Lesions of the Biceps Tendon Diagnosis and Classification
A Retrospective Study of 25 Cases in 23 Dogs and One Cat
The author presents the clinical signs, radiographic and arthroscopic finding of the disorders of the biceps tendon seen in 25 shoulders. All biceps tendon lesions may be classified in one of the six subtypes. Partial or complete tears are the most frequent pathology. Degenerative joint disease is seen in 84% of the shoulders.
This paper presents the clinical signs, radiographic and arthroscopic findings in 23 dogs and a cat having a lesion of the biceps tendon. Several conditions were recognized: partial or complete rupture; avulsion of the biceps tendon from the supraglenoid tubercle, tendinitis, mid-substance tear, bipartite tendon, dislocations and tenosynovitis of the bicipital tendon. Osteoarthritis of the shoulder joint was seen in 84% of the cases and osteophytosis of the bicipital groove was recognized in 38%. Biceps tendon rupture was associated with shoulder joint instability 76% of the time. Shoulder arthroscopy is a very reliable diagnostic method allowing direct visualization of intra-articular pathologies. In man, the tendon of the biceps brachii is the proverbial stepchild of the shoulder. It has been blamed for numerous painful conditions of the shoulder from arthritis to adhesive capsulitis. Kessell described the tendon as "somewhat of a maverick, easy to inculpate but difficult to condemn (1). Its function has been often misunderstood. It has been tenodesed, translocated, pulled through drill holes in the humeral head, and debrided with an arthroscope, oftentimes with marginal results". Lippmann likened the biceps tendon to the appendix: "An unimportant vestigial structure unless something goes wrong with it" (2). Neer II has stressed the fact that 95 to 98 per cent of patients with a diagnosis of biceps tendinitis have, in reality, a primary diagnosis of impingement syndrome with secondary involvement of the biceps tendon (3). He has condemned routine biceps tenodesis. The veterinary literature on the biceps tendon in dogs is sparse (4-8). Tenosynovitis of the biceps tendon is "a common cause of forelimb lameness in medium and large breed dogs" (7). "Definitive diagnosis of bicipital tenosynovitis is often not possible, and the diagnosis is backed into by eliminating other causes of lameness. Proof of the diagnosis often depends on response to treatment" (7). There are not any reviews of cases of rupture of the tendon of the biceps brachii muscle except for anecdotal case reports (7). Arthrography has been described as diagnostic of rupture (10, 11). Calcifying tendinopathy of the biceps tendon was seen on radiographic views of the scapulo-humeral joint in four dogs (9). Two-dimensional real-time ultrasonography was found helpful in the diagnosis of strain of the infraspinatus muscle in a dog (12). This paper reviews the pertinent anatomy, explains the function of the biceps tendon, and presents a review of current concepts on the diagnosis of lesions of the biceps tendon.
Anatomy of the biceps tendon
The biceps tendon originates at the supraglenoid tubercle and glenoid labium on the cranial portion of the glenoid (2). The tendon may originate from the supraglenoid tubercle (Fig. 1) or from the glenoid labrum (Fig. 2). In some instances it. has its origin from both of these structures (Fig. 3). It courses across the cranio-medial aspect of the humeral head in the inter-tubercular groove (Fig. 4). It then continues down the humerus, becoming musculo-tendinous, and it is intra-articular but extra-synovial (Figs. 4, 5). The proximal layer of the synovial sheath reflects back on itself to form a visceral sheath (13). There is, apparently, an intra-articular portion of the biceps tendon that becomes extra-articular at the insertion of the capsule (Fig. 6). In reality, the humeral head glides up and down on the biceps tendon so that at some point (i.e., at full extension), there is only a very small portion of tendon that is intra-articular, while at others (i.e., during flexion), the intra-articular portion is longer. The extra-articular component of the biceps begins distal to the synovial sheath. The humerus moves on the tendon rather than the tendon moving within the groove.
The inter-tubercular groove is formed between the lesser and greater tubercle of the humerus. The medial wall is made up of the lesser tubercle, while the lateral wall is made up of the edge of the greater tubercle. Anomalies of the shape of the groove has been implicated in the pathogenesis of biceps tendon rupture, subluxation of the biceps tendon, tendinitis and tenosynovitis in human medicine (15). Such a study in dogs and cats has not been reported.
From flexion to complete extension of the leg, a given point in the groove moves along the tendon for some distance. In order to facilitate this motion, the synovial pouch extends from the shoulder joint to lie in the intertubercular groove for the greater part of its extent. Below this bursa, the tendon glides through its peritendineum. Motion of the humerus on the tendon occurs in all movements of extension of the shoulder. When the forelimb is in internal rotation at the shoulder, the tendon works against the medial wall of the groove, and the lesser tubercle acts as a pulley. Although the biceps tendon has been shown to be an extremely efficient stabilizer preventing glenohumeral subluxation in man (16-17), its function as a cranial stabilizer has not been studied in dogs (18).
