Magnetic resonance imaging of entheses. Part 1

Entheses are the sites of attachment of a tendon, ligament, or joint capsule to bone. Many features of entheses are adapted to disperse stress and accommodate compressive and shear forces at, or near, boundaries between tendons or ligaments and bone. Of particular interest is calcified and uncalcified fibrocartilage, which has mechanical properties that differ from those of tensile regions of tendons or ligaments, and from bone. Ultrashort echo time (UTE) pulse sequences can identify the specific tissue components of entheses and differentiate cortical bone, calcified fibrocartilage, uncalcified fibrocartilage, and fibrous connective tissue. Magic angle imaging can also differentiate tissues, such as fibrocartilage and tendon, which have different fibre orientations. Understanding the magnetic resonance (MR) appearance of entheses involves consideration of tissue properties, fibre-to-field angle, magic angle effects, pulse sequences, and geometrical factors including fibre-to-section orientation and partial volume effects. New approaches using MR imaging, allow entheses to be visualised with much greater detail than previously possible, and this may help in biomechanical studies, diagnosis of disease including overuse syndromes and spondyloarthropathies, as well as monitoring tissue repair and healing.     

Magnetic resonance: an introduction to ultrashort TE (UTE) imaging

The background underpinning the clinical use of ultrashort echo-time (UTE) pulse sequences for imaging tissues or tissue components with short T2s is reviewed. Tissues properties are discussed, and tissues are divided into those with a majority of short T2 relaxation components and those with a minority. Features of the basic physics relevant to UTE imaging are described including the fact that when the radiofrequency pulse duration is of the order T2, rotation of tissue magnetization into the transverse plane is incomplete. Consequences of the broad line-width of short T2 components are also discussed including their partial saturation by off-resonance fat suppression pulses as well as multislice and multiecho imaging. The need for rapid data acquisition of the order T2 is explained. The basic UTE pulse sequence with its half excitation pulse and radial imaging from the center of k-space is described together with options that suppress fat and/or long T2 components. Image interpretation is discussed. Clinical features of the imaging of cortical bone, tendons, ligaments, menisci, and periosteum as well as brain, liver, and spine are illustrated. Short T2 components in all of these tissues may show high signals. Possible future developments are outlined as are technical limitations.     

Structure-function relationships of entheses in relation to mechanical load and exercise

Entheses are regions of high-stress concentration that are commonly affected by overuse injuries in sport. This review summarizes current knowledge of their structure-function relationships - at the macroscopic, microscopic and molecular levels. Consideration is given to how stress concentration is reduced at fibrocartilaginous entheses by various adaptations which ensure that stress is dissipated away from the hard-soft tissue interface. The fundamental question of how a tendon or ligament is anchored to bone is addressed - particularly in relation to the paucity of compact bone at fibrocartilaginous entheses. The concept of an "enthesis organ" is reviewed - i.e. the idea of a collection of tissues adjacent to the enthesis itself, which jointly serve a common function - stress dissipation. The archetypal enthesis organ is that of the Achilles tendon and the functional importance of its subtendinous bursa, with its fibrocartilaginous walls and protruding fat pad, is emphasized. The distribution of adipose tissue elsewhere at entheses is also explained and possible functions of insertion-site fat are evaluated. Finally, a brief consideration is given to enthesopathies, with attention drawn to the possibility of degenerative changes affecting other regions of an enthesis organ, besides the enthesis itself.     

Entheses: tendon and ligament attachment sites

The current brief review focuses on certain issues relating to form–function relationships that are evident at tendon or ligament attachment sites (entheses). It evaluates the development of entheses (both fibrocartilaginous and fibrous) and highlights again an issue largely ignored for decades – i.e. how entheses attached to the metaphyses of long bones manage to keep the same relative position as the bones grow in length. Attention is drawn to the manner in which enthesis fibrocartilage prevents direct cell–cell communication between osteocytes and tendon/ligament cells and how (in a healthy enthesis) it presents a physical barrier separating the blood supply of bone from that of tendon/ligament. The possibility that the thoracolumbar fascia, with its multitude of muscular associations and numerous sites of ligamentous attachment could increase stress concentration at entheses is raised, the structure and development of enthesophytes (bony spurs) is reviewed as is the concept of a synovio-entheseal complex (SEC). How these functional anatomical units (SECs) could trigger pain and inflammation in athletes is briefly discussed.     

