Enthesis: A brief review

Bone is a living tissue capable of changing its structure as the result of the stress to which it is subjected. It consists of cells, fibers and matrix. Calcification of extra cellular matrix makes it hard. The slight degree of elasticity in the bone is due to the presence of the organic fibers. The main function of the bone is protection of some of the vital organs like brain, spinal cord, heart and lungs. It also acts as a lever which helps in locomotion and movement. It is the main storage house of the calcium salts. The cavity of the bone consists of delicate blood forming bone marrow.1 The two forms of bones are compact and cancellous bone. Compact bone exists as a solid mass however the cancellous bone has a branching network of trabeculae. The arrangement of trabeculae is such that it resists the stress and strain to which the bone is exposed. Entheses is an interface where the tendon meets bone. These are the sites of stress concentration at the hard and soft tissue function where mechanical properties differ. They play a pivotal role in the diagnosis of various types of arthritis. However, not much importance has been given by the anatomists and the clinicians towards the study on entheses. This article aims to provide a brief account on entheses to draw the attention towards the known but ignored entity called entheses.

1. Enthesis: A brief review

2. Review Article
Enthesis: A brief review
Nitya Waghray
a,*
, G. Aruna Jyothi
b
, Mariya Imran
b
, Sabah Yaseen
c
,
Upasana Chaudhary
d
a
Tutor, Department of Anatomy, Apollo Institute of Medical Sciences, Hyderabad, Telanganna, India
b
Professor and Head, Department of Anatomy, Apollo Institute of Medical Sciences, Hyderabad, Telanganna, India
c
Assistant Professor, Department of Anatomy, Shadan Institute of Medical Sciences, Hyderabad, Telanganna, India
d
Post Graduate Student, Department of Anatomy, Shadan Institute of Medical Sciences, Hyderabad,
Telanganna, India
article info
Article history:
Received 29 December 2014
Accepted 16 January 2015
Available online xxx
Keywords:
Entheses
Calcification
Cancellous
Trabeculae
abstract
Bone is a living tissue capable of changing its structure as the result of the stress to which it
is subjected. It consists of cells, fibers and matrix. Calcification of extra cellular matrix
makes it hard. The slight degree of elasticity in the bone is due to the presence of the
organic fibers. The main function of the bone is protection of some of the vital organs like
brain, spinal cord, heart and lungs. It also acts as a lever which helps in locomotion and
movement. It is the main storage house of the calcium salts. The cavity of the bone con-
sists of delicate blood forming bone marrow.
1
The two forms of bones are compact and
cancellous bone. Compact bone exists as a solid mass however the cancellous bone has a
branching network of trabeculae. The arrangement of trabeculae is such that it resists the
stress and strain to which the bone is exposed. Entheses is an interface where the tendon
meets bone. These are the sites of stress concentration at the hard and soft tissue function
where mechanical properties differ. They play a pivotal role in the diagnosis of various
types of arthritis. However, not much importance has been given by the anatomists and
the clinicians towards the study on entheses. This article aims to provide a brief account on
entheses to draw the attention towards the known but ignored entity called entheses.
Copyright©2015, Indraprastha Medical Corporation Ltd. All rights reserved.
1. Introduction
Vertebrate skeleton is an adaptive tissue serving several
fundamental mechanical metabolic functions throughout life.
The primary role of skeleton is to provide a scaffold for the soft
tissue while protecting the vital areas of the body that are
necessary for one's survival. Apart from this, the skeleton also
maintains its tissue integrity. Hence, the tissue is capable of
sustaining the mechanical loads throughout the life of an in-
dividual. Skeletal tissue is anisotropic and hence changes its
macro and micro structured properties in relation to the di-
rection and concentration of various mechanical stimuli. Bone
*Corresponding author. Department of Anatomy, Apollo Institute of Medical Sciences and Research, Jubilee Hills, Hyderabad 500096,
Telanganna, India. Tel.:þ91 9160003290 (mobile).
E-mail address:[email protected] (N. Waghray).
Available online atwww.sciencedirect.com
ScienceDirect
journal homepage: www.elsevier.com /locate/apme
apollo medicine xxx (2015) 1 e7
Please cite this article in press as: Waghray N, et al., Enthesis: A brief review, Apollo Medicine (2015), http://dx.doi.org/10.1016/
j.apme.2015.01.003
http://dx.doi.org/10.1016/j.apme.2015.01.003
0976-0016/Copyright©2015, Indraprastha Medical Corporation Ltd. All rights reserved.

