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AJR 2002; 179:187-192
© American Roentgen Ray Society


Original Report

Contrast-Enhanced Magic-Angle MR Imaging of the Achilles Tendon

Helen Marshall1, Clare Howarth, David J. Larkman, Amy H. Herlihy, Angela Oatridge and Graeme M. Bydder

1 All authors: Imaging Sciences Department, The Robert Steiner Magnetic Resonance Unit, MRC Clinical Sciences Centre, Imperial College Faculty of Medicine, Hammersmith Hospital, Du Cane Rd., London W12 0HS, England.

Received October 8, 2001; accepted after revision January 14, 2002.

 
Supported by Diagnostic Investigations of Spinal Conditions and Sciatica, the Arthritis Research Campaign, and Marconi Medical Systems.

Address correspondence to G. M. Bydder.


Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of this study was to image the Achilles tendon with MR imaging at the magic angle (the long axis of the tendon at 55° relative to the direction of the main static magnetic field [B0]) to detect signal from the tendon, to measure the T1 of the tendon, and to determine patterns of contrast enhancement in control subjects and patients.

CONCLUSION. Mean T1 values of 311 ± 30 msec (at 1.0 T) were found in six volunteers. In six control volunteers, slow uptake of contrast material that dispersed over 40 min-1.5 hr was shown without focal change, with elimination in most cases occurring within 18-24 hr. Small rapidly enhancing focal areas of enhancement were seen next to the insertion of the tendon and centrally within 5-10 min in two control volunteers. The focal areas were located at the sites of the blood supply. A patient with chronic tendinopathy showed early local contrast enhancement that extended widely within the tendon over several hours. Two patients with a partially ruptured or repaired tendon showed marked rapid contrast enhancement. The enhancement was obvious with the tendon at the magic angle but was not evident with the tendon in the usual orientation for MR examinations parallel to B0.


Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
With conventional MR imaging pulse sequences and orientation parallel to B0, the normal Achilles tendon usually has a low signal intensity [1]. The low signal is a consequence of strong dipolar interactions between ordered protons, which lead to rapid loss of the MR imaging signal after excitation. This is manifest as a very short T2 with little or no signal detectable with the TEs available on most clinical systems.

Although the lack of detectable signal is an advantage for some diagnostic purposes, it also means that it is not possible to detect effects due to contrast agents in normal tendons because the tendon signal remains undetectable even if its T1 or T2 is shortened by the contrast agent.

With in vitro studies, the T2s of tendons vary with orientation relative to the static B0 field [2, 3], and, in particular, T2 may be increased when the tendon is placed at the magic angle (i.e., at {theta} = 55° relative to B0). The magnitude of the dissipative dipolar interactions that lead to rapid signal loss is modulated by the term "3 cos2{theta}-1," which is equal to zero at 55°. The high signal intensity produced in the tendon because of increases in T2 has previously been recognized in clinical practice as an artifact [4]. Steps have been taken to avoid artifacts by placing the tendons parallel or perpendicular to B0 and increasing the pulse sequence TE [5]. Only recently has the magic-angle effect been deliberately exploited for imaging purposes by placing tendons at 55° relative to B0 to increase their T2s and to allow the signal to be detected from them [6].

We have studied a small group of volunteers and patients with their Achilles tendon at the magic angle and used this technique to measure T1 values of the tendon and to study the effects of contrast enhancement in the tendon over time.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
With the permission of the local research ethics committee and informed consent from each subject, we studied eight control volunteers and three patients with diseases of the Achilles tendon.

Two-dimensional multislice spin-echo (TR/TE, 500/16) and inversion recovery (1500/16; inversion time, 300 msec) pulse sequences were used with a matrix of 192 x 256 and a slice thickness of 3 mm. A three-dimensional radiofrequency spoiled gradient-echo image (21/6) with a flip angle of 35° and an isotropic resolution of 1.6 mm was also obtained. Studies were performed with a 1.0-T MR imaging system (Marconi Medical Systems, Cleveland, OH). The subjects were examined in the lateral decubitis position with their Achilles tendons oriented at 55° relative to B0 and placed at the center of a 10-cm-diameter surface coil positioned in the system couch. The ankle was dorsiflexed to 90° to place the Achilles tendon under some tension, and the ball of the foot was placed against a rigid support to reduce patient motion. For illustrative purposes, two volunteers also had these sequences performed with their Achilles tendons at 0° relative to B0.

