In the early 1980s it was not uncommon to see patients who had undergone isolated biceps tenodesis when in reality their symptoms emanated from rotator cuff disease and impingement syndrome. It is quixotic to think, however, that the biceps escapes the degenerative process or is unable to produce symptoms either on its own or in conjunction with other pathologic entities of the shoulder.
The long head of the biceps brachii is the proverbial stepchild of the shoulder. Kessell and Watson described the tendon as “somewhat of a maverick, easy to inculpate but difficult to condemn.” Lippman likened the long head of the biceps to the appendix: “An unimportant vestigial structure unless something goes wrong with it.” At various times in history, surgeons have subjected this tendon to tenodesis, translocation, pulling it through drill holes in the humeral head, debridement with an arthroscope, and tenotomy. Still others have worshipped at the altar of the biceps, keeping it sacrosanct, contending that it must be there for a reason, even if it is unclear what exactly that reason is or ever was.
The advent of magnetic resonance imaging (MRI), ultrasound, and arthroscopy has allowed clinicians to visualize this tendon through noninvasive and minimally invasive modalities. These techniques have provided fundamental insights into various shoulder pathologies, which in turn have influenced thinking about how lesions of the long head of the biceps tendon (LHBT) are treated. Specifically, the LHBT is intimately related—both anatomically and pathologically—to the superior labrum proximally and to the bicipital groove and beyond distally. Understanding these relationships is crucial to making an accurate diagnosis and devising an appropriate treatment plan for patients with shoulder problems.
This chapter discusses how these lesions have been treated historically, reviews the pertinent anatomy, and attempts to understand the function of this unique tendon. The chapter also reviews current concepts on the etiology, diagnosis, and management of lesions involving the long head of the biceps.
Historical Review
The history of our understanding of the long head of the biceps is long and full of controversy. The long head of the biceps has at times been indicted as the source of all shoulder pain; at other times it has been seen as an incidental structure of no real consequence. Hippocrates was the first to call attention to the pathologic displacement of muscles and tendons in dislocations. Accurate depictions of the anatomy of the biceps region and intertubercular groove appeared in the 1400s ( Fig. 17-1A ).
The first reported case of a long head of the biceps brachii tendon dislocation was in 1694 by William Cowper. He presented a case of a woman who was wringing clothes when she suddenly felt something displace in her shoulder. When Cowper examined her 3 days after the injury, he noted a depression of the deltoid, rigidity in the lower biceps, and an inability to extend the forearm. According to Cowper’s report, the tendon was reduced by manipulation, and with reduction, the patient immediately recovered use of the arm. Such sudden disabling episode followed by a miraculous recovery is seldom seen in our practice, but so are women who wring clothes, for that matter. Cowper had his supporters, and his theory was accepted by Boerhaave and Bromfield. His observations came under suspicion, however, because of his plagiarism of the Dutch anatomist Godfried Bidloo. Before Cowper’s description, many biceps injuries were undoubtedly the result of a direct trauma (see Fig. 17-1B ).
In 1803 Monteggia reported a second case of dislocation, but one in which the mechanism was habitual. Subsequently, numerous additional clinical reports appeared in the literature. Soden reported one such case in 1841 and was able to confirm the diagnosis at autopsy. Hueter, in 1864, very nicely documented the signs and symptoms of lesions of the LHBT.
However, even during this relatively early period of our knowledge, there was controversy. Jarjavey believed that most of the symptoms were attributable to subacromial bursitis and did not believe in the existence of simple luxation as a clinical phenomenon. Some authors believed that the biceps lesion was in fact secondary to arthritis or other concomitant pathology. Callender mentioned one case of recurring dislocation, which he attributed to fibrous tissue within the groove. Duplay described périarthrite scapulo-humérale , a syndrome that included tendinitis of the biceps. McClellan believed the LHBT to be an important depressor of the humeral head. He wrote:
Furthermore, the long tendon of the biceps muscle which is lodged below the tuberosities pierces the capsular ligament and passes over the head of the humerus to the top of the glenoid cavity, strengthens the upper anterior part of the joint and prevents the head of the humerus from being brought against the acromion, processing the normal upward movements of the arm. In fact it is mainly by the normal position of this tendon, assisted somewhat by atmospheric pressure, that the head of the humerus is retained in its natural position.
Bera, in 1910, believed that osteitis reduced the height of the lesser tuberosity and thus led to biceps instability. In the 1920s valuable contributions were made by Meyer, who discussed observations based on 59 spontaneous dislocations and 20 complete ruptures of the LHBT. He was the first to describe the supratubercular ridge ( Fig. 17-2 ), degenerative changes on the undersurface of the acromion, the acromioclavicular joint, and the coracoacromial ligament. Meyer thought that attrition, particularly after the use of the extremity in abduction and external rotation, led to a gradual destruction of the capsule proximal to the lesser tuberosity and in the region around it. Dislocation resulted as a consequence of capsular weakness in this region.
According to Schrager, F. Pasteur recognized all facets of biceps tendinitis and described it fully, elevating its status as a distinct clinical entity. In 1934 the diagnosis of biceps tendinitis was questioned by Codman, who wrote, “Personally, I believe that the sheath of the biceps is less apt to be involved than are other structures. I have never proved its involvement in a single case. I think that the substance of the tendon of the supraspinatus is most often involved.” In the 1940s Lippmann, Tarsy, and Hitchcock and Bechtol all believed that biceps tendinitis was an important cause of shoulder pain, and each independently described tenodesis procedures. In 1950 DePalma described degeneration of the biceps tendon with aging and reported on both operative and nonoperative care. Based on gross and microscopic examination of 78 cases, he believed bicipital groove tenosynovitis was the most common cause of a painful and stiff shoulder.
In 1972 Neer described the anterior impingement syndrome, in which anterior acromial spurring with thickening and fibrosis of the coracoacromial ligament causes impingement wear on the rotator cuff and biceps tendon. He pointed out a close association between rupture of the biceps tendon and rotator cuff tears.
Although in the 1970s and 1980s the focus moved away from primary biceps tendinitis and isolated biceps tendon instability, these have definitely regained attention in the last 20 years. Even during the period of skepticism about isolated biceps tendinitis and dislocation, there still were advocates of the significance of these conditions, and several authors published the results of their diagnosis and treatment. Post presented a series of patients with primary bicipital tenosynovitis, and O’Donoghue reported on surgical techniques for treating the subluxating biceps tendon in athletes.
Since the late 1980s and early 1990s, the increased use of MRI and arthroscopy has provided valuable information about the LHBT and its lesions. In 1985 Andrews described tears in the superior labrum of the glenohumeral joint at the attachment of the biceps tendon. In 1990 Snyder first coined the term SLAP lesion (superior labrum anterior and posterior lesion) and described a classification system for it.
In the early 1990s Walch classified various subluxations and dislocations of the biceps tendon. Since then, he has described the biceps pulley and pulley lesions ( Fig. 17-3 ). Pulley lesions involve the rotator interval and cuff and therefore affect the stabilizers of the LHBT. These hidden lesions, as described by Walch, are not always visible on arthroscopic examination, and open exploration of the rotator interval is sometimes required to identify them. Study of these lesions has directly implicated the superior glenohumeral and coracohumeral ligaments and the subscapularis and supraspinatus in allowing biceps subluxation and dislocation. Bennett has shown that good visualization of the rotator interval, including the coracohumeral and superior glenohumeral ligaments, is possible with the arthroscope.
Further study has helped to delineate the relationship between the LHBT and its anatomic neighbors—the superior labral complex proximally and the bicipital tunnel and beyond distally. Romeo, Provencher, Mazzocca, and colleagues have extensively studied the use of biceps tenodesis as a treatment for superior labral injuries. O’Brien and colleagues have defined the anatomy and histology of the bicipital tunnel, studied the validity of arthroscopy as a tool to diagnose bicipital lesions, and established arthroscopic biceps transfer as a useful treatment for bicipital lesions. Increasingly, lesions of the biceps are seen more in a proximal and distal continuum of the biceps-labral complex rather than in isolation.
It has been more than 300 years since Cowper described his first case. Despite an ever-increasing amount of research, the role of the LHBT and the clinical significance of the lesions associated with it remain controversial.