Contrast enhancement of short T2 tissues using ultrashort TE (UTE) pulse sequences

AIM: To review the effects of contrast administration on tissues with short T2s using a pulse ultrashort echo time (UTE) sequence. MATERIALS AND METHODS: Pulse sequences were implemented with echo times of 0.08 ms and three later gradient echoes. A fat-suppression option was used and later echo images were subtracted from the first echo image. Contrast enhancement with gadodiamide (0.3 mmol/kg) was used for serial studies in a volunteer. The images of 10 patients were reviewed for evidence of contrast enhancement in short T2 tissues. RESULTS: Contrast enhancement was seen in normal meninges, falx, tendons, ligaments, menisci, periosteum and cortical bone. In addition more extensive enhancement than with conventional pulse sequences was seen in meningeal disease, intervertebral disc disease, periligamentous scar tissue and periosteum after fracture. Subtraction of an image taken with a longer TE from the first image was of value in differentiating enhancement in short T2 tissues from that in long T2 tissues or blood. CONCLUSION: Contrast enhancement can be identified in tissues with short T2s using UTE pulse sequences in health and disease.     

Magnetic resonance imaging of short T2 components in tissue

The most widely used clinical magnetic resonance imaging techniques for the diagnosis of parenchymal disease employ heavily T(2)-weighted sequences to detect an increase or decrease in the signal from long T(2) components in tissue. Tissues also contain short T(2) components that are not detected or only poorly detected with conventional sequences. These components are the majority species in tendons, ligaments, menisci, periosteum, cortical bone and other related tissues, and the minority in many other tissues that have predominantly long T(2) components.The development and clinical application of techniques to detect short T(2) components are just beginning. Such techniques include magic angle imaging, as well as short echo time (TE), and ultrashort TE (Ute) pulse sequences. Magic angle imaging increases the T(2) of highly ordered, collagen-rich tissues such as tendons and ligaments so signal can be detected from them with conventional pulse sequences. Ute sequences detect short T(2) components before they have decayed, both in tissues with a majority of short T(2) components and those with a minority. In the latter case steps usually need to be taken to suppress the signal from the majority of long T(2) components. Fat suppression of different types may also be helpful. Once signal from short T(2) components has been detected, different pulse sequences can be used to determine increases or decreases in T(1) and T(2) and study contrast enhancement.Using these approaches, signals have been detected from normal tissues with a majority of short T(2) components such as tendons, ligaments, menisci, periosteum, cortical bone, dentine and enamel (the latter four tissues for the first time) as well as from the other tissues in which short T(2) components are a minority. Some diseases such as chronic fibrosis, gliosis, haemorrhage and calcification may increase the signal from short T(2) components while others such as loss of tissue, loss of order in tissue and an increase in water content may decrease them. Changes of these types have been demonstrated in tendonopathy, intervertebral disc disease, ligament injury, haemachromatosis, pituitary perivascular fibrosis, gliomas, multiple sclerosis and angiomas.Use of these techniques has reduced the limit of clinical detectability of short T(2) components by about two orders of magnitude from about 10 ms to about 100 micros. As a consequence it is now possible to study tissues that have a majority of short T(2) components with both "bright" and "dark" approaches, with the bright (high signal) approach offering options for developing tissue contrast of different types, as well as the potential for tissue characterization. In addition, tissues with a minority of short T(2) components may demonstrate changes in disease that are not apparent with conventional heavily T(2)-weighted sequences.     

Magnetic resonance imaging with ultrashort TE (UTE) PULSE sequences: technical considerations

It is now possible to detect signals from tissues and tissue components with short T(2)s, such as cortical bone, using ultrashort TE (UTE) pulse sequences. The background to the use of these sequences is reviewed with particular emphasis on MR system issues. Tissue properties are discussed, and tissues are divided into those with a majority and those with a minority of short T(2) components. UTE pulse sequences and their variants are described and clinical applications are illustrated. System design requirements for sequences of this type, including gradient performance, RF switching, and data-processing issues, are outlined.     

