- Email: [email protected]
Magnetic resonance imaging of entheses. Part 2
Clinical Radiology (2008) 63, 704e711
PICTORIAL REVIEW
Magnetic resonance imaging of entheses. Part 2 M. Benjamina, S. Milzb, G.M. Bydderc,* a
School of Biosciences, Cardiff University, Cardiff, UK, bAO Research Institute, Davos, Switzerland, and Department of Radiology, University of California San Diego, San Diego, USA
c
Received 16 November 2007; received in revised form 16 November 2007; accepted 17 December 2007
Entheses are the sites of attachment of a tendon, ligament, or joint capsule to bone. In a previous article new options for visualizing entheses and related structures, including ultrashort echo time (UTE) pulse sequences, and magic angle imaging were described. In this article an approach to image interpretation is described together with normal examples using UTE and other pulse sequences with and without magic angle imaging. Examples of images seen in disease are included. The new options for imaging entheses may provide useful options for biomechanical study and recognition of involvement in disease. ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction This paper aims to integrate and extend information from the previous paper1 in order to provide a basis for interpreting images of normal entheses and recognizing involvement in disease.
Image interpretation In disease, the common changes are an increase in T1 and T2, although conditions such as chronic calcification may decrease these parameters. Loss of order in collagen-rich tendon or ligaments may not only lead to an increase in T2, but also a reduction in the increase in T2 produced by the magic angle effect. The imaging sequences available on clinical systems for general musculoskeletal use can be divided into three groups1: long echo time [TEs; T2weighted fast spin-echo (FSE), proton density, and short tau inversion recovery (STIR)],2 short TE (T1weighted conventional CSE/FSE, spoiled gradient * Guarantor and correspondent: G.M. Bydder, Department of Radiology, University of California San Diego, 200 West Arbor Drive, San Diego, CA 92103-8226, USA. Tel.: þ1 619 471 0500; fax: þ1 619 471 0503. E-mail address: [email protected] (G.M. Bydder).
FSE, and other gradient echo), and2 ultrashort TE (UTE) imaging techniques. In general, the signal levels of enthesis tissues using the first two classes of sequences are low or zero, apart from magic angle effects. UTE sequences provide moderate or high signal intensity. Magic angle effects have lesser effects with long TE and UTE sequences and more obvious effects with short TE sequences. The magic angle effects depend on the baseline T2 (T2 with the majority of fibres at 0 to B0) and the fibre to B0 angle with a maximum increase in T2 around 55 and a lesser one at about 90 . The appearance of fibre structures is affected by the internal contrast, such as the difference between the principal fibre signal intensity and the endotenon signal intensity, but also the fibre to section orientation with a fascicular, punctuate or speckled pattern apparent with fibres perpendicular to the section, a blurred appearance when they are oblique and a linear pattern when fibres are parallel to the section. Contrast optimization follows from a consideration of T1, T2 and magic angle effects in health and disease. For T1, a general aim is to use a repetition time (TR; for T1-weighted SE sequences and spoiled gradient echo sequences) intermediate between the normal T1 and the usually longer T1 produced by disease whilst
0009-9260/$ - see front matter ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2007.12.010
Magnetic resonance imaging of entheses
allowing for the effect of flip angle. The same type of general rule applies to T2-weighted sequences in the short or long range with TE chosen to be between the two T2s of interest. Note that ‘‘T1weighted’’ sequences are also T2-weighted for the short T2s of enthesis tissues. To maximize contrast from magic angle effects, TE is typically chosen between the baseline T2 and the increased T2 produced by the magic angle effect. UTE sequences may behave somewhat differently as their signal may be augmented by an increased in T2 of very short T2 species, which are not detectable with fibres at 0 to B0. Many of the enthesis tissues are present as thin layers at boundaries and are subject to partial volume effects. The calcified layer of fibrocartilage may not be apparent in sections oblique to it as a consequence of this, and other effects. Contrast enhancement is affected by all the above considerations. It is not observable unless detectable signal is present. The effect then depends on the agent, its concentration, and the time course, as well as tissue vascularity and contrast transport properties. Normal uncalcified fibrocartilage (including enthesis and sesamoid fibrocartilage) is avascular, and contrast agents enter into this tissue slowly and by diffusion. Vascularity and the degree of contrast enhancement may be increased in disease. UTE sequences are subject to issues concerned with section selection, detection of short T2 components, as well as gradient performance and eddy current issues, which may result in blurring at tissue boundaries. Chemical shift artefacts of the first kind are typically radial and not a linear displacement in the (single) frequency encoded direction as with Cartesian mapping of k-space. There are a number of differential diagnoses arising from these and other considerations including1: normal fibrocartilage, partial volume effects from oblique fibres, magic angle effects with longitudinal fibres isointense to endotenon, and tissue fibrosis (or scar). Each of these may produce a loss of fascicular, punctuate, or speckled pattern in a localized area. The keys to differentiating these entities are fibre-to-B0 and fibreto-section considerations, as well as the location of the changes with respect to known sites of enthesis and sesamoid fibrocartilage.2