Anatomy
It is fitting to begin any discussion of the anatomy of the biceps tendon with a discussion of the anatomy of the superior labrum. The labrum consists of dense fibrocartilage circumferentially covering the glenoid. The fibrocartilage of the labrum is distinctly different from the hyaline articular cartilage of the joint surface, and from tendinous tissue of the biceps. Labral fibers are confluent with articular cartilage through a transitional zone and with the biceps tendon near the biceps anchor.
The long head of the biceps brachii originates, in most cases, at the supraglenoid tubercle and is confluent with the glenoid labrum in the superiormost portion of the glenoid ( Fig. 17-4 ). Some authors have described the absence of the intra-articular portion of the long head of the biceps or an extra-articular structure. The tendon itself is approximately 9 cm long. At its origin, it varies in insertion: it may be bifurcated or trifurcated, or it can have a single insertion point.
In a study by Habermeyer and colleagues the biceps was found to originate off the supraglenoid tubercle in 20% of specimens studied. In 48% of the specimens the origin was off the superoposterior aspect of the labrum, and in 28% of the specimens the origin was from both the tubercle and the labrum.
Classically, the anterior-to-posterior distribution of the biceps attachment has been classified into four types as described by Vangsness ( Fig. 17-5A to D ). The attachment is primarily posterior most of the time, with fewer specimens showing contributions from the anterior labrum. Tuoheti and colleagues questioned whether the anterior labrum contributes at all to the biceps origin. They looked macroscopically as well as microscopically at the attachment site of the LHBT in a series of 101 cadaveric specimens. When the attachment of the biceps was assessed macroscopically, they found the distribution to be 27% all posterior, 55.4% posterior dominant, 16.8% equal anterior and posterior, and 0% all anterior. However, when these same specimens were assessed microscopically, the attachment site of the LHBT was seen to be predominantly posterior in all cases. This was the case even in specimens that had macroscopically appeared to have equal contributions from anterior and posterior. The authors noted that the macroscopic assessment was often influenced by the variable attachment of the inferior glenohumeral ligament to the labrum. When this attachment was close to that of the long head of the biceps, the macroscopic impression given was of a posterior-dominant or equal anteroposterior (AP) insertion. Microscopic examination however revealed that the attachment, even in these cases, was predominantly posterior.
The cross-sectional characteristics of the long head of the biceps change during its course from the supraglenoid tubercle down to the musculotendinous junction. The shape of the proximal tendon differs from that of the middle and distal portions. The proximal part is flatter and becomes more circular as it enters the bicipital groove.
McGough and colleagues tested the tensile properties of the LHBT in normal specimens. They measured the cross-sectional area of the biceps tendon at three regions: proximal (22.7 ± 9.3 mm 2 ), middle (22.7 ± 3.5 mm 2 ), and distal (10.8 ± 2.8 mm 2 ). There was no significant difference between these three regions. The mean ultimate tensile strength, ultimate strain, and strain energy density for the specimens were found to be 32.5 ± 5.3 MPa, 10.1% × 2.7%, and 1.9 ± 0.4 MPa, respectively. The modulus of elasticity was calculated to be 421 ± 212 MPa. The mode of failure of the tendons in all cases was complete rupture within the midpoint of the tendon substance.
The course of the LHBT is oblique over the top of the humeral head and down into the bicipital (intertubercular) groove. Once out of the groove, the tendon continues down the ventral portion of the humerus and becomes musculotendinous near the insertion of the deltoid and the pectoralis major.
The angle formed by a line from the bottom of the groove to a central point on the humeral head is constant and corresponds to the retrotorsion angle measured from the epicondyles ( Fig. 17-6 ). This angle can be referenced as a guide when placing a humeral head prosthesis. The bicipital tendon, although intra-articular, is extrasynovial. The synovial sheath reflects on itself to form a visceral sheath that encases the biceps tendon ( Fig. 17-7 ). The sheath is open; it communicates directly with the glenohumeral joint and ends in a blind pouch at the level of the bicipital groove.
The long head of the biceps muscle receives its blood supply from the brachial artery. Three arteries supply blood to the bicipital tendon. The distal portion of the tendon receives branches from the deep brachial artery. The proximal part of the tendon also receives branches from the anterior humeral circumflex artery. In the intertubercular sulcus a branch of this artery gives rise to two small branches running in cranial and caudad directions.
The LHBT can be divided into two zones. The first is the traction zone, in which the tendon of the biceps closely resembles a normal tendon. The second is the sliding zone, the fibrocartilaginous portion of the tendon that is in contact with the bony groove. The density of intratendinous vessels in the traction zone is comparable to the vascularization of other tendons, but vascularization of the biceps tendon is markedly decreased in the sliding zone. There are no vessels in the part of the tendon on which the humerus slides. A difference in blood supply between the sliding and intra-articular portions has been reported. This area has also been shown to be composed of fibrocartilage. The portion of the long head of the biceps inside the bicipital groove possesses a mesotendon that arises from the posterolateral portion of its groove. Vascularization appears to play a minor role in the pathogenesis of biceps tendon rupture.
The biceps tendon has classically been described as having an intra-articular portion and a groove portion. Experimental studies have shown that this type of classification is not entirely accurate. Because of the humeral head sliding on the biceps tendon, the position of the arm dictates the amount of intra-articular tendon present. The maximal amount of intra-articular tendon occurs with the arm in adduction and extension, whereas very little of the tendon actually resides within the joint in extremes of abduction.
Distally, the long and the short head of the biceps come together to form a common tendon before inserting onto the radial tubercle. A third muscle belly has been described in some specimens. Mercer and Gilcreest measured the tensile strength of the distal biceps tendon and found it to range from 150 to 200 lb. The blood supply of the muscle belly of the long head of the biceps is via the brachial artery. The nerve supply to this muscle is via the musculocutaneous nerve arising from C5-C7.
Soft Tissue Restraint
As the LHBT courses from its origin on the superior aspect of the glenoid labrum and supraglenoid tubercle to its muscular insertion, it is kept in its anatomic position by several structures. Among the most important of these structures are the capsuloligamentous tissues, which play a major role in keeping the LHBT in the groove. The supraspinatus, subscapularis, coracohumeral ligament, and superior glenohumeral ligament all play a vital role in stabilizing the biceps.
Rotator Interval
The rotator interval is the area bounded by the anterior edge of the supraspinatus superiorly, the superior border of the subscapularis tendon inferiorly, and the coracoid process medially. This triangular area includes both the coracohumeral and the superior glenohumeral ligaments. In its anatomic position, the intra-articular portion of the biceps tendon runs underneath the coracohumeral ligament, which lies within the interval between the subscapularis and supraspinatus, increasing its strength.
The rotator interval is an integral part of the cuff and capsule and is distinguishable only by sharp dissection. The most important retaining structure in this area is the portion of the shoulder capsule thickened by the coracohumeral ligament and the edges of the subscapularis and supraspinatus tendons; this bridges the tuberosities in the uppermost portion of the sulcus (see Fig. 17-3 ). This portion of the capsule is the first and foremost obstacle to medial dislocation of the tendon . Meyer found in his series that in cases of dislocation of the long head of the biceps, this portion of the capsule was always stretched or torn. Codman, commenting on Meyer’s work, was of the opinion that “displacement of the tendon is a result of rupture at that portion of the musculotendinous cuff, which is inserted into the inner edge of the intratubercular notch.” This opinion is supported by the findings of Sakurai and colleagues, who observed the transverse humeral ligament to be intact in 25 specimens that nonetheless had medial displacement of the biceps. The rotator interval contains two structures that are important in stabilizing the biceps tendon within the groove: the coracohumeral ligament and the superior glenohumeral ligament.
The coracohumeral ligament has a broad, thin origin on the coracoid along its lateral border. As the ligament passes laterally, it divides into two main bands. One band inserts onto the anterior edge of the supraspinatus tendon and the greater tuberosity. The other inserts onto the superior border of the subscapularis, the transverse humeral ligament, and the lesser tuberosity ( Figs. 17-8 and 17-9 ). The coracohumeral ligament has extensions that envelop the cuff tendons and blend into the superficial and deep layers of the supraspinatus and subscapularis tendons and the articular capsule. These extensions reinforce the capsule in the rotator interval at the border of the tendinous cuff. The coracohumeral ligament is superficial to the shoulder capsule and overlies the biceps tendon.
