Tendon Injury and Repair

Function of Tendons

Tendons are a vital component of the locomotor system and are a vital link between muscle and bone. Tendon function includes the transfer of force developed by muscles, joint movement, limb support, gliding motion, and the storage and release of energy. Tendons do not possess contractile elements; however, their elasticity may serve to attenuate sudden forces, thereby protecting the associated muscle, and to enable a final velocity of movement to be attained that is greater than that of the contracting muscle [1]. Muscles possess a tendon attachment whenever their point of insertion is distant or when the muscle must exert its forces of contraction across a joint. Tendons are highly resistant to extension but are relatively flexible and, therefore, can be angulated around bones or a joint.

Tendon Anatomy

The tendon is a complex composite material consisting of collagen fibrils embedded in a matrix of proteoglycans [2]. Collagen fascicles are oriented parallel to the long axis of the tendon, with type I collagen being the major constituent [2]. Fibroblasts are the predominant cell type within the tendon and are arranged in parallel rows in the spaces between the parallel collagen bundles. Collagen chains are arranged in a left-handed configuration, with three collagen chains combined into a collagen molecule. The tertiary structure of type I collagen consists of three collagen chains coiled together in a right-handed triple helix held together by hydrogen and covalent bonds [2]. Collagen molecules are then arranged in a quarter stagger, forming the quaternary structure with the alignment of oppositely charged amino acids providing a great part of the strength of the structure [2]. Five collagen molecules combine to form ordered units of microfibrils, which are arranged to form subfibrils, and these in turn are combined to form fibrils. Collagen fibrils are bound together by a matrix consisting of proteoglycans and glycoproteins in combination with water to form fascicles. A loose connective tissue called the endotendon binds the fascicles within the tendon together and permits longitudinal movement of collagen fascicles as well as support for blood vessels, lymphatics, and nerves. The epitenon covers the surface of a tendon; with tendons that are enclosed by a tendon sheath, a mesotenon originates on the side opposite the pulley friction surface and joins the epitenon. Tendons that are not enclosed within a synovial sheath are surrounded by a looser areolar connective tissue called the paratenon. A tendon sheath surrounds a tendon in areas where there is a marked change in direction, when tendons pass under ligamentous bands or through fascial slings, or when tendons pass across a joint. The tendon sheath consists of a visceral (inner) layer and a parietal (outer) layer and is lined by a secretory endothelium. Sesamoid bones are osseous or cartilaginous structures that protect the tendon as it passes over a bony surface, and the opposed surfaces of the sesamoid and underlying bone are covered by cartilage. This entire structure is enveloped in a bursa or sheath. Tendons receive their blood supply from surrounding tissues via vessels in the paratenon or mesotenon. Tendons surrounded by paratenon have been described as "vascular tendons", with multiple points of vessel entry from the periphery; these vessels anastomose with a longitudinal system of capillaries. Tendons surrounded by a tendon sheath have been described as "avascular tendons" in which the blood supply in the mesotenon is reduced to vessels in the vincula, which divide into dorsal, proximal, and distal branches and vascular loops into the tendon substance.

Pathophysiology of Tendon Injury

Tendon injury results from both direct and indirect trauma. Direct trauma includes lacerations and contusions; indirect trauma results from tensile overload resulting in sprains, rupture, avulsions, and displacements. Most tendons can withstand larger tensile forces exerted by their muscles or sustained by bones, resulting in avulsion fractures of the bone to which the tendon is attached, avulsions of the tendon attachment to bone, or ruptures at the muscle-tendon junction. Preexisting pathology in the tendon can result in midsubstance tears from mechanical overload. Underlying conditions that can predispose to tendon injury include hyperadrenocorticism, excessive administration of corticosteroids, and intratendinous injection of corticosteroids [3,4]. Repeated microstrains and mechanical overload with hyperthermia, free-radical production, and hypoxia are pathophysiologic mechanisms important in the development of tendinitis. Tendon sprains are more commonly diagnosed in horses; however, it is likely that many tendon injuries are unrecognized in small animals. Tendon sprains seen in dogs include the insertion of the flexor carpi ulnaris in racing greyhounds, the deep digital flexor tendon to the digits, and various components of the Achilles mechanism. Tendons commonly undergoing displacements include the biceps tendon, the superficial digital flexor tendon, and the long digital extensor tendon. Tendon avulsions commonly involve the long digital extensor tendon and the gastrocnemius tendon.

Tendon Biomechanics

The presence of collagen and the arrangement of collagen fibers parallel to the direction of the tensile forces provide tendons with considerable tensile strength. As with other collagenous soft tissues such as ligaments, the load-deformation curve of tendons is characterized by a toe region, which corresponds to the straightening of the crimped fibrils and orienting of the fibers in the direction of loading. The toe region for tendons, however, is relatively small owing to the preexistence of collagen fibers nearly parallel with the long axis of the tendon. The toe region is followed by a linear region, and the slope of this region represents the elastic modulus of the tendon. The yield point is the point of the load deformation curve that is followed by the failure region in which plastic deformation leads to irreversible changes in the tendon. Tendons do have viscoelastic properties, with the elongation depending not only on the amount of force applied but also on the rate of force application [2].