705
short T2 components due to fat or other forms of saturation, use of multiple-section acquisitions or section profile issues, as well as pathological changes.3
Magic angle effects and disease producing an increase in T2 Both may result in an increase in signal and a loss of fascicular pattern. The key is fibre to field angle.4
Normal appearance of enthesis with age This is yet to be determined in detail, but postmortem findings show signs of degeneration and vascularization with increasing age. The differential diagnosis may be any of the many overuse syndromes.5
Contrast enhancement This reflects vascularity and may be absent in fibrocartilage, but increased as a consequence of angiogenesis in diseased tendon and fibrocartilage. The time course is typically longer than that for normal tissues.6
The extent of enthesis and sesamoid fibrocartilage This may vary with compressive load, which may depend, for example, on the degree of prominence
Loss of signal from the calcified zone, which is a thin layer This may arise normally (or as a normal variant), from partial volume effects due to oblique sections, image blurring, reduction in signal from
Figure 1 Pronator teres insertion into the radius: axial difference UTE image (TR/TE ¼ 500/0.12 minus 4 ms). The tendon of pronator teres has a high signal (arrow) and merges with the periosteum of the shaft of the radius.
706
M. Benjamin et al.
of the superior tuberosity of the calcaneus for the Achilles tendon.7
Normal examples of magnetic resonance imaging (MRI) of entheses
Calcification
The radial enthesis of pronator teres is shown in Fig. 1 using a difference UTE image. It is an example of a fibrous enthesis. The tendon has a high signal (arrow) and becomes continuous with the surrounding high signal periosteum. The underlying bone is thick cortical rather than the thin shell and trabecular bone typically seen with fibrocartilaginous enthesis. The insertion of the Achilles tendon has been described as the premier enthesis and it exemplifies many of the features described previously. The sagittal image in Fig. 6a displays sesamoid and enthesis fibrocartilage as higher signal regions, and there is a close correspondence with the anatomical appearances. The higher signal from fibrocartilage is probably a consequence of its shorter T1. On the axial image (Fig. 2b) enthesis fibrocartilage has a higher signal and there is a higher signal region again (arrow) which probably represents calcified fibrocartilage. Fig. 3 shows an axial view of the long plantar ligament that has an amorphous fibrocartilaginous component with a higher signal in its proximal part, and a distal region in which linear fascicles are readily seen. The distal end of the patellar ligament shows an increase in signal in the sagittal plane5 (Fig. 4a; see later) and the axial image shows high signal in the deep part of the ligament adjacent to the tibia with reduction in the visibility
Which may have a relative long T2 in the acute phase but a short T2 in chronic form. In imaging of entheses, valuable information may be obtained from other techniques including plain films2 and ultrasound.3,4
Figure 2 Achilles tendon enthesis, sagittal (a) and axial (b) UTE images (TR/TE ¼ 500/0.12 ms) with the tendon at about 30 to B0. Sesamoid fibrocartilage has a high signal in (a) (arrow). Uncalcified sesamoid fibrocartilage is also posterior to the calcaneus seen in (b) together with calcified fibrocartilage (arrow).
Figure 3 Long plantar ligament axial UTE (TR/ TE ¼ 500/0.012 ms) image with the ligament at the magic angle. The fibrocartilaginous component has a high signal (arrows). The anterior portion has a linear pattern.
Magnetic resonance imaging of entheses
Figure 4 Patellar ligament: sagittal (a) and axial (b) gradient echo images (TR/TE ¼ 500/3.8 ms) with the tendon at about 30 to B0. The distal part of the ligament shows a high signal at its junction with the tibia (a) (arrow). The axial image shows a high signal and a relative loss of fascicular pattern in the deep portion of the ligament adjacent to the tibia (arrow).
of the fascicular pattern (Fig. 4b). This represents fibrocartilage in a region of the tendon which is subject to compression. The posterior cruciate ligament shows high signal at its femoral end (Fig. 5a) and a root-like trabecular bone pattern deep to the enthesis (Fig. 5b). The lateral collateral ligament of the knee shows a lower signal in its central region (arrow) and a higher signal in its femoral and fibular attachments (Fig. 6a) where the tendon is at 0 to B0. Less contrast is seen between the central and attachment regions when the tendon is oriented closer to the magic angle (Fig. 6b). The quadriceps tendon is an example of an extended enthesis organ, for when the knee is
707
Figure 5 Posterior cruciate ligament. Coronal (a) and sagittal (b) UTE (TR/TE ¼ 500/01.2 ms) and non-fat saturated gradient echo (TR/TE ¼ 500/4.6 ms) close to the magic angle. High signal is seen at the junction of the ligament with the femur (a) (arrow). A tree root-like pattern of trabecular bone is seen deep to the ligament in (b) (arrow).