The superior glenohumeral ligament is the second structure stabilizing the biceps in the rotator interval. It arises from the labrum adjacent to the supraglenoid tubercle, inserts onto the superior lateral portion of the lesser tuberosity, and blends into the medial aspect of the coracohumeral ligament. It crosses the floor of the rotator interval. Along with the coracohumeral ligament, the superior glenohumeral ligament forms a reflection pulley for the biceps tendon. This pulley is in direct contact with the insertion of the subscapularis tendon. All of these structures blend together to form a sleeve above the entrance to the bicipital groove that is analogous to the flexor tendon pulleys of the hand. This sleeve prevents medial dislocation of the long biceps tendon. Although the superior glenohumeral ligament has previously been considered insignificant, it is now considered an important stabilizer for the biceps tendon.
Cole and colleagues described the anatomy of the rotator interval in both adults and fetuses. They found two distinct types. Type I intervals have a contiguous layer of capsule in the region of the superior and middle glenohumeral ligaments. In contrast, type II intervals have a defect in the capsule between the superior and middle glenohumeral ligaments. The type II interval was more common (observed in 28 of 37 specimens). Their study results suggest that interval defects may be a congenital phenomenon. In Werner and colleagues’ study of the rotator interval, the superior glenohumeral ligament was found to make a U -shaped sling that stabilized the biceps tendon in the groove. The fasciculus obliquus also plays a significant role in investing the biceps tendon, as has been revealed on microscopic examination. The subscapularis was not found to be involved in this suspensory sling, a mechanism that protects the biceps against anterior shearing stresses. The authors concluded that the superior glenohumeral ligament is the most important stabilizing structure for the biceps tendon and that injury to this sling may lead to anterior bicipital instability.
The Groove
The supraspinatus and subscapularis tendons fuse to form a sheath that surrounds the biceps tendon at the proximal end of the groove. Fibers from the superior portion of the subscapularis tendon pass below the biceps tendon and join with fibers from the superior part of the supraspinatus to form the floor of the sheath ( Fig. 17-10 ). A slip from the supraspinatus forms the roof of the sheath along with the superior glenohumeral and coracohumeral ligaments. The deep portion of the sheath runs adjacent to the bone and forms a fibrocartilaginous lining in the groove that extends approximately 7 mm distal to the entrance of the groove.
The role of the transverse humeral ligament in stabilizing the biceps in its sulcus has been disputed by several authors. Traditionally, the LHBT was thought to be maintained within the sulcus by the action of the transverse ligament ( Fig. 17-11 ), but Meyer found that this ligament was in fact either too weak or often entirely absent. Gleason and colleagues even disputed the very existence of the transverse ligament as a separate discrete structure, showing continuation of fibers from the supraspinatus and subscapularis tendons even in the distal portion of the groove. Paavolainen and colleagues were unable to dislocate the biceps even after sectioning the intertubercular transverse ligament, provided the rotator cuff was intact.
Once the tendon has entered the groove, the principal structure maintaining the tendon within the groove is the falciform ligament, a tendinous expansion from the sternocostal portion of the pectoralis major. It forms a margin with the deep aspect of the main tendon that stabilizes the biceps. The falciform ligament is attached to both lips of the groove and blends with the capsule at the shoulder joint.
O’Brien and colleagues have rigorously studied the anatomy of the biceps, both where it traverses through the bicipital groove and distally. They defined the bicipital tunnel as a specific fibro-osseous structure that encloses the long head of the biceps. The bicipital tunnel begins at the articular margin of the humeral head and ends in the subpectoral region; it has three zones. Zone 1 begins at the articular margin and ends at the distal end of the subscapularis tendon. Zone 2 begins at the distal margin of the subscapularis and ends at the proximal portion of the pectoralis major tendon. Zone 3 is defined as the subpectoral region. This zoning is clinically significant as zone 2 is a “no man’s land” in which pathology cannot be visualized at arthroscopy or in open subpectoral surgery.
Osseous Anatomy
The bicipital groove is formed between the lesser tuberosity medially and the greater tuberosity laterally. Cone and colleagues have extensively studied the bicipital groove, measuring the width and depth of the intertubercular groove and the angle of the medial wall ( Fig. 17-12 ). In assessing the width of the intertubercular sulcus, they obtained two separate measurements from the bicipital groove view. The first of these was the top width or the distance between the medial and lateral lips of the intertubercular sulcus. The second was the middle width or the distance between the walls of the sulcus but taken at a depth halfway into the sulcus. The difference between measurements varied, but the ratio of the top width to the middle width was constant at 1.6. The average depth of the groove was found to be 4.3 mm (range, 4 to 6 mm), and the mean medial wall angle was 56 degrees (range, 40 to 70 degrees).
In a separate study Ueberham and Le Floch-Prigent measured the intertubercular sulcus in dry bones. They found the total length of the groove to be 27.5 mm. On average, the proximal part of the intertubercular sulcus was 12.4 mm, and the most distal part was 15.1 mm. They noted that the groove was deepest in the middle and shallower at its proximal and distal ends. They measured the angle between the proximal segment of the groove and the distal segment and found it to have a mean of 142 degrees but with a high degree of variability. A supratubercular ridge was present in 45% of specimens and was thought to force the biceps anteriorly, thereby increasing the risk of dislocation. This abnormality was found in isolation in 17% of specimens and in association with one other lesion in 18%.
Variability in the medial wall angle was confirmed in studies by Hitchcock and Bechtol, Habermeyer, and Cone. Hitchcock and Bechtol found that the medial wall angle was 90 degrees in 10% of specimens, 75 degrees in 35%, 60 degrees in 34%, 45 degrees in 13%, 30 degrees in 6%, and 15 degrees in 2% ( Fig. 17-13 ). They found (as did Habermeyer) that the medial wall angle correlated with the probability of subluxation of the LHBT. Cone, however, did not find a correlation between the incidence of subluxation and low medial wall angles.
Vettivel and colleagues found that the shape of the intertubercular sulcus correlated with hand dominance: the intertubercular sulcus on the dominant extremity was wider and had a more acute medial wall angle. They attributed this difference to greater stress passing through the tendon in the dominant extremity, especially during manual activities.
Comparative Anatomy
Hitchcock and Bechtol, using specimens from the Field Museum of Natural History in Chicago, outlined changes in the relationship between the scapula and bicipital groove from the quadruped to the erect biped ( Fig. 17-14 ). They described a progressive AP flattening of the thorax that resulted in an increased angle between the scapula and the thorax and a relative lateral displacement of the scapula. Humans have a relatively short forearm and lateral part of the scapula. Such anatomy necessitates greater medial rotation of the humerus to enable the hand to reach the midline. The AP flattening of the thorax and the short forearm were compensated for, but only incompletely, by torsion of the humerus. In the quadruped opossum, the biceps tendon takes a straight course through the bicipital groove and is an effective abductor of the forelimb in the forward plane. In contrast, in humans the tendon is lodged against the lesser tuberosity, where a supratubercular ridge or shallow groove can traumatize the tendon. Humans are unique among the primates in having marked variation in the configuration of the bicipital groove.
The human arm is derived from the foreleg of the quadruped. Whereas in the quadruped the forelimb is designed to bear weight, the upper limb in humans is moved away from the body. For effective use of the limb, it must move not only against its own weight but also against the weight of other objects. This short power arm has to act against a long lever arm, a situation that produces unfavorable mechanical conditions that can lead to tendinitis of the rotator cuff and biceps.
Developmental Anatomy
During the ninth week of gestation, the limbs undergo rotation. The upper limb rotates dorsally at the elbow. This rotation is reflected in the shoulder as humeral retroversion, which averages 35 degrees. In essence, this rotation leaves the biceps tendon behind on the anterior aspect of the shoulder in the groove and requires the biceps to cross the joint obliquely at an angle of 30 to 45 degrees rather than proceeding in a lateral straight line, as in quadrupeds.
