The Ability of Ultrasonography, Magnetic Resonance Imaging and Bone Mineral Densitometry to Predict the Strength of Human Achilles' Tendons

Article Outline

• Abstract
• Methods
  • Subjects
  • Ultrasonography
  • Magnetic Resonance Imaging
  • Bone Mineral Density
  • Mechanical Properties
  • Data Analysis
• Results
  • Ultrasonography and Magnetic Resonance Imaging
  • Bone Mineral Density
  • Mechanical Testing
• Discussion
  • Study Limitations
• Conclusions
• Acknowledgments
• References
• Copyright

Abstract 

Devitt D, Koike Y, Doherty GP, Ramachandran N, Dinh L, Uhthoff HK, Lecompte M, Trudel G. The ability of ultrasonography, magnetic resonance imaging and bone mineral densitometry to predict the strength of human Achilles' tendons.

Objective

To assess the value of ultrasonography (US), magnetic resonance imaging (MRI), and bone mineral densitometry (BMD) in evaluating human Achilles' tendon strength.

Design

Cross-sectional observational study.

Setting

Tertiary care hospital.

Participants

Ninety-eight Achilles' tendons from 49 consecutive cadavers (26 men and 23 women with a mean age of 66.6 years) undergoing hospital autopsy were assessed.

Interventions

Not applicable.

Main Outcome Measures

Tendon dimensions on US and MRI, and T1-weighted optical density were measured. Areas of hypodensity, hyperdensity, calcification, and heterogeneity were identified on US. The BMD of each calcaneus was recorded. The tendons were mechanically tested to determine peak load at failure.

Results

Sixteen patients (32.7%, 27 tendons) had abnormalities in 1 or both tendons on US and/or MRI (17 on US, 17 on MRI). Fifty-seven tendons (58%) ruptured in their midsubstance, at an average peak load of 4722±990N. Tendons with and without abnormalities on imaging had similar strengths (P>.05). Calcaneal BMD correlated weakly with peak load at failure (r=.21, P<.05).

Conclusions

The prevalence of Achilles' tendons abnormalities on US or MRI was 32.7% in our study group. Abnormalities on clinical imaging (US or MRI) were not predictive of the load at failure. Therefore, tendons with imaging abnormalities are not necessarily weaker, and one cannot predict the likelihood of rupture based on imaging results. Further, higher-powered studies could explore the ability of BMD to detect minimal clinically important differences and to predict Achilles' tendon weakness.

Key Words: Achilles tendon, Bone density, Magnetic resonance imaging, Rehabilitation, Ultrasonography

List of Abbreviations: AP, anterior-posterior, BMD, bone density, MRI, magnetic resonance imaging, US, ultrasonography

CHRONIC ACHILLES' tendinopathy can affect both athletes and people with sedentary lifestyles who perform leisure athletic activities.¹ It is usually caused by tendinosis, which can be complicated by partial rupture.² When a complete rupture occurs, the Achilles' tendon usually fails 2 to 6cm proximal to its insertion on the tuberosity of the calcaneus.² Whether there is a role for clinical imaging in assessing Achilles' tendon strength and risk of rupture needs to be clarified.³ Demonstrating a relationship between abnormalities on clinical imaging and mechanical strength of Achilles' tendons could allow such markers to predict the health of tendons and guide investigations, rehabilitation, and return to work after a tendon injury.

The traditional role of imaging in clinical practice has included diagnosis and monitoring of clinical progress.³ Both US and MRI are frequently used for this purpose. US is an accurate, safe, and cost-effective method of assessing Achilles' tendons.⁴, ⁵, ⁶, ⁷ It is readily available, even in some clinics, and can provide dynamic real-time information. Its sensitivity and specificity for detecting tendon abnormalities (compared with the criterion standard of clinical symptoms) have been reported at 80% and 76%, respectively.⁸ Abnormalities detected on US include an increase in the AP diameter of the tendon, a spindlelike rounded appearance, discontinuity of fibers, focal hypoechoic and hyperechoic areas, calcifications, and microcalcifications.⁶, ⁹ These changes may be related to a poorer prognosis, because Nehrer et al¹⁰ found that 9 of 33 (28%) Achilles' tendons with thickening and intratendinous hypoechoic lesions went on to rupture spontaneously, whereas none of the 39 Achilles' tendons without thickening and hypoechoic lesions did. However, in a study by Khan et al³ US could not differentiate between cases that would improve and those that would worsen.