flexed, the tendon is compressed against the underlying lateral femoral condyle (Fig. 7a). It is this region of the quadriceps tendon that shows increased signal and loss of fascicular pattern within the tendons on the axial images, consistent with the presence of fibrocartilage (Fig. 7b). However, this awaits microscopic confirmation. The transverse ligament of the atlas is subject to compression by the dens (odontoid process) and sesamoid fibrocartilage has been described at this
708
Figure 6 Lateral collateral ligament of the knee. Gradient echo (TR/TE ¼ 500/4.6 ms) coronal (a) and sagittal (b) images. At 0 to B0 (a) lower signal is seen in the central area of the ligament (arrow). The signal is more uniform at an orientation closer to the magic angle (b).
site in histological studies. This cartilage is readily apparent using UTE imaging (Fig. 8).
MRI of diseased entheses Histology of the overuse syndromes shows degenerative features rather than those typical of inflammation with tendon thinning, disruption of collagen fibres, microtears, increased granulation tissue, accumulation of lipids, amorphous debris, and calcium deposits. These are associated with
M. Benjamin et al.
Figure 7 Quadriceps tendon (an extended enthesis organ). Sagittal (a) and transverse (b) gradient echo (TR/TE ¼ 500/4.6 ms) images at about 30 to B0. With the knee flexed the tendon is compressed by the femur (a). The axial image shows high signal due to fibrocartilage in the region that is compressed (arrow).
a loss of morphological detail and an increase in T1 and T2 with MRI. Diffuse idiopathic skeletal hyperostosis is associated with enthesopathy.6,7 Metabolic diseases, including chondrocalcinosis, gout, hyperparathyroidism, primary hypoparathyroidism, fluorosis, and acromegaly, are also associated with enthesopathy. Involvement of entheses may precede that of cartilage in osteoarthritis. The seronegative spondyloarthropathies have been the principal diseases of interest and the pathology has been described in detail. This includes microfoci of inflammation often beginning as an erosion in a subchondral location. There may
Magnetic resonance imaging of entheses
709
Figure 8 Transverse ligament of the atlas. UTE (TR/ TE ¼ 500/0.08 ms) image. The transverse tensile fibres are lower signal than the fibrocartilaginous tissue adjacent to the odontoid process.
be marrow involvement resembling subacute or chronic osteomyelitis. Finally, the erosive lesions may heal by reactive formation of new bone within fibrous connective tissue. This may result in a new enthesis that protrudes relative to the initial enthesis. There has also been considerable interest in fibrocartilage involvement remote from traditional entheses and the significance of this in terms of the aetiology of the disease. Imaging involvement in asymptomatic regions has been described with conventional sequences and with UTE sequences (Figs. 9 and 10). Changes in the enthesis of the collateral ligament of the finger are seen in Fig. 11. There is increased signal in the ligament adjacent to bone (arrow). Enthesial changes are seen in the early stages of osteoarthritis.8,9
Healing and repair at entheses Several studies have focused on the problem of how tendons or ligaments can best be surgically re-attached to bone.10,11 Sharpey’s fibres are reported to develop at the new fibrocartilaginous attachment sites, although they are a normal
Figure 9 Achilles tendon in Reiter’s disease. Sagittal (a) and axial (b) UTE (TR/TE ¼ 500/0.08 ms images). The enthesis is thickened and has a higher signal intensity.
feature of fibrous rather than fibrocartilaginous entheses. This suggests that, at least during the early stages of repair, the mechanism may be different from that by which healthy fibrocartilaginous entheses initially develop.12 Enthesis fibrocartilage can be reconstituted in time; however, authors often comment on the poor quality of repair of reconstructions,13 the slow nature of the healing process,14 and the greater time for the entheses to be structurally restored.15 Of recent interest is the fact that restoration of a normal enthesis can be significantly enhanced by treating tendon bone grafts with a variety of biologically active modulators. These include osteogenic protein,16 suturing of periosteum along the surface of reattached
710
M. Benjamin et al.
Summary
Figure 10 Extensor tendon of the great toe; psoriatic arthropathy sagittal UTE (TR/TE ¼ 500/0.08 ms) image. The distal end of the tendon (in a region known from histology to have a sesamoid fibrocartilage within it) shows higher signal (arrow) probably due to inflammatory change.
tendons, which increases the availability of stem cells17 and direct application of stem cells.18 The use of imaging in this type of study has hardly begun.