The development of the glenohumeral joint is similar to that of other synovial joints in the human body. According to Gardner and Gray, it involves two basic processes. Initially, an inner zone forms between the two developing bones of the joint. This is followed by the creation of cavities by enzymatic action. The inner zone often comprises three layers: a chondrogenic layer on either side of a looser layer of cells. The joint capsule and many of the intra-articular structures, such as the synovial membrane, the ligaments, the labrum, and the biceps tendon, are formed from this inner zone of tissue. Giuliani and colleagues confirmed that the tendon of the long head of the biceps brachii arises in continuity with the anlage of the glenoid labrum. At approximately 7 weeks of gestation, the joint is well formed; the humeral head is spherical; and the tendons of the infraspinatus, subscapularis, and biceps, as well as the glenoid labrum can be seen ( Fig. 17-15 ).
Pathologic Anatomy
Some authors consider tenosynovitis to be the chief cause of pain in biceps tendinitis and believe that it leads to an altered gliding mechanism of the tendon sheath. They describe gradual pathologic changes in the area of the biceps tendon. Initially, there can be capillary dilation, and edema of the tendon with progressive cellular infiltration of the sheath and synovium. Filmy adhesions can then form between the tendon and the tendon sheath. In the chronic stage fraying and narrowing of the biceps tendon occurs along with minimal to moderate synovial proliferation and fibrosis. Ultimately, the tendon is replaced by fibrous tissue, and dense fibrous adhesions become organized. The biceps tendon passes directly under the critical zone of the supraspinatus tendon.
Claessens and Snoek described microscopic changes consistent with a relatively avascular state, including atrophic irregular collagen fiber, fissuring and shredding of tendon fibers, fibrinoid necrosis, and a productive inflammatory reaction with an increase in fibrocytes. Refior and Sowa found that the origin of the tendon and the portion of the tendon that exits the sulcus were predisposed to microscopic degeneration and concluded that these areas were at the highest risk for tendon rupture. Cadaver studies by DePalma and by Claessens and colleagues noted a number of macroscopic changes, including the following: tendinitis with shredding of the tendon by osteophytes, adhesions of the synovial sheaths and of the tendon and its osteofibrous compartment, subluxation or dislocation of the tendon, and rupture of the tendon with retraction of the distal portion or adhesion of the distal portion to the sulcus.
Although it was commonly believed that the dislocated tendon always displaces medially and rides over the subscapularis tendon, Petersson found only one such case in his series. In most cases he noted internal degeneration of the subscapularis in the region of the lesser tuberosity, which allowed the tendon to dislocate medially and under the subscapularis. Similar pathologic findings were described by DePalma.
Sakurai and colleagues studied three groups of patients with chronic shoulder pathology. Patients with an intact rotator cuff (group 1) had no flattening of the tendon in the intertubercular region. Half of the patients with partial-thickness tearing or small rotator cuff tears (group 2) had flattening of the tendon in the intertubercular groove. For the patients with massive rotator cuff tears (group 3), tendon flattening was observed in 66% of the specimens. Bicipital fraying was seen in 16% of these cases. Medial displacement was noted in 12% of group 2 and 38% of group 3. Rupture of the biceps tendon was seen in 16% of group 3 specimens. These authors measured bicipital height, which included the height of the soft tissues, demonstrating a significant difference in height of the medial wall between patients with medial displacement of the biceps and those without instability. The authors were unable to show differences in height of the medial wall between the three groups. They concluded that the LHBT could potentially compensate for deficient rotator cuff function, resulting in relative stenosis of the tendon in the groove. Other gliding disorders can also result from this mismatch between the enlarged tendon size and the noncompliant bony groove. The mismatch may be responsible for degeneration of the soft tissue along the medial wall of the sulcus, causing a pulley lesion and resulting instability.
The biceps tendon and its enveloping synovial sheath can be affected by inflammatory or infectious processes of the glenohumeral joint as a result of their anatomic location and course. Tumorous conditions affecting the synovium of the shoulder can also involve the sheath of the tendon. Therefore tenosynovitis of the biceps accompanies septic arthritis of the shoulder. Similarly, rheumatic inflammation, osteoarthritis, hemodialysis arthropathy, and crystalline arthritis of the glenohumeral joint affect the biceps tendon. The clinical syndrome in such cases is dominated by the articular pathology. Biceps rupture has been reported to occur in conjunction with tuberculosis and syphilis.
Osteochondromatosis has also been reported in the shoulder and bicipital sheath. This disorder causes pain and the formation of loose bodies in the shoulder. Detection of loose bodies in the bicipital sheath on radiography or MRI should arouse suspicion of this pathologic process. Treatment by synovectomy has been successful.
Osseous Pathoanatomy
The shape of the groove has often been implicated in the pathogenesis of biceps tendon ruptures. A shallow, flattened groove ( Fig. 17-16 ) is commonly associated with subluxation or dislocation of the biceps tendon, and a narrow groove with a sharp medial wall. An osteophyte at the aperture is often associated with biceps tendinitis and rupture ( Fig. 17-17 ). Spurs on the floor of the groove can erode the tendon. Although these groove abnormalities can contribute to bicipital tendon problems, it is likely that some are changes in response to pathology of the soft tissues around the shoulder rather than to the underlying cause. In all degenerative conditions about the shoulder, soft tissue changes precede bony changes. For instance, in rotator cuff disorders, the formation of spurring in the anterior acromion is preceded by fibrosis, bursitis, and tendinosis or enthesopathy. Synovitis and cartilage degeneration precede spur formation in the acromioclavicular joint. It seems logical that changes in the bicipital groove and the entrance to the groove would follow changes in the tendon, capsule, ligaments, and synovium around it.
Bony anomalies and variations have been proposed as a cause of subluxation and tendinitis of the biceps tendon. The supratubercular ridge has been described by Meyer as a ridge that extends forward and downward from the region of the articular cartilage to the upper and dorsal portions of the lesser tuberosity ( Fig. 17-18 ). According to Cilley, the incidence of this structure in 200 humeri examined was 17.5%. The ridge decreases the depth of the sulcus and diminishes the effectiveness of the tuberosity as a trochlea. Meyer believed that the ridge pushes the biceps tendon against the transverse ligament, thereby favoring dislocation.
In Hitchcock and Bechtol’s series the supratubercular ridge was found to be markedly developed in 8% and moderately developed in 59%. They found a direct correlation between the presence of a supratubercular ridge and spurs on the lesser tuberosity (medial wall spurs). In their series medial wall spurs were found in approximately 45% of patients with a supratubercular ridge. When no supratubercular ridge was present, only 3% of the humeri had spurs on the lesser tuberosity (see Fig. 17-18C ). The authors concluded that spurs on the lesser tuberosity developed in response to the biceps tendon being pressed against the tuberosity by the supratubercular ridge.
A supratubercular ridge was found in approximately 50% of patients in a study by Cone and colleagues. They did not however find a correlation between its presence and the presence of bicipital groove spurs. It was their belief that the medial wall spur was related more to a traction enostosis or a reactive bone formation. In one specimen they found that the transverse humeral ligament had completely ossified, converting the bicipital groove into a bony tunnel. They agreed with DePalma that the presence of bony spurs on the floor of the bicipital groove was related to chronic bicipital tenosynovitis ( Fig. 17-19 ).
Pfahler and colleagues prospectively compared the ultrasound and radiographic findings of patients with chronic shoulder pain to those of normal control subjects. They found that 43% of those with radiographically evident degenerative changes of the bicipital groove also had sonographic evidence of biceps tendon inflammation. Conversely, ultrasound findings of biceps tendinitis correlated with a smaller total opening angle (<80 degrees) on radiographs in 65% of cases. Of the patients with a flatter medial angle, 47% showed signs of biceps tendinitis. Among patients with bicipital rupture 61% had a shallow medial angle. The authors concluded that 65% of patients in their series with anterior shoulder pain had “conspicuous anatomic findings of the bicipital groove.”
Function of the Biceps Tendon (and the Biceps-Labral Complex)
Basmajian and Latif characterized the action of the biceps brachii muscle as flexion of the elbow joint when the forearm is in the neutral or supinated position but contributing little when the forearm is in a pronated position. They also considered the biceps to be important in decelerating the rapidly moving arm, such as occurs during forceful overhand throwing. There is now general agreement that the biceps brachii is in fact a strong supinator of the forearm and only a weak flexor of the elbow. Debate continues, however, on the exact function of the biceps proximally at the shoulder, and the function of the biceps in connection with the superior labrum. Most anatomy texts regard the biceps as a weak flexor of the shoulder. Studies on function of the biceps tendon can be divided into three broad categories: direct observation, electromyographic (EMG) studies, and biomechanical cadaver studies. The first two of these categories are discussed below.