Tendon Healing

Tendon healing is an important area of orthopedic research to maximize strength and rate of repair to facilitate early and complete return to athletic function. Tendon healing is important to enable both sufficient tendon strength and to maintain appropriate tendon length to ensure appropriate function. A healing tendon must also maintain the ability to glide, which is the most difficult aspect of tendon repair to preserve. Healing tendons, as other tissues, undergo four overlapping phases of wound healing, which are inflammation, debridement, repair, and maturation. Immediately after injury, the wounded tendon fills with inflammatory products, neutrophils, and fibrin. The remnants of disrupted tendon are removed during the inflammatory phase, resulting in demarcation of the lesion [5]. The inflammatory and debridement phases of healing delay the onset of the repair phases, necessitating gentle tissue handling, wound lavage, surgical debridement, and resolution of infection to shorten the duration of the inflammatory phase. During the repair phase, undifferentiated mesenchymal cells from the surrounding connective tissues migrate into the wound and differentiate into fibroblasts. The fibroblasts secrete ground substance and collagen, which together with capillary buds, form granulation tissue between the tendon ends. The growth and migration of collagen fibers between the tendon ends are oriented perpendicularly to the long axis of the tendon; however, by the third and fourth weeks, the fibroblasts and collagen fibers orient themselves along the lines of stress [2]. The reorganization of collagen fibers is part of the maturation phase and is partly responsible for the increase in tensile strength. An increase in intermolecular bonds between collagen fibers also contributes to an increase in tensile strength, and this, as well as fiber orientation and collagen production, depends on the application of stresses to the healing tendon [2]. As the maturation phase ensues, the fibroblasts switch from type III collagen to type I collagen.

A distinction has been made with regard to the healing of unsheathed, vascular tendons versus sheathed, avascular tendons. With unsheathed tendons, the undifferentiated mesenchymal cells and capillary buds migrate from the paratenon and blend with the epitenon. With sheathed tendons, contrary to previous investigations indicating that the fibroblasts were derived only from the tendon sheath, tendon cells themselves do have some intrinsic capabilities of repair. The intrinsic response originates from the epitenon and is stimulated by passive range of motion, which results in less adhesion formation and an improvement in healing over the traditional "one wound one scar" theory of avascular tendon healing. Revascularization of ensheathed canine flexor tendons in conjunction with passive range of motion has been shown to occur from vessels in the epitenon, in the absence of ingrowth of peripheral adhesions [6]. Thus repair of sheathed tendons in the correct environment can occur with minimal contribution from cells of the tendon sheath or surrounding connective tissue, thereby avoiding restrictive adhesion formation.

More recent research, particularly in the human and equine fields, has focused on molecular techniques for the improvement in tendon healing. Important growth factors that are involved in tendon healing include insulin-like growth factor-1, transforming growth factor- beta1, growth and differentiation factors (GDFs), epidermal growth factor, platelet-derived growth factor, vascular endothelial growth factor, and bone morphogenic proteins 2 and 7 [7-10]. These growth factors form the basis of molecular techniques and gene manipulation techniques to enhance tendon healing [11]. Mesenchymal stem cells found in the bone marrow have been shown to stimulate healing and have additive effects with growth factors [12]. Other therapies to optimize tendon repair have included tissue engineering, extracorporeal shock-wave therapy, therapeutic ultrasound, low-level laser therapy, hyperbaric oxygen therapy, and nitric oxide [13-17].

Tendon Repair

Tendon repair techniques must follow certain principles to ensure a successful outcome. These include the apposition of the severed ends with minimal disruption of blood supply, minimum amount of suture material for repair, elimination of gap formation, and use of suture techniques with maximum mechanical strength. Gap formation of greater than 3 mm at the site of tendon repair has been shown to delay healing and significantly increase the risk of rupture during the first 6 weeks of rehabilitation [18]. A gap of less than 1 mm is required for a tendon to heal without scar and adhesion formation [19]. Tendon suturing techniques have followed the principle that sutures passed between the fascicles are easily pulled out of the tendon, whereas maximum mechanical strength has been achieved with the placement of sutures perpendicular to the tendon before passing across the site of injury. The optimum rehabilitation of tendon injuries is difficult to achieve in small animals. Excessive activity early in the repair process will result in gap formation and failure of the repair, whereas controlled early passive mobilization stimulates repair and increases the strength of the tendon in the first few months following repair. Early motion also limits adhesion formation and, therefore, enhances the gliding function of the tendon. Vascular tendons achieve 56% and 79% of the original strength at 6 weeks and 1 year, respectively, following repair [20]. Normal forces associated with muscle contraction stress the tendon to approximately 25 to 33% of maximum strength, indicating that by 6 weeks postoperatively the repair should be able to withstand limited exercise [1,21,22]. Numerous suture patterns for the repair of tendons have been developed. The Bunnel-Mayer technique is limited by compromise of the blood supply and a resultant decrease in tensile strength [23]. The Kessler technique was developed to maximize strength by the placement of suture bites perpendicular to the tendon, and the modified Kessler or locking-loop technique allows the knot to be placed at one end of the tendon rather than between the tendon ends. Superior tensile strength has been demonstrated by the three-loop pulley technique over a single and double locking-loop technique [24]. The three-loop pulley technique, owing to its superior tensile strength, is recommended for larger weight-bearing tendons and round tendons, and also for collateral ligament repair. The locking-loop technique is useful for flat tendons, although a continuous cruciate pattern has been shown to be superior to the locking-loop technique for tenorraphy of canine deep gluteal tendons [25].

