
Eccentric Resistance Training in Youth: Perspectives for Long-Term Ath...
-
The efficacy of loading programmes for improving patient‐reported outc...
-
Insulin‐like growth factor 1 signaling in tenocytes is required for ad...
-
Tendon Stem/Progenitor Cells and Their Interactions with Extracellular...
-
Injection with autologous conditioned serum has better clinical result...
-
Patellar Tendinopathy in Athletes
-
Altered Strength Profile in Achilles Tendinopathy: A Systematic Review...
-
Influence of Oral Contraceptive Use on Adaptations to Resistance Train...
-
Nonsurgical Treatments of Patellar Tendinopathy: Multiple Injections o...
-
The impact of loading, unloading, ageing and injury on the human tendo...
-
Transverse tendon stiffness is reduced in people with Achilles tendino...
-
More tendon degeneration in patients with shoulder osteoarthritis
-
Management of Profound Pain and Functional Deficits From Achilles Inse...
-
Comparison of the sonographic features of the Achilles Tendon complex ...
-
Patellapeestendinose
-
Oefenprogramma patellapeestendinose: heavy slow resistance (HSR) progr...
-
Patellar Tendon Stiffness in Elite Breakdancers Assessed by Myotonomet...
-
Tendon Remodeling in Response to Resistance Training, Anabolic Androge...
-
Effects of a strength protocol combined with electrical stimulation on...
-
Effects of isometric, eccentric, or heavy slow resistance exercises on...
-
Are the Mechanical or Material Properties of the Achilles and Patellar...
-
Frog tendon structure and its relationship with locomotor modes
-
Insertional and mid-substance Achilles tendinopathies: eccentric train...
-
Substrate fiber alignment mediates tendon cell response to inflammator...
-
Achilles and patellar tendinopathy display opposite changes in elastic...
-
Tendinous framework of anurans reveals an all-purpose morphology
-
Effects of footwear and heel elevation on tensile load in the Achilles...
-
Physiotherapy Management of Patellar Tendinopathy in Tennis Players
-
Parámetros de la rehabilitación deportiva
-
Tendinopathy
-
Beneficial effects of resistance training on the protein profile of th...
-
The Influence of External Load on Quadriceps Muscle and Tendon Dynamic...
-
Achilles Tendon Penetration for Continuous 810 nm and Superpulsed 904 ...
-
Achilles Tendon Load is Progressively Increased with Reductions in Wal...
-
Three Months of Progressive High-Load Versus Traditional Low-Load Stre...
-
Revisión sistemática de la eficacia de la electrolisis percutánea en e...
-
Alterations in mechanical properties of the patellar tendon is associa...
-
Association of psychological variables and outcome in tendinopathy: a ...
-
El continuum de la patología de tendón: concepto actual e implicacione...
-
Pathogenesis and Treatment of Patellar Tendinopathy
-
Kniegelenk
-
Conservative treatments for greater trochanteric pain syndrome: a syst...
-
Muscle and tendon adaptation in adolescent athletes: A longitudinal st...
-
Arthroscopic Treatment of Patellar Tendinopathy: Use of 70° Arthroscop...
-
Revisiting the continuum model of tendon pathology: what is its merit ...
-
Chondroitin sulphate glycosaminoglycans contribute to widespread infer...
-
Do isometric and isotonic exercise programs reduce pain in athletes wi...
-
Faster Movement Speed Results in Greater Tendon Strain during the Load...
-
Proximal Hamstring Tendinopathy: Clinical Aspects of Assessment and Ma...
-
A chilles tendon structure improves on UTC...
-
Ultrasound-Based Tendon Micromorphology Predicts Mechanical Characteri...
-
Human Achilles tendon glycation and function in diabetes
-
Collagen Homeostasis and Metabolism
-
Photobiomodulation and eccentric exercise for Achilles tendinopathy: a...
-
Tendinopathy and Aging
-
Progressive high-load strength training compared with general low-load...
