Review
The skeletal attachment of tendons—tendon ‘entheses’

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Abstract

Tendon entheses can be classed as fibrous or fibrocartilaginous according to the tissue present at the skeletal attachment site. The former can be ‘bony’ or ‘periosteal’, depending on whether the tendon is directly attached to bone or indirectly to it via the periosteum. At fibrocartilaginous entheses, the uncalcified fibrocartilage dissipates collagen fibre bending and tendon narrowing away from the tidemark; calcified fibrocartilage anchors the tendon to the bone and creates a diffusion barrier between the two. Where there are additional fibrocartilaginous specialisations in the tendon and/or bone next to the enthesis, an ‘enthesis organ’ is created that reduces wear and tear. Little attention has been paid to bone at entheses, despite the obvious bearing this has on the mechanical properties of the interface and the clinical importance of avulsion fractures. Disorders at entheses (enthesopathies) are common and occur in conditions such as diffuse idiopathic skeletal hyperostosis and the seronegative spondyloarthropathies. They are also commonly seen as sporting injuries such as tennis elbow and jumper's knee.

Introduction

An ‘enthesis’ is the region where a tendon, ligament or joint capsule attaches to bone, i.e. an ‘attachment site’ or ‘insertion site’. In the context of a tendon, it ensures that the contractile forces generated by the muscle belly are transmitted to the skeleton. Biermann (1957) and Knese and Biermann (1958) have suggested that an enthesis must serve to balance the differing elastic moduli of tendon and skeletal tissue so that local peaks in tension are avoided. This reflects a general engineering principle that stress concentrates at interfaces between structures with different mechanical properties. As we shall see, the structure of tendon entheses relates to the need to dissipate stress away from the interface and into the tendon and/or bone itself. As at the myotendinous junction, transmitting tensile load by promoting shear across the interface creates a stronger union than the direct transmission of tensile load (Huijing, 1999). Nevertheless, entheses are still subject to considerable wear and tear. Pathology (‘enthesopathy’) is common and many conditions are familiar to the layman, e.g. tennis elbow and jumper's knee. Although we have attempted to cover many aspects of entheses, we have paid particular attention to certain topics that have received rather scant treatment in previous reviews (Benjamin and Ralphs, 1995, Benjamin and Ralphs, 1997, Benjamin and Ralphs, 1998, Benjamin and Ralphs, 1999, Benjamin and Ralphs, 2000, Benjamin and McGonagle, 2001). Thus, we have given special consideration to fibrous entheses and Sharpey's fibres, and to the hard tissue elements of fibrocartilaginous entheses. Inevitably, certain fundamental aspects of enthesis biology must be covered, but wherever possible we have tried to develop the concepts further, present them in different ways or illustrate them with references that we have not cited previously.

It must be recognised at the outset that not all muscles attach to bone by means of tendons and that not all tendons have entheses. There are many muscles that attach to relatively large areas of the skeleton by ‘fleshy’ fibres, a few tendons that link one region of a muscle to another and others that are simply present on the surface of a muscle as aponeuroses that enable one muscle to glide over another (Jones, 1944). Furthermore, in certain powerful pennate muscles, there may be many small intramuscular tendons that attach it to the bone, rather than a single discrete tendon. Even where muscles attach to bone by fleshy fibres and thus lack tendons completely, skeletal muscle fibres still do not anchor directly to bone, for it is the fibrous connective tissue associated with the muscle that promotes the attachment.

Tendons come in many shapes and sizes. Some are flattened bands; others rounded cords, and the shape of the enthesis often matches that of the tendon. Thus, the tendons of pectoralis major and latissimus dorsi are flattened sheets of connective tissue that attach to the upper part of the humerus in a linear fashion that extends over a distance of several centimetres. In sharp contrast, the more rounded tendons at the wrist attach to bones in the hand in a more circumscribed fashion. Such tendons are often associated with muscles that promote intricate movements that are only possible if their entheses are located precisely at the site on the bone best suited for promoting them. Yet if the area occupied by the enthesis is too small, there is the danger that the muscle will pull the tendon away from the bone, i.e. it will avulse. So a gross inspection of many entheses shows that tendons often fan out at their attachment sites, so as to distribute force over a greater area. Accompanying the fanning out of the tendon fibres, there may be a reorganisation of fibre bundles so that a plexus is formed that either ensures that the pull of the tendon is uniform over the entire enthesis, or that different parts of the enthesis bear the strain at different positions of the joint.

Section snippets

Types of entheses

Entheses have been described by us as fibrous or fibrocartilaginous, according to the character of the tissue at the bone-tendon interface, i.e. dense fibrous connective tissue or fibrocartilage, respectively (Benjamin and Ralphs, 1995, Benjamin and Ralphs, 1997, Benjamin and Ralphs, 1998, Benjamin and Ralphs, 2000). In the terminology promoted by the pioneering German literature (Biermann, 1957, Knese and Biermann, 1958), fibrous entheses equate with die diaphysären-periostalen Ansätze (which

The osteological appearance of entheses

It is sometimes possible to ‘read’ dried bones in a macerated skeleton, either in a way that enables one to predict the histological type of enthesis from the site and nature of the marking left on the bone or to comment on the body frame of the individual. This has occasionally proved useful for archaeological studies (Miles, 1996, Miles, 1999). It is a well-known anatomical principal that the many ridges, tubercles and tuberosities that decorate bones serve for the attachment of tendons and

The ‘enthesis organ’ concept

It is well known that many tendons have subtendinous bursae at their insertion sites, which promote frictionless changes in insertional angle to accompany joint movement (Canoso, 1981). In some cases, these bursae are associated with fibrocartilaginous specialisations in both the tendon and bone, adjacent to the enthesis, in the region where the two tissues are pressed together. As the bursa, the fibrocartilages in its wall, and the enthesis itself, all share a common function of reducing the

Trabecular architecture

Relatively little attention has been paid to the bone present either at or just beneath entheses, despite the obvious bearing that the mechanical properties of such bone must have on force transmission. One of the most striking features of fibrocartilaginous entheses is the paucity of compact bone immediately beneath the attachment site (Fig. 1c). The subchondral bone plate (i.e. the bone together with its associated CF) is represented by the thinnest of shells, but perhaps this contributes to

Enthesopathies

An enthesopathy is a pathological change that occurs at an enthesis. If there is inflammation involved, the enthesopathy is an ‘enthesitis’. A considerable, though highly diverse clinical literature has built up around this subject, which is particularly relevant not only to many common sporting injuries, but also to diffuse idiopathic hyperostosis (DISH) and a whole range of diverse conditions known as seronegative spondyloarthropathies (Benjamin and McGonagle, 2001). Mechanically-induced

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    This paper was presented at ‘Tendon – Bridging the Gap’, a symposium at the 2002 Society of Integrative and Comparative Biology. Participation was funded by SICB, The Shriners Hospitals for Children, and the National Science Foundation (IBN-0127260).

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