When US is indecisive, MRI is often recommended.¹¹ Its sensitivity and specificity for detecting tendon abnormalities (with histology as the criterion standard) were better than those of US, at 94% and 81%, respectively.², ¹² One study showed that MRI changes at baseline were associated with clinical symptoms of Achilles' tendinopathy 12 months later.³ However, MRI studies have shown significant overlap in Achilles' tendon abnormalities between symptomatic and asymptomatic patients.¹², ¹³ At this point, clinicians are cautioned to exercise discretion in ordering imaging to monitor progress or determine readiness to return to sport in chronic Achilles' tendon disorders because both US and MRI commonly have false-positive results.³

BMD is another imaging modality that can possibly be used in Achilles' tendinopathy. BMD of the calcaneus has been related to physical activity. Heinonen et al¹⁴ demonstrated higher calcaneal BMD values in women athletes than in sedentary women. The increased ground reaction forces and the increased tensile pull of the Achilles' tendon with activity may be responsible for this increased BMD. It is unknown whether BMD of the calcaneus is related to Achilles' tendon strength. In 1 study on middle-age recreational athletes with unilateral Achilles' tendinopathy, improved calf muscle strength from an eccentric exercise program was not related to BMD of the calcaneus.¹⁵

Our primary objective was to determine the potential of clinically available imaging (US, MRI, BMD) to predict the tensile strength, stiffness, and stress of human Achilles' tendons. We hypothesized that tendons with abnormalities on imaging would rupture at a lower peak load. The secondary objectives were to characterize the demographics and anthropometric and radiologic features on US and MRI of a sample of human Achilles' tendons in an older population.

Back to Article Outline

Methods 

The protocol for these experiments was approved by the University Hospital Ethics Committee.

Subjects 

We harvested a convenience sample of 98 Achilles' tendons from 49 consecutive cadavers undergoing hospital autopsy. Demographics and diagnoses were recorded, but clinical information on Achilles' tendon pain or pathology was unavailable. Each Achilles' tendon-calcaneus unit was harvested, wrapped in gauze, moistened in saline solution without fixation, and stored at –13°C in double airtight plastic bags until imaging was performed. The tendons were thawed, imaging was performed in series, and the tendons were frozen again. The tendons were thawed a second time for biomechanical testing.

Ultrasonography 

Axial images of the Achilles' tendons were obtained at 5-mm intervals, starting at the calcaneal insertion and proceeding proximally to the musculotendinous junction, approximately 20cm proximal to the calcaneus, with an HDI 5000 ultrasound unit and compact linear array 10-5 MHz transducer.^a Three sagittal images, at the medial, mid, and lateral aspects of the tendon, were obtained with a linear array 12-5 MHz 50-mm transducer. Maximal AP dimensions of the Achilles' tendon were measured. Tendon ultrasound abnormalities were defined as focal hypoechoic or hyperechoic areas, calcifications, microcalcifications, or heterogeneity.

Magnetic Resonance Imaging 

The tendons were aligned and imaged in groups of 6 in a specially designed saline-filled waterproof box. MRI was performed using a Symphony 1.5-T unit and its extremity coil.^b T1-weighted optical density was read from axial T1-weighted spin-echo (repetition time=513; echo time=12; field of view=130mm; matrix=512×512; number of excitations=2; slice thickness=3mm) and sagittal T1-weighted spin-echo (repetition time=615; echo time=12; field of view=130mm; matrix=512×512; number of excitations=2, slice thickness=3mm).

On the sagittal images, we measured the maximal AP diameter of the Achilles' tendon (which occurred 2–7cm proximal to the calcaneus). Separate axial images at 21mm, 45mm, and 69mm proximal to the calcaneal insertion were exported and used to measure cross-sectional areas (Image J processing program, version 1.32j). Tendon MRI abnormalities were defined as focal areas of high signal intensity.

