Medicine & Science in Sports & Exercise:
Clinical Sciences: Clinical Investigations
Immediate Achilles Tendon Response after Strength Training Evaluated by MRI
SHALABI, ADEL1; KRISTOFFERSEN-WIBERG, MARIA1; ASPELIN, PETER1; MOVIN, TOMAS2
1Department of Radiology and 2Department of Orthopedic Surgery, Huddinge University Hospital, Karolinska Institute, Stockholm, SWEDEN
Address for correspondence: Adel Shalabi, M.D., Ph.D., Center for Surgical Sciences, Division of Radiology, Huddinge University Hospital, SE-14186 Stockholm, Sweden; E-mail: firstname.lastname@example.org.
Submitted for publication November 2003.
Accepted for publication July 2004.
Purpose: To evaluate the tendon response after acute strength training in chronic Achilles tendinosis using magnetic resonance imaging (MRI).
Methods: Twenty-two patients (44 Achilles tendons, 15 males, 8 patients with bilateral symptoms) with a median age of 45 yr (range 28–57 yr) were included in the study. In all patients, both Achilles tendons were examined with MRI before and immediately after a standardized training program. The most painful side underwent 6 sets and 15 repetitions of heavy-loaded eccentric training. The contralateral tendons underwent only concentric loading during the training program. The tendon volume and the intratendinous signal were evaluated and calculated by MRI using a seed-growing technique.
Results: The immediate response of eccentric loading on the symptomatic tendons resulted in a 12% increase of the tendon volume, evident on T2-WI, from 7.8 ± 2.0 to 8.8 ± 2.7 cm3 (P < 0.001), and a 31% increase of the intratendinous signal evident on PD-WI, from 221 ± 74 to 278 ± 78 signal units (SU) (P < 0.001). The corresponding sequences on the contralateral concentrically loaded tendons showed an increase of 17% of tendon volume, from 6.1 ± 1.5 to 7.0 ± 1.6 cm3 (P < 0.001), and an increase of 27% of the intratendinous signal, from 170 ± 55 to 211 ±57 SU (P < 0.001). There was no significant difference of the mean of the increased tendon volume and the intratendinous signal between the eccentrically heavily loaded symptomatic tendons and the concentrically loaded contralateral tendons.
Conclusions: Both eccentric and concentric loading of the Achilles tendon resulted in increased total tendon volume and intratendinous signal. This increase may be explained by a higher water content and/or hyperemia in the Achilles tendon during and/or immediately after strength training of the gastrocnemius-soleus complex.
The incidence of overuse injury in sports has risen enormously during the last three decades (25). The causes of Achilles tendinopathy remain unclear (2). Various theories link tendinopathies to overuse stresses, poor vascularity, lack of flexibility in genetic makeup, sex, and endocrine or metabolic factors (14). Excessive repetitive overload of the Achilles tendon is regarded as the main pathological stimulus leading to tendinopathy (2). Chronic pain in the Achilles tendon region (achillodynia) is commonly seen in athletes (9,10,15), but also in individuals with a low physical activity level (3,21).
The Achilles tendon may respond to repetitive overload beyond the physiological threshold by either inflammation of its sheath, or degeneration of its body, or by a combination of the two (23). Eccentric strengthening of the gastrocnemius-soleus muscle and loading of the Achilles tendon has been effective in the conservative management of chronic Achilles tendinosis (1,19,30,31). Nonsurgical treatment with heavy-load eccentric calf muscle strength training of patients with chronic Achilles tendinosis gave very good clinical results and markedly reduced the need for surgical treatment (1). However, there is an almost complete lack of knowledge on mechanisms involved in physiologic tendon response to strength training (12,20).
Recently, we reported that daily eccentric calf muscle strength training in patients with chronic Achilles tendinosis resulted in both decreased tendon volume and intratendinous MR signal, and was correlated to improved clinical outcome (26). Tendon cells communicate their response to mechanical loading by up-regulation of the gene expression important for the synthesis of the collagen protein (5). The aim of the present study was to evaluate the immediate tendon response (change in tendon volume and intratendinous signal intensity) after acute strength training of the gastrocnemius-soleus complex in patients with chronic Achilles tendinosis by the aid of MRI.
A total of 22 patients (44 Achilles tendons, 15 males and 7 females) with clinical diagnosis of chronic Achilles tendinosis were included in the study. All patients were referred to our orthopedic university clinic by either general practitioners or by orthopedic surgeons. They ranged in age from 28 to 57 yr (median 45 yr). All patients had pain, swelling, and local tenderness at palpation of the mid-portion of the Achilles tendon, 2–7 cm proximal to the tendon insertion. The contralateral Achilles tendons, eight of which were symptomatic, only underwent concentric loading during the training program. Thus, in total, there were 30 symptomatic and 14 asymptomatic tendons. These were divided into four overlapping groups (Table 1).
The prescribed treatment was 3 months of eccentric calf muscle strength training program according to the model developed by Alfredson et al. (1). Approximately 1 wk before the examination by MRI, the patients visited the physiotherapy unit and obtained instructions for the eccentric training program, and fulfilled the exercises under the supervision of a physiotherapist. Eccentric loading of the calf was done with the knee in straight and bent positions. The symptomatic tendons underwent 3 sets and 15 repetitions of heavy-loaded eccentric training in each knee position. The patient's body weight alone was used in the eccentric protocol.
The contralateral side was not specifically trained and underwent only standardized concentric loading during the training program (when the body was elevated by bilateral calf muscle contraction to the tip-toe position) (Fig. 1). In all patients, both Achilles tendons were investigated with MRI before and immediately after the heavy-loaded eccentric training program on the symptomatic side. The exercises were made within 30 min after the examination at the MR unit, and the patients were reexamined immediately after with a second MRI. The ethics committee at the Karolinska Institute approved the study, and the patients were informed of the procedures before giving their written consent.
The MRI examinations were performed with a Magnetom Vision (Siemens) using a commercially available CP flexible 21 × 52-cm coil for all patients. Both Achilles tendons were examined simultaneously.
The images were obtained with the patient in a supine position and the feet kept in a resting position in the coil with a maximum plantar flexion of 15°. The slice thickness was 3 mm, with a 0.3-mm gap in all sequences. The following sequences were performed in all cases: Sagittal FLASH 2 D-weighted spin-echo: TR/TE 460/10 ms, 2 acquisitions (acq), time of acquisition (TA) 6.19 min, field of view (FOV) 180 mm, 410 × 512 matrix. Sagittal PD/T2-weighted turbo spin-echo: TR/TE 3500/17 and 119, 1 acq, TA 4.48 min, FOV 180 mm, 400 × 512 matrix) were done. All the three sequences mentioned above were repeated within 30 min of completing the training program.
The volume of the Achilles tendon was evaluated at a distance of 2–12 cm proximal to the tendon insertion in the symptomatic, and the contralateral tendon and was calculated in all sagittal sequences. Seven consecutive sagittal slices formatted as 512 × 512 matrices were used to cover each tendon. The pixel size was 0.35 × 0.35 mm2 and the slice to slice distance 3.3 mm, giving a voxel volume of 0.35 × 0.35 × 3.3 mm3. The volume of each tendon was masked using a seed-growing technique on a Hermes work station (Nuclear Diagnostics, Sweden). The data set was preprocessed by depicting the 10-cm interval and masking it to give a 3-D region, including the tendon of interest. A seed was manually marked well within the tendon; the seed-growing algorithm automatically marked the tendon volume. In some tendons, the algorithm leaked out into the surrounding tissue. If this occurred, the tendon had to be manually masked. The region grown with this algorithm was used as a binary mask when data for the tendon were extracted from the original data set. The volume of the tendon was calculated by summing all voxels within the tendon and multiplying with the size of the voxel volume. The mean signal of all tendons was estimated from the masked volume (Fig. 2).
FIGURE 2Sagittally m...Image Tools
This method in evaluation of MRI using a 3-D seed-growing technique showed excellent inter- and intraobserver reliability in measuring the total volume and mean intratendinous signal (26). The same radiologist interpreted all the MRI studies.
Variables of continuous and ordinal types are presented as a mean and standard deviation. Student's t-test was used to compare tendon volume and intratendinous signal on MRI examinations before and after the training program. Confidence intervals were used for giving the difference between means of the symptomatic eccentric heavy-loaded tendon and the concentric loaded contralateral side. A P value of <0.05 was considered statistically significant.
Our main finding is a significant increase in both total tendon volume and intratendinous signal in all MRI sequences, immediately after eccentric and concentric strength training of the gastrocnemius-soleus complex (P < 0.001; Figs. 3 and 4).
The immediate response to eccentric training on the symptomatic tendons (group A) was a 12% increase of the total tendon volume, measured on T2-WI, from 7.8 ± 2.0 to 8.8 ± 2.7 cm3 (P < 0.001), and a 31% increase of the intratendinous signal, measured on PD-WI, from 221 ± 74 to 278 ± 78 signal units (SU) (P < 0.001) (Figs. 2 and 5). The corresponding sequences on the contralateral concentrically loaded tendons (group B) showed an increase of 17% of the total tendon volume, from 6.1 ± 1.5 to 7.0 ± 1.6 cm3 (P < 0.001), and an increase of 27% of the intratendinous signal, from 170 ± 55 to 211 ± 57 SU (P < 0.001).
FIGURE 5Sagittal PD-...Image Tools
There was no significant difference in the mean increased tendon volume and intratendinous signal (95% confidence interval) between the eccentric and concentric loaded tendons measured at different MR pulse sequences (Tables 2A and 2B). The total tendon volume measured on T2-WI and intratendinous signal on PD-WI of the 30 symptomatic Achilles tendons (group C) increased 12% (from 7.5 to 8.4 cm3, P < 0.001) and 29% (from 209 to 262 SU, P < 0.001), respectively. The corresponding values of the 14 asymptomatic tendons (group D) increased in the order of 20% (from 5.8 to 6.8 cm3, P < 0.001) regarding total volume, and 29% (from 165 to 212 SU, P < 0.001) for the intratendinous signal, respectively (Table 3A and B). Although the percentage increase was greater in the concentric group, the absolute value of the increase in both variables was similar in both groups. This may merely reflect the greater starting volume of the symptomatic tendons.
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.
Pathophysiology behind volume and signal intensity changes.
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).
Langberg et al. (17) have found that the human peritendinous Achilles tendon tissue reacts with a reduced collagen synthesis immediately after exercise, followed by a dramatic increase in subsequent days (17). However, the changes occurring immediately after strength training observed in the present study cannot be explained by metabolic effects.
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.
ACHILLES TENDON; ECCENTRIC TRAINING; CONCENTRIC TRAINING; MRI; TOTAL TENDON VOLUME; INTRATENDINOUS SIGNAL
©2004The American College of Sports Medicine
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