Entheses are important regions of the body where it is possible to link anatomy, histology, and biochemistry to function, and understand features of these regions in biomechanical terms. The key tissues all show little or no signal with conventional imaging techniques, but provide a detectable signal and can be differentiated with UTE pulse sequences and magic angle imaging. It is then possible to observe features that have only previously been shown with histological studies. Understanding of the appearances of entheses involves consideration of tissue MR properties, fibre-to-field angle, magic angle effects, pulse sequences, geometrical factors including fibre-to-slice orientation and partial volume effects. There are likely to be new opportunities to study diffusion, magnetization transfer, perfusion, and T1 in the rotating frame of enthesis tissues using newer pulse sequences. In vivo recognition of these anatomical structures may provide new options for biomechanical study and diagnosis of earlier or milder forms of disease. This may include overuse syndromes, osteoarthritis, metabolic and seronegative disease. It is also possible that study of the regions of attachment of tendons and ligaments to bone may provide a better understanding of the process of repair following medical treatment and surgery.
References
Figure 11 Coronal image of the collateral ligament of the proximal interphalangeal joint in osteoarthritis. Spoiled gradient echo (SGE; TR/TE ¼ 500/1.8 ms). An area of increased signal is seen extending from the enthesis (arrow).
1. Benjamin M, Milz S, Bydder GM. Magnetic resonance imaging of entheses. Part 1. Clin Radiol 2008;63(6):691e703. 2. Resnick D, Niwayama G. Entheses and enthesopathy. Anatomical, pathological, and radiological correlation. Radiology 1983;146:1e9. 3. Morel M, Boutry N, Demondion X, et al. Normal anatomy of the heel entheses: anatomical and ultrasonographic study of their blood supply. Surg Radiol Anat 2005;27: 176e83. 4. Kamel M, Eid H, Mansour R. Ultrasound detection of heel enthesitis: a comparison with magnetic resonance imaging. J Rheumatol 2003;30:774e8. 5. Evans EJ, Benjamin M, Pemberton DJ. Fibrocartilage in the attachment zones of the quadriceps tendon and patellar ligament of man. J Anat 1990;171:155e62. 6. Gaucher AA, Pere PG, Gillet PM. From ankylosing spondylitis to Forestier’s disease: ossifying enthesopathy, a unifying concept. J Rheumatol 1990;17:854e6. 7. Littlejohn GO. More emphasis on the enthesis. J Rheumatol 1989;16:1020e2. 8. Tan AL, Grainger AJ, Tanner SF, et al. A high-resolution magnetic resonance imaging study of distal interphalangeal joint arthropathy in psoriatic arthritis and osteoarthritis: are they the same? Arthritis Rheum 2006;54:1328e33. 9. Tan AL, Toumi H, Benjamin M, et al. Combined high-resolution magnetic resonance imaging and histological examination to explore the role of ligaments and tendons in the phenotypic
Magnetic resonance imaging of entheses
10.
11.
12.
13.
14.
expression of early hand osteoarthritis. Ann Rheum Dis 2006; 65:1267e72. Shaieb MD, Singer DI, Grimes J, et al. Evaluation of tendon-tobone reattachment: a rabbit model. Am J Orthop 2000;29: 537e42. Aoki M, Oguma H, Fukushima S, et al. Fibrous connection to bone after immediate repair of the canine infraspinatus: the most effective bony surface for tendon attachment. J Shoulder Elbow Surg 2001;10:123e8. Gao J, Messner K, Ralphs JR, et al. An immunohistochemical study of enthesis development in the medial collateral ligament of the rat knee joint. Anat Embryol (Berl) 1996; 194:399e406. Jones JR, Smibert JG, McCullough CJ, et al. Tendon implantation into bone: an experimental study. J Hand Surg [Br] 1987;12:306e12. Thomopoulos S, Hattersley G, Rosen V, et al. The localized expression of extracellular matrix components in healing
711
15.
16.
17.
18.
tendon insertion sites: an in situ hybridization study. J Orthop Res 2002;20:454e63. Silva MJ, Boyer MI, Ditsios K, et al. The insertion site of the canine flexor digitorum profundus tendon heals slowly following injury and suture repair. J Orthop Res 2002;20: 447e53. Helm GA, Li JZ, Alden TD, et al. A light and electron microscopic study of ectopic tendon and ligament formation induced by bone morphogenetic protein-13 adenoviral gene therapy. J Neurosurg 2001;95:298e307. Chen CH, Chen WJ, Shih CH, et al. Enveloping the tendon graft with periosteum to enhance tendon-bone healing in a bone tunnel: a biomechanical and histologic study in rabbits. Arthroscopy 2003;19:290e6. Lim JK, Hui J, Li L, et al. Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy 2004;20:899e910.