3. metabolism and adaptation occurs throughout life in humans
and other mammals in 4 distinct envelopes:
1) Periostealeouter cortical
2) Intracortical
3) Endosteal
4) Trabecular
Each of these surfaces varies in their response to the local
systemic influences as well as their tissue volume to surface
area ratio.
2
The main effector cells are however similar in all
the four envelopes and hence the bone formation and
resorption along these surfaces has the same physiological
mechanisms. The two main effector cells of the skeletal tissue
that maintains the functional integrity of the bone are oste-
oblasts and osteoclasts.
1.1. Osteoblasts
Cells forming new bone by synthesizing and secreting
unmineralized bone matrix are termed as osteoblasts. These
osteoblasts are the specialized fibroblasts and are related by
lineage to osteocytes and bone lining cells.
1.2. Osteoclasts
These are the multi nucleated cells. Originate from the union
of mononuclear phagocytes in the hematopoietic red marrow
found within the trabecular envelope.
3
These cells digest the
bones collagenous matrix and are similar to the macrophages
present in all the tissues.
Both of these cell types are responsible for physiological
modeling and remodeling responses wherein the skeletal
tissue is spatially distributed and renewed to adapt to its
altering systemic and local mechanical environment.
1.3. Entheses
An interface where the tendon meets bone is called entheses
(Fig. 1). These are the sites of stress concentration at the hard
and soft tissue function where mechanical properties differ.
4
They not only provide fare transmission but also anchor
tendons thereby enabling the static and dynamic load resis-
tance. To achieve this tendon fibers splay, forming a plexus at
the insertion point that provides a firm anchor, equally
resistive to insertion angle change in response to variable
directional loads occurring during joint movement.
5
Often,
the entheses intermingles with one another (eg. Insertion of
vastus lateralis, vastus intermedius, adductor magnus and
adductor brevis muscles along the lateral tip of linea aspera)
overlapping attachment sites for greater tendon security.
4
Additionally, Knese and Biermann (1958)
6
have proposed
that the splaying of entheses is not only vital for anchorage
but also in limiting the degree to which a tendon stretches. As
tendons stretch they narrow increasing their vulnerability to
rupture.
Entheses has two categorical units:
Fibrous and fibrocartilagenous: depending on the tissue
type present at the osteotendinous junction.
Fibrocartilagenous entheses are only present on the
epiphyseal or apophyseal long bone ends, whereas fibrous
entheses attach to long bone diaphyses (Fig. 2). This distinc-
tion between entheses type and location corresponds to the
bone origin, either intramembranous or endochondral
ossification.
Entheses (Fig. 3) rooted in the thick layer of cortical bone
are fibrous ossifying intra membranously while those
attaching to the thick cortical layers are fibrocartilagenous
ossifying endochondrally. Benjamin et al (2002),
7
suggests this
may relate to nutrient foramen access. However, the under-
standing of early postnatal enthesial development is limited.
Herrov in 1986,
5
described the periosteal surface of diaph-
yseal entheses in fetal rabbit long bones to be coarse fibered
compositely falling between fibrocartilage&lamellar bone.
Fig. 1eDepicts the site of entheses on radius.
Fig. 2eDiagrammatic representation of entheses.
apollo medicine xxx (2015) 1 e72
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4. The two significant proteins that play an important role in
remodeling of periosteal surface are vimentin and desmin.
5
Periosteum however has a separate pathway for growth
compared to the associated bone. Elongation of the epiphyseal
plates leads to the interstitial expansion of the periosteum in
conjunction with the underlying bone.
8
As this envelope mi-
grates, so do the attached tendons which form a complex
union that occurs once the emerging muscle tendons seek out
the nearly ossifying bone during later fetal stages.
1.4. Fibrous entheses
Characterized by the fleshy fibers, attach directly to the bone
or indirectly via the periosteum.
5
These entheses are associ-
ated with large, powerful muscle bodies such as quadriceps
and deltoideus.
5
The fibrous entheses that lack tendons typically insert the
dense connective tissue fibers directly into the periosteum,
equally allowing stress transmission over a large area. With
age, many periosteal fibrous entheses become bony attach-
ments as the periosteum disintegrates over time.
9
Mechanical
strain transmitted from a tendon to the outer periosteal en-
velope of bone may be responsible for the morphological in-
dicator used in behavioral reconstructions such as pit feature
forming via compressive forces or small protuberances or
both developing via tensile forces.
