RHEUMATOLOGY Rheumatology 2012;51:vii13vii17 doi:10.1093/rheumatology/kes342 Spondyloarthritis: a journey within and around the joint Peter V. Balint1 and Maria Antonietta D’Agostino2 Downloaded from https://academic.oup.com/rheumatology/article/51/suppl_7/vii13/1787041 by guest on 30 September 2021 Abstract Imaging has always been an integral part of the assessment of SpA. This group of diseases involving the axial skeleton and peripheral joints is a particularly intriguing area for sonographers, because it requires the evaluation of both articular and extra-articular regions. Among extra-articular features enthesitis has recently emerged as an area of special interest for both basic science and clinical researchers as well as for those working in the field of musculoskeletal imaging. This review provides information about research in this area focusing on the current concept and definition of enthesitis by US. Key words: spondyloarthritis, enthesitis, ultrasound, power Doppler. Introduction Enthesitis or enthesopathy? US in the past decade was often used for assessing In the literature, the term enthesitis (i.e. inflammatory peripheral involvement of SpA for clinical, educational involvement of the enthesis) and enthesopathy (i.e. patho- and research purposes rather than for the assessment logical involvement of the enthesis whatever the cause) of the more frequent axial manifestations of the disease are often used as synonyms; however, we prefer to use such as sacroiliitis. US can visualize most of the relevant enthesitis only for inflammatory involvement related to musculoskeletal pathologies associated with SpA, includ- SpA. Clinicians and researchers investigated enthesitis ing enthesitis, bone erosions, synovitis, bursitis and as the probable fundamental lesion responsible not only tenosynovitis. The exception is osteitis, since the US for entheseal involvement in itself, but also as an initial beam is not capable of penetrating the bony cortex. and/or additional process of synovitis, dactylitis and While conventional radiography allows a clear docu- sacroiliitis [1]. mentation of the later stages of the inflammatory changes In addition to peripheral arthritis and dactylitis, enthesi- of joint involvement, US (both grey-scale and Doppler) tis is included in several available classification criteria for are sensitive enough to also detect early inflammatory SpA, including the most recent criteria [2]. lesions. Examining the morphology and function of entheses is US features of synovitis, erosion and tenosynovitis in essential to understanding the process and phenomenon SpA patients generally do not differ from those observed of enthesitis. in other inflammatory arthritides including RA or PsA. The We can distinguish two types of enthesis according to main difference is related to the US appearance of enthe- their anatomical properties: fibrocartilaginous and fibrous. sitis, i.e. inflammation at the insertion of tendons, liga- The two types have different histological features. The ments and capsules into the bone. fibrocartilaginous enthesis consists of the tendon, non- calcified fibrocartilage, calcified fibrocartilage and adja- cent bone. The two layers of fibrocartilage are virtually separated by the tidemark. Defining fibrocartilage remains 1Third Department of Rheumatology, National Institute of Rheumatology and Physiotherapy, Budapest, Hungary and 2Service a challenge since it is considered by many as a sort of de Rhumatologie, Hoˆ pital Ambroise Pare´ , APHP, Universite´ Paris half-way structure between cartilage and dense collage- Ouest-Versailles Saint Quentin en Yvelines, Boulogne-Billancourt, nous connective tissue, but is actually closer in its con- France. formation to connective tissue than to cartilage [3]. Most Submitted 28 February 2012; revised version accepted 16 October 2012. of the histological studies describing this tissue are based Correspondence to: Maria Antonietta D’Agostino, Service de on the analysis of lower limb entheses. Rhumatologie, Hoˆ pital Ambroise Pare´ , APHP, Universite´ Paris Fibrocartilage was described as being within the Ouest-Versailles Saint Quentin en Yvelines, UPRES EA 2506, 9 Avenue Achilles enthesis itself (entheseal fibrocartilage); however, Charles de Gaulle, 92100 Boulogne-Billancourt, France. E-mail: [email protected] analogous tissue may also be found on the surface of the ! The Author 2012. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: [email protected] vii13 Peter V. Balint and Maria Antonietta D’Agostino calcaneus facing the enthesis (periosteal fibrocartilage) Despite considerable developments in US technique, and also in the inner surface of the Achilles tendon the past 10 years have seen the emergence of more re- which faces the calcaneus (sesamoid fibrocartilage) [3]. search questions that need to be answered. In the near This seems to denote that the retrocalcaneal bursa is future, high-end US machines will be capable of depicting only partly covered by a synovial lining, while the rest is fibrocartilage. At this moment ultrasonographic scans of covered by fibrocartilage. The same phenomenon may fibrocartilage have only been published using bovine spe- also be observed at other entheses, including the tibial cimens [4]. Differentiating between normal and patho- tuberosity enthesis and the deep infrapatellar bursa. logical fibrocartilage by US remains a challenge. This observation, associated with the clinical symptoms One explanation that may provide a link between the reported by patients, who frequently describe articular two concepts can be related to the duration of disease pain far from the anatomical entheseal attachment, has at the attachment site. If the disease is long-standing or Downloaded from https://academic.oup.com/rheumatology/article/51/suppl_7/vii13/1787041 by guest on 30 September 2021 led a group of researchers to distinguish between two very active, the inflammation transcends the limits of the concepts of entheseal involvement: one strictly localized anatomical insertion to involve the adjacent structures as to the bony interface in which the involved structures in- well. clude fibrocartilage, subchondral bone and related bone Demonstrating the presence of local inflammation at the marrow and its respective neural and vascular network; entheseal insertion establishes the enthesitis as a land- and the other more related to clinical symptoms in which mark feature of SpA. Examination of the pathological adjacent structures are also included, such as adjacent enthesis in SpA has demonstrated local inflammation bursae or synovial membrane-lined fat pads [3]. In this with CD4+ and CD8+ T lymphocyte cell infiltration, sense, this group has suggested that the enthesis oedema, angiogenesis, fibrosis, osteitis, erosion and should be considered as an organ or unit in which all con- new bone formation [5]. Inflammation may occur at any tinuous collagenous connective tissue fibres running over enthesis in SpA, but clinically detected symptoms of and along a fibrocartilage structure are considered as part enthesitis are more frequently detected in the entheses of the enthesis, even without the presence of an actual of the lower limbs, probably for mechanical reasons. The tendon or ligament insertion. Figure 1a shows knee and US examination of these entheses confirms the frequency Fig. 1b shows heel anatomy, including the superior pole, of their involvement [6]. However, we cannot exclude that inferior pole of the patella and tibial tuberosity enthesis the frequency of enthesitis may be artificially increased and the Achilles and plantar aponeurosis enthesis. and explained by the accessibility of those entheses to FIG.1Continuous fibres run along the length of the tendon or aponeurosis and may even connect two or three entheses (arrows). Images from P. V. Balint’s Doctor of Philosophy thesis (US imaging in joint and soft tissue inflammation), University of Glasgow, 2002. Courtesy of Miklo´ sTo´ th, Szabolcs Benis and Lajos Patonay. vii14 www.rheumatology.oxfordjournals.org US visualization of enthesitis in SpA US. In fact, when the entheses of the upper arms are consensus definitions of the most frequently detected examined, the entheses of the elbow, in particular the in- pathologies [10]. The group at that time decided to sertion of the common extensor tendon, appears to be define enthesopathy (general involvement of the enthesis frequently involved [6]. irrespective of the origin) instead of enthesitis: abnormally hypoechoic (loss of normal fibrillar architecture) and/or US appearance of enthesitis thickened tendon or ligament at its bony attachment (may occasionally contain hyperechoic foci consistent Extensive description of entheseal involvement in SpA pa- with calcification), seen in two perpendicular planes that tients by US was initially provided by Lehtinen et al.in may exhibit a Doppler signal and/or bony changes includ- 1994 [7] followed by the study of Balint et al. in 2002 [8] ing enthesophytes, erosions or irregularity. and that of D’Agostino et al. in 2003 [6]. The first two au- Taking into account other aspects such as age and Downloaded from https://academic.oup.com/rheumatology/article/51/suppl_7/vii13/1787041 by guest on 30 September 2021 thors described the grey-scale US abnormalities of lower gender may cause considerable problems when attempting limb enthesitis of SpA, revealing a high frequency of