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The Enthesis Organ Concept - Why Enthesopathies May Not Present As Focal Insertional Disorders. Arthritis & Rheumatism 2004
The Enthesis Organ Concept - Why Enthesopathies May Not Present As Focal Insertional Disorders. Arthritis & Rheumatism 2004
Objective. The Achilles tendon insertion is asso- organs, sesamoid and/or periosteal fibrocartilage was
ciated with a complex of adjacent fibrocartilages, a present in close association with synovium.
bursa, and a fat-pad, and is functionally much more Conclusion. The concept of an enthesis organ is of
than a focal insertion. This has important implications general significance in understanding attachment sites
for a better understanding of the spondylarthropathies and may explain the diverse pathologic changes, includ-
(SpA). However, the degree to which other insertions ing synovitis, bursitis, and extracapsular changes, seen
form comparable “enthesis organs” has not been estab- adjacent to tendon/ligament entheses in SpA. These
lished. The aim of this study was to demonstrate the findings may provide insight into the reason the target
applicability of the enthesis organ concept to other tissues in SpA are apparently so diverse.
insertion sites.
Methods. Both joint-related (articular) and extra- The enthesis is the region in which a tendon,
articular entheses were removed from 28 sites in the ligament, or joint capsule attaches to bone, and much of
limbs of formalin-fixed cadavers (age at death 70–101 the pathology in the spondylarthropathies (SpA) can be
years) that had been donated for anatomic study. The directly attributed to disease at that site. Although
samples were prepared for paraffin histologic analysis enthesopathies are traditionally viewed as focal, inser-
and sectioned longitudinally. The presence and extent of tional disorders, findings on magnetic resonance and
enthesis organs was evaluated at each site in serial ultrasound imaging suggest the presence of more diffuse
sections stained with Masson’s trichrome and toluidine changes with involvement of the adjacent bone and soft
blue. tissue. Thus, in SpA, inflammatory changes may occur
Results. Articular enthesis organs were found at some distance from the insertion site (1–4), and lateral
14 entheses, including the attachments of the digital epicondylitis is linked to degenerative changes not only
extensor tendons and collateral ligaments, the cruciate at the entheses associated with the common extensor
ligaments, tibialis anterior, the lateral collateral liga- origin, but also in adjacent ligaments (5–8). We believe
ment of the knee, and the popliteal tendon. Extraarticu- such findings are best understood by viewing insertion
lar enthesis organs were seen at 2 sites, the biceps sites not merely as focal attachments, but as parts of an
brachii and patellar tendon insertions. In all enthesis “enthesis organ complex” that may dissipate stress con-
centration at the bony interface away from the attach-
ment site itself (9).
Supported by Action Medical Research and Search, Hor- The archetypal enthesis organ is that of the
sham, UK. Professor Emery is an ARC Professor of Rheumatology. Achilles tendon, which Canoso has aptly described as
Professor McGonagle is an MRC Clinical Scientist.
1
M. Benjamin, PhD, S. Redman, PhD: University of Cardiff, having the “première enthesis” (10). Here, stress is
Cardiff, UK; 2B. Moriggl, MD, PhD, E. Brenner, MD, PhD, MME: dissipated away from the osteotendinous junction by
Medical University of Innsbruck, Innsbruck, Austria; 3P. Emery, MA, contact between the adjacent parts of the tendon and
MD, FRCP, D. McGonagle, FRCPI: Leeds Hospital Medical School,
Leeds, UK. bone in a dorsiflexed foot (9–11). The enthesis organ
Address correspondence and reprint requests to M. Ben- comprises not only the enthesis itself, but also fibrocar-
jamin, PhD, School of Biosciences, Cardiff University, Museum Ave- tilages in the walls of the adjacent retrocalcaneal bursa,
nue, Cardiff CF10 3US, UK. E-mail: benjamin@cardiff.ac.uk.