10
1.5. Fibrocartilagenous entheses
Fibrocartilagenous entheses typically attach the tendons to
small, localized regions of bone lacking a thick cortical layer
and periosteum. This allows for a more precise limb move-
ment about the joint and may dissipate stress as the thin
cortical shell deforms under stress.
5
Moving distally towards the insertion site, the first zone is a
dense fibrous connective tissue which contains type I collagen
and proteoglycans forming the tendon proper.
Second zone consists of uncalcified fibrocartilage, con-
taining multiple collagen types, with type II and type III most
prevalent.
Third zone contains calcified fibrous cartilage, which is
predominantly type II collagen. This zone anchors the tendon
to bone, forming a highly irregular junction between collagen
fibers and lamellae.
5
The cartilage that anchors tendons dur-
ing endochondral ossification remains and calcifies via
metaplasia; thus calcified fibrocartilage is the functional
equivalent of collagenous fibers present in fibrous entheses
that calcify within interstitial bone.
4
Separating the uncalci-
fied fibrocartilage and calcified fibrocartilage zones is an
avascular calcification front or tidemark that serves as a
boundary between soft and hard tissues.
5
Mineralization at
the tidemark produces a straight flat surface which thereby
minimizes the damage as the soft tissue insertion angles
change from their natural perpendicular approach during
movement.
5
The fourth zone is bone containing mainly type I
collagen. In 2005, it was suggested that these four regions
correspond to transitional zones of increased stiffness out-
lined on stress/strain for tendon.
11
According to a study, there may be an association between
subchondral avulsion fractures and accumulated micro
damage adjacent to the entheses.
1.6. Entheses organ
An entheses organ is an interface where a subtendinous bursa
is present for friction reduction as the insertion angle of the
collagen fibers changes during joint movement. This allows
direct tendon-bone contact dissipating the stress away from
entheses which is similar to mechanics involved in fibrous
attachments.
1.6.1. Osteologic entheseal remnants
Despite the biomechanical efficiency of entheses in dissi-
pating stress away from the tendon insertion point, wear&
tear is inevitable. In dry skeletal material, the tendon attach-
ment sites are visible along external bone surfaces. Tissue
type present at insertion defines the morphology of an
entheses.
Bony fibrous attachments along the diaphyses leave
rugous landmarks characterized as raised ridges and rough-
ened bone. However the periosteal fibrous entheses appear
osteologically as smooth markings.
5
Fibrocartilagenous at-
tachments are also smooth, often slightly depressed and
better circumscribed resulting from the tidemark boundary
separating the uncalcified fibrocartilage from calcified fibro-
cartilage. Hawkey&Merbs (1995)
12
classified entheseal
morphology as robust, pitted or ossified.
According to their study the robust markers are produced
through normal activity resulting from an increase in the
attachment area to avoid tendon avulsion.
Pitted entheses result from regular micro trauma at the
insertion site that induce necrosis due to an interruption in
the blood supply as tendon fibers avulse and reattach.
Exostosis is due to complete tendon avulsion, that result in
classification of tendon tissue during healing. According to
Molnar 2006,
13
they have carried out a study and removed the
indicator of exostosis demonstrating less frequently occurring
Fig. 3eDiagrammatic representation of normal anatomy
of entheses.
apollo medicine xxx (2015) 1 e7 3
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5. tendon avulsions or containing the ranked scores of robus-
ticity and pitting to calculate total muscle use.
In 2007, Havelkova and Villote
14
focused their methodology
upon fibrocartilagenous entheses.
According to Villote et al (2010),
15
have developed a
recording technique that distinguishes between varying ex-
panses of tendon fiber insertion along the attachment site,
along with morphological signatures found within the distinct
smooth attachment surface of fibrocartilagenous entheses.
1.6.2. Clinical highlights of entheses
Inflammation of tendons, ligaments or joint capsule in-
sertions is known as Enthesitis (Figs. 4 and 5). It applies to a
disease associated with the spondyloarthritis (SpA) (Fig. 6)
including various arthritis such as ankylosing spondylitis,
psoriatic arthritis, reactive arthritis and undifferentiated SpA.
Enthesopathy however indicates all the pathological ab-
normalities of insertions including inflammatory changes and
degenerative problems.