Bone Mineral Density 

BMD of the calcaneus was measured using a DPX-alpha dual energy x-ray absorptiometer.^c Each specimen was placed in a container filled with raw rice simulating the soft tissue density. The x-rays were directed from medial to lateral aspects of the calcaneus. The BMD of the tuberosity of the calcaneus, the body of the calcaneus, and the whole calcaneus was measured with software adapted for small bone.^d All measurements were performed by a single experienced nuclear medicine technologist.

Mechanical Properties 

To test the Achilles' tendon mechanically, we used a dual cryogenic fixation assembly and Sintech 1/G material testing machine^e and followed our published protocol.¹⁶ A 2-cm length of Achilles' tendon proximal to calcaneal insertion was placed into the saline-filled ice container of the top cryo-assembly and was frozen by pouring liquid nitrogen into the surrounding nitrogen container. This allowed the distal end to be gripped securely when ice formed around the tendon. The top cryo-assembly was then mounted onto the top moving crosshead of the testing machine. A similar freezing procedure was repeated with the proximal end of the Achilles' tendon (7cm proximal to the tendon insertion) using the bottom cryo-assembly fixed to the base of the testing machine. The tendon test length in between the 2 cryo-assemblies was 5cm. Two semicircular heaters were placed around the tendon to ensure that they were tested at 37°C. A layer of petroleum jelly was applied to the exposed tendon to prevent dehydration. Ten preconditioning cycles were conducted to a peak load of 1500N and a loading rate of 296N/s to straighten the collagen fibers. The tendon was then loaded at an elongation rate of 4mm/s until a 50% decrease from peak load was detected. The load and crosshead displacement data were recorded at 100Hz. The outcome measures of interest included peak load reached by the tendon before rupturing, and stiffness and stress measured with TestWorks.^f Stiffness was calculated by fitting a linear regression line to the load displacement data between 30% and 90% of the peak load.

Data Analysis 

We used SPSS 11.5.0 for Windows^g to constitute the database and for statistical analysis. All data are presented as means ± 1SD. Outcome measures were AP diameter on MRI and US; cross-sectional area 45mm proximal to tendon insertion on MRI; T1-weighted optical density on MRI; and bone mineral densitometry of the whole calcaneus, body of calcaneus, and tuberosity of calcaneus. Both the AP diameters on MRI and US and the AP diameters of the tendons with and without abnormalities on imaging were compared with t tests. The t tests compared the BMD at the body of the calcaneus, tuberosity of the calcaneus, and whole calcaneus. The t tests were performed for each imaging outcome measure between tendons that ruptured in the midsubstance (n=57) and tendons for which the cryogenic fixation failed (n=41). The t tests compared the mechanical properties of the tendons with and without abnormalities on imaging. We performed simple linear regressions between the mechanical properties of the tendons that failed at midsubstance and the subject demographic variables and imaging outcome measures. A P value <.05 was considered statistically significant.

Back to Article Outline

Results 

The tendons were obtained from 26 men and 23 women with a mean age of 66.6 years (range=30–89y). Their demographic data are shown in table 1. Sixteen patients (27 tendons) had abnormalities on US, MRI, or both, giving a point prevalence of 32.7%. Seven tendons (7%) had imaging abnormalities on both US and MRI. Eleven of 16 patients had abnormalities in bilateral tendons, while 5 of 16 had abnormalities unilaterally.

Table 1. Demographic Characteristics and Cause of Death of the 49 Subjects

Variable	Mean (Range)
Age (y)	66(30–89)
Weight (kg)	79(48–127)
Height (cm)	168(149–188)

Ultrasonography and Magnetic Resonance Imaging 

Seventeen tendons showed abnormalities on US. Of these, 11 had hypodensities within the tendon substance, 5 had calcifications, 3 contained hyperdensities, and 2 contained diffuse heterogeneity. The mean AP diameter of the tendons with abnormalities was significantly larger than that of the tendons without abnormalities (8.2±2.7mm vs 6.6±0.8mm; P<.05).

The mean maximal AP diameter on MRI was similar to the value on US (table 2). Seventeen tendons had an increased signal on T1-weighted spin-echo imaging, and these tendons were not exactly the same 17 that had abnormalities on US. There were no statistically significant differences between tendons with and without abnormalities for AP diameter on MRI or cross-sectional area.