Submitted for publication April 2, 2004; accepted in revised together with the bursal cavity and its associated
form June 30, 2004. synovium-covered fat-pad (9,11). The fibrocartilages in-
3306
THE “ENTHESIS ORGAN” CONCEPT 3307
clude a sesamoid fibrocartilage in the deep part of the structures in SpA without adjacent synovitis, since they
tendon and a periosteal fibrocartilage on the opposing are so intimately linked (9).
superior tuberosity of the calcaneus. They replace the While the “enthesis organ” concept is clearly
synovial membrane that lines the bursa more proximally, relevant for understanding Achilles insertional tendi-
and it would be difficult to envisage disease of these nopathies, the extent to which it applies to other attach-
3308 BENJAMIN ET AL
We have described enthesis organs as being highlight the contribution of synovium to many enthesis
articular or extraarticular. All have in common the organs, and we thus suggest that synovitis would be an
presence of sesamoid and/or periosteal cartilage or anticipated consequence of enthesis organ inflamma-
fibrocartilage juxtaposed to a synovial cavity and thus tion. This applies to both articular and extraarticular
close to a synovial membrane. This either lines the joint enthesis organs. This is especially the case since the
cavity or forms part of a subtendinous bursa at the synovium, unlike the enthesis, contains macrophages.
attachment site. Articular enthesis organs include those Like the Achilles enthesis organ, those described here in
where the tendon/ligament fuses with a joint capsule association with the insertions of the biceps brachii and
(e.g., digital extensor tendons) or attaches inside a joint patellar tendons lack a synovial lining in part of the
cavity (e.g., the tibial attachment of the anterior cruciate bursa. This is not surprising since the tendon presses
ligament and the insertion of popliteus). The presence of against the bone, and compression would occlude syno-
elaborate enthesis organs in direct association with syno- vial vessels. It is exactly for this reason that synovium is
vial cavities, especially in joints such as the knee, enables absent over articular cartilage and at functional entheses
better understanding of the anatomic basis of entheseal- (wrap-around regions of tendons [9]). Indeed, the local
related diseases, including SpA. We have shown, for absence of synovium reinforces the similarities between
example, that the femoral enthesis of the lateral collat- many subtendinous bursae and typical synovial joints
eral ligament merges imperceptibly with that of the (9,10). Consequently, deep infrapatellar bursitis and
popliteal tendon. This was also evident in the magnetic bicipital bursitis may involve fibrocartilage degeneration
resonance imaging studies reported by Recondo et al in the bursal walls, as well as synovitis.
(16). Consequently, the 2 structures, together with the In conclusion, this study shows that the concept
associated synovium, form an enthesis organ as complex of the enthesis organ is not unique to the Achilles
as that of the tibialis posterior (12). Evidently, stress insertion, but is more general: enthesis organs are
could be dissipated between the ligament and the ten- present at many articular and extraarticular sites. The
don enthesis, and thus what may seem to be a pathologic intimate relationship between enthesis organs and syno-
process restricted to an extrasynovial structure (the vial cavities and the presence of enthesis organ compo-
lateral collateral ligament enthesis) could affect the nents in joint capsules may have important implications
inside of the joint as well. for understanding the clinical pattern of SpA, including
We have reported here that cartilage-covered, synovitis and extracapsular changes. It is important to
bony pulleys lie immediately adjacent to many entheses acknowledge, however, that entheses do not always form
and often contribute to the formation of enthesis organs. parts of archetypal enthesis organs like that of the
Either the enthesis itself lies in a shallow depression Achilles tendon, and this probably reflects local biome-
below the level of the adjacent bone (i.e., so that the chanical factors that influence stress dissipation. Signif-
adjacent bone acts as a pulley) or there is a small bony icantly, however, stress dissipation away from a single
protuberance next to the attachment site. The former is focused attachment site is virtually universal, because
exemplified by the insertion of popliteus, and the latter most tendons and ligaments fuse with adjacent struc-
by the tibial spine (intercondylar eminence) that contrib- tures or attach at more than one bony point.
utes to the tibial enthesis organ of the anterior cruciate
ligament, the radial tuberosity near the insertion of
biceps brachii, and the unnamed tubercle near the ACKNOWLEDGMENT
attachment of the tibialis anterior. All such pulleys
We are grateful to E. Richter for technical assistance.
dissipate stress concentration so that the risk of wear
and tear at entheses is reduced.
It has been proposed that the fundamental dif- REFERENCES
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