Most entheses of rheumatological significance are fibro-
cartilagenous. The presence of this tissue at an entheses
stiffens the tendon/ligament and thus helps to create a more
gradual change in mechanical properties between soft and
hard tissues. This ensures that any bending of tendon/liga-
ment fibers during joint movements is spread gently away
from the bone thereby dissipating the stress concentration.
Until the middle of the last century both rheumatoid arthritis
and spondyloarthritis were considered a part of the same
spectrum of inflammatory diseases. However the work carried
out by Wright in Leeds and pathological studies carried out by
Bywaters and Ball led to the eventual recognition that enthe-
ses was an important distinguishing feature between these
two categories of disease.
16
The advent of modern imaging
modalities including ultrasound and MRI (Magnetic Reso-
nance Imaging) has transformed the understanding of the
clinical significance of enthesitis (Fig. 4) since clinically un-
recognized enthesitis is very commonly found in early SpA
when these modalities are used.
Enthesitis manifesting as pain, protracted stiffness and
prominent swelling of large insertions, including those of the
Achilles and patellar tendons is characteristically seen in
ankylosing spondylitis, psoriatic arthritis and reactive
arthritis.
Haglund's deformity is a mechanically related condition of
the entheses organs in the vicinity of the Achilles tendon. In
those scenarios radiographic examination may be normal and
blood inflammatory markers may not be elevated. Conversely,
when there is an evidence of extensive bone edema during
imaging of isolated entheseal based pathologies unnecessary
investigations may be undertaken if primary clinical in-
vestigations remain unrecognized.
However, enthesitis presents as a pain, stiffness and
tenderness of insertions without much swelling. Swelling is a
prominent feature at large insertions in lower limb. This dis-
ease is very commonly recognized at the Achilles enthesis and
patellar tendon insertions, plantar fascia, the elbow spondy-
litis, other insertions about the knees, spurious process of the
vertebrae and at other sites, including the iliac crest. Generally
this type of enthesitis presents itself with other features of
Fig. 4eDepicts enthesitis at calcaneum.
Fig. 5eRepresentation of enthesitis at bone muscle
interface.
Fig. 6eSchematic representation of SpA.
apollo medicine xxx (2015) 1 e74
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6. SpA including synovial joint swelling, dactylitis or social dis-
ease. All these present an entheseal associated or entheseal
based pathology on imaging. If there is no joint swelling,
enthesitis may be difficult to recognize.
Although SpA is a truly inflammatory disorder, the
enthesis being a relatively avascular structure, the inflam-
matory makers such as Erythrocyte sedimentation rate and E
reactive protein may not be elevated in enthesis related
pathologies.
Mechanically related enthesopathy/tendinopathy may
occur from injury, including sports-related activity. Imaging
studies may confirm the presence of entheseal pathology but
the appearances whether at the annulus or bone disc in-
terfaces in the spine or plantar fascia may be similar in both
mechanical&inflammatory disease.
17
Incase of Achilles
tendon, degenerative tendon disease typically occurs 2e6cm
proximal to the enthesis itself, whereas the inflammatory
disease is leased around the insertion and adjacent bone.
18
Enthesis are the sites of high mechanical stressing and with
age normal enthesis are subject to wear and tear, thus
degenerative changes occur at their fibrocartilages that are
similar to those seen in osteoarthritic articular cartilage. Im-
aging of small joints in osteoarthritis and psoriatic arthritis
shows that enthesis related abnormalities are common to
both conditions, changes are qualitatively similar in the two
but quantitatively greater in primary inflammatory disor-
ders.
5
Several systems have been developed for storing
enthesitis and all basically rely on applying pressure over an
insertion point to elicit pain. This is taken to be indicative of
enthesitis.
The joint inflammation in rheumatoid arthritis is associ-
ated with bone loss and this underpins joint damage and
disability. Suppression of synovitis prevents bone damage and
ultimately disability. Conversely, inflammation in ankylosing
spondylitis is associated with new bone formation. This new
bone forming between two adjoining entheses attached to
adjacent vertebra in the axial skeleton leads to spinal anky-
losis which itself leads to disability. Thus the relationship
between inflammation, new bone formation and disability in
ankylosing spondylitis appears to be something of a paradox
since inflammation generally has a catabolic effect on bone.
There is a tendency for new bone formation and disability in
ankylosing spondylitis that appears to be something of a
paradox since inflammation generally has a catabolic effect
on bone. There is a tendency for new bone formation to occur
at normal entheses with age.