Direct Observation
The function of the superior labrum, in both intact and torn states, has been the focus of extensive study. The superior labrum is recognized as contributing to the static stability of the shoulder. The role of the biceps tendon on the static and dynamic stability of the shoulder is controversial, but in one of the seminal papers on superior labral injuries, Andrews noted a dynamic tensioning of the biceps-labral complex with electric stimulation of the biceps tendon. However, the dynamic relationship between the biceps tendon and superior labral complex and their combined role in glenohumeral stability remains unclear; this is an area in need of further study.
Many investigators have pointed out that the biceps tendon does not slide in the groove. Rather, the humerus moves on the stationary biceps tendon during shoulder motion like a monorail car on a track. From full adduction to full elevation of the arm, the groove moves a distance of up to 2 to 5 cm along the tendon. Maximal excursion of the humeral head along the tendon results when the shoulder is in a position of maximal external rotation. Minimal excursion is seen when the shoulder is in a position of maximal internal rotation. To facilitate excursion along the tendon, the synovial pouch extends from the shoulder joint, lining the greater part of the intertubercular groove (see Fig. 17-7 ). Within this bursa, the tendon glides through its peritendineum.
The LHBT is sometimes divided into an intra-articular portion and an intratubercular portion. Lippman noted that with the arm in a position of full abduction, 1.3 cm of the LHBT lies within the shoulder joint. This changes however when the arm is adducted and externally rotated such that the length of tendon within the joint increases to 5 cm. He therefore questioned the utility of such a distinction given that the portions of the tendon that are intracapsular or within the groove depend on the position of the arm ( Fig. 17-20 ).
When the arm is in full external rotation, the tendon occupies the floor of the groove, and its more proximal portion presses on the humeral head. Because of this, it was originally believed that in external rotation the long head of the biceps acted as a head depressor at the shoulder to enhance abduction strength at the shoulder. Lucas used a force vector diagram to demonstrate how the long head of the biceps could act as a dynamic humeral head depressor. In addition, the biceps can potentially act as a static humeral head depressor, preventing migration of the humeral head into the acromion with contraction of the deltoid ( Fig. 17-21 ). Rowe believed that the function of the biceps tendon as a humeral head depressor increased in the context of a chronic rotator cuff tear. He pointed to the hypertrophy often seen in the tendon in these situations as evidence. Bush went as far as to transfer the LHBT laterally when repairing cuff defects and claimed that humeral head depression increased with this procedure.
Andrews and colleagues arthroscopically observed the biceps tendon and the superior glenoid-labrum complex during electrical stimulation of the biceps. They noted superior lifting of the labrum and compression of the glenohumeral joint and concluded that in this respect the biceps is a “shunt muscle of the shoulder” and that it helps to stabilize the glenohumeral joint during throwing. They agreed that its primary role during throwing is still to decelerate the elbow. It is this sudden deceleration that leads to tearing of the superior glenoid-labrum complex by the biceps tendon.
In a study by Itoi and colleagues both the long and short heads of the biceps were shown to function as anterior stabilizers of the glenohumeral joint with the arm in abduction and external rotation. They further demonstrated that with increasing instability from sectioning of the inferior glenohumeral ligament (as occurs with the development of a Bankart lesion), both heads of the biceps have an increased stabilizing function to resist anterior displacement of the humeral head. They concluded that during rehabilitation of patients with chronic anterior instability, biceps strengthening should be included in the nonoperative treatment of these lesions.
Kumar and colleagues also studied the stabilizing role of the biceps tendon. They were able to show that severing the LHBT while both heads were tensed caused significant upward migration of the humeral head. The long head of the biceps is therefore important in stabilizing the humeral head in the glenoid during powerful elbow flexion and forearm supination. They warned against sacrifice of the intra-articular portion of the LHBT because of the danger of this resulting in instability during forced elbow flexion and supination.
Other authors have published evidence for the role of the LHBT in glenohumeral stability. Pagnani and colleagues studied cadaveric shoulders subjected to anterior, posterior, and inferior forces at varying arm angles. They measured the amount of translation that occurred with and without an applied force to the biceps, showing decreased translation of the glenohumeral joint in all directions when a 55-N force was applied to the biceps. The effect was greatest at middle and lower elevations. Rotation of the shoulder joint also influenced translation: external rotation reduced posterior translation, whereas internal rotation reduced anterior translation. This applied force to the biceps also reduced superior and inferior translation of the glenohumeral joint. The authors concluded that the biceps helped to center the humeral head on the glenoid, thus stabilizing the fulcrum at which motion can occur.
Malicky and colleagues showed that the biceps provided a 30-N stabilizing force to the humeral head when the arm was in neutral rotation. This stabilizing force depended on the relative position of the groove, with the stabilizing effect at its minimum when the arm was in external rotation. In neutral rotation the biceps added concavity compression as well as a posteriorly directed force on the head against the glenoid. In external rotation the biceps applied an anteriorly directed force on the humeral head and could actually destabilize the joint.
Warner and McMahon studied seven patients with isolated rupture of the LHBT, documented either surgically or with MRI. They demonstrated an increased superior translation of the humeral head at all angles of humeral abduction when compared with the contralateral (control) side. This increased superior translation was not present with the arm at 0 degrees of elevation. They concluded that isolated loss of the biceps could lead to impingement.
Electromyographic Evaluation
Basmajian and Latif were pioneers in evaluating the musculoskeletal system, including the shoulder, with integrated-function and dynamic-spectrum EMG. They reported that both heads of the biceps are active during shoulder flexion, with the long head being the more active of the two. Habermeyer and colleagues found clear EMG activity in the biceps during abduction, greatest at 132 degrees of abduction. Interestingly, he found the muscle to be active even with the arm in neutral rotation; that is, the biceps is active in abduction even when the arm is not externally rotated. The authors found the greatest activity in flexion during the first 90 degrees of flexion and showed that the biceps was active in external but not internal rotation. The effectiveness of the long head of the biceps is greatest in external rotation when its tension is maximal. With the arm adducted and internally rotated, the long head was always inactive; the short head was active in half the cases of adduction and only rarely active in internal rotation. The biceps was totally inactive in extension.
Laumann calculated the percentage contribution of each shoulder muscle to shoulder flexion. He estimated that the biceps contributed approximately 7% of the power of flexion.
Furlani studied EMG activity of the biceps during movements at the glenohumeral joint. He found that during flexion of the shoulder with an extended elbow, both the long and short heads of the biceps brachii were active in the majority of cases. This was regardless of whether resistance was applied. This differed in abduction. With abduction without resistance, there was no biceps activity. The addition of resistance, however, increased biceps activity to 10%.
Ting and colleagues analyzed the EMG activity of the long head of the biceps in patients with rotator cuff tears, correlating their EMG findings with their operative findings. During both shoulder abduction and flexion, four of five subjects demonstrated significantly greater EMG activity of the biceps in the presence of a rotator cuff tear than that of the biceps in the contralateral (uninjured) shoulder. In addition, all shoulders with compromised rotator cuffs proved to have a significantly larger tendon at the time of surgery than those observed in controls. (This finding correlates with the observations of Rowe. ) Ting and colleagues suggested that the lateral head of the biceps may be more important to abduction and flexion in the compromised shoulder than in the normal shoulder and that the concomitant enlargement of the tendon may represent use-induced hypertrophy. They therefore recommended against sacrificing the intracapsular portion of the tendon (e.g., for graft material) or tenodesing the tendon indiscriminately in the groove as a routine part of rotator cuff repair and acromioplasty.
The contribution of the biceps to the shoulder during throwing has been evaluated by Jobe and colleagues and by Perry. In these studies biceps function correlated with motion that occurred at the elbow but not in the shoulder. A relatively stable elbow position during acceleration was accompanied by a marked reduction in the muscle’s firing intensity. During follow-through, the need for deceleration of the rapidly extending elbow and pronating forearm was accompanied by peak biceps action. There was no activity in the biceps muscle during the act of throwing, except in conjunction with elbow activity. Peak activity was only 36% of maximum. With a 9-cm 2 cross section and only half of the muscle related to the long head, the humeral force is small. In Perry’s words, “It seems doubtful that the long head (biceps tendon) is a significant stabilizing force at the glenohumeral joint.” Conversely, Glousman and colleagues reported increased activity in the biceps during throwing in patients with unstable shoulders, suggesting that the biceps may increase in importance if the primary stabilizers are injured.