PICTORIAL REVIEW
Magnetic resonance imaging of entheses. Part 2 M. Benjamina, S. Milzb, G.M. Bydderc,* a
School of Biosciences, Cardiff University, Cardiff, UK, bAO Research Institute, Davos, Switzerland, and Department of Radiology, University of California San Diego, San Diego, USA
c
Received 16 November 2007; received in revised form 16 November 2007; accepted 17 December 2007
Entheses are the sites of attachment of a tendon, ligament, or joint capsule to bone. In a previous article new options for visualizing entheses and related structures, including ultrashort echo time (UTE) pulse sequences, and magic angle imaging were described. In this article an approach to image interpretation is described together with normal examples using UTE and other pulse sequences with and without magic angle imaging. Examples of images seen in disease are included. The new options for imaging entheses may provide useful options for biomechanical study and recognition of involvement in disease. ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction This paper aims to integrate and extend information from the previous paper1 in order to provide a basis for interpreting images of normal entheses and recognizing involvement in disease.
Image interpretation In disease, the common changes are an increase in T1 and T2, although conditions such as chronic calcification may decrease these parameters. Loss of order in collagen-rich tendon or ligaments may not only lead to an increase in T2, but also a reduction in the increase in T2 produced by the magic angle effect. The imaging sequences available on clinical systems for general musculoskeletal use can be divided into three groups1: long echo time [TEs; T2weighted fast spin-echo (FSE), proton density, and short tau inversion recovery (STIR)],2 short TE (T1weighted conventional CSE/FSE, spoiled gradient * Guarantor and correspondent: G.M. Bydder, Department of Radiology, University of California San Diego, 200 West Arbor Drive, San Diego, CA 92103-8226, USA. Tel.: þ1 619 471 0500; fax: þ1 619 471 0503. E-mail address: [email protected] (G.M. Bydder).
FSE, and other gradient echo), and2 ultrashort TE (UTE) imaging techniques. In general, the signal levels of enthesis tissues using the first two classes of sequences are low or zero, apart from magic angle effects. UTE sequences provide moderate or high signal intensity. Magic angle effects have lesser effects with long TE and UTE sequences and more obvious effects with short TE sequences. The magic angle effects depend on the baseline T2 (T2 with the majority of fibres at 0 to B0) and the fibre to B0 angle with a maximum increase in T2 around 55 and a lesser one at about 90 . The appearance of fibre structures is affected by the internal contrast, such as the difference between the principal fibre signal intensity and the endotenon signal intensity, but also the fibre to section orientation with a fascicular, punctuate or speckled pattern apparent with fibres perpendicular to the section, a blurred appearance when they are oblique and a linear pattern when fibres are parallel to the section. Contrast optimization follows from a consideration of T1, T2 and magic angle effects in health and disease. For T1, a general aim is to use a repetition time (TR; for T1-weighted SE sequences and spoiled gradient echo sequences) intermediate between the normal T1 and the usually longer T1 produced by disease whilst
0009-9260/$ - see front matter ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2007.12.010
Magnetic resonance imaging of entheses
allowing for the effect of flip angle. The same type of general rule applies to T2-weighted sequences in the short or long range with TE chosen to be between the two T2s of interest. Note that ‘‘T1weighted’’ sequences are also T2-weighted for the short T2s of enthesis tissues. To maximize contrast from magic angle effects, TE is typically chosen between the baseline T2 and the increased T2 produced by the magic angle effect. UTE sequences may behave somewhat differently as their signal may be augmented by an increased in T2 of very short T2 species, which are not detectable with fibres at 0 to B0. Many of the enthesis tissues are present as thin layers at boundaries and are subject to partial volume effects. The calcified layer of fibrocartilage may not be apparent in sections oblique to it as a consequence of this, and other effects. Contrast enhancement is affected by all the above considerations. It is not observable unless detectable signal is present. The effect then depends on the agent, its concentration, and the time course, as well as tissue vascularity and contrast transport properties. Normal uncalcified fibrocartilage (including enthesis and sesamoid fibrocartilage) is avascular, and contrast agents enter into this tissue slowly and by diffusion. Vascularity and the degree of contrast enhancement may be increased in disease. UTE sequences are subject to issues concerned with section selection, detection of short T2 components, as well as gradient performance and eddy current issues, which may result in blurring at tissue boundaries. Chemical shift artefacts of the first kind are typically radial and not a linear displacement in the (single) frequency encoded direction as with Cartesian mapping of k-space. There are a number of differential diagnoses arising from these and other considerations including1: normal fibrocartilage, partial volume effects from oblique fibres, magic angle effects with longitudinal fibres isointense to endotenon, and tissue fibrosis (or scar). Each of these may produce a loss of fascicular, punctuate, or speckled pattern in a localized area. The keys to differentiating these entities are fibre-to-B0 and fibreto-section considerations, as well as the location of the changes with respect to known sites of enthesis and sesamoid fibrocartilage.2