Gadodiamide (0.3 mmol/kg) was administered by slow IV injection after the first pulse sequence cycle. The cycle was repeated four times during the first examination. When possible, the volunteers underwent further imaging (a single cycle) approximately 8-18 hr and 20-36 hr after the initial contrast injection. The spin-echo (1500/16) and inversion recovery (1500/16; inversion time, 300 msec) pulse sequences were used to calculate T1 with a simplex iterative root finding the algorithm. Three regions of interest were selected for these calculations. The three patients had the initial five-cycle examination followed by a cycle with their Achilles tendons oriented at 0° relative to B0.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
The change in signal intensity due to the magic-angle effect is illustrated in a control volunteer in Figure 1A,1B using a spin-echo (1500/16) pulse sequence. No signal is apparent in the tendon when it is orientated at 0° relative to B0 (Fig. 1A), but the signal is obvious when it is placed at 55° relative to B0 (Fig. 1B).



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Fig. 1A. 57-year-old male control volunteer. Spin-echo MR image (TR/TE, 1500/16) at 0° shows no signal in tendon (arrow).

 


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Fig. 1B. 57-year-old male control volunteer. Spin-echo MR image (1500/16) at 55° shows obvious signal intensity in tendon (arrow).

 

Eight asymptomatic male volunteers (age range, 27-58 years) were studied. The unenhanced T1 values of six volunteers are shown in Table 1 (the other subjects had images with artifacts) together with T1 values in the three patients.


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TABLE 1 Achilles Tendon T1 Values in Six Volunteers and Three Patients

 

Six volunteers showed generalized enhancement without focal features. This enhancement was most apparent on the inversion recovery MR images, in which a slow increase in signal intensity occurred over 40 min-1.5 hr, with a subsequent decrease that was complete at 24 hr in all but one control subject. Values of T1 computed from regions of interest placed centrally within the tendon in these subjects and plotted against time are shown in Figure 2A,2B. The large error bars seen in these measurements reflect tissue heterogeneity in the region of interest rather than intrinsic uncertainty in T1. This is shown by the clear trends seen in the data in the error bars.



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Fig. 2A. Six male control volunteers between 27 and 45 years old. Plots of T1 against time in Achilles tendon show decrease in T1 over 40 min-1.5 hr followed by return to normal values over 1-22 hr. Large error bars seen in these measurements reflect tissue heterogeneity in region of interest rather than intrinsic uncertainty in T1, which is shown by clear trends seen in data.

 


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Fig. 2B. Six male control volunteers between 27 and 45 years old. Plots of T1 against time in Achilles tendon show decrease in T1 over 40 min—1.5 hr followed by return to normal values over 1-22 hr. Large error bars seen in these measurements reflect tissue heterogeneity in region of interest rather than intrinsic uncertainty in T1, which is shown by clear trends seen in data.

 

Two other control volunteers showed areas of focal enhancement that were apparent on the first contrast-enhanced scans. The areas of focal enhancement were central and close to the insertion of the tendon. The changes did not diffuse widely in the tendon.

One control volunteer (who ran 20-25 miles [32-40 km] per week) was subsequently clinically diagnosed with chronic tendinopathy. His sequential scans showed uptake and dispersion of the contrast agent over time (Fig. 3A,3B,3C,3D,3E). An initial enhancement peak was seen close to the myotendinous junction at 5 min, whereas maximum enhancement was seen centrally at 7 hr. T1 values for the region located centrally and adjacent to the myotendinous junction are shown in Figure 3E.



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Fig. 3A. 57-year-old man with chronic tendinopathy. Inversion recovery MR images (TR/TE, 1500/16; inversion time, 300 msec) before (A), 5 min after (B), 1 hr after (C), and 7 hr after (D) administration of IV gadodiamide. Early enhancement is seen adjacent to myotendinous junction and more centrally in B (arrows). This enhancement diffuses more widely in C (arrows) and occupies most of tendon in D (arrows).

