Chapter 68Pathophysiology of Tendon Injury
Tendons passively transfer force generated by muscle to bony attachments on the opposite side of a joint, or joints, to provide movement. In contrast the function of a ligament is to resist distraction of its two bony attachments (e.g., collateral ligaments and suspensory ligament [SL]). Although this function is true for most tendons and ligaments, the horse has evolved its digital flexor tendons and SL to exhibit additional functions. These tendons and ligaments, situated on the palmar distal aspect of the equine limb (Figure 68-1), receive large weight-bearing loads because of the hyperextended metacarpophalangeal and metatarsophalangeal joints. As a result the tendons and ligaments on the palmar aspect of the distal limb act to support the metacarpophalangeal and metatarsophalangeal joint during normal weight bearing.
(From Goodship AE, Birch HL, Wilson AM: The pathobiology and repair of tendon and ligament injury, Vet Clin North Am Equine Pract 10:323, 1994.)
In addition, the equine digital flexor tendons exhibit considerable elasticity that is used to store energy for energy-efficient locomotion.1 In the case of the superficial digital flexor tendon (SDFT), its muscle is highly pennate (the muscle fibers are arranged at an oblique angle to the line of pull of the muscle, which maximizes power and minimizes contraction distance) and is unable to contract by more than a few millimeters.2 Therefore the action of the muscle, together with its accessory ligament, is largely passive to fix the origin of the SDFT in space. Although the muscle contracts only a short distance, its action, together with the tendon elasticity, also provides shock absorption.2 The gait of a horse at speed can be compared with a weight (the horse’s body) bouncing up and down on elastic springs (the digital flexor tendons and SL) in a similar fashion to a pogo stick’s bouncing.3 This arrangement allows horses to reach and maintain high speeds while minimizing energy expenditure (see Chapter 26).
When a tendon is loaded, it stretches. The relationship between the force and the elongation defines the structural properties of the specific tendon or ligament. Because these properties depend on the size of the structure, comparison between tendons and ligaments is better made from the material properties of the tissue, which are determined by plotting the force per unit area (stress) against the percentage elongation (strain). A stylized example of such a stress-strain curve for tendon is shown in Figure 68-1. The curve has the following four regions:
A number of simple biomechanical parameters, which are derived from their structural and material properties, can be ascribed to tendons. Some of the values of these parameters for the palmar supporting structures of the distal limb are shown in Table 68-1. A parameter not frequently calculated, but probably more relevant to the in vivo situation, is the force or stress at the yield point, after which irreversible damage is occurring.
The ultimate tensile strength is the load at which the tendon breaks. The SDFT receives in excess of 1 metric ton at maximum weight bearing in vivo and breaks at 1.2 to 2 metric tons when tested ex vivo in a materials testing apparatus. Within any population of horses, large variation occurs in the ultimate tensile force, with up to a twofold difference between the weakest and strongest tendons.5
One property is the ultimate tensile stress. As the SDFT is only about 1 cm2 in cross-sectional area, the ultimate tensile stress (force at failure per unit area) in the horse is close to 100 MPa, which is at the upper limit of previously documented figures for other species (45 to 125 MPa).6,7 The large variation seen for the structural strength also exists for ultimate tensile stress, indicating that the variation does not result merely from differences in cross-sectional area. It is hypothesized that the horses with weaker tendons are more prone to tendon injury. Another property is the modulus of elasticity or stiffness (E), which is a constant determined from the ratio of stress to strain for the linear part of the stress-strain curve. The modulus of elasticity for the SDFT is about 1000 MPa. Frequently it is correlated with ultimate tensile stress, so that the stronger the tendon, the stiffer it is.
The property, ultimate tensile strain, is the percentage extension of the tendon at its breaking point. In vitro testing of equine digital flexor tendons indicates that they usually extend by 10% to 12% of the original length before they rupture, although values of up to 20% have been reported.8 However, the ultimate tensile strain reflects only the final strain before rupture and includes that yield portion of the stress-strain curve that represents irreversible damage to the tendon tissue (see Figure 68-1). In addition, the ultimate tensile strain is not constant along the length of the SDFT in vitro9; the highest ultimate tensile strain occurs in the metacarpal region (the region most frequently injured).