705
short T2 components due to fat or other forms of saturation, use of multiple-section acquisitions or section profile issues, as well as pathological changes.3
Magic angle effects and disease producing an increase in T2 Both may result in an increase in signal and a loss of fascicular pattern. The key is fibre to field angle.4
Normal appearance of enthesis with age This is yet to be determined in detail, but postmortem findings show signs of degeneration and vascularization with increasing age. The differential diagnosis may be any of the many overuse syndromes.5
Contrast enhancement This reflects vascularity and may be absent in fibrocartilage, but increased as a consequence of angiogenesis in diseased tendon and fibrocartilage. The time course is typically longer than that for normal tissues.6
The extent of enthesis and sesamoid fibrocartilage This may vary with compressive load, which may depend, for example, on the degree of prominence
Loss of signal from the calcified zone, which is a thin layer This may arise normally (or as a normal variant), from partial volume effects due to oblique sections, image blurring, reduction in signal from
Figure 1 Pronator teres insertion into the radius: axial difference UTE image (TR/TE ¼ 500/0.12 minus 4 ms). The tendon of pronator teres has a high signal (arrow) and merges with the periosteum of the shaft of the radius.
706
M. Benjamin et al.
of the superior tuberosity of the calcaneus for the Achilles tendon.7
Normal examples of magnetic resonance imaging (MRI) of entheses
Calcification
The radial enthesis of pronator teres is shown in Fig. 1 using a difference UTE image. It is an example of a fibrous enthesis. The tendon has a high signal (arrow) and becomes continuous with the surrounding high signal periosteum. The underlying bone is thick cortical rather than the thin shell and trabecular bone typically seen with fibrocartilaginous enthesis. The insertion of the Achilles tendon has been described as the premier enthesis and it exemplifies many of the features described previously. The sagittal image in Fig. 6a displays sesamoid and enthesis fibrocartilage as higher signal regions, and there is a close correspondence with the anatomical appearances. The higher signal from fibrocartilage is probably a consequence of its shorter T1. On the axial image (Fig. 2b) enthesis fibrocartilage has a higher signal and there is a higher signal region again (arrow) which probably represents calcified fibrocartilage. Fig. 3 shows an axial view of the long plantar ligament that has an amorphous fibrocartilaginous component with a higher signal in its proximal part, and a distal region in which linear fascicles are readily seen. The distal end of the patellar ligament shows an increase in signal in the sagittal plane5 (Fig. 4a; see later) and the axial image shows high signal in the deep part of the ligament adjacent to the tibia with reduction in the visibility
Which may have a relative long T2 in the acute phase but a short T2 in chronic form. In imaging of entheses, valuable information may be obtained from other techniques including plain films2 and ultrasound.3,4
Figure 2 Achilles tendon enthesis, sagittal (a) and axial (b) UTE images (TR/TE ¼ 500/0.12 ms) with the tendon at about 30 to B0. Sesamoid fibrocartilage has a high signal in (a) (arrow). Uncalcified sesamoid fibrocartilage is also posterior to the calcaneus seen in (b) together with calcified fibrocartilage (arrow).
Figure 3 Long plantar ligament axial UTE (TR/ TE ¼ 500/0.012 ms) image with the ligament at the magic angle. The fibrocartilaginous component has a high signal (arrows). The anterior portion has a linear pattern.
Magnetic resonance imaging of entheses
Figure 4 Patellar ligament: sagittal (a) and axial (b) gradient echo images (TR/TE ¼ 500/3.8 ms) with the tendon at about 30 to B0. The distal part of the ligament shows a high signal at its junction with the tibia (a) (arrow). The axial image shows a high signal and a relative loss of fascicular pattern in the deep portion of the ligament adjacent to the tibia (arrow).
of the fascicular pattern (Fig. 4b). This represents fibrocartilage in a region of the tendon which is subject to compression. The posterior cruciate ligament shows high signal at its femoral end (Fig. 5a) and a root-like trabecular bone pattern deep to the enthesis (Fig. 5b). The lateral collateral ligament of the knee shows a lower signal in its central region (arrow) and a higher signal in its femoral and fibular attachments (Fig. 6a) where the tendon is at 0 to B0. Less contrast is seen between the central and attachment regions when the tendon is oriented closer to the magic angle (Fig. 6b). The quadriceps tendon is an example of an extended enthesis organ, for when the knee is
707
Figure 5 Posterior cruciate ligament. Coronal (a) and sagittal (b) UTE (TR/TE ¼ 500/01.2 ms) and non-fat saturated gradient echo (TR/TE ¼ 500/4.6 ms) close to the magic angle. High signal is seen at the junction of the ligament with the femur (a) (arrow). A tree root-like pattern of trabecular bone is seen deep to the ligament in (b) (arrow).