Materials and Methods
Twenty-five shoulder joints were examined in 23 dogs and one cat between September 1, 1993 and April 1, 1997, because of a front leg lameness associated with a lesion of the biceps tendon. The history included: the age, sex, breed, weight, onset and duration of clinical signs, progression of signs, activity of the animal, prior medical treatment and influence of activity. When the cause of lameness was located to the shoulder, the orthopaedic examination included: range of motion, presence of pain in hyperextension, biceps tendon test (the forelimb applied along the chest and flank) (7) and palpation to assess joint instability. Each animal was anaesthetized and the same orthopaedic examination was repeated. Mediolateral, craniocaudal and medio-lateral stress radiographs (19) were taken of each shoulder with the patient anaesthetized. The pre-operative radiographic status of osteoarthritis of the shoulder joint was graded as absent, light (osteophytes less 2 mm), moderate (2 to 4 mm), and severe (osteophytes of more than 4 mm). Following radiography, prior to any treatment arthroscopy of the affected joint was performed. The technique of arthroscopy of the shoulder in dogs has already been de-scribed (20-23). Arthroscopic examination was performed with a 2.7 mm 30° fore-oblique arthroscope(a) in a 3,5 mm outside-diameter sleeve. Light was supplied by a xenon source(b). Using a camera(c) the arthroscopic procedure was visualized on a monitor. The joint was distended and irrigated with Lactated Ringer's solution. Photographic documentation was made with a colour printer(d). The procedure was recorded as necessary(e). Fluid inflow was maintained via a sterile infusion set connected to the stopcock of the trocar sleeve. Fluid leaving the outflow canula was drained away via a silastic tube (21). The patient was positioned in lateral recumbency and the leg prepared aseptically. The joint was dilated with 10 to 15 ml of Lactated Ringer solution after being punctured with a 19 gauge needle craniolaterally between the acromion and caudal part of the greater tubercule in a caudomedial direction. A stab incision was made 1 cm caudally and 1 cm distally to the acromion (28) using an #11 Bard-Parker blade. The joint capsule was then penetrated using the blunt trocar locked in the arthroscopic sleeve. The trocar was replaced by the arthroscope and the light cable, camera and inflow line were connected. Joint inspection was then performed. a. Karl Storz Veterinary Endoscopy, Tuttlingen, Germany b. Light Source Storz Xenon Nova. Tuttlingen. Germany c. Telecam SL camera: Karl Storz, Tuttlingen. Germany d. Sony color printer manigraph. Sony, Paris, France e. U-Matic videocassette recorder VO-7630, Sony. Paris. France
The dogs were 11 months to 11 years of age with a mean of five years and 3 months. There were 16 males and 7 females. Among the 23 dogs of 11 breeds, there were six French Poodles, five Labradors, two German Shepherds, Iwo Greyhounds, and two Springers (Table 1). One dog, a Cocker Spaniel had bilateral involvement (4.3%). Before entering the study each dog and the cat underwent a complete physical and orthopaedic examination. The joint was examined from caudal to cranial. The synovial membrane was identified and signs of inflammation were classified as absent, moderate severe or fibrous. The articular cartilage of the humeral head and glenoid cavity was observed and any signs of osteophytes, chondromalacia, or erosion were recorded. The biceps tendon was explored in a systematic manner from proximal to distal through intertubercular groove. All of the dogs and the cat were admitted because of a foreleg lameness in all of the dogs and cats with a duration of 10 days to 5 years. Biceps tendon rupture appeared to be associated with shoulder instability in 16 cases (Table 2). In seven cases, the rupture was related to trauma and in five shoulders, the rupture was iatrogenic after medial or lateral transposition of the biceps tendon. In four instances the rupture was not related to any pertinent history. Two dogs were referred for cervical disk disease. Of the 25 shoulders five dogs had a non-weight-bearing lameness for 10 days to 21 days. One patient had been administered prednisolone for five years prior to admission. All of the dogs and one cat had a moderate to non-weight-bearing lameness during the clinical examination, and each had pain on shoulder hyperextension. The biceps tendon test was positive in all of them.
The preoperative radiographic examination of the shoulder revealed only four normal shoulders (16%). Osteoarthritis was observed in 21 cases (84%). Osteoarthritis was classified as minimal in five cases (20%), moderate in four cases (16%), and severe in nine cases (36%). Osteophytosis of the bicipital groove was obvious in eight shoulders (32%), and a demineralization of the supraglenoid tubercle was observed in five patients (20%). There was a calcification of the origin of the biceps tendon and mineralization of the tendon of the supraspinatus muscle in one case each (Table 3).
With the arthroscope in the lateral portal, a systematic arthroscopic examination was carried out with inspection of the synovium, articular cartilage surfaces, glenohumeral ligaments, labrum, tendon of the biceps muscle, tendon of the subscapularis muscle and joint capsule. The synovial membrane of these 25 shoulders was found to be normal in three cases, synovitis was graded as moderate in five, severe in 12, and fibrous in five cases. Abnormalities of the articular cartilage were observed on the glenoid cavity and the humeral head (Table 3). The most common findings were chondromalacic cartilage in 11 cases and osteophyte formation in seven shoulders. The tendon of insertion of the subscapularis muscle was found partially torn in one shoulder. Joint mice were found in one dog's shoulder. The biceps tendon was found partially torn from the supraglenoid tubercle (SGT) in five cases (Table 3; Fig. 7). In four instances the labrum was partially torn from the SGT (Fig. 8). When a partial rupture was observed, the biceps tendon or the labrum was palpated to evaluate the depth of the avulsion. In seven instances, there was a partial tear of the biceps tendon from the SGT (Fig. 9) associated with an enlargement of the remaining biceps tendon (Fig. 10). In the cat, the laceration appeared to be fresh (Fig. 11) and the biceps tendon synovial sheath was swollen. A midsubstance partial tear was only seen once (Fig. 12) whereas there were four complete midsubstance ruptures of the biceps tendon (Fig. 13) observed following its medial or lateral transposition. In a German Shepherd dog the biceps tendon was only completely avulsed off the supraglenoid tubercle (Fig. 14). One patient had severe tendinitis and a small tear of the biceps tendon from the SGT (Fig. 15). The biceps tendon was found to be bipartite in two patients (Fig. 16) and luxated in one patient (Fig. 17). In the last dog the intertubercular groove was filled by the proliferative synovial villi (Fig. 18). Synovial biopsy via arthroscopy revealed a tenosynovitis associated with a severe synovitis of the shoulder joint. After assessing the biceps tendon, the evaluation of the medial glenohumeral ligaments (MGHL) was performed. The MGHL was torn or incompetent in 14 patients and the joint capsule was avulsed from the caudo-lateral aspect of the glenoid cavity in two dogs. These abnormal findings were associated with 14 shoulder subluxations and two luxations.
Lesions of the biceps tendon appear as the third most common cause of shoulder lameness after shoulder instability and osteochondritis dissecans of the humeral head in dogs (24). Many breeds were affected, French Poodles and Labradors are most commonly involved (Table 1). The most common clinical sign was a foreleg lameness. Pain on hyperextension of the shoulder joint was present in every case, and the "biceps tendon test" was also positive in every patient. When compared with dogs having a shoulder subluxation (25), the pain appears to be more intense, some of the dogs complaining spontaneously. The history often referred to a lameness of several weeks or months duration, with a sudden onset of non-weight-hearing lameness accompanied by intense pain. Degenerative joint disease (DM) was present in 84% of the cases. Osteophytosis of the bicipital groove was observed in one third of the cases (32%), whereas demineralization of the SGT was seen in 20% of the shoulders. Shoulder osteoarthritis reflects more an intra-articular pathology than a primary disease. The presence of shoulder osteoarthritis justifies further diagnostic imaging of intra-articular anatomical structures, such as arthroscopy. All of the biceps lesions could be classified in 6 subtypes: 1. complete or partial avulsion, tear from the SGT, 2. midsubstance tear, 3. tendinitis, 4. bi-partite tendon, 5. luxation and, 6. tenosynovitis of the biceps tendon. Proximal or midsubstance tear of the biceps tendon represents 21 of the 25 cases (84%). Of the 21 tears of the biceps tendon, seven (33%) showed an enlargement and associated tendinitis. Sixteen of the 25 tendon lesions (76%) were associated with shoulder subluxation or luxation (20). Based on the tensile strength of collagen fibers a tendon is one of the strongest soft-tissue structure in the body. Various factors affect the properties of tendons, including anatomical locations, exercise, weight and aging. Exercise has a positive long-term effect on tendons, increasing their stiffness and ultimate strength (27, 28). Age may have a significant role in alterating the mechanical properties of tendons. Aging is associated with a decrease in collagen cross-linking, collagen fibril diameter, the amount of insoluble collagen, an increase in mucopolysaccharide and water content. These biochemical and structural changes may contribute to chronic overuse injuries. In this clinical study there were only four dogs under the age of two years; all of the others including the cat, were older. with a mean of five years and three months. All four dogs under the age of two years had a partial rupture of the biceps tendon from the SGT associated with tendinitis. This tendinitis may be a sign of overload activity (27). In fact, injury or damage to tendons may result from one of three mechanisms: 1. transection within the substance (direct injury); 2. avulsion from bone at the origin (indirect injury); 3. intrasubstance damage from intrinsic or extrinsic factors and subsequent failure. Because most tendons can withstand tensile forces greater than can be exerted by their muscles, avulsion fractures and muscle-tendon junction ruptures are far more common than the rupture of tendons (27). Substance rupture is considerably less common and may require the existence of a pre-existing pathological condition, as seen in chronic overuse injuries (27). Micro-traumatic tendon injury may lead to degenerative lesions of the tendon and spontaneous rupture (28). In one study of the histopathological changes preceding spontaneous rupture in 891 human patients, 97% of the tendons showed prior pathological changes (29). The physiological range of load necessary for maintenance of normal tendon junction, or improvement of the material properties of tendon, is unknown. Similary, the threshold load responsible for tendon injury is also not known. Repetitive overload may result in a disruption of the normal inflammatory and healing response, thus affecting the synthesis and remodeling capacity of the tendon (27). Extensive discussion continues concerning the role of tendinitis in the pathophysiological process of overuse injuries. Traditionally, injuries near the tendon-osseous junction are attributed to tendinitis, an inflammatory condition resulting from overuse (27). However the absence of inflammatory cells has led to a new classification of tendon injuries (25). The term "tendinosis" would appear to be more appropriate since the histology of two torn biceps tendons showed disorganization of the collagen fibres and chondroid metaplasia. Further pathological studies would be required. All of the tears were located in the glenohumeral joint, outside the inter-tubercular groove and off the SGT. This may be explained by a relative zone of avascularity in the biceps tendon, as is the situation in humans (31). A similar vascular study of the normal biceps tendon is required in the dog. The association of the biceps tendon tear with shoulder instability (76%) is similar to that seen in humans. In dogs, the primary restraints of the shoulder joint are the glenohumeral ligaments and the joint capsule (18). The biceps tendon is not known to play a role in canine shoulder stability. However in humans, the long head of the biceps tendon is known as a useful depressor of the humeral head which contributes to humeral head stability during overhead activity (32). Recently, the long head of the biceps tendon has been shown to contribute significantly to anterior and posterior joint stability (33). This is substantiated by the hypertrophy of the tendon that occurs when the rotator cuff has been torn (34). One may speculate that shoulder instability increases the load applied on the biceps tendon and may favour overload injury by repetitive microtraurna. Since most of the dogs were observed to be more active than the average pet, traction load tendinitis may be cause of pathology. Several of the dogs were sport dogs that had been running behind a bike or horse. Shoulder instability may increase the load on the biceps tendon. In five instances of transfer of the biceps tendon for correction of an unstable shoulder, there was a complete midsubstance tear of the tendon. The treatment of shoulder subluxation and luxation should be revisited as in human medicine because of the high rate of failure following transfer (24). A partial tear of the biceps tendon was seen as a fraying of the intra-articular portion of the tendon. Following complete rupture of the biceps tendon, an intra-articular stump of the proximal tendon may be left in the joint. When seen arthroscopically, the biceps tendon stump may initially be difficult to recognize since it is frequently very frayed and degenerated; it blocks the view through the arthroscope, making interpretation difficult. It is then mandatory to distend the joint and flex the shoulder to improve visualization of the bicipital groove (Figs. 12, 13). A severe glenohumeral synovitis is most often associated with biceps rupture as well as shoulder osteoarthritis. The cause of the osteoarthritis may be related to the glenohumeral instability. The osteophytes in the intertubercular groove appear to be an extension of the intra-articular pathology. Dislocation of the biceps tendon out of the intertubercular groove, bipartite biceps tendon and tenosynovitis of the biceps appeared infrequently. The first two pathologies are associated with shoulder instability and tearing of the tendon of the subscapularis muscle (25). The only case of tenosynovitis of the bicipital groove without any intra-articular pathology but associated with inflammatory synovial fluid was probably an autoimmune synovitis. The dog only improved with high doses of prednisolone. In conclusion, this paper presents direct visualization, via arthroscopy, of the biceps tendon and its associated pathologies in clogs and one cat. The biceps tendon may be subject to several pathologies: partial or complete rupture avulsion, tendinitis, midsubstance tear, luxation, and splitting tenosynovitis. Localization of pain to the shoulder joint in dogs and cat requires an organized work-up including proper examination of the shoulder joint with and without anaesthesia, radiographs, synovial fluid analysis and arthroscopy. Arthroscopy has been recognized as superior to other diagnostic procedures for intra-articular shoulder pathologies in man (1). However, in the absence of intra-articular pathologies, the clinician must differentiate between pain that is localized to the shoulder and pain from another sources, such as periarticular and regional disorders (36).
The author gratefully recognizes the aid of Karl Storz GmbH + Co. D-78532 Tuttlingen. Germany for the supporting the publication of the coloured pictures.
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