In vivo, the normal strains in the digital flexor tendons (in ponies) are about 2% to 4% at the walk and 4% to 6% at the trot.10 At the gallop in Thoroughbreds (TBs), maximum strains in the metacarpal region of the SDFT can reach 16%.11 Such strains are far greater than usually expected in tendons from most species and reflect the highly specialized nature of the equine digital flexor tendon. If these high strains are truly representative of the strains within the tendon, they indicate that equine tendon is operating at or close to its ultimate tensile strain. This suggests little tolerance in the system, which explains the high incidence of injury in this structure. However, some caution in the interpretation of in vitro measurements is necessary, because studies have shown different results obtained between in vivo and in vitro tests.10
Hysteresis refers to the energy loss between the loading and unloading cycles of tendon (Figure 68-2), determined from the area between these two curves. Hysteresis is usually about 5% in equine tendons.12 Some of this energy is responsible for the rise in temperature within the tendon core associated with repeated loading (as in an exercising horse), which has been suggested as a causative factor in equine superficial digital flexor tendonitis13 (see the following discussion).
Research has demonstrated that tendons possess different properties depending on function.8,14 The tendons in the horse, like those in people, can be divided into two broad categories: those with the primary function of withstanding the weight of the horse (weight-bearing tendons) and those with the primary function of flexing, extending, or rotating joints (positional tendons). Weight-bearing tendons, such as the equine digital flexor tendons, are more elastic than positional tendons (e.g., the equine digital extensor tendons), which reflects the function of the digital flexor tendons as elastic energy stores. Positional tendons require stiffness for accurate positioning of the limb or digit. Human finger tendons are stiff for such a purpose, and although equine digital extensor tendons are not required for accurate placement of the digit, they nevertheless resemble this category of positional tendons. 14 These differences in biomechanical properties are reflected in the anatomical features of the tendons.
Tendon is composed of a hierarchical structure of subunits. To the naked eye, in cross-section the tendon substance is divided into a number of fascicles, which are in turn composed of ever decreasingly sized subunits: fibers and then fibrils.
The fascicles are held together by the loose connective tissue, the endotendon, which is confluent with the outside of the tendon, the epitendon. The endotendon contains vascular and neural elements. In regions where the tendons are not surrounded by a tendon sheath, a thick fibrous layer, the paratendon, further surrounds the tendon.
In longitudinal section, under a light microscope, the collagen fibers in tendon have a wavy appearance known as crimp. This pattern is responsible in part for the elasticity of the tendon, and it is eliminated in the toe region of the stress-strain curve when the mechanical behavior of the tendon is nonlinear. A generalized reduction in the crimp angle occurs with aging, with a differentially greater reduction in the central fibers.15,16 As a tendon stretches, the central fibers straighten first and therefore receive differentially greater load than the peripheral fibers, which may explain the site of pathological damage in those horses with centrally positioned core lesions. The reason for lesions situated peripherally in a tendon is less clear, unless these are also focal regions of the tendons that have developed atypically straightened fibers. Lesions involving the entire cross-section of the tendon represent a more generalized disruption of the tendon matrix.
The collagen fibrils are composed of many triple helical collagen molecules arranged in a quarter stagger, which gives a characteristic banding pattern on electron microscopy. These collagen molecules are synthesized by the tenocytes within the tendon, where early events of collagen fibril formation are associated with cellular projections (fibripositors),17,18 which are thought to be responsible for laying down the template of linearly arranged collagen fibrils during development. Subsequent enlargement of the collagen fibrils occurs extracellularly, by covalent intermolecular cross-linking (see the following discussion). Fusion of adjacent fibrils is responsible for the increasing size of collagen fibrils with age.19,20 Soon after birth, foals develop the characteristic of a bimodal or trimodal pattern of fibril diameters in the SDFT, in which the fibrils can be grouped into two or three populations (small [40 nm], medium [120 nm], and large [>200 nm]), whereas positional tendons tend to have a more consistent unimodal distribution of larger diameter fibrils in adults.21
Tendons obtain nutrients from two primary processes: perfusion and diffusion. Diffusion of nutrients from compartments other than blood occurs predominantly where the tendon is enclosed in a sheath, the synovial fluid playing an important role in tendon nutrition.