Table 2. AP Diameter, Cross-Sectional Area, and BMD of Tendons With Midsubstance Ruptures and Tendons for Which the Cryogenic Fixation Failed

Bone Mineral Density 

The mean BMD of the tuberosity was significantly greater than that of the whole calcaneus, which was greater than that of the body of the calcaneus (both P values <.05) (see table 2). There were no statistically significant differences between tendons with and without abnormalities for BMD at all 3 sites.

Mechanical Testing 

Forty-one tendons failed at the site of cryogenic fixation and were excluded from the mechanical analyses. The remaining 57 tendons failed in the midsubstance, between 3.4 and 5.6cm from the calcaneal insertion. Of the 57, US identified 8 with abnormalities, and MRI identified 9 with abnormalities. The mean peak load, stiffness, and stress of the tendons with abnormalities on US or MRI were not significantly different from those of the tendons without abnormalities (all P values >.05) (fig 1).

• 
  • View Large Image
  • Download to PowerPoint

• Fig 1. 

  Mechanical properties of human Achilles' tendons with and without abnormalities on US and MRI.

There was a single predictor of decreased tendon strength: BMD of the body of the calcaneus was correlated with peak load of the tendon (r=0.21, P<0.05) (fig 2). None of the demographic variables (age, sex, weight, height) or the US or MRI outcome measures correlated with peak load at failure (all P values >.05) (table 3). Stiffness of the tendon increased with increasing subject age (r=.32, P<.05). Stress was greater in the tendons from women than in those from men (P<.05).

• 
  • View Large Image
  • Download to PowerPoint

• Fig 2. 

  BMD of body of calcaneus correlated with the peak load at failure of human Achilles' tendons (r=.21; P<.05, n=57).

Table 3. Linear Regressions Between Demographic and Imaging Data, and Mechanical Outcome Measures

Back to Article Outline

Discussion 

Contrary to our hypothesis, we found that an abnormality on clinical imaging did not predict lower strength of the Achilles' tendon and, by extension, did not predict a higher likelihood of rupture. We therefore concluded that imaging with MRI and US would not be useful to detect Achilles' tendon weakness or evaluate the risk of tendon tear or rupture in an older population.

An Achilles' tendon must be weakened in order to rupture. Excessive forces applied to the foot in plantar flexion will lead to avulsion fracture of the calcaneus or tear of the gastrocnemius-soleus muscle, both of which have shown weaker tensile strength than a normal Achilles' tendon.², ⁶, ¹³, ¹⁷ As well, Moller et al¹⁸ found no correlation between clinical muscle strength and US or MRI findings during healing in 58 patients with Achilles' tendon rupture.

Five groups of researchers have mechanically tested human Achilles' tendons.¹⁹, ²⁰, ²¹, ²², ²³, ²⁴ The mean peak loads are 1189N, 4119N, 6072N, 4371N, and 4805N. The lower loading rate in the study by Louis-Ugbo et al¹⁹ may explain their lower peak load. The peak load data in our study and in the remainder of these studies are valid because the peak loads are greater than the calculated loads required for jumping and hopping (2233N and 3786N, respectively²⁵).

Besides the peak load recorded at failure, the mode of failure is important to derive the mechanical properties of Achilles' tendons. While midsubstance failures provide direct information on tendon properties, clamp failures or bone avulsions do not. As such, we examined the 57 midsubstance ruptures in more detail. These constitute the largest series of mechanically tested human Achilles' tendons available for generalizing to clinical situations.

In clinical practice, after an acute Achilles' tendon injury, imaging is warranted to assess for a rupture that may need surgical repair. Short of a rupture, our results suggest the clinical relevance of imaging abnormalities is limited. Whether the abnormalities preceded or coincided with the symptoms is difficult to ascertain. In chronic Achilles' tendinopathy, our results suggest that neither US nor MRI indicates whether the tendon is at higher risk of rupture than a healthy tendon. Furthermore, the rehabilitation process should be guided by clinical signs and symptoms, because imaging cannot predict weakness.

In this group with a mean age of 66 years, there was a point prevalence of 32.7% for tendon abnormalities on imaging. We found no previous data on Achilles' tendinopathy in this age group but did find a similarly high prevalence of 30% tendon degeneration in asymptomatic younger subjects (mean age=44y).⁴ These results suggest no increase in the prevalence of Achilles' tendinopathy with aging. A high prevalence of abnormalities in tendons with normal strength might represent a chronic stable postinjury status. We found no significant correlation between the abnormalities on imaging and tendons dimensions.