Specific Tendon Injuries

Luxation of the Tendon of the Biceps Brachii Muscle

Luxation of the tendon of the biceps muscle occurs because of a displacement of the tendon out of the intertubercular groove as a result of rupture of the transverse humeral ligament [26]. Affected dogs present with forelimb lameness; flexion of the shoulder with external rotation can promote luxation of the tendon. Surgical treatment involves placement of sutures between the remnants of the transverse humeral ligament to the insertion of the supraspinatus muscle, or it involves using a prosthetic suture to replace the transverse humeral ligament [26].

Severed Superficial and Deep Digital Flexor Tendons

Severance of the digital flexor tendons commonly occurs on the palmar or plantar aspect of the distal extremity where the tendons are superficial; the injury is commonly the result of a penetrating wound. Severance of the deep digital flexor tendon(s) causes hyperextension of one or more digits with hyperextension of the distal interphalangeal joint and dorsal elevation of the claw from the ground during weight bearing. Surgical apposition of the transected tendon ends with a monofilament nonabsorbable locking-loop suture or three-loop pulley suture; an appositional pattern in the tendon sheath has been recommended [27]. Postoperative management should involve a cast or splint designed to maintain the digits in flexion for 6 weeks [27]. Although early passive range of motion is recommended for human tendon repair, such controlled activity is difficult to achieve in canine patients.

Avulsion of Proximal Tendon of the Long Digital Extensor Muscle

Avulsion of the long digital extensor muscle from the lateral femoral condyle commonly affects young, large and giant breeds. Affected dogs present with a weight-bearing pelvic limb lameness with pain and crepitus palpated in the stifle [28,29]. Diagnosis can be made via radiography, computed tomography, or magnetic resonance imaging [28,29]. The avulsion is repaired by reattaching the avulsed bone to the origin on lateral femoral condyle [28,29]. If no bone remains for fixation, the tendon can be sutured to the stifle joint capsule near its point of penetration.

Achilles Mechanism Injury

The Achilles tendon is composed of the gastrocnemius tendon, the common tendon of the biceps femoris, gracilis and semitendinosus muscles, and the superficial digital flexor tendon. Injuries to the Achilles mechanism result in tarsal hyperflexion and a flaccidity of the Achilles tendon when the tarsus is flexed. Flexion of the digits with tarsal hyperflexion resulting in a "claw" appearance occurs when the superficial digital flexor tendon is intact. Ruptures of the Achilles mechanism commonly occur at the musculocutaneous junction rather than the muscle belly. Primary tenorrhaphy of each of the three tendon components is recommended, with additional support provided by a fascia lata autograft or polypropylene mesh. A modified three-loop pulley suture pattern has been shown to be a superior technique for reattachment of the tendon to bone than the locking loop suture [30]. Postoperative immobilization is important to protect the repair from excessive weight-bearing forces and can be achieved with external coaptation using a cast, orthotics, linear external fixator, or a circular fixator.

Luxation of Superficial Digital Flexor Tendon

The superficial digital flexor tendon can become luxated as it crosses the tuber calcanei. Lateral luxation owing to breakdown of the medial retinaculum is more common. It appears that Shetland sheepdogs [31] are predisposed. Possible contributing factors include exercise, trauma, obesity, rotation around the joint with the tarsus in a flexed position, structural deformities of the calcaneus, and a weaker medial attachment of the tendon to the calcaneus [31,32]. Palpation of instability of the superficial digital flexor tendon during talocrural manipulation is pathognomonic for the injury [32]. The injury is repaired by suturing the retinaculum opposite the side of luxation. With lateral luxations, appositional sutures are placed in the medial retinaculum, and bone tunnels can be placed in the calcaneus for additional purchase if required. Polypropylene mesh has been used for failed repairs to reinforce the medial calcaneal retinaculum [33].