flexed, the tendon is compressed against the underlying lateral femoral condyle (Fig. 7a). It is this region of the quadriceps tendon that shows increased signal and loss of fascicular pattern within the tendons on the axial images, consistent with the presence of fibrocartilage (Fig. 7b). However, this awaits microscopic confirmation. The transverse ligament of the atlas is subject to compression by the dens (odontoid process) and sesamoid fibrocartilage has been described at this
708
Figure 6 Lateral collateral ligament of the knee. Gradient echo (TR/TE ¼ 500/4.6 ms) coronal (a) and sagittal (b) images. At 0 to B0 (a) lower signal is seen in the central area of the ligament (arrow). The signal is more uniform at an orientation closer to the magic angle (b).
site in histological studies. This cartilage is readily apparent using UTE imaging (Fig. 8).
MRI of diseased entheses Histology of the overuse syndromes shows degenerative features rather than those typical of inflammation with tendon thinning, disruption of collagen fibres, microtears, increased granulation tissue, accumulation of lipids, amorphous debris, and calcium deposits. These are associated with
M. Benjamin et al.
Figure 7 Quadriceps tendon (an extended enthesis organ). Sagittal (a) and transverse (b) gradient echo (TR/TE ¼ 500/4.6 ms) images at about 30 to B0. With the knee flexed the tendon is compressed by the femur (a). The axial image shows high signal due to fibrocartilage in the region that is compressed (arrow).
a loss of morphological detail and an increase in T1 and T2 with MRI. Diffuse idiopathic skeletal hyperostosis is associated with enthesopathy.6,7 Metabolic diseases, including chondrocalcinosis, gout, hyperparathyroidism, primary hypoparathyroidism, fluorosis, and acromegaly, are also associated with enthesopathy. Involvement of entheses may precede that of cartilage in osteoarthritis. The seronegative spondyloarthropathies have been the principal diseases of interest and the pathology has been described in detail. This includes microfoci of inflammation often beginning as an erosion in a subchondral location. There may
Magnetic resonance imaging of entheses
709
Figure 8 Transverse ligament of the atlas. UTE (TR/ TE ¼ 500/0.08 ms) image. The transverse tensile fibres are lower signal than the fibrocartilaginous tissue adjacent to the odontoid process.
be marrow involvement resembling subacute or chronic osteomyelitis. Finally, the erosive lesions may heal by reactive formation of new bone within fibrous connective tissue. This may result in a new enthesis that protrudes relative to the initial enthesis. There has also been considerable interest in fibrocartilage involvement remote from traditional entheses and the significance of this in terms of the aetiology of the disease. Imaging involvement in asymptomatic regions has been described with conventional sequences and with UTE sequences (Figs. 9 and 10). Changes in the enthesis of the collateral ligament of the finger are seen in Fig. 11. There is increased signal in the ligament adjacent to bone (arrow). Enthesial changes are seen in the early stages of osteoarthritis.8,9
Healing and repair at entheses Several studies have focused on the problem of how tendons or ligaments can best be surgically re-attached to bone.10,11 Sharpey’s fibres are reported to develop at the new fibrocartilaginous attachment sites, although they are a normal
Figure 9 Achilles tendon in Reiter’s disease. Sagittal (a) and axial (b) UTE (TR/TE ¼ 500/0.08 ms images). The enthesis is thickened and has a higher signal intensity.
feature of fibrous rather than fibrocartilaginous entheses. This suggests that, at least during the early stages of repair, the mechanism may be different from that by which healthy fibrocartilaginous entheses initially develop.12 Enthesis fibrocartilage can be reconstituted in time; however, authors often comment on the poor quality of repair of reconstructions,13 the slow nature of the healing process,14 and the greater time for the entheses to be structurally restored.15 Of recent interest is the fact that restoration of a normal enthesis can be significantly enhanced by treating tendon bone grafts with a variety of biologically active modulators. These include osteogenic protein,16 suturing of periosteum along the surface of reattached
710
M. Benjamin et al.
Summary
Figure 10 Extensor tendon of the great toe; psoriatic arthropathy sagittal UTE (TR/TE ¼ 500/0.08 ms) image. The distal end of the tendon (in a region known from histology to have a sesamoid fibrocartilage within it) shows higher signal (arrow) probably due to inflammatory change.
tendons, which increases the availability of stem cells17 and direct application of stem cells.18 The use of imaging in this type of study has hardly begun.