 


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Fig. 3B. 57-year-old man with chronic tendinopathy. Inversion recovery MR images (TR/TE, 1500/16; inversion time, 300 msec) before (A), 5 min after (B), 1 hr after (C), and 7 hr after (D) administration of IV gadodiamide. Early enhancement is seen adjacent to myotendinous junction and more centrally in B (arrows). This enhancement diffuses more widely in C (arrows) and occupies most of tendon in D (arrows).

 


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Fig. 3C. 57-year-old man with chronic tendinopathy. Inversion recovery MR images (TR/TE, 1500/16; inversion time, 300 msec) before (A), 5 min after (B), 1 hr after (C), and 7 hr after (D) administration of IV gadodiamide. Early enhancement is seen adjacent to myotendinous junction and more centrally in B (arrows). This enhancement diffuses more widely in C (arrows) and occupies most of tendon in D (arrows).

 


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Fig. 3D. 57-yeard-old man with chronic tendinopathy. Inversion recovery MR images (TR/TE, 1500/16; inversion time, 300 msec) before (A), 5 min after (B), 1 hr after (C), and 7 hr after (D) administration of IV gadodiamide. Early enhancement is seen adjacent to myotendinous junction and more centrally in B (arrows). This enhancement diffuses more widely in C (arrows) and occupies most of tendon in D (arrows).

 


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Fig. 3E. 57-year-old man with chronic tendinopathy. Plot of T1 versus time shows myotendinous junction (region 1) and central area (region 2). Myotendinous junction shows early uptake, whereas central area shows delayed and lower uptake. Unenhanced inversion recovery sequence has low signal not because of short T2 of tendon but because its inversion time is close to null point.

 

A partial rupture in an Achilles tendon 17 months after injury in a 34-year-old woman is shown in Figure 4A,4B,4C,4D. Marked rapid uptake and elimination of contrast material took place over a 1-hr period. The contrast enhancement was obvious with the tendon at 55° relative to B0 (Fig. 4B) but not with the tendon at 0° relative to B0 (Fig. 4C). The reduction in T1 (with the tendon imaged at 55° relative to B0) is shown in Figure 4A,4B,4C,4D. Similar findings were seen in a 42-year-old man who had suffered a partial rupture of the tendon.



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Fig. 4A. 34-year-old woman with previous tendon rupture. Inversion recovery sequence (TR/TE, 1500/16; inversion time, 300 msec) at 55° is shown before IV gadodiamide was administered.

 


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Fig. 4B. 34-year-old woman with previous tendon rupture. Inversion recovery sequence (1500/16; inversion time, 300 msec) at 55° is shown after IV gadodiamide was administered. Note widespread enhancement in thickened tendon (arrows).

 


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Fig. 4C. 34-year-old woman with previous tendon rupture. Inversion recovery sequence (1500/16; inversion time, 300 msec) at 0° is shown after IV gadodiamide was administered. This enhancement is not apparent with tendon orientated at 0°.

 


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Fig. 4D. 34-year-old woman with previous tendon rupture. Plot of T1 versus time in contrast-enhancing area shows rapid uptake and elimination of contrast material in abnormal region.

 


Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
This study shows that by positioning the Achilles tendon at the magic angle of 55° relative to B0, it is possible to obtain signal from the tendon, to measure the T1 of the tendon, and to show the uptake and elimination of contrast material over time.

The T1 values measured in vivo in this study (311 ± 30 msec at 1.0 T) are longer than those of the in vitro bovine samples published by Fullerton et al. [2] (163 ± 3 msec at 0.25 T) but shorter than those obtained by Henkleman et al. [3] (508 ± 30 msec at 1.5 T). The values obtained using a short TE technique [7] are also shorter than those obtained in three control human volunteers (490 ± 20 msec at 1.5 T). The variations may reflect differences in field strength.

The pattern of contrast enhancement is of interest. To our knowledge, there is no previous description of contrast enhancement in the normal Achilles tendon, which may be because techniques used in this study, such as triple-dose contrast enhancement, delayed studies, a highly T1-sensitive inversion recovery sequence, and magic-angle imaging, increased the sensitivity of MR imaging to contrast enhancement.