Magnetic resonance imaging of entheses. Part 2

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.     

Magnetic resonance imaging of the Achilles tendon using ultrashort TE (UTE) pulse sequences

AIM: To assess the potential value of imaging the Achilles tendon with ultrashort echo time (UTE) pulse sequences. MATERIALS AND METHODS: Four normal controls and four patients with chronic Achilles tendinopathy were examined in the sagittal and transverse planes. Three of the patients were examined before and after intravenous gadodiamide. RESULTS: The fascicular pattern was clearly demonstrated within the tendon and detail of the three distinct fibrocartilaginous components of an "enthesis organ" was well seen. T2* measurements showed two short T2* components. Increase in long T2 components with reduction in short T2 components was seen in tendinopathy. Contrast enhancement was much more extensive than with conventional sequences in two cases of tendinopathy but in a third case, there was a region of reduced enhancement. CONCLUSION: UTE pulse sequences provide anatomical detail not apparent with conventional sequences, demonstrate differences in T2* and show patterns of both increased and decreased enhancement in tendinopathy.     

Using adiabatic inversion pulses for long-T2 suppression in ultrashort echo time (UTE) imaging.

Ultrashort echo time (UTE) imaging is a technique that can visualize tissues with sub-millisecond T(2) values that have little or no signal in conventional MRI techniques. The short-T(2) tissues, which include tendons, menisci, calcifications, and cortical bone, are often obscured by long-T(2) tissues. This paper introduces a new method of long-T(2) component suppression based on adiabatic inversion pulses that significantly improves the contrast of short-T(2) tissues. Narrow bandwidth inversion pulses are used to selectively invert only long-T(2) components. These components are then suppressed by combining images prepared with and without inversion pulses. Fat suppression can be incorporated by combining images with the pulses applied on the fat and water resonances. Scaling factors must be used in the combination to compensate for relaxation during the preparation pulses. The suppression is insensitive to RF inhomogeneities because it uses adiabatic inversion pulses. Simulations and phantom experiments demonstrate the adiabatic pulse contrast and how the scaling factors are chosen. In vivo 2D UTE images in the ankle and lower leg show excellent, robust long-T(2) suppression for visualization of cortical bone and tendons.     

Attachment sites of the coracoclavicular ligaments are characterized by fibrocartilage differentiation: a study on human cadaveric tissue

We analyzed the immunohistochemical labeling patterns of the extracellular matrix of the coracoclavicular ligaments (CCL) in order to relate the molecular composition of the attachment sites to their mechanical environment. Ligaments were exposed from 12 fresh‐frozen human cadaveric samples (four males, mean age: 48.6±12.1 years). Cryosection of methanol‐fixed and decalcified tissue was cut and sections were labeled with a panel of monoclonal antibodies directed against collagens, proteoglycans and proteins of vascular components. Attachment sites of both ligaments showed characteristic fibrocartilaginous labeling of collagen type II, aggrecan and link protein in all samples. Labeling for type II collagen was most conspicuous at the insertion of the coracoid process. Morphometry of adjacent samples revealed a fibrocartilage zone of 10–15% in relationship with the ligament proper, where labeling for type II collagen, aggrecan and link protein was negative. The presence of fibrocartilage at both entheses of the trapezoid and conoid ligament suggests that the CCL complex is subject to shear/compression forces. A variable fibrocartilage differentiation at the entheses of both ligaments may be related to the marked change in loading and insertion angle that the ligaments undergo during shoulder movement.     

UTE imaging in the musculoskeletal system

Tissues, such as bone, tendon, and ligaments, contain a high fraction of components with "short" and "ultrashort" transverse relaxation times and therefore have short mean transverse relaxation times. With conventional magnetic resonance imaging (MRI) sequences that employ relatively long echo times (TEs), there is no opportunity to encode the decaying signal of short and ultrashort T₂/T₂* tissues before it has reached zero or near zero. The clinically compatible ultrashort TE (UTE) sequence has been increasingly used to study the musculoskeletal system. This article reviews the UTE sequence as well as various modifications that have been implemented since its introduction. These modifications have been used to improve efficiency or contrast as well as provide quantitative analysis. This article reviews several clinical musculoskeletal applications of UTE. J. Magn. Reson. Imaging 2015;41:870–883 . © 2014 Wiley Periodicals, Inc .     

Ultrashort echo time imaging with bicomponent analysis

Biological tissues frequently contain different water compartments, and these often have distinct transverse relaxation times. Quantification of these may be problematic on clinical scanners because spin echo sequences usually have initial echo times that are too long to accurately quantify shorter relaxation time components. In this study, an ultrashort echo time pulse sequence was used together with bicomponent analysis to quantify both the short and long T(2) components in tissues of the musculoskeletal system. Feasibility studies were performed using numerical simulation, and on phantoms and in vitro tissues including bovine cortical bone, ligaments, menisci, tendons, and articular cartilage. The simulation and phantom studies demonstrated that this technique can quantify T(2) * and fractions of the short and long T(2) components. The tissues studies showed two distinct components with short T(2) *s ranging from 0.3 ms for bovine cortical bone to 2.1 ms for menisci, and long T(2) *s ranging from 2.9 ms for bovine cortical bone to 35.0 ms for articular cartilage. The short T(2) * fraction ranged from 18.5% for patella cartilage to 80.9% for ligaments. The results show that ultrashort echo time imaging with bicomponent analysis can quantify the short and long T(2) water components in vitro in musculoskeletal tissues.     

The structure of the coracoacromial ligament: fibrocartilage differentiation does not necessarily mean pathology

The coracoacromial ligament forms part of the coracoacromial arch and is implicated in impingement syndrome and acromial spur formation. Here, we describe its structure and the composition of its extracellular matrix. Ligaments were obtained from 15 cadavers, nine from older people (average age 74.7 years) and six from younger individuals (average age 24.2 years). Cryosections of methanol-fixed tissue were cut and sections were immunolabelled with monoclonal antibodies against collagens, glycosaminoglycans, proteoglycans, matrix proteins and neurofilament proteins. Both ligament entheses were highly fibrocartilaginous and immunolabelled strongly for type II collagen, aggrecan and link protein. The area of labelling was more extensive in older people. However, fibrocartilage also characterized the ligament midsubstance, particularly with increased age. Signs of fibrocartilage degeneration were more common in older people. Ligament fat (containing blood vessels and nerve fibers) was conspicuous in both age groups, especially between fiber bundles at the entheses. We conclude that fibrocartilage is a normal feature but becomes more pronounced with age. It is not necessarily pathological, for it simply indicates that the ligament is subject to compression and/or shear. Nevertheless, the prominence of fibrocartilage at the acromial enthesis may relate to the frequency with which enthesophytes develop.     

Assessment of anterior cruciate ligament reconstruction using 3D ultrashort echo‐time MR imaging

This work demonstrates the potential of ultrashort TE (UTE) imaging for visualizing graft material and fixation elements after surgical repair of soft tissue trauma such as ligament or meniscal injury. Three asymptomatic patients with anterior cruciate ligament (ACL) reconstruction using different graft fixation methods were imaged at 1.5T using a 3D UTE sequence. Conventional multislice turbo spin‐echo (TSE) measurements were performed for comparison. 3D UTE imaging yields high signal from tendon graft material at isotropic spatial resolution, thus facilitating direct positive contrast graft visualization. Furthermore, metal and biopolymer graft fixation elements are clearly depicted due to the high contrast between the signal‐void implants and the graft material. Thus, the ability of UTE MRI to visualize short‐T₂ tissues such as tendons, ligaments, or tendon grafts can provide additional information about the status of the graft and its fixation in the situation after cruciate ligament repair. UTE MRI can therefore potentially support diagnosis when problems occur or persist after surgical procedures involving short‐T₂ tissues and implants. J. Magn. Reson. Imaging 2009;29:443–448. © 2009 Wiley‐Liss, Inc.     

Comparison of optimized soft-tissue suppression schemes for ultrashort echo time MRI

Ultrashort echo time (UTE) imaging with soft-tissue suppression reveals short-T(2) components (typically hundreds of microseconds to milliseconds) ordinarily not captured or obscured by long-T(2) tissue signals on the order of tens of milliseconds or longer. Therefore, the technique enables visualization and quantification of short-T(2) proton signals such as those in highly collagenated connective tissues. This work compares the performance of the three most commonly used long-T(2) suppression UTE sequences, i.e., echo subtraction (dual-echo UTE), saturation via dual-band saturation pulses (dual-band UTE), and inversion by adiabatic inversion pulses (IR-UTE) at 3 T, via Bloch simulations and experimentally in vivo in the lower extremities of test subjects. For unbiased performance comparison, the acquisition parameters are optimized individually for each sequence to maximize short-T(2) signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR) between short- and long-T(2) components. Results show excellent short-T(2) contrast which is achieved with these optimized sequences. A combination of dual-band UTE with dual-echo UTE provides good short-T(2) SNR and CNR with less sensitivity to B(1) homogeneity. IR-UTE has the lowest short-T(2) SNR efficiency but provides highly uniform short-T(2) contrast and is well suited for imaging short-T(2) species with relatively short T(1) such as bone water.     

Designing long-T2 suppression pulses for ultrashort echo time imaging.

Ultrashort echo time (UTE) imaging has shown promise as a technique for imaging tissues with T2 values of a few milliseconds or less. These tissues, such as tendons, menisci, and cortical bone, are normally invisible in conventional magnetic resonance imaging techniques but have signal in UTE imaging. They are difficult to visualize because they are often obscured by tissues with longer T2 values. In this article, new long-T2 suppression RF pulses that improve the contrast of short-T2 species are introduced. These pulses are improvements over previous long-T2 suppression pulses that suffered from poor off-resonance characteristics or T1 sensitivity. Short-T2 tissue contrast can also be improved by suppressing fat in some applications. Dual-band long-T2 suppression pulses that additionally suppress fat are also introduced. Simulations, along with phantom and in vivo experiments using 2D and 3D UTE imaging, demonstrate the feasibility, improved contrast, and improved sensitivity of these new long-T2 suppression pulses. The resulting images show predominantly short-T2 species, while most long-T2 species are suppressed.     

The bone-ligament junction: A comparison between biological and artificial ACL reconstruction

The physiological bone-ligament junction is composed of four zones: ligament, fibrocartilage, calcified fibrocartilage and bone. It plays a very important part in the distribution of mechanical loads applied to ligaments so as to diminish stress concentration or shearing at the interface. This paper examines types of bone and neoligament insertion after anterior cruciate ligament (ACL) reconstruction with a Dacron prothesis, the Leeds-Keio scaffold ligament (LK), patellar tendon with LAD augmentation (PT+LAD) and bone patellar tendon bone alone (PT). The anterior cruciate reconstructions were implanted in 16 sheep via double-isometric bone tunnels without postoperative knee immobilization. Histological examination of the new insertions (using haematoxylin-cosin, Giemsa, Masson, and Mallory stains) was performed following animal sacrifice after 2, 3, 6 and 9 months. A layer of fibrocartilage between the bone and the ligament was observed with PT, followed by a nearly normal insertion after 6 months. With PT, followed by PT+LAD, the augmentation was surrounded by fibrous tissue (also noted inside the LAD). The PT insertion was virtually physiological after 3–6 months. With the LK scaffold, fibrous tissue was noted in and around the scaffold, even after 6 and 9 months. With the Dacron prosthesis, fibrous tissue around the ligament was unaccompanied by ingrowth into the prosthesis. Nerve endings (pacinian corpuscles) were only present in the PT. These findings show that even after 9 months artificial ligaments are separated from bone by fibrous tissue and devoid of the histological and biomechanical features of a physiological junction. PT alone was the only technique that resulted in formation of a structure very similar to the physiological junction, capable of protecting the bone against excessive shearing stress and the tendon against excessive strains.     

影响短T2成分MR三维超短回波时间双回波脉冲序列成像质量因素的探讨

目的 探讨3D超短回波时间(UTE)舣回波脉冲序列成像的相关成像参数及后处理技术对图像质量的影响.方法 对主要含短T2成分的人于燥股骨标本及一组健康志愿者的胫骨、膝关节、踝部肌腱行MR 3D UTE舣回波脉冲序列成像.通过计算、比较图像的信噪比(SNR)或对比噪声比(CNR)及对图像伪影的分析,探讨系统内部不同轨道延迟时间(-6、-3、-2、-1、0、1、2、3 s)、不同反转角(4°、8°、12°、16°、20°、24°)、不同TE1(0.08、0.16、0.24、0.35 ms)及不同后处理技术(超短回波减影差异图、容积超短回波减影差异图)对图像质量的影响.结果 骨皮质、骨膜、半月板、肌腱、韧带等在UTE图像上表现为高信号.所设的不同轨道延迟时间中,获得最佳SNR的轨道延迟时阳间为2 s.活体人UTE成像的最佳反转角为8°～12°.不同TE1时间的图像质量不同,TE1为0.08 ms时,图像的CNR最佳.随TE1时阳延长,图像伪影逐渐增多.将原始双回波图经多平面重组后再相减(容积超短回波减影差异图),图像SNR明显增加.结论 短T2成分在3D UTE双回波脉冲序列成像上表现为高信号.通过改变反转角和将2次回波图像经MPR后再相减可增加图像SNR.缩短TE1时间可增加图像质量.

Abstract：

Objective To investigate the effect of imaging parameters and postprocessing methods on the quality of MR imaging of short T2 components with 3D ultrashort TE (UTE) double echo pulse sequence. Methods 3D UTE double echo pulse sequence was performed on dry human femoral specimen and the tibial diaphyses, knee joints, and tendons of ankles of a group of healthy volunteers. To investigate the effect of different trajectory delays of the imaging system(-6, -3, -2, - 1,0, 1,2, 3 s), different flip angles(4°, 8°, 12°, 16°, 20°, 24°), different TEs (0. 08, 0. 16, 0. 24, 0. 35 ms)and different postprocessing methods(difference imaging of subtracted volume and non-volume UTE)on the 3D UTE MR imaging quality, the SNR and CNR were calculated and compared, and the artifacts of the images were analysed. Results The cortical bone, periosteum, tendon and meniscus showed high signal intensity on the images of UTE pulse sequence. The best SNR was acquired with 2 s trajectory delay. The best flip angle was 8° to 12° for the human UTE imaging in vivo. The highest CNR was obtained from the TE of 0. 08 ms. The longer the TE was, the more artifacts appeared. The SNR of difference imagewas improved when image subtraction was performed afer multiplanar reconstruction (MPR) of the primary double echo images.Conclusions The short T2 components show high signal intensity on the MRI of 3D UTE double echo pulse sequence. The imaging quality can be improved by shortening TE, using appropriate flip angle and performing subtraction for difference image after MPR of the primary double echo images.     

Assessment of cortical bone with clinical and ultrashort echo time sequences

We describe the use of ultrashort echo time (UTE) sequences and fast spin echo sequences to assess cortical bone using a clinical 3T scanner. Regular two‐ and three‐dimensional UTE sequences were used to image both bound and free water in cortical bone. Adiabatic inversion recovery prepared UTE sequences were used to image water bound to the organic matrix. Two‐dimensional fast spin echo sequences were used to image free water. Regular UTE sequences were used together with bicomponent analysis to measure T*₂s and relative fractions of bound and free water components in cortical bone. Inversion recovery prepared UTE sequences were used to measure the T*₂ of bound water. Saturation recovery UTE sequences were used to measure the T₁ of bone water. Eight cadaveric human cortical bone samples and a lower leg specimen were studied. Preliminary results show two distinct components in UTE detected signal decay, a single component in inversion recovery prepared UTE detected signal decay, and a single component in saturation recovery UTE detected signal recovery. Regular UTE sequences appear to depict both bound and free water in cortical bone. Inversion recovery prepared UTE sequences appear to depict water bound to the organic matrix. Two‐dimensional fast spin echo sequences appear to depict bone structure corresponding to free water in large pores. Magn Reson Med 70:697–704, 2013. © 2012 Wiley Periodicals, Inc.