The principal blood supply in tendon arises from three sources: proximally, the musculotendonous junction; distally, the osseous insertion; and between these two, the tendon is supplied by intratendonous and extratendonous vessels. The extratendonous supply arises from the paratendon in extrasynovial tendon and from mesotendon attachments within synovial tendon sheaths (such as the vinculum between the fetlock annular ligament and the SDFT). The predominance of either source in the midtendon region depends on the species and the tendon. In the equine SDFT, two major parallel vessels run longitudinally in the lateral and medial borders of the midmetacarpal tendon, accompanied by an extensive anastomosing network of vessels.22 These vessels anastomose with paratendon blood vessels, although removal of the paratendon blood supply in the horse failed to produce gross pathological damage. However, ligation of the intratendonous supply in the midmetacarpal region produced ischemic pathological damage, demonstrating the importance of the intratendonous supply. The deep digital flexor tendon (DDFT) also has an anastomosing vascular network, except for its dorsal aspect as it passes over the metacarpophalangeal joint, where it has a more fibrocartilaginous phenotype to resist the compressive forces in this region.23
Tendon has been shown to have a good blood supply based on a number of techniques, usually involving clearance measurements of various radionuclides injected intratendonously (most commonly 133Xe and 24Na). The SDFT appears to have good blood supply similar to that of resting skeletal muscle, although findings have been inconsistent among studies and among animals on successive measurements. The large variation in the blood flow under different circumstances may indicate that external factors, as yet undefined, influence blood flow on a day-to-day basis.
Differences in blood flow between the SDFT and DDFT are affected by age, exercise, and injury (Figure 68-3).24 The SDFT has a slightly higher blood flow than the DDFT, which reflects its good vascular anatomy (see the previous discussion). However, studies showed similar functional blood flow throughout the metacarpal region of the SDFT, although histologically and microangiographically the middle and distal regions were less well vascularized.25 However, not surprisingly, the DDFT in the metacarpophalangeal joint region has a significantly lower blood flow, associated with its fibrocartilaginous phenotype, with few blood vessels because of the high compressive forces in this region, which would limit any blood flow.
Fig. 68-3 Absolute blood flow in equine digital flexor tendons derived from 133Xe clearance half-times. Numbers above the columns indicate the numbers of tendons evaluated. DDFT, Deep digital flexor tendon; E, exercised; MC, metacarpal region; MCP, metacarpophalangeal region; NE, not exercised; SDFT, superficial digital flexor tendon; SDFTcl, contralateral “normal” SDFT; SDFTi, superficial digital flexor tendonitis.
(From Jones AJ: Normal and diseased equine digital flexor tendon: blood flow, biochemical and serological studies, PhD thesis, 1993, University of London.)
Injury provokes a considerable increase in blood flow (>300%), which occurs in both clinically affected and clinically unaffected limbs, consistent with the bilateral nature of tendonitis in the horse, even though one limb is more severely affected than the other. Other measurements carried out in injured tendons have yielded variable results, which have been interpreted as representing the coexistence of fibrous tissue with low blood flow and hyperemic areas of acutely inflamed tendon.
Although the biomechanical characteristics of tendon are determined by the composition and organization of the extracellular matrix, tenocytes are essential for the formation and maintenance of tendon tissue. At least three different populations of tenocytes are identifiable within the fascicles of normal equine tendon and ligament8,26 (Figure 68-4):
Fig. 68-4 Histological features of equine tendon and ligament. A, Foal superficial digital flexor tendon (SDFT) showing obvious crimp and predominantly type II cells (arrow). B, Young SDFT showing reduction in crimp and increased number of type I cells (arrow). Note also the endotendon septa (star). C, Aged deep digital flexor tendon from the metacarpophalangeal region showing acellular regions and type III cells (arrow), resembling the chondrocyte phenotype associated with compressive loading in this region. D, Chondroid metaplasia (arrow) in an aged SDFT. The acellular areas are visible between the regions of chondroid metaplasia. E, Suspensory ligament branch showing the lines of type II cells (arrows) characteristic of ligament.
The proportion of these cells varies between tendons and ligaments, with tendon site, and with age.27 Young tendon has considerably larger numbers of type II cells arranged between collagen bundles. With aging, type I cells predominate, whereas in the areas subjected to compressive forces, type III cells can be identified.