The early rapid uptake in small focal areas in two of the control volunteers may reflect local blood supply in sites of known vascularity. The slower, more generalized change in T1 in tendons probably reflects perfusion and diffusion of the contrast agent into the tendon, with the gadodiamide functioning as a monitor of solute transport. The blood supply of the Achilles tendon comes from the muscle at its origin, the bone at its insertion, and the paratenon. The tendon as a whole is relatively avascular with a more avascular zone 2-6 cm from its insertion [8,9,10], and the slow normal uptake in the bulk of the tendon may reflect this low level of perfusion and transport by diffusion. The pattern of contrast uptake and retention may also depend on tendon proteoglycan content, because these negatively charged molecules are associated with retention of water and probably of gadodiamide. The results in the volunteer studies may reflect differences in age and exercise status and subclinical degenerative change; these factors should be controlled in future studies.

The rapid contrast enhancement in disease may be due to increased vascularity as described in chronic tendonitis [11]. The rapid elimination of contrast material may be a consequence of reduced proteoglycan content in the healing tendon. Although contrast enhancement has been shown to be useful in the diagnosis of Achilles tendonosis [12], routine clinical images obtained at the conventional angle of 0° may underestimate the extent of enhancement and thus the extent of disease.

The use of very short TEs (i.e., 0.228 msec) increases the signal detectable from the Achilles tendon without placing it at the magic angle [7]. However, this technique may require higher performance hardware and specialized pulse sequences (such as projection reconstruction and half pulse excitation), whereas placing the tendon at 55° is achievable on most MR imaging systems, and no specialized pulse sequences are required to detect signal from it.

Magic-angle imaging may allow a wide range of MR imaging techniques to be applied to the study of tendons and ligaments throughout the body and may provide new options to show contrast enhancement and other MR imaging parameters in both health and disease.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Schweitzer ME, Karasick D. MR imaging of disorders of the Achilles tendon. AJR 2000;175:613 -625[Free Full Text]
  2. Fullerton GD, Cameron IL, Ord VA. Orientation of tendons in the magnetic field and its effect on T2 relaxation times. Radiology 1985;155:433 -435[Abstract/Free Full Text]
  3. Henkleman RM, Stanisz GJ, Kim JK, Bronskill MJ. Anisotropy of NMR properties of tissues. Magn Reson Med 1994;32:592 -601[Medline]
  4. Erickson SJ, Cox IH, Hyde JS, Carrera GF, Standt JA, Etkuski LD. Effect of tendon orientation on MR imaging signal intensity: a manifestation of the "magic angle" phenomenon. Radiology 1991;81:389 -392
  5. Peh WCG, Chan JHM. The magic angle phenomenon in tendons: effect of varying the MR echo time. Br J Radiol 1998;71:31 -36[Abstract]
  6. Oatridge A, Herlihy AH, Thomas RW, et al. Magnetic resonance: magic angle imaging of the Achilles tendon. Lancet 2001;358:1610 -1611[Medline]
  7. Gold GE, Tishya ALW, Krishna N, Nishimura DG, Beaupre G. In vivo short echo time imaging of Achilles tendon: proceedings of the International Society for Magnetic Resonance in Medicine (ISMRM). Berkeley, CA: ISMRM, 2001:244
  8. Schmidt-Rohlfing B, Graf J, Scheider U, Niethard FU. The blood supply of the Achilles tendon. Int Orthop 1992;16:29 -31[Medline]
  9. Carr AJ, Norris SH. The blood supply of the calcaneal tendon. J Bone Joint Surg Br 1989;71:100 -101
  10. Ahmed IM, Lagopoulas M, McConnell P, Soames RW, Sefton GK. Blood supply of the Achilles tendon. J Orthop Res 1998;16:591 -596[Medline]
  11. Astrom M. Laser Doppler flowmetry in the assessment of tendon blood flow. Scand J Med Sci Sports 2000;10:365 -367[Medline]
  12. Shalabi A, Kristoffersen-Wiberg M, Aspelin P, Movin T. MR evaluation of chronic Achilles tendonosis. Acta Radiol 2001;42:269 -276[Medline]

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