EMG activity in patients with rotator cuff tears of less than 5 cm was found by Ozaki to be higher than activity in healthy subjects. This increased activity could be an attempt to compensate for the decreased function of the torn rotator cuff. Ozaki, like Ting, postulated that this increased activity could be responsible for the hypertrophy of the tendon often seen accompanying small and medium rotator cuff tears. Patients with massive rotator cuff tears and dislocated biceps tendons did not show a similar increase in activity.
EMG activity of the biceps and rotator cuff was found to precede motion of the glenohumeral joint in a study by David and colleagues. They found that the EMG activity in these muscles occurred before actual internal or external rotation movement (preceding the movement by 0.092 ± 0.038 to 0.215 ± 0.045 seconds). The deltoid and pectoralis major muscles were also active before glenohumeral motion, but significantly later (at 0.030 ± 0.047 to 0.12 ± 0.053 seconds before the movement). They postulated that the biceps and rotator cuff muscles were stiffening the joint, providing a stable platform before the initiation of movement. Once movement was initiated, the activity of the biceps depended on the direction of motion. Little activity was found in the biceps during internal rotation, whereas greater activity was seen during external rotation.
Sakurai and colleagues studied EMG activity in the biceps while maintaining the elbow in neutral rotation in a brace. Surface electrodes were used to measure EMG activity of the deltoid and biceps muscles. Their results showed there to be EMG activity in both the long and short heads of the biceps with all types of motion of the shoulder, independent of elbow position. This indicated that the biceps acted as an active flexor and abductor of the shoulder. There was also activity with rotation, and external rotation induced more activity than internal rotation did. In addition, they demonstrated greater fatigability of the biceps compared with the deltoid. Accordingly, they considered the biceps at higher risk of injury than the deltoid.
In direct contradiction two other studies found no significant dynamic role for the biceps in glenohumeral stability. Yamaguchi and colleagues fixed the elbow at 100 degrees of flexion and held the forearm in neutral rotation with a brace in an attempt to relax the elbow flexors. EMG activity of the brachioradialis was used as a control for biceps EMG activity. They found little to no activity in the biceps tendon with shoulder motion, even in patients in whom the head-depressor effect of the cuff musculature had been compromised. Furthermore, they observed no difference in EMG activity between the brachioradialis and the biceps. They concluded that the role of the biceps in shoulder stability was probably a passive one.
Using a similar experimental design, Levy and colleagues studied the EMG activity of the biceps and rotator cuff muscles with intramuscular electrodes during motion of the shoulder. Again, a brace was used to control elbow motion. Three different elbow positions were tested. The shoulders were moved in flexion, external rotation, and internal rotation at two different speeds and with a 5-lb weight. They found no activity in the biceps when elbow motion was controlled. The authors pointed out that many activities performed by the arm require both elbow and shoulder motion. Their experimental design intentionally eliminated elbow motion, and the lack of biceps activity seems to have been a reflection of the elbow being controlled. The EMG activity of the biceps in other studies may therefore have been a consequence of active motion or stabilization of the elbow and not the shoulder. Based on this, they concluded that the biceps was not active in isolated motion of the shoulder.
Summary
It appears from a review of the literature that the biceps tendon might have a weak active head depressor or stabilizing effect that is clinically insignificant in the normal shoulder. Because of its anatomic position, the tendon serves as a superior checkrein to humeral head excursion and therefore acts as a weak static head depressor as long as it is anatomically positioned. Attempts to understand the dynamic role of the biceps at the shoulder have been confounded by its associated function at the elbow. Immobilization of the elbow with a brace has been used in various studies to circumvent this, but at the same time this creates an artificial scenario that only approximates how the arm is actually used in activities of daily living. Nonetheless, these studies offer compelling evidence that the role of the biceps is minimal during shoulder motion.
The tendon’s importance seems to increase in pathologic states of the shoulder, such as rotator cuff tears and shoulder instability; this is evidenced by the increased EMG activity and by the observed hypertrophy and resistance to translation. The observation of increased superior translation of the humeral head in patients with confirmed bicipital rupture reinforces these findings. However, the clinical relevance of this is questionable given that measurable deterioration in shoulder function has not been demonstrated in patients who have undergone biceps tenotomy or tenodesis. Therefore if the LHBT is implicated as a possible source of a patient’s symptoms (either through physical examination or at surgery), the risk of decreased shoulder function from tenotomy or tenodesis is negligible compared with the risk of continued pain from biceps pathology.
Classification of Bicipital and Labral Lesions
Superior labral anterior posterior (SLAP) lesions were first described by Snyder and colleagues in 1990. Their original classification divided SLAP lesions into four types. A type I lesion is characterized by superior labral degeneration. Type II lesions involve a detachment of the superior labrum and biceps anchor. A type III lesion is typified by a bucket handle tear of the superior labrum, with the biceps anchor still attached, and a type IV lesion is a type III lesion in which the tear extends into the biceps tendon root.
Maffet and colleagues expanded Snyder’s original classification to include three additional types (types V through VII): type V is an extension of a superior labral injury to include an anteroinferior labral tear, type VI is characterized by an unstable labral flap and biceps tendon separation, and type VII represents a detachment of the biceps-labral complex, with extension to the middle glenohumeral ligament. The most recent expansion of SLAP classification was devised by Knesek et al. to include VIII to X: type VIII is a posterior extension of a type II lesion to the 6 o’clock position, type IX represents a circumferential labral tear, and type X is type II tear with a reverse Bankart lesion.
Morgan and colleagues subclassified type II lesions into anterior, posterior, and AP variants.
Biceps lesions have historically been divided into biceps tendinitis and biceps instability. Often, however, much like with rotator cuff tears or lateral epicondylitis, a preponderance of inflammation is not present and the lesion would more accurately be termed tendinosis or tendinopathy . Biceps tendinitis has been subdivided into primary tendinitis (due to pathology of the biceps tendon sheath) and secondary biceps tendinitis (resulting from associated pathology, such as osteoarthritis or rheumatoid arthritis.) Many authors believe that the pathology seen in the biceps is directly related to its intimate relationship with the rotator cuff. As they pass under the coracoacromial arch, both can be involved in the impingement syndrome. A classification by anatomic locale has been offered by Walch.
Primary biceps tendinitis has been likened to de Quervain’s tenosynovitis by Lapidus and Guidotti, who demonstrated the presence of thickening and stenosis of the transverse ligament and sheath as well as narrowing of the tendon underneath the sheath. Post found consistent inflammation within the intertubercular portion of the tendon, a proliferative tenosynovitis, and irregularity of the walls of the groove. This inflammation can be visualized arthroscopically if the extra-articular portion of the tendon is pulled into the joint; it has been referred to as the lipstick sign . There are no reports of inflammation involving the intra-articular portion of the biceps. Codman believed that primary biceps tendinitis was a rare entity. In contrast, DePalma considered it to be a common cause of stiff and painful shoulders. In DePalma’s series 39% of cases had associated disorders. Crenshaw and Kilgore were also proponents of the significance of primary biceps tendinitis, although 40% of their patients also had an associated lesion. They concluded that whether the biceps tendon or its sheath was involved primarily or secondarily was not important. The important point was that tenosynovitis was the chief cause of pain and limitation of motion.
Isolated rupture of the biceps tendon has been described by several authors. Neer believed that most biceps tendon ruptures were associated with supraspinatus tendon tears. Some studies have shown isolated rupture of the biceps tendon to occur in 25% of patients. When computed tomography (CT) arthrograms are performed for patients who meet the clinical criteria for isolated long head of the biceps rupture, the incidence of isolated lesions decreases to 6%. In an arthroscopically controlled study of isolated LHBT lesions, a 2.2% rate of isolated rupture was documented. These studies show that isolated rupture is rare. Many authors have described bicipital groove osteophytes that were thought to be the cause of rupture of the long head of the biceps. Studies using CT scans have shown that the depth and width of the bicipital groove do not have pathognomonic significance.