Entheses are important regions of the body where it is possible to link anatomy, histology, and biochemistry to function, and understand features of these regions in biomechanical terms. The key tissues all show little or no signal with conventional imaging techniques, but provide a detectable signal and can be differentiated with UTE pulse sequences and magic angle imaging. It is then possible to observe features that have only previously been shown with histological studies. Understanding of the appearances of entheses involves consideration of tissue MR properties, fibre-to-field angle, magic angle effects, pulse sequences, geometrical factors including fibre-to-slice orientation and partial volume effects. There are likely to be new opportunities to study diffusion, magnetization transfer, perfusion, and T1 in the rotating frame of enthesis tissues using newer pulse sequences. In vivo recognition of these anatomical structures may provide new options for biomechanical study and diagnosis of earlier or milder forms of disease. This may include overuse syndromes, osteoarthritis, metabolic and seronegative disease. It is also possible that study of the regions of attachment of tendons and ligaments to bone may provide a better understanding of the process of repair following medical treatment and surgery.
References
Figure 11 Coronal image of the collateral ligament of the proximal interphalangeal joint in osteoarthritis. Spoiled gradient echo (SGE; TR/TE ¼ 500/1.8 ms). An area of increased signal is seen extending from the enthesis (arrow).
1. Benjamin M, Milz S, Bydder GM. Magnetic resonance imaging of entheses. Part 1. Clin Radiol 2008;63(6):691e703. 2. Resnick D, Niwayama G. Entheses and enthesopathy. Anatomical, pathological, and radiological correlation. Radiology 1983;146:1e9. 3. Morel M, Boutry N, Demondion X, et al. Normal anatomy of the heel entheses: anatomical and ultrasonographic study of their blood supply. Surg Radiol Anat 2005;27: 176e83. 4. Kamel M, Eid H, Mansour R. Ultrasound detection of heel enthesitis: a comparison with magnetic resonance imaging. J Rheumatol 2003;30:774e8. 5. Evans EJ, Benjamin M, Pemberton DJ. Fibrocartilage in the attachment zones of the quadriceps tendon and patellar ligament of man. J Anat 1990;171:155e62. 6. Gaucher AA, Pere PG, Gillet PM. From ankylosing spondylitis to Forestier’s disease: ossifying enthesopathy, a unifying concept. J Rheumatol 1990;17:854e6. 7. Littlejohn GO. More emphasis on the enthesis. J Rheumatol 1989;16:1020e2. 8. Tan AL, Grainger AJ, Tanner SF, et al. A high-resolution magnetic resonance imaging study of distal interphalangeal joint arthropathy in psoriatic arthritis and osteoarthritis: are they the same? Arthritis Rheum 2006;54:1328e33. 9. Tan AL, Toumi H, Benjamin M, et al. Combined high-resolution magnetic resonance imaging and histological examination to explore the role of ligaments and tendons in the phenotypic
Magnetic resonance imaging of entheses
10.
11.
12.
13.
14.
expression of early hand osteoarthritis. Ann Rheum Dis 2006; 65:1267e72. Shaieb MD, Singer DI, Grimes J, et al. Evaluation of tendon-tobone reattachment: a rabbit model. Am J Orthop 2000;29: 537e42. Aoki M, Oguma H, Fukushima S, et al. Fibrous connection to bone after immediate repair of the canine infraspinatus: the most effective bony surface for tendon attachment. J Shoulder Elbow Surg 2001;10:123e8. Gao J, Messner K, Ralphs JR, et al. An immunohistochemical study of enthesis development in the medial collateral ligament of the rat knee joint. Anat Embryol (Berl) 1996; 194:399e406. Jones JR, Smibert JG, McCullough CJ, et al. Tendon implantation into bone: an experimental study. J Hand Surg [Br] 1987;12:306e12. Thomopoulos S, Hattersley G, Rosen V, et al. The localized expression of extracellular matrix components in healing
711
15.
16.
17.
18.
tendon insertion sites: an in situ hybridization study. J Orthop Res 2002;20:454e63. Silva MJ, Boyer MI, Ditsios K, et al. The insertion site of the canine flexor digitorum profundus tendon heals slowly following injury and suture repair. J Orthop Res 2002;20: 447e53. Helm GA, Li JZ, Alden TD, et al. A light and electron microscopic study of ectopic tendon and ligament formation induced by bone morphogenetic protein-13 adenoviral gene therapy. J Neurosurg 2001;95:298e307. Chen CH, Chen WJ, Shih CH, et al. Enveloping the tendon graft with periosteum to enhance tendon-bone healing in a bone tunnel: a biomechanical and histologic study in rabbits. Arthroscopy 2003;19:290e6. Lim JK, Hui J, Li L, et al. Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy 2004;20:899e910.