-
The (dys)functional extracellular matrix
-
Gluteal Tendinopathy: Integrating Pathomechanics and Clinical Features...
-
Eccentric or Concentric Exercises for the Treatment of Tendinopathies?
-
An update on the constitutive relation of ligament tissues with the ef...
-
Lipids, adiposity and tendinopathy: is there a mechanistic link? Criti...
-
The neuromechanical adaptations to Achilles tendinosis
-
Heavy Slow Resistance Versus Eccentric Training as Treatment for Achil...
-
Progress in cell-based therapies for tendon repair
-
Cómo puede afectar el componente genético la lesionabilidad de los dep...
-
Treating Tendinopathy
-
Tendinopathy Alters Cumulative Transverse Strain in the Patellar Tendo...
-
Eccentric exercise training in chronic mid‐portion A ...
-
The influence of physical activity during youth on structural and func...
-
Tendons and Ligaments: Current State and Future Directions
-
Exercise and Regulation of Bone and Collagen Tissue Biology
-
Changes in Morphological and Elastic Properties of Patellar Tendon in ...
-
Evaluation of elastic bands for lower extremity resistance training in...
-
Life-long endurance running is associated with reduced glycation and m...
-
Region-Specific Tendon Properties and Patellar Tendinopathy: A Wider U...
-
Effect of tear size, corticosteroids and subacromial decompression sur...
-
Do structural changes (eg, collagen/matrix) explain the response to th...
-
3‐ D ultrastructure and collagen compositi...
-
Muscle and tendon connective tissue adaptation to unloading, exercise ...
-
Chronic alterations in growth hormone/insulin-like growth factor-I sig...
-
Eccentric strengthening effect of hip-adductor training with elastic b...
-
Effect of growth hormone on aging connective tissue in muscle and tend...
-
Functionally distinct tendon fascicles exhibit different creep and str...
-
Tendon and skeletal muscle matrix gene expression and functional respo...
-
The Microvascular Volume of the Achilles Tendon Is Increased in Patien...
-
Analysis of the Load on the Knee Joint and Vertebral Column with Chang...
-
Short-term acetaminophen consumption enhances the exercise-induced inc...
-
Mechanical properties of the patellar tendon in elite volleyball playe...
-
Fatigue loading of tendon
-
Patellar tendon adaptation in relation to load-intensity and contracti...
-
Impact of oral contraceptive use and menstrual phases on patellar tend...
-
Achilles and Patellar Tendinopathy Loading Programmes
-
Differences in tendon properties in elite badminton players with or wi...
-
Rehabilitation of tendopathies in human athletes
-
In vitro tendon tissue development from human fibroblasts demonstrates...
-
Local biochemical and morphological differences in human Achilles tend...
-
Eccentric hip abductor weakness in patients with symptomatic external ...
-
Influence of acetaminophen consumption and exercise on Achilles tendon...
-
The magnitude and character of resistance-training-induced increase in...
-
Assessment of collagen fibril spacing in relation to selected region o...
-
Computation methods affect the reported values of in vivo human tendon...
-
Type V Collagen Genotype and Exercise-Related Phenotype Relationships
-
Tensile Force Transmission in Human Patellar Tendon Fascicles Is Not M...
-
Influence of acetaminophen and ibuprofen on in vivo patellar tendon ad...
-
Tensile Properties of Human Collagen Fibrils and Fascicles Are Insensi...
-
Conceptos actuales de la fisiopatología de las tendinopatías. Ingenier...
Figures and tables
Figures & Media
Tables
View Options
Get access
Access options
If you have access to journal content via a personal subscription, university, library, employer or society, select from the options below:
loading institutional access options
AOSSM members can access this journal content using society membership credentials.
AOSSM members can access this journal content using society membership credentials.
Alternatively, view purchase options below:
Purchase 24 hour online access to view and download content.
Access journal content via a DeepDyve subscription or find out more about this option.