We found a weak but positive correlation between tendon strength and BMD of the body of the calcaneus. This correlation had also been reported by Wren et al²², ²³ in 22 human Achilles' tendons. Lower calcaneal BMD may indicate decreased ground reaction forces during walking or less pull of the Achilles' tendon on the calcaneal tuberosity from gastrocnemius-soleus muscle disuse or Achilles' tendon weakness.

BMD at both the tuberosity (cortical bone) and the body (trabecular bone) of the calcaneus correlated with Achilles' tendon strength. This suggests a generalized effect of limb disuse as opposed to a localized decreased pull from the Achilles' tendon. Disuse would influence negatively both the calcaneus and the Achilles' tendon. BMD has been shown to detect a difference of 0.03g/cm² in the calcaneus.²⁶ In our study, a decrease of 0.6g/cm² corresponded to a decrease in peak load of the tendons of 1000N (20%), which is clinically significant. Further study is warranted to determine whether low calcaneal BMD, correlating with a weaker Achilles' tendon, predisposes to increased severity or duration of symptoms and tear/rupture. If so, a finding of low calcaneal BMD would warrant restriction of the patient from certain activities and might also be used to monitor recovery.

Size of the tendon has been used to comment on the integrity of the Achilles' tendon. Although normative data have not been obtained systematically, a few investigators suggested that an Achilles' tendon AP diameter 2mm larger than contralateral or greater than 6mm signifies disease.², ¹², ¹³, ²⁷ The mean AP diameter in our study was 6.9mm and did not correlate with peak load or with abnormalities on imaging. Louis-Ugbo et al¹⁹ also reported no correlation between cross-sectional area and ultimate strength of the Achilles' tendon. It has also been suggested that age increases Achilles' tendon size in humans and animals.²⁸, ²⁹ However, there was no correlation in our study or in the studies by Narici and Maganaris²⁸ and Louis-Ugbo et al¹⁹ between increasing Achilles' tendon dimensions and increasing age. Interestingly, frequent exercise also increases the cross-sectional area of Achilles' tendons.¹⁹ The subjects in our study were not likely to have been training regularly, making exercise an unlikely confounding variable. Therefore, the definition of disease based on AP dimensions may need to be revisited for the older population. The lack of correlation between US and MRI is explained by the fact that the 2 modalities detect different types of abnormalities: US better detects calcifications, while MRI better detects edema.

Study Limitations 

Our study produced original data for an older patient group that may not be generalizable to a middle-age, physically active, working population. Forty-one tendons failed at the site of cryogenic fixation (mean peak load=5250±154N). Improvements to the cryogenic fixation device would increase the mean peak load at failure and may or may not affect the correlation with imaging. As well, the power of our study (20% to detect a change of 300N [the difference in peak load between tendons with and without abnormalities] with an α of .05) was insufficient to certify the absence of a difference in peak load at rupture between the tendons with and without abnormalities on imaging for immediate clinical application.

Back to Article Outline

Conclusions 

This study represents the largest series of human Achilles' tendons mechanically tested to midsubstance failure. Although tendon abnormalities on US and MRI were common, they did not predict tendon strength. We found no conclusive evidence to support the use of imaging to predict the likelihood of rupture in a clinical setting. The usefulness of calcaneal BMD in the management of patients with Achilles' tendon disease needs to be explored further in prospective clinical studies.

Suppliers

Back to Article Outline

Acknowledgments 

We thank Eric Murray, MRT(R)(MR), and Alain Berthiaume, BSc MRT (RT)(MR), for their MRI expertise; Josianne Dodier, CRGS, ARDMS for her US expertise; and Philippe St-Laurent, MRT (N), for his bone densitometry expertise. We also thank Julie Courchesne for the specimen preparation; Varun Sharma, Bsc, for assistance with measurements; Soraya Bailey, BASc, for assistance with biomechanical testing; Tim Ramsay, PhD, with statistics; and David Jackson, PhD, and Gloria Baker, BA, for reviewing the article.

Back to Article Outline

References 

1. Schweitzer M, Karasick D. MR imaging of disorders of the Achilles tendon. AJR Am J Roentgenol. 2000;175:613–625
   • View In Article
   • MEDLINE
2. Koike Y, Uhthoff HK, Ramachandran N, et al. Achilles tendinopathy. Crit Rev Phys Rehabil Med. 2004;16:109–132
   • View In Article
3. Khan KM, Forster BB, Robinson J, et al. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? (A two year prospective study). Br J Sports Med. 2003;37:149–153
   • View In Article
   • MEDLINE
   • CrossRef
4. Astrom M, Gentz C, Nilsson P, Rausing A, Sjoberg S, Westlin N. Imaging in chronic Achilles tendinopathy: a comparison of ultrasonography, magnetic resonance imaging and surgical findings in 27 histologically verified cases. Skeletal Radiol. 1996;25:615–620
   • View In Article
   • MEDLINE
   • CrossRef
5. Azzoni R, Cabitza P. Achilles tendon pathology: the role of ultrasonography. J Orthop Traumatol. 2004;5:172–177
   • View In Article
   • CrossRef
6. Gibbon WW, Cooper JR, Radcliffe GS. Distribution of sonographically detected tendon abnormalities in patients with a clinical diagnosis of chronic Achilles tendinosis. J Clin Ultrasound. 2000;28:61–66
   • View In Article
   • MEDLINE
   • CrossRef
7. Peers KH, Brys PP, Lysens RJ. Correlation between power Doppler ultrasonography and clinical severity in Achilles tendinopathy. Int Orthop. 2003;27:180–183Epub 2003 Feb 5
   • View In Article
   • MEDLINE
8. Sell S, Schulz R, Balentsiefen M, Weber H, Kusswetter W. Lesions of the Achilles tendon: a sonographic, biomechanical and histological study. Arch Orthop Trauma Surg. 1996;115:28–32
   • View In Article
9. Paavola M, Kannus P, Jarvinen TA, Khan K, Jozsa L, Jarvinen M. Achilles tendinopathy. J Bone Joint Surg Am. 2002;84-A:2062–2076
   • View In Article
   • MEDLINE
10. Nehrer S, Breitenseher M, Brodner W, Kainberger F, Fellinger EJ. Clinical and sonographic evaluation of the risk of rupture in the Achilles tendon. Arch Orthop Trauma Surg. 1997;116:14–18
    • View In Article
11. Neuhold A, Stiskal M, Kainberger F, Schwaighofer B. Degenerative Achilles tendon disease: assessment by magnetic resonance and ultrasonography. Eur J Radiol. 1992;14:213–220
    • View In Article
    • MEDLINE
    • CrossRef
12. Karjalainen PT, Soila K, Aronen HJ, et al. MR imaging of overuse injuries of the Achilles tendon. AJR Am J Roentgenol. 2000;175:251–260
    • View In Article
    • MEDLINE
13. Haims AH, Schweitzer ME, Patel RS, Hecht P, Wapner KL. MR imaging of the Achilles tendon: overlap of findings in symptomatic and asymptomatic individuals. Skeletal Radiol. 2000;29:640–645
    • View In Article
    • MEDLINE
    • CrossRef
14. Heinonen A, Oja P, Kannus P, et al. Bone mineral density in female athletes representing sports with different loading characteristics of the skeleton. Bone. 1995;17:197–203
    • View In Article
    • Abstract
    • Full-Text PDF (823 KB)
    • CrossRef
15. Alfredson H, Nordström P, Pietilä T, Lorentzon R. Bone mass in the calcaneus after heavy loaded eccentric calf-muscle training in recreational athletes with chronic Achilles tendinosis. Calcif Tissue Int. 1999;64:450–455
    • View In Article
    • MEDLINE
    • CrossRef
16. Ramachandran N, Koike Y, Poitras P, Backman D, Uhthoff H, Trudel G. Dual cryogenic fixation for mechanical testing of soft musculoskeletal tissues. IEEE Trans Biomed Eng. 2005;52:1792–1795
    • View In Article
    • MEDLINE
    • CrossRef
17. Koivunen-Niemela T, Parkkola K. Anatomy of the Achilles tendon (tendo calcaneus) with respect to tendon thickness measurements. Surg Radiol Anat. 1995;17:263–268
    • View In Article
    • MEDLINE
    • CrossRef
18. Moller M, Kalebo P, Tidebrant G, Movin T, Karlsson J. The ultrasonographic appearance of the ruptured Achilles tendon during healing: a longitudinal evaluation of surgical and nonsurgical treatment, with comparisons to MRI appearance. Knee Surg Sports Traumatol Arthrosc. 2002;10:49–56Epub 2001 Dec 18
    • View In Article
    • MEDLINE
    • CrossRef
19. Louis-Ugbo J, Leeson B, Hutton WC. Tensile properties of fresh human calcaneal (Achilles) tendons. Clin Anat. 2004;17:30–35
    • View In Article
    • MEDLINE
    • CrossRef
20. Lewis G, Shaw KM. Tensile properties of human tendo Achillis: effect of donor age and strain rate. J Foot Ankle Surg. 1997;36:435–445
    • View In Article
    • Abstract
    • Full-Text PDF (1889 KB)
    • CrossRef
21. Wilhelm K, Steger ER, Schmidt GP. [New experimental method to test the tensile strength of Achilles tendons] [German]. Res Exp Med (Berl). 1973;160:80–88
    • View In Article
    • MEDLINE
    • CrossRef
22. Wren T, Yerby S, Beaupre G, Carter D. Mechanical properties of the human Achilles tendon. Clin Biomech (Bristol, Avon). 2001;16:245–251
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (185 KB)
    • CrossRef
23. Wren T, Yerby S, Beaupre G, Carter D. Influence of bone mineral density, age and strain rate on the failure mode of human Achilles tendons. Clin Biomech (Bristol, Avon). 2001;16:529–534
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (103 KB)
    • CrossRef
24. Thermann H, Frerichs O, Biewener A, Krettek C, Schandelmaier P. [Biomechanical studies of human Achilles tendon rupture] [German]. Unfallchirurg. 1995;98:570–575
    • View In Article
    • MEDLINE
25. Fukashiro S, Komi PV, Jarvinen M, Miyashita M. In vivo Achilles tendon loading during jumping in humans. Eur J Appl Physiol Occup Physiol. 1995;71:453–458
    • View In Article
    • MEDLINE
    • CrossRef
26. Trudel G, Koike Y, Ramachandran N, et al. Mechanical alterations of rabbit Achilles tendon after immobilization correlate with bone mineral density but not with magnetic resonance or ultrasound imaging. Arch Phys Med Rehabil. 2007;88:1720–1726
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (186 KB)
    • CrossRef
27. Shalabi A, Kristofferson-Wilberg M, Svensson L, Aspelin P, Movin T. 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. 2004;32:1286–1296Epub 2004 May 18
    • View In Article
    • MEDLINE
    • CrossRef
28. Narici MV, Maganaris CN. Adaptability of elderly human muscles and tendons to increased loading. J Anat. 2006;208:433–443
    • View In Article
    • MEDLINE
    • CrossRef
29. Viidik A, Lewin T. Changes in tensile strength characteristics and histology of rabbit ligaments induced by different modes of postmortal storage. Acta Orthop Scand. 1966;37:141–155
    • View In Article
    • MEDLINE

• a HDI 5000 ultrasound unit; Philips Medical Systems, 281 Hillmount Rd, Markham, ON, Canada L6C 2S3.
• b Symphony 1.5-T MRI unit; Siemens Medical Systems, 186 Wood Ave, S Iselin, NJ 08830.
• c Dual energy X-ray absorptiometer, DPX-alpha; Lunar Corp, 726 Heartland Trail, Madison, WI 53717.
• d Lunar-Small Animal Software, Version 4.7; Aymes Medical Lunar Canada, 78 Windham Trail, Aurora, ON, Canada L4G 5L5.
• e Material testing machine, Sintech 1/G; MTS Systems Corp, 14000 Technology Dr, Eden Prairie, MN 55344.
• f TestWorks; MTS Systems Corp, 14000 Technology Dr, Eden Prairie, MN 55344.
• g SPSS 11.5.0; SPSS Inc, 233 S Wacker Dr 11th Fl, Chicago, IL 60606.