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Enthesis represents the site of insertion of tendon, ligament, fascia, or joint capsule into the bone.
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Ultrasound is able to visualize the entheseal involvement in the course of many inflammatory and noninflammatory rheumatic diseases.
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Power Doppler is important for detecting inflammation of enthesis.
The enthesis is the site of insertion of a tendon, ligament, fascia, or joint capsule into the bone ( Fig. 9-1 ). Knowledge regarding the function, anatomy, and physiology of the enthesis has led to improved understanding of entheseal pathology in the course of many inflammatory and noninflammatory rheumatic diseases.
The two types of enthesis are fibrous and fibrocartilaginous. The latter consists of four anatomic zones: the collagen zone (e.g., ligament, capsule, tendon, aponeurosis, annulus); noncalcified fibrocartilaginous zone; tidemark-calcified fibrocartilaginous zone; and subchondral bone zone. The fibrocartilaginous enthesis is usually observed in the attachment of peripheral muscles.
Involvement of the enthesis in any pathologic process—metabolic, inflammatory, traumatic, or degenerative—is referred to as enthesopathy , and the term enthesitis is restricted to inflammatory enthesopathy, which appears to be a cardinal feature of spondylarthritis. Although Niepel and colleagues first used the term for describing inflammatory symptoms at insertional sites as an important feature of ankylosing spondylitis, enthesitis is a common characteristic feature of all spondylarthritis complexes, which include psoriatic arthritis, reactive arthritis, arthritis associated with inflammatory bowel disease, and the undifferentiated forms. In his “Heberden Oration,” Ball suggested that ankylosing spondylitis and rheumatoid arthritis were different primarily in the organs they targeted. He suggested that inflammation at the enthesis is the distinctive pathologic feature of ankylosing spondylitis. In contrast, the characteristic feature of rheumatoid arthritis is a persistent inflammatory synovitis symmetrically involving mainly the peripheral joints.
Enthesitis
Imaging Findings
Understanding the imaging findings of peripheral enthesitis hinges on a thorough knowledge of the joint anatomy. Historically, the radiographic features of enthesitis have played a pivotal role in defining enthesitis lesions of spondylarthritis. They include bone insertion osteopenia, bone cortex irregularity at the insertion, erosion, entheseal soft tissue calcification, and new bone formation ( Fig. 9-2 ). However, entheseal bone changes appear late and are also common in mechanical disorders and in crystal-related pathology. Moreover, aging is associated with an increased prevalence of asymptomatic radiographic enthesopathy . Before the extensive use of magnetic resonance imaging (MRI) and ultrasound for studying inflammatory changes of articular and periarticular structures, scintigraphic studies revealed a diffuse increase in bone and articular uptake in patients with active spondylarthritis. However, the poor spatial resolution of this technique does not permit an anatomic explanation of these findings.
Ultrasound identification of the involvement of entheses in spondylarthritis patients was described for the first time by Lehtinen and colleagues in 1994 and then by Balint and colleagues in 2002. The investigators described the gray-scale abnormalities of lower limb enthesitis of spondylarthritis and the high frequency of asymptomatic findings. Gray-scale ultrasound can depict signs of acute and chronic inflammation of enthesis and show structural damage. Enthesitis seen on gray-scale ultrasound is characterized by the loss of normal fibrillar echogenicity of the tendon insertion with an increased thickness of the insertion or by intralesional focal changes of the tendon insertion, such as calcific deposits, fibrous scars, and periosteal changes (i.e., erosions or new bone formation). Clear involvement of the body of the tendon far from the enthesis and of the adjacent bursae can be observed.
Later, discordant data were published about the capability of gray-scale ultrasound to differentiate enthesis involvement in spondylarthritis from involvement in other pathologies, including rheumatoid arthritis. This discordance can be explained by the absence in those studies of a common clear definition of enthesis involvement (most included in such definitions the involvement of tendon and bursa), and by the lack of a clear definition of inflammatory changes by using gray-scale ultrasound only. Inflammation on gray-scale ultrasound mainly is seen as edema, which is characterized by the loss of normal echo structure (associated or not with increased thickness of the tendon insertion) and which is usually difficult to objectively quantify. The use of power Doppler for visualizing abnormal vascularization and hyperemia of soft tissues in inflammatory joint diseases was extensively demonstrated.
The first description of the usefulness of power Doppler ultrasound for studying enthesitis was published by D’Agostino and colleagues in 2003. Power Doppler ultrasound was used to detect enthesitis in spondylarthritis patients and in controls (i.e., rheumatoid arthritis patients and mechanical spinal disease patients). Abnormal vascularization at the enthesis insertion was exclusively detected in spondylarthritis patients. This method may permit differentiation of involvement in spondylarthritis from involvement in other mechanical and metabolic disorders.
These original results have been confirmed by other studies outlining the ability of power Doppler ultrasound to reveal inflammation of the enthesis in spondylarthritis patients, and the results led to the proposal of several scoring systems. Despite these promising results, power Doppler ultrasound has not been used for the management of spondylarthritis as often as for rheumatoid arthritis. This discrepancy probably can be attributed to the perception that ultrasound is an inseusitive imaging technique and to the greater difficulty of assessing vascular blood flow with Doppler in the entheses than in other tissues such as the synovium, because of the greater abundance of vessels in the inflamed synovium than in the enthesis and because there are more Doppler artifacts at the enthesitic site because of the proximity of a highly reflecting surface, the cortical bone.
Another important limitation is the lack of criterion validity. Histologic investigation is considered the gold standard for the demonstration of soft tissue inflammation. In spondylarthritis, because of the difficulties in obtaining tissues for histologic evaluation, there are no studies comparing histologic evidence of inflammation and signs of enthesitis assessed with ultrasound. One small study used ultrasound-guided biopsy of acute Achilles enthesitis in patients with spondylarthritis and sampled regions of gray-scale change and thickening. The procured tissues showed macrophage infiltration, increased vascularity, and edema. Moreover, two histologic studies have demonstrated that aged, normal entheses may have bone microdamage at the enthesis associated with microscope vascular changes, which are likely involved in the repair response. Vascular changes also occur adjacent to enthesophytes in the normal, aged enthesis. This “normal” vascularization cannot be visualized by using power Doppler ultrasound, even when the Doppler signal is enhanced by using medium ultrasound contrast agents.
In this context, two competencies are critically needed for sonographers to optimize enthesitis assessment by power Doppler ultrasound: thorough knowledge of the anatomy of each enthesis (particularly the location of normal nutrition vessels), and the ability to differentiate very slow vascular flow (the hallmark of the inflammatory process in the enthesis) from artifacts on power Doppler. Another factor affecting the quality of the ultrasound assessment is the type of Doppler device used.
Ultrasound Definition of Enthesitis
The Outcome Measures in Rheumatoid Arthritis Clinical Trials (OMERACT) ultrasound group proposed an ultrasound definition for elementary pathologic joint findings, including enthesopathy. These experts decided to define enthesopathy instead of enthesitis to include mechanical and inflammatory pathologies. The preliminary definition of enthesopathy proposed by the OMERACT ultrasound group was an “abnormal hypoechoic (loss of normal fibrillar architecture) and/or thickened tendon or ligament at its bony attachment (may occasionally contain hyperechoic foci consistent with calcification), seen in two perpendicular planes that may exhibit Doppler signal and/or bony changes, including enthesophytes, erosions, or irregularity” ( Fig. 9-3 ). In this definition, acute and chronic inflammatory aspects in gray-scale ultrasound (i.e., loss of normal echo structure, increased thickness, or focal calcific deposits) and Doppler ultrasound are combined with findings of structural damage (i.e., enthesophytes and bony erosions). This combination may be helpful for diagnostic purpose (i.e., presence or absence of enthesis involvement) but probably not for responsiveness or for the differential diagnosis of inflammatory diseases (i.e., spondylarthritis versus rheumatoid arthritis versus mechanical or metabolic entheseal involvement).
Normal Ultrasound Aspects of Peripheral Enthesis
Under normal conditions, the four zones of fibrocartilaginous enthesis are not visible or are barely visible due to the small thickness of the fibrocartilage and to the quality and resolution of ultrasound equipment ( Fig. 9-4 ). The normal ultrasound aspect of the enthesis is difficult to distinguish from the ultrasound aspect of the body of tendon or ligament, and it appears as a normal continuity of the tendon or ligament into the bone.
Ultrasound Definitions of Elementary Components of Enthesitis
Recently the OMERACT and European League Against Rheumatism (EULAR) ultrasound group tried to standardize the definition of each elementary component contributing to the definition of enthesitis. They first considered enthesitis as involvement of the enthesis, which is different from involvement of the bursa and the body of the tendon. The bursa and tendon can be involved in the inflammatory process of spondylarthritis, but they should be evaluated as different structures and not included in the ultrasound definition of enthesitis. On gray-scale ultrasound, enthesitis is characterized by the following elementary components:
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Hypoechogenicity of the insertion of the tendon, ligament, or capsule into the bone, which can be defined as a lack of the homogeneous echotexture pattern with a loss of tightly packed echogenic lines after correcting for anisotropy artifact ( Fig. 9-5 )
