The results of this study show that there is an immediate tendon physiologic response to strength training with increase in volume. There has so far been a complete lack of knowledge on how the physiologic response process works in response to strength training in human tendons. We showed that the human Achilles tendon response to heavy- or light-loaded strength training in patients with unilateral or bilateral Achilles tendinosis resulted in an increased total tendon volume and increased intratendinous signal at MRI, in both symptomatic and asymptomatic tendons.
MRI is a very sensitive method to depict pathological changes in the tendons. However, MRI may not be very specific. For example, one MRI study demonstrated that MRI findings can occur in asymptomatic individuals as well, with a sensitivity of 75%, but a specificity of only 29% in predicting symptomatic patellar tendinopathy (29). Other researchers have found that the tendon remain abnormal after surgical treatment, despite clinical resolution. Khan et al. (13) performed MRI on subjects before surgical debridement for refractory patellar tendinosis. Preoperative MRI and ultrasound revealed characteristic findings of patellar tendinopathy. Postoperatively, imaging studies remained abnormal despite clinical resolution. The radiologist's assessment of tendon abnormality had no correlation with the clinical ranking. Imaging was unable to differentiate patients with good to excellent results from those with poor results (13).
The normal tendon has low water content, resulting in lack of intratendinous signals; consequently, the normal tendon appears black in all MR sequences. Pathological changes in the tendon are accompanied by an increase of water content, whereby structural changes within the tendon can be recognized. Furthermore, by using different MR pulse sequences, the technique is able to distinguish between different intratendinous physiologic and pathologic alterations. The importance and ability of MRI in evaluating and following up tendon healing have gained increasing interest. Recent reports indicate that pathologic intratendinous MR signals fade or disappear 2 yr after surgical treatment. However, the anterio-posterior diameter was unchanged (27,28). The healing process after surgically repaired Achilles tendon ruptures has been examined in MR studies (11). The size of the tendon lesion is of clinical importance in the management and in follow-up of the healing process in chronic Achilles tendinosis. Exact measurements of the intratendinous signal alterations are sometimes ambiguous due to irregularity and ill-defined, poorly limited demarcation of lesion in the tendon.
Evidently, measurements of tendon volume and intratendinous signals using the 3-D seed-growing technique can facilitate the estimation of the severity of tendinosis and the following-up of the healing process in chronic Achilles tendinosis (26). Furthermore, the intratendinous signal changes may be indicators of the blood flow (or vascularization) in the tendon.
Inside the tendon, collagen fibers and fiber bundles are enclosed in the endotenon, which serves to carry blood vessels, lymphatics, and nerves (24). These portions of the tendon, provided by the paratenon, may allow for intratendinous gliding and may therefore play a role in coping with intratendinous shear forces during loading.
The Achilles tendon receives its blood supply in three regions: at musculotendinous junction, along its whole length and in the region of insertion, and at the bone–tendon junction (8). Anteriorly, the tendon is attached to a richly vascularized tissue, where vessels can enter the tendon. These vessels are considered the most important ones to the Achilles tendon (6). Human data suggest that the blood flow during rest is evenly distributed in healthy Achilles tendons (4). However, chronic Achilles tendinosis is associated with increased blood flow in the painful region (4). Öhberg et al. (22) studied Achilles tendinosis with gray-scale ultrasonography combined with color Doppler examination. Neovascularization was seen in the area with tendon changes in all tendons with a painful nodule but was lacking in the normal pain-free tendons. The vascularized area seen by the color Doppler technique disappeared when the tendon was tensed, suggesting a valve mechanism (22).
The blood flow associated with the tendon increases up to sevenfold during exercise, independent of age of the individual (7,16). It has further been observed that the blood flow around the tendon during exercise only reaches 20% of maximal blood-flow capacity observed during reactive hyperemia (7). These data suggest that the Achilles tendon blood flow may be remarkably low during rest. The alterations of Achilles tendon blood flow during and immediately after eccentric training may thus contribute to the observed increased tendon volume and altered tendon composition.
The fibrillar collagen is embedded in a hydrophilic extracellular matrix consisting of proteoglycans and glycoproteins. The noncollagenous extracellular matrix contributes in important ways to the mechanical integrity of the tendon. Proteoglycans are complex macromolecules consisting of a protein core with at least one glycosaminoglycan (GAG) chain, such as dermatan sulfate, chondroitin sulfate and heparan sulfate. Large proteoglycans like versican and aggrecan provide mechanical support and are strongly hydrophilic, thereby attracting osmotically active cations, forcing water into the matrix, and also enabling rapid diffusion of water soluble molecules and migration of cells. The GAG may trap water in amounts as much as 50 times their own weight (32). Increased amounts of GAG are, along with increased vascularity and altered fiber structure and arrangement, the characteristic morphological features in chronic Achilles tendinosis (21). In healthy Achilles tendons, the amounts of GAG are low within the tendon itself, higher in the paratenon. The water binding potential of the proteoglycans appears to be a major factor in bringing about the immediately increased tendon volume and increased tendon signal in the Achilles tendon after eccentric strength training. However, the pathologic amounts of GAG, commonly found in symptomatic tendinosis tissue, did not affect the immediate physiologic tendon response to loading compared with the asymptomatic concentrically trained tendons as the response was of similar magnitude in our study.
The fibroblasts of the tendons synthesize and maintain several elements of the extracellular matrix, including collagens, proteoglycans, and other proteins. It appears that the proliferative response of fibroblasts is under the influence of mechanical strain (18).
It is interesting to speculate over how the acute response to training involving increased tendon volume (and increased cross-sectional area) at exercise affects the biomechanics of the tendon. In terms of force transfer, a thick tendon may be advantageous, as there would be a decrease of the average force per area, thereby lessening the potential risk for injury. However, this may only be adequate if the water retaining capacity of the noncollagenous matrix contributes to the mechanical properties. Further, fluid may act as a lubricant at the endotenon, thereby reducing the intratendinous shear forces.
In conclusion, eccentric and concentric training resulted in increased total tendon volume and intratendinous signal in the Achilles tendon. This may be explained by increased water content and/or vascular hyperemia in the Achilles tendon during and/or immediately after strength training of the gastrocnemius-soleus complex.
It is thus important to standardize the training activity before MRI examinations, when MRI is used to evaluate the effect of treatment on the Achilles tendon.
1. Alfredson, H., T. Pietila, P. Jonsson, and R. Lorentzon. Heavy-load eccentric calf muscle training for the treatment of chronic Achilles tendinosis. Am. J. Sports Med
. 26:360–366, 1998.
2. Åström, M. On the nature and etiology of chronic Achilles tendinopathy. PhD thesis. Lund University, Sweden, 1997.
3. Åström, M., and A. Rausing. Chronic Achilles tendinopathy: a survey of surgical and histopathologic findings. Clin. Orthop
. 316:151–164, 1995.
4. Åström, M., and N. Westlin. Blood flow in chronic Achilles tendinopathy. Clin. Orthop
. 308:166–172, 1994.
5. Banes, A. J., G. Horesovsky, C. Larson, et al. Mechanical load stimulates expression of novel genes in vivo and in vitro in avian flexor tendon cells. Osteoarthritis Cartilage
6. Barfred, T. Achilles tendon rupture: aetiology and pathogenesis of subcutaneous rupture assessed on the basis of the literature and rupture experiments on rats. Acta Orthop. Scand. Suppl
. 152:3–126, 1973.
7. Boushel, R., H. Langberg, S. Green, D. Skovgaard, J. Bulow, and M. Kjaer. Blood flow and oxygenation in peritendinous tissue and calf muscle during dynamic exercise in humans. J. Physiol
. 524(Pt. 1):305–313, 2000.
8. Carr, A. J., and S. H. Norris. The blood supply of the calcaneal tendon. J. Bone Joint Surg. Br
. 71:100–101, 1989.
9. Clement, D. B., J. E. Taunton, and G. W. Smart. Achilles tendinitis and peritendinitis: etiology and treatment. Am. J. Sports Med
. 12:179–184, 1984.
10. James, S. L., B. T. Bates, and L. R. Osternig. Injuries to runners. Am. J. Sports Med
. 6:40–50, 1978.
11. Karjalainen, P. T., H. J. Aronen, H. K. Pihlajamaki, K. Soila, T. Paavonen, and O. M. Bostman. Magnetic resonance imaging during healing of surgically repaired Achilles tendon ruptures. Am. J. Sports Med
. 25:164–171, 1997.
12. Khan, K. M., and J. L. Cook. Overuse tendon injurers: where does the pain come from? Sports Med. Arthroscopy
13. Khan, K. M., P. J. Visentini, Z. S. Kiss, et al. Correlation of ultrasound and magnetic resonance imaging with clinical outcome after patellar tenotomy: prospective and retrospective studies. Victorian Institute of Sport Tendon Study Group. Clin. J. Sport Med
. 9:129–137, 1999.
14. Khan, K. M., and N. Maffulli. Tendinopathy: an Achilles “heel” for athletes and clinicians. Clin. J. Sport Med
. 8:151–154, 1998.
15. Kvist, H., and M. Kvist. The operative treatment of chronic calcaneal paratenonitis. J. Bone Joint Surg. Br
. 62:353–357, 1980.
16. Langberg, H., L. Rosendal, and M. Kjaer. Training-induced changes in peritendinous type I collagen turnover determined by microdialysis in humans. J. Physiol
. 534:297–302, 2001.
17. Langberg, H., D. Skovgaard, L. J. Petersen, J. Bulow, and M. Kjaer. Type I collagen synthesis and degradation in peritendinous tissue after exercise determined by microdialysis in humans. J. Physiol
. 521(Pt. 1):299–306, 1999.
18. Mackenna, D., S. R. Summerour, and F. J. Villarreal. Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis. Cardiovasc. Res
. 46:257–263, 2000.
19. Mafi, N., R. Lorentzon, and H. Alfredson. Superior short-term results with eccentric calf muscle training compared to concentric training in a randomized prospective multicenter study on patients with chronic Achilles tendinosis. Knee Surg. Sports Traumatol. Arthrosc
. 9:42–47, 2001.
20. Magnusson, S. P., P. Hansen, and M. Kjar. Tendon properties in relation to muscular activity and physical training. Scand. J. Med. Sci. Sports
21. Movin, T., A. Gad, F. P. Reinholt, and C. Rolf. Tendon pathology in long-standing achillodynia: biopsy findings in 40 patients. Acta Orthop. Scand
. 68:170–175, 1997.
22. Öhberg, L., R. Lorentzon, and H. Alfredson. Neovascularization in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg. Sports Traumatol. Arthrosc
. 9:233–238, 2001.
23. Puddu, G., E. Ippolito, and F. Postacchini. A classification of the Achilles tendon disease. Am. J. Sports Med
. 4:145–150, 1976.
24. Schatzker, J. and P. I. Brånemark. Intravital observations on the microvascular anatomy and microcirculation of the tendon. Acta Orthop. Scand. Suppl
. 126:1–23, 1969.
25. Selvanetti, A., M. Cipolla, and G. Puddu. Overuse Tendon Injuries: Basic Science and Classification
. 5:110–117, 1997.
26. Shalabi, A., M. Kristoffersen-Wiberg, L. Svensson, P. Aspelin, and T. Movin. Eccentric training of the gastrocnemius-soleus complex in chronic Achilles tendinopathy results in decreased tendon volume and intratendinous signal as evaluated by MRI. Am. J. Sports Med
. 32:1286–1296, 2004.
27. Shalabi, A., M. Kristoffersen-Wiberg, P. Aspelin, N. Papadogiannakis and T. Movin. Dynamic contrast-enhanced MR imaging and histopathology in chronic Achilles tendinosis: a longitudinal MR study of 15 patients. Acta Radiologica
28. Shalabi, A., M. Kristoffersen-Wiberg, P. Aspelin, and T. Movin. MR evaluation of chronic Achilles tendinosis: a longitudinal study of 15 patients preoperatively and two years postoperatively. Acta Radiologica
29. Shalaby, M., and L. C. Almekinders. Patellar tendinitis: the significance of magnetic resonance imaging findings. Am. J. Sports Med
. 27:345–349, 1999.
30. Silbernagel, K. G., R. Thomee, P. Thomee, and J. Karlsson. Eccentric overload training for patients with chronic Achilles tendon pain–a randomized controlled study with reliability testing of the evaluation methods. Scand. J. Med. Sci. Sports
31. Stanish, W. D., R. M. Rubinovich, and S. Curwin. Eccentric exercise in chronic tendinitis. Clin. Orthop
. 208:65–68, 1986.
32. Wolfe, S. L. Molecular and Cellular Biology
. Belmont, CA: Wadsworth Publishing Co., 1993, pp. 274–287.