18
At the Achilles tendon bony
spurs usually develop at the most distal part of insertion. In
SpA, erosion formation occurs at the proximal part of the
entheses in early disease, but in late disease erosion seen to
heal and large spur formation again occurs at the distal part of
the attachment site.
Entheses has historically been considered as a disorder of a
focal attachment site, however entheses together with adja-
cent tissues may form mini organs, dubbed “entheses or-
gans”.
19
This ensures that the stress dissipation at attachment
sites is distributed over a wide area. Perhaps, for this reason
the pain with tennis elbow may sometimes be diffuse rather
than focally located at the common extensor origin.
Rheumatologists need to appreciate that enthesitis asso-
ciated pain may be over a greater territory than the insertions
themselves. This likely applies to the Achilles tendon enthe-
ses and the retrocalcanean bursa, as entheses related carti-
lages actually form the walls of the bursa itself. This explains
why bursitis may be a prominent feature of Achilles
enthesitis.
There is a close anatomical integration between the
entheses and synovium which has recently being turned a
synovio entheseal complex.
20
Fibrocartilages that occupy a
location adjacent to synovium (in joint, bursae or tendons) are
dependant on the synovium for lubrication, oxygenation and
removal of micro debris. The entheses insertion being itself
fibrocartilagenous is avascular. Therefore derangements in
the entheses would be expected to trigger and inflammatory
response in the adjacent vascular synovium. These micro
anatomical considerations may be vital for understanding the
importance of entheses in synovial joint disease in general.
Entheses of hand forms an important aspect of enthesial
study. Foster et al, carried out a study on entheses of the hand
and studies of activity, its possibilities and limitations. They
classified the muscles of the hand into two groups: Strength
grips and Precision grips. They studied the various parameters
like entheses development, sex, age, and body size. The study
has demonstrated that the entheses of the hand show suffi-
cient variation in expression to be used in activity studies, and
that the differences in activity between groups can be identi-
fied through analysis of this variation. Entheses of muscles
which cross the joints are more compositely and mechani-
cally different from those that originated and inserted along
the same long bone diaphyses and thus deserve a separate
analytical and interpretive considerations. Additionally, there
remains a large knowledge gap in understanding the devel-
opment and maintenance of entheses throughout their
functional life, thereby requiring further investigation into
alternate mechanical and systemic influences. Low levels of
preservation may preclude the analysis of certain entheses.
This is particularly important in hand where preservation and
identification levels are often low.
2. Conclusion
Entheses forms an integral part of study both for the clinicians
specially orthopaedicians and surgeons as well as anatomists.
However, not many studies have been reported on entheses.
This review aims at providing an insight into some brief as-
pects of entheses with the hope to develop a keen interest on
the entheses which have become a cause of primary concern
in the current society. As discussed in the review entheseal
morphology is partially influenced by mechanical strain.
Further research can be conducted to determine the strain
levels that are required to initiate the periosteal modeling
within designated entheseal zones. Apart from this the me-
chanical strain generated by repeated muscular contractions
may not exceed normal threshold levels to activate the
remodeling process and hence the entheseal morphology may
be more indicative of sporadic strains that are outside one's
normal activity level (Fig. 7).
Enthesial morphology has increasingly gained prominence
in studies investigating skeletal signatures of occupational
stress in both modern and past human populations. However,
apollo medicine xxx (2015) 1 e7 5
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7. the relationship tendons have with bone, especially within the
enthesial interface, is not as straightforward as has been
generally assumed. Our knowledge of these mechanisms has
steadily increased in recent years, yet there are still many
gaps in understanding how entheses develop and maintain
themselves throughout their functional life. While there is an
extensive body of literature documenting skeletal responses
to mechanical loads, there are fewer comprehensive studies
addressing this relationship within discrete tendon insertion
sites frequently incorporated into occupation-based studies.
With so many uncertainties concerning potential me-
chanical, systemic, and genetic influences in tendon insertion
site development and maintenance, inclusion of enthesial
size and morphological expression in occupationally related
Therefore, innovative investigations into factors clouding this
issue are needed before the value of enthesial data in activity
reconstructions can be fairly assessed. Finally, signatures of
repetitively applied strain are not restricted to the periosteal
envelope. Thus, to truly assess the relationship between
entheses and mechanical load, bones'compacta, where the
real scars of physical activity may be found, must not be
ignored in future examinations and the research must be
conducted cautiously.
Conflicts of interest
All authors have none to declare.
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