Although primary biceps tendinitis was commonly recognized as the cause of shoulder pain in the 1940s and 1950s, today it is a much less frequent diagnosis. We do not doubt its existence, but it is clinically very uncommon and should be considered a diagnosis of exclusion.
Slatis and Aalto Classification
Slatis and Aalto have offered a useful clinical classification of biceps lesions ( Box 17-1 ) based on pathoanatomy. According to their review, this appears to have prognostic significance.
Type A: Impingement tendinitis
Type B: Subluxation of the biceps
Type C: Attrition is primary
Type A: Impingement Tendinitis
Type A is tendinitis secondary to impingement syndrome and rotator cuff disease. The torn cuff exposes the biceps to the rigid coracoacromial arch, and such exposure results in tendinitis (tendinosis) ( Figs. 17-22 and 17-23 ).
Type B: Subluxation of the Biceps Tendon
The type B category includes all pathologies of the biceps that involve subluxation and dislocation of the tendon ( Fig. 17-24 ). In this category, lesions of the coracohumeral ligament allow the biceps tendon to gradually become displaced medially.
Type C: Attrition Tendinitis
Type C represents lesions of the biceps tendon that occur within the groove. These are associated with inflammation, stenosis, spur formation, and shredding of the biceps tendon ( Fig. 17-25 ). This condition is considered to be rare but extremely painful.
Habermeyer and Walch Classification
Habermeyer and Walch classified lesions of the biceps tendon in a different way ( Box 17-2 ). They noted that the biceps tendon could be involved in pathology in different anatomic locations. In their classification lesions of the biceps are found at the origin, in the rotator interval, or in association with rotator cuff tears.
- I.
Origin
- II.
Interval Lesions
- A.
Biceps tendinitis
- B.
Isolated ruptures
- C.
Subluxation
Type I : Superior
Type II : At the groove
Type III : Malunion or nonunion of the lesser tuberosity
- A.
- III.
Associated with RCT
- A.
Tendinitis
- B.
Dislocation
Type IA: Extra-articular with a partial subscapularis tear
Type IB: Extra-articular with an intact subscapularis
Type II: Intra-articular
- C.
Subluxation with RCT
- D.
LHB rupture with RCT
- A.
LHB, long head of the biceps; RCT, rotator cuff tear.
Origin Lesions
Origin lesions are described as lesions that affect the attachment of the biceps tendon to the supraglenoid tubercle and to the superior glenoid labrum. These lesions have been observed to occur with the use of muscle stimulation. Biomechanical data by Grauer and colleagues have shown that strain on the labrum from the working biceps is greatest when the arm is in overhead abduction.
Interval Lesions
Habermeyer and Walch divided interval lesions into three types: biceps tendinitis, subluxation of the LHBT, and isolated rupture.
Biceps Tendinitis
Biceps tendinitis is clinically characterized by chronic shoulder pain with tenderness over the bicipital groove and a positive Speed test. When these criteria are used, 90% of all painful shoulders could be considered to have biceps tendinitis, but pathologic examination of biceps tendons in these shoulders rarely shows degenerative or microtraumatic lesions. Such changes of the biceps tendon have been reported in only 5% of cases.
According to Habermeyer and Walch, primary biceps tendinitis can be diagnosed only by arthroscopy. Findings of erythema and a vascular reaction around the long head of the biceps and in the groove are usually observed. For this diagnosis to be made, the shoulder must have a complete passive range of motion. The tendon should not be subluxated or dislocated out of its groove. Mechanical fraying of the bicipital tendon caused by osteophytes or narrowing of the groove from fracture is considered secondary. Habermeyer and Walch reported that although they looked specifically for isolated biceps tendinitis during more than 3 years of arthroscopy of the shoulder, they were unsuccessful in finding a single case. Isolated biceps tendinitis remains a diagnosis of exception.
Subluxation of the Long Head of the Biceps Tendon
The definition of instability of the LHBT is poorly standardized and controversial. Walch defined subluxation of the LHBT as partial or incomplete loss of contact between the tendon and its bony groove and defined dislocation as complete loss of contact between these two. He divided subluxation into three types.
Superior Subluxation (Type I)
Superior subluxation occurs when the superior glenohumeral and the coracohumeral ligaments are partially or completely torn. The result of this tearing is that the LHBT above the entrance of the groove is subluxated superiorly. The subscapularis tendon remains intact, and this prevents true dislocation of the tendon. A type I lesion is a discontinuity of the tendoligamentous rotator interval sling surrounding the LHBT that allows the tendon to migrate superiorly.
Subluxation in the Groove (Type II)
The lesion responsible for the type II subluxation is located inside the bony groove. The tendon slips over the medial rim of the bone of the groove and rides on the border of the lesser tuberosity. This lesion is caused by tearing of the outermost fibers of the subscapularis tendon as well as of some fibers that line the floor. The principal criterion for type II biceps tendon subluxation is partial rupture of the outer superficial tendinous portion of the subscapularis muscle. This lesion can involve the whole groove or only part of it.
Malunion and Nonunion of the Lesser Tuberosity (Type III)
Fracture-dislocation of the lesser tuberosity with malunion or nonunion can allow the biceps tendon to slip in and out of its groove. This lesion is seen after proximal humeral fractures. Affected patients complain of pain with internal rotation of the humerus.
Isolated Rupture of the Biceps Tendon Occurring in the Rotator Interval
Severe primary tendinitis of the tendon in the interval can cause weakening of the tendon and its eventual rupture in this area.
Biceps Tendinitis Associated With Rotator Cuff Tears
Patients in whom tendinitis is associated with a rotator cuff tear experience tendinitis of the biceps secondary to exposure of the biceps to the rigid coracoacromial arch. These patients have a rotator cuff tear but no dislocation or subluxation of the biceps tendon. The biceps is inflamed and painful and can appear hypertrophic when viewed through the arthroscope.
Dislocation Associated With Rotator Cuff Tears
Extra-Articular Dislocation Associated With Subscapularis Lesions (Type IA)
Extra-articular dislocation combined with a partial tear of the subscapularis tendon occurs when the biceps tendon is completely dislocated over the lesser tuberosity. Despite superficial tearing of the subscapularis tendon, the deep portion of the subscapularis is intact, allowing the biceps tendon to line up over the lesser tuberosity and preventing the biceps from entering the joint. In this type of dislocation the outer layer of the subscapularis tendon is always torn. This injury is an evolutional type II subluxation.
Extra-Articular Dislocation of the Long Head of the Biceps Tendon Associated With an Intact Subscapularis (Type IB)
The biceps tendon can dislocate over an intact subscapularis tendon. This condition is extremely rare. The LHBT is found lying superficial to the intact subscapularis tendon, and an associated tear of the supraspinatus tendon is always seen. Type IB was found in 3% of 70 patients with biceps dislocations.
Intra-Articular Dislocation of the Long Head of the Biceps Tendon (Type II)
This type involves intra-articular dislocation of the long biceps tendon combined with a complete tear of the subscapularis tendon. Complete dislocation of the biceps is found in the intra-articular location. This usually occurs in conjunction with extensive tearing of the rotator cuff. The subscapularis tendon is torn completely from its attachment on the lesser tuberosity, and the biceps tendon can become interposed into the joint. The biceps tendon is then apposed to the glenoid labrum and can be entrapped in the anterior joint space during rotational movements of the humerus. Subluxation of the biceps can also be associated with rotator cuff tearing.
Ruptures of the Biceps Associated With Rotator Cuff Tears
The biceps can also rupture as a consequence of rotator cuff tears. Walch has shown the frequency with which these lesions are associated. An isolated rupture of the biceps tendon is extremely rare; most biceps tendon ruptures are associated with rotator cuff tears, usually as a result of impingement of the biceps and supraspinatus tendons in the area of the biceps sulcus.
TLC Classification
In an attempt to simplify how best to think about these complex lesions, one of the authors of this chapter (W.Z.B.) uses the simple mnemonic “TLC.” The TLC system ( Box 17-3 ) takes into account three distinct factors: the status of the biceps tendon (T), the anatomic location (L) of the pathologic process, and associated pathologic conditions of the rotator cuff (C). With this classification, subtypes, such as I, IIA, IIB, IIC, III, or IV do not need to be memorized; there are merely three entities to remember when assessing the biceps.
Incidence
In 1934 DePalma stated that tenosynovitis of the long head of the biceps brachii tendon was the most common antecedent of painful and stiff shoulders. He believed that this was true in both younger and older patients. In his 1954 series he observed the lesion in 77 men and 98 women ranging in age from 16 to 69 years. The highest incidence was between the ages of 45 and 55 years. Bilateral involvement was observed in 8% of cases. Lesions of greater severity were found in the later decades of life, when more severe degenerative changes prevail. In 61.2% of cases the bicipital tenosynovitis was a localized pathologic process; in the remaining 38.8% of cases, inflammation in the biceps tendon and sheath was part of a generalized and chronic inflammatory process. DePalma believed that bicipital tenosynovitis was the initiating agent in 80% of cases of frozen shoulder. Regardless of the cause, bicipital tenosynovitis was always seen in conjunction with a frozen shoulder.
Calcific tendinitis of the long head of the biceps brachii is uncommon. This lesion has been described at two locations: the first is at the insertion of the biceps tendon into the supraglenoid tubercle and superior labrum, and the second is in the distal portion of the groove near the musculotendinous junction. Calcific tendinitis occurred more often in a series by Goldman. He found 9 cases of insertion tendinitis in 119 cases of calcific tendinitis of the shoulder, as opposed to 11 of 19 for the more distal location.
Injuries to the superior labrum and biceps tendon complex are uncommon. In a series by Andrews and colleagues, 7 of 73 throwing athletes had associated partial tears of the biceps tendon and labral pathology. Burkhart and Fox described two cases of complete tears of the biceps associated with SLAP lesions.
According to McCue and colleagues and O’Donoghue, biceps tendinitis and subluxation are common causes of anterior shoulder pain in throwing athletes. They are common in football quarterbacks because of the weight of the ball and the need for additional pushing action and in softball pitchers because of the forceful supinator strain with arm and forearm flexion.
Lapidus and Guidotti identified 89 patients with tendinitis of the long head of the biceps in a total of 493 patients treated for shoulder pain (an incidence of 18%). Paavolainen and colleagues reported on patients who failed to respond to conservative care and were referred to a shoulder center. A preoperative diagnosis of biceps tendinitis was made before arthrotomy in 38 (30%) of 126 cases. Postoperatively, the incidence was much higher, with 54% of operative specimens showing some evidence of biceps tendinitis. In patients with cuff ruptures the incidence was as high as 60%. If the rotator cuff was intact (with no full-thickness tear), the incidence was approximately 50%. Although this study defined cuffs without a full-thickness rotator cuff tear at surgery as being intact, most of these cuffs showed some evidence of degeneration, edema, and signs of type I and II impingement. Medial dislocation of the biceps tendon occurred in 12 of 51 patients with a ruptured rotator cuff and in 9 of 75 patients when the cuff was intact, for an overall incidence of dislocation of 17%. Frank rupture of the biceps tendon was seen in 8 (6%) of the 126 patients.
Because bicipital tenosynovitis occasionally accompanies impingement syndrome, it remains a relatively common cause of anterior shoulder pain. However, as an isolated entity (i.e., as primary bicipital tenosynovitis), it is much less common.
Etiology
Although the majority of biceps tendon dislocations occur secondarily as a result of degeneration and attrition of the anterior cuff and coracohumeral ligament, there have been reports of acute traumatic dislocation of the tendon. Abbott and Saunders presented six such cases in 1939 along with their operative findings. Four were caused by a fall, resulting in either a direct blow to the shoulder or an indirect blow after falling on the outstretched hands. Two occurred during heavy lifting. All but one of these patients had a concomitant injury to the rotator cuff.
DePalma and later Michele divided the etiology of biceps tendinitis according to age group. In younger patients anomalies of the bicipital groove together with repeated trauma are the major inciting factors. In older patients degenerative changes in the tendon are the predominant etiologic factor.
As with most other musculoskeletal problems, the etiology of biceps pathology is most likely to be multifactorial. Chief among the causes is the anatomic location of the tendon. The blood supply of the tendon has been studied by Rathbun and Macnab, who showed it to be diminished, with a critical zone similar to that seen in the supraspinatus. In abduction there is a zone of avascularity in the intracapsular portion of the tendon. This is thought to be caused by pressure from the head of the humerus, the “wringing out” phenomenon. Occupational causes also exist because patients who perform repetitive overhead lifting and throwing are more prone to rupture, elongation, and dislocation of the biceps. Meyer reasoned that capsular defects leading to problems with the biceps resulted from repeated and continual use of the arm in a position of marked abduction and external rotation. Borchers and later DePalma explained spontaneous rupture within the groove in terms of osteophytic excrescences, which eventually wear through the tendon. Etiologic factors based on variations in the groove have been discussed earlier.
The etiology of calcific deposits in the biceps may be active or passive. Hydroxyapatite deposition disease has been described and can occur in various tendons throughout the body. In a study by Refior and Sowa, histologic analysis of the biceps tendon showed degeneration at the biceps origin and in the region in which the biceps tendon exits the groove. They noted kinking and destruction of the collagen fibers in both these areas. Whether this degeneration is responsible for inducing calcification in some susceptible patients is debatable.
Intra-articular lesions of the biceps and superior labrum can be caused by several mechanisms. The first is a fall on the outstretched hand that drives the humeral head up into the labrum and the tendon. Andrews and colleagues noted that excessive and forceful contraction of the biceps in throwing athletes, especially baseball pitchers and quarterbacks, can induce traction and avulsion of the biceps and superior labral complex in the deceleration phase of throwing. SLAP lesions can also be created by traction on an adducted arm. Burkhart described a “peel-back” mechanism in the etiology of SLAP tears. This phenomenon of superior labral injury is the end result of a pathologic chain of events that begins with functional deficiencies in the core and includes pathologic glenohumeral internal rotation deficit and the SICK scapula syndrome ( s capular malposition on rib cage, i nferior medial scapular winging, c oracoid tenderness, and scapular dys k inesis).
Gerber and Sebesta described an anterior internal impingement syndrome similar to the posterior internal impingement syndrome described by Walch and colleagues. In their study, contact between the superior glenohumeral ligament and the anterior rim of the glenoid occurred while performing the Hawkins modified impingement test at 120 degrees of anterior elevation. The undersurface of the subscapularis tendon came into contact with the anterior glenoid rim when the arm was placed between flexion of 80 and 100 degrees. Contact of the superior glenohumeral ligaments and subscapularis on the anterior glenoid rim could explain fraying of these deep structures that do not come into contact with the anterior acromion. These findings were most commonly found in the dominant arm of manual laborers.
Patients maintained on dialysis with long-standing kidney failure can have shoulder pain and symptoms similar to biceps tendinitis. Often, the etiology of this syndrome is a synovitis caused by the deposition of amyloid-like substances. This is a rare cause of shoulder pain. Another rare cause of bicipital pain and degeneration is a tumoral condition, such as osteochondromatosis of the bicipital sheath.
Prevention
Prevention of biceps tendon injuries includes warmup, passive stretching, strengthening exercise, and avoidance of painful activities while symptomatic. Strengthening should include all the muscles of the rotator cuff to improve the force couple and reduce impingement. The parascapular muscles should also be rehabilitated. Better balance of the shoulder musculature will theoretically diminish the vicious circle of tendinitis, irritation, and muscle weakness, followed by altered biomechanics, cuff tears, subluxation, and further impingement. Manual laborers, such as carpenters, who do a lot of heavy lifting or repetitive overhead work should probably spend as much time stretching before undertaking their jobs as football and baseball players do before undertaking theirs. Stretching of the biceps tendon is maximal when the shoulder is fully extended and externally rotated and the elbow is fully extended as well.
Overhand athletes, especially pitchers and quarterbacks, should warm up and stretch their capsule to avoid glenohumeral internal rotation deficit and its attendant consequences for the superior labrum and biceps. They should be encouraged to strengthen the muscles of their upper extremity, especially the rotator cuff. Athletes should also be monitored closely to prevent overuse syndromes and capsular contracture.
Clinical Features of Bicipital Lesions
As with all medical conditions, an accurate history and physical examination is vital. This is especially true for subtle lesions of the shoulder, such as biceps tendinitis and biceps instability.
Patients with biceps tendinitis typically complