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ARTHRITIS & RHEUMATISM

Vol. 50, No. 10, October 2004, pp 3306–3313


DOI 10.1002/art.20566
© 2004, American College of Rheumatology

The “Enthesis Organ” Concept

Why Enthesopathies May Not Present as Focal Insertional Disorders

M. Benjamin,1 B. Moriggl,2 E. Brenner,2 P. Emery,3 D. McGonagle,3 and S. Redman1

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

Table 1. Entheses examined


Type of
Enthesis enthesis organ Comments*
Upper limb
Biceps brachii insertion Extraarticular SF and PF conspicuous where the area of the enthesis attachment
is small; closely related to synovium
Extensor pollicis longus insertion Articular Prominent SF in the deep surface of the tendon; articular
cartilage acts as a PF; closely related to synovium
Extensor digitorum communis insertion Articular Prominent SF in the deep surface of the tendon; articular
cartilage acts as a PF; closely related to synovium
Collateral ligament of proximal interphalangeal Articular SF in the deep surface of the ligament; articular cartilage acts as
joint a PF; closely related to synovium
Triceps insertion None Blends with adjacent fascia as well as attaching to olecranon
Abductor pollicis brevis and abductor pollicis Articular The tendon fuses with the joint capsule which contains SF, is
longus insertion closely related to synovium, and is juxtaposed to articular
cartilage, which acts as a PF
Flexor carpi ulnaris insertion None Continuous with attachment of ligaments to pisiform
Flexor digitorum profundus insertion Articular The tendon fuses with the volar plate, which is fibrocartilaginous;
articular cartilage acts as a PF for the volar plate; closely
related to synovium
Lower limb
Tibialis anterior insertion Articular One slip of the tendon contributes to forming an enthesis organ
for the other; closely related to synovium
Patellar tendon insertion Extraarticular A PF of variable prominence is present, depending on the shape
of the bone near the enthesis; closely related to synovium and
fat-pad
Patellar tendon origin None Superficial fibers are continuous with those of the quadriceps
tendon; closely related to Hoffa’s fat-pad
Quadriceps tendon insertion None Superficial fibers are continuous with those of the quadriceps
tendon
Fibularis brevis insertion None The tendon fuses with the joint capsule, which in turn is closely
related to synovium; no SF or PF
Fibularis longus insertion None Fat present in abundance near enthesis, but no other evidence of
an enthesis organ; separate tendon slips to medial cuneiform
and first metatarsal bone
Popliteal tendon (femoral attachment ⫹ lateral Articular Forms a complex enthesis organ; SF sometimes present in deep
collateral ligament) surface; articular cartilage acts as a PF; closely related to
synovium
Anterior cruciate ligament (tibial attachment) Articular The tibial spine is covered with articular cartilage, which acts as a
PF; No SF; closely related to synovium
Anterior cruciate ligament (femoral attachment) None Also attached to the lateral meniscus
Posterior cruciate ligament (tibial attachment) Articular No SF, but lies close to the horn of the posterior meniscus, which
acts as a PF; closely related to synovium
Posterior cruciate ligament (femoral attachment) None Also attached to the lateral meniscus
Lateral head of gastrocnemius None Tendon also arises from the knee joint capsule
Iliopsoas insertion None Some fibers extend beyond the lesser trochanter to the adjacent
part of the femur
Pes anserinus insertion None Subtendinous bursa present; no SF or PF, but thick periosteum
Adductor longus origin None Fuses with tendons of rectus abdominis and gracilis
Extensor hallucis longus insertion Articular Prominent SF in the deep surface of the tendon; articular
cartilage acts as a PF; closely related to synovium
Flexor hallucis longus insertion Articular Fuses with fibrocartilaginous volar plate and articular cartilage
acts as a PF for this; closely related to synovium
Extensor digitorum longus Articular SF in the deep surface of the tendon; articular cartilage acts as a
PF; closely related to synovium

* SF ⫽ sesamoid fibrocartilage; PF ⫽ periosteal fibrocartilage.

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

ment sites is less clear. From a clinical perspective, the


changes in SpA may include synovitis, bursitis, and
diffuse, fusiform, synovial joint swelling. Such changes
attest to the fact that the enthesis-related pathology is
more than insertion-point inflammation. The purpose of
this study was to determine the general applicability of
the enthesis organ concept, by evaluating a wide range of
entheses including those within joints, adjacent to joints,
and at extraarticular sites. We demonstrated that inser-
tions at many sites frequently form part of enthesis
organs that are intimately associated with a synovial
cavity and thus with synovial membrane. These findings
may be central to elucidation of the relationship be-
tween enthesitis and synovitis and for recognition of the
diverse clinical presentations of SpA. They thus have
implications with regard to a better understanding of the
disease mechanisms.

MATERIALS AND METHODS


A wide range of entheses from 28 different sites were
obtained from the upper and lower limbs of cadavers (both Figure 1. The articular enthesis organ of the popliteal tendon (PT)
sexes; age at death 70–101 years) at the University of Cardiff and the lateral collateral ligament (LCL). a, Note the complete
and the University of Innsbruck. The cadavers had been continuity of the tendon and ligament entheses (arrows). F ⫽ femur.
donated for anatomic study (medical histories were not avail- Bar ⫽ 2 mm. b, An integral part of the enthesis organ is the popliteal
able) and had been perfused with a solution containing form- groove of the femur, which is covered with articular cartilage (AC).
aldehyde and alcohol; details have been reported previously The popliteal tendon bends over the groove, and there is an interven-
(11). Between 2 and 11 specimens were examined for each ing fold of synovial tissue (arrow), which is particularly prominent in
enthesis. The attachment sites chosen are listed in Table 1. The this specimen. The enthesis itself lies just out of the picture, to the
rationale for the selection of sites was 1) the inclusion of right. Bar ⫽ 2 mm. c, In some specimens, a sesamoid fibrocartilage is
“articular” entheses that attached within a synovial joint (e.g., present in the tendon opposite the groove. Here it shows evidence of
the cruciate ligaments [which are entirely intraarticular, yet mucoid degeneration (arrow). Bar ⫽ 100 ␮m. d, Evidence of cartilage
extrasynovial] and the popliteal tendon/lateral collateral liga- differentiation (arrows) in the synovial fold associated with the
ment complex) or replaced part of the joint capsule (e.g., enthesis organ. Bar ⫽ 50 ␮m. (Masson’s trichrome–stained in a, b, and
digital extensor tendons, interphalangeal joint collateral liga- d; toluidine blue–stained in c.)
ments, and the insertional tendons of tibialis anterior and
fibularis brevis) and were thus intimately juxtaposed with its
synovium, 2) the inclusion of extraarticular entheses that were
close to joints and associated with subtendinous bursae (e.g., general architecture of the whole enthesis organ in the context
the pes anserinus and biceps brachii insertional tendons), and of neighboring structures).
3) the inclusion of entheses from regions in which periostitis
occurs. RESULTS
In sampling the entheses, 2 fine saw cuts were made Enthesis organs can be broadly classified as joint
into the bone, parallel to the long axis of the tendon, and 2
further cuts were made at right angles to the long axis, related (hereinafter called “articular”) or extraarticular,
proximal and distal to the enthesis itself. Because of the size of according to whether the enthesis lies internal or exter-
the patellar tendon enthesis, only the central third of the nal to the capsule of a synovial joint. We found that
attachment site was sampled. In accordance with our previ- many entheses formed part of an enthesis organ—some
ously described protocol (12), all specimens were further fixed simple, but others complex (see Table 1). In articular
for at least 1 week in 10% neutral buffered formol saline
before being decalcified in 5% nitric acid, dehydrated with enthesis organs, the synovial membrane with which the
graded alcohol, cleared with chloroform, and embedded in enthesis is associated was a joint cavity. In extraarticular
58oC paraffin wax. Longitudinal sections of the enthesis and enthesis organs, it was that of a subtendinous bursa.
adjacent structures were cut at 8 ␮m, at 1-mm intervals Articular enthesis organs. The lateral collateral
throughout the block. ligament and the popliteal tendon were shown to con-
At each sample point, 16 sections were collected and
mounted on 8 slides. Adjacent slides were stained with tolu- tribute to the formation of one of the most elaborate of
idine blue (to highlight the presence of fibrocartilage by its articular enthesis organs (Figure 1). Their entheses were
metachromasia) and Masson’s trichrome (to illustrate the directly continuous with one another (Figure 1a), and
THE “ENTHESIS ORGAN” CONCEPT 3309

where it normally bifurcated into 2 slips—a deeper


cuneiform slip and a more superficial, metatarsal slip
(Figure 2a). At such attachments, the enthesis fibrocar-
tilage of the cuneiform slip also served as a periosteal
fibrocartilage for the metatarsal slip—this latter slip
passed over the former. Indeed, adjacent to the cunei-
form attachment site, the enthesis fibrocartilage was
directly continuous with a periosteal cartilage/
fibrocartilage covering a small bony elevation (Figure

Figure 2. The articular enthesis organ of the insertional tendon of the


tibialis anterior. a, The region where the tendon splits into a metatarsal
(MT) and a cuneiform (C) slip. The enthesis fibrocartilage (EF) of the
latter “doubles” as a periosteal fibrocartilage for the former. Note also
that there is a bursa between the 2 slips (arrow) and that the deep
surface of the tendon has a sesamoid fibrocartilage (SF) in the region
indicated. Bar ⫽ 2 mm. b, Immediately adjacent to the enthesis of the
cuneiform slip (not shown), there is a small bony elevation on the
medial cuneiform (MC) that is covered with a thick periosteal fibro-
cartilage (arrow). The metatarsal slip of the tendon also passes over
this tubercle (as well as over the cuneiform enthesis itself; see a) and
fuses with the joint capsule (JC) to form a single enthesis (E). Bar ⫽
2 mm. c, A prominent and highly vascular synovium (S) protrudes from
the undersurface of the capsule (CAP) into the joint cavity. AC ⫽ Figure 3. Macroscopic views of the articular enthesis organs associ-
articular cartilage at the base of the first metatarsal bone. Bar ⫽ 500 ated with digital tendons and ligaments. a, Extensor pollicis longus:
␮m. (Toluidine blue–stained in a; Masson’s trichrome–stained in b and sagittal section of the interphalangeal joint of the thumb. The enthesis
c.) organ consists of the enthesis (E) itself (at the base of the distal
phalanx [DP]), a sesamoid fibrocartilage (SF) near the deep surface of
the tendon, articular cartilage (AC) on the head of the proximal
phalanx (PP), and the intervening joint cavity (asterisk). Note the
the adjacent tendon pressed against the cartilage-lined, unusual presence of a sesamoid bone (arrow) within the tendon and
popliteal groove on the femur (Figure 1b). Occasionally, the fold of synovial membrane (SM) extending into the joint cavity.
Bar ⫽ 1 mm. b, Extensor digitorum communis: sagittal section of the
there was a hint of a sesamoid fibrocartilage on the deep distal interphalangeal joint of a finger. The enthesis organ consists of
aspect of the tendon within the popliteal groove (Figure the enthesis itself (at the base of the distal phalanx), sesamoid
1c). There could also be a synovial, meniscoid fold in the fibrocartilage in the deep surface of the extensor tendon, articular
interval between tendon and bone (Figure 1b). Such cartilage on the head of the intermediate phalanx (IP), and the
folds occasionally showed slight evidence of fibrocarti- intervening joint cavity (asterisk). Bar ⫽ 1 mm. c, Collateral ligament
(CL): coronal section of the proximal interphalangeal joint of a finger.
lage differentiation (Figure 1d). Although part of the The enthesis organ consists of the enthesis (at the base of the
tendon was lined with synovium, this was absent where intermediate phalanx), a sesamoid fibrocartilage at the deep surface of
the tendon was in contact with the groove. However, the collateral ligament, and a thin layer of articular cartilage which has
detached fragments of synovium may be present in the extended around the side of the proximal phalanx from the joint
joint cavity. surface. Bar ⫽ 1 mm. d, Collateral ligament: higher-magnification view
of the boxed region in c, where the sesamoid fibrocartilage in the
Another complex articular enthesis organ was collateral ligament lies adjacent to articular cartilage on the side of the
that of the tibialis anterior (Figure 2). The tendon lay in proximal phalanx. There is evidence of degeneration in the sesamoid
a furrow on the medial side of the medial cuneiform, fibrocartilage (arrow). Bar ⫽ 100 ␮m. (Masson’s trichrome–stained.)
3310 BENJAMIN ET AL

enthesis, a sesamoid fibrocartilage can be a prominent


feature of the joint capsule. Stress can thus be dissipated
from the tendinous to the capsular enthesis (and vice

Figure 4. Macroscopic views of the articular enthesis organ of the


anterior cruciate ligament (tibial enthesis). Note how the ligament
bends over the “tibial spine” (TS) that is covered with articular
cartilage (AC). EF ⫽ enthesis fibrocartilage. Bar ⫽ 3 mm (Masson’s
trichrome–stained).

2b). As a consequence of this complex arrangement, the


deep aspect of the metatarsal slip showed some evidence
of sesamoid fibrocartilage differentiation where it
passed over the cuneiform enthesis (Figure 2a). Distal to
that attachment site, the metatarsal slip replaced the
joint capsule and thus contacted the cuneiform–
metatarsal joint cavity directly. In this region, meniscoid
synovial folds protruded into the joint space from the
deep surface of the tendon (Figures 2b and c). Occa-
sionally, the joint cavity extended between the 2 tendon
slips as a bursal space (Figure 2a), and in some speci-
mens, a bursa (not lined by synovium) extended into the
narrow interval between the cuneiform slip and the
bone; in others the region was filled with vascular,
adipose tissue.
Where a tendon merged with a joint capsule,
there was often a fairly simple articular enthesis organ. Figure 5. Macroscopic views of the extraarticular enthesis organs at
This consisted of the enthesis itself, a sesamoid fibrocar- the insertions of biceps brachii and patellar tendons and at the
tilage in the tendon adjacent to the attachment site, insertion of the pes anserinus. a, Biceps brachii. The tendon enthesis
(E) is associated with sesamoid fibrocartilage (SF) and periosteal
articular fibrocartilage covering a neighboring bone, and fibrocartilage (PF). These are separated by a bursa (B), which is only
a joint cavity that allowed movement between sesamoid partly lined with synovium (S). A synovial membrane is absent from
and articular fibrocartilages—the latter being function- the region of the periosteal and sesamoid fibrocartilages. ST ⫽
ally equivalent to periosteal fibrocartilage typical of that subsynovial tissue; RT ⫽ radial tuberosity. b, Biceps brachii: low-power
seen in the Achilles enthesis organ. Such a definition view of an attachment site where the periosteal fibrocartilage is
tenuously linked to the adjacent tendon by strands of tissue (arrows)
covers the enthesis organs of the digital extensor ten- crossing the bursa. The comparatively small area over which the
dons (Figures 3a and b) and the collateral ligaments of tendon is attached to the bone suggests that the periosteal fibrocarti-
the interphalangeal joints (Figures 3c and d). However, lage is the result of a partial tear at the enthesis itself. Note the
there may also be a meniscoid synovial fold extending presence of skeletal muscle fibers (MF) in the subsynovial tissue
into the joint cavity from the deep surface of the associated with the bursa. c, Patellar tendon. A small periosteal
fibrocartilage covers the tibial tuberosity (TT) immediately proximal to
tendons, immediately distal to the sesamoid fibrocarti- the enthesis, and a bursa intervenes between the tendon and the bone.
lage (Figures 3a and b). In all such tendons, analogous to Except in the region of the periosteal fibrocartilage, the bursa is lined
the retrocalcaneal bursa in the Achilles region, synovium with synovium, beneath which there is a substantial quantity of fatty
was absent from the opposing surfaces of tendon and and highly vascular subsynovial tissue. d, Pes anserinus. Although a
bone where these contact one another. A related type of prominent bursa intervenes between the tendon and the tibial metaph-
ysis (TM) immediately adjacent to the enthesis, there is no periosteal
enthesis organ is that where tendons reinforced, rather or sesamoid fibrocartilage and thus no enthesis organ. Nevertheless,
than replaced, joint capsules. This was exemplified by the periosteum (P) is thickened. Bars ⫽ 2 mm. (Toluidine blue–stained
the insertion of abductor pollicis longus. Near this in a, c, and d; Masson’s trichrome–stained in b.)
THE “ENTHESIS ORGAN” CONCEPT 3311

and the patellar tendon entheses (Figures 5a and c),


much of Hoffa’s fat-pad lay proximal to the level at
which the specimens were removed from the cadavers
for histologic processing. Despite the presence of a
subtendinous bursa and a thick periosteum adjacent to
the pes anserinus enthesis, no enthesis organ was
present at this site (Figures 5d and 6c). There was no
cartilage differentiation within the periosteum, and
blood vessels were conspicuous (Figure 6c). Where both
periosteal and sesamoid fibrocartilages were prominent
at the insertion of the biceps brachii tendon, they largely
replaced the synovial membrane of the intervening bursa
in this region (Figure 6b). In the pes anserinus tendon,
where neither fibrocartilage was present, the synovium
was still visible (Figure 6c). At the insertion of biceps
brachii, the fatty subsynovial tissue occasionally con-
tained a small number of skeletal muscle fibers, together
with associated “microtendons” (Figure 5b).
Sesamoid fibrocartilage was restricted to biceps
Figure 6. Detail of the enthesis organs/entheses shown in Figure 5. a, brachii–and then only to specimens in which the perios-
Biceps brachii: periosteal fibrocartilage (PF) on the radial tuberosity teal fibrocartilage was also conspicuous (Figure 5a).
(RT). Note the presence of large fibrocartilage cells (arrows). b, Cadavers in which sesamoid and periosteal fibrocarti-
Patellar tendon. Periosteal fibrocartilage on the tibial tuberosity (TT) lages were most prominent were those with a small area
directly lines the deep infrapatellar bursa (B), without any covering
layer of synovium. Arrows indicate fibrocartilage cells. c, Pes anserinus.
of tendon–bone attachment.
The thick periosteum covering the surface of the tibia is purely fibrous
(no fibrocartilage cells), contains numerous blood vessels (BV), and is
DISCUSSION
covered with a synovial membrane (SM). Bars ⫽ 100 ␮m. (Toluidine
blue–stained in a; Masson’s trichrome–stained in b and c.) The Achilles insertion is a common site of disease
in SpA and has rightly been described as the “première
enthesis” (10). It forms part of a complex enthesis organ
versa) by the continuity of the attachment sites. The
relationship between enthesis and synovium is main- that comprises not only the insertion itself, but also
tained because the latter lines the inside of the joint adjacent tendon and bone fibrocartilage, together with a
capsule. fat-pad, bursa, and synovium. The purpose of the
The tibial attachment of the anterior cruciate present work was to investigate the extent to which other
ligament also formed part of a simple articular enthesis enthesis organs exist at diverse articular and extraarticu-
organ (Figure 4). It consisted of the enthesis itself, an lar sites. We have shown that the concept of an “enthesis
articular cartilage/fibrocartilage that covered the lateral organ” can be applied to many (but not all) tendon and
tubercle of the intercondylar eminence of the tibia ligament attachments, and we thus argue that the con-
(“tibial spine”), and the intervening cavity of the knee cept is central to understanding of the spondylarthropa-
joint. There was no sesamoid fibrocartilage in the liga- thies. If stress is dissipated away from a bony insertion
ment where it passes over the tibial spine, but neither because of the existence of an enthesis organ, this can
was there a synovial membrane covering the ligament in explain why pathologic changes are seen adjacent to
this region. entheses as well as at them, why subtendinous bursae are
Extraarticular enthesis organs. Extraarticular often affected in the disease (1,2,4,13), and why bursitis
enthesis organs were exemplified by those associated can mimic enthesitis (14). It also illuminates the obser-
with the biceps brachii and patellar insertional tendons vation that periostitis is a common feature of SpA
(Figures 5a–c). A subtendinous bursa occupied the (15)—fibrocartilaginous periostea are a typical feature
insertional angle between the tendon and the bone, and of many enthesis organs. Finally, the complexity of
there was periosteal fibrocartilage of variable thickness enthesis organs that are intimately associated with a
near the attachment sites (Figures 6a and b). Although synovial cavity may have implications regarding the
some fat was visible in association with both the biceps mechanisms of synovitis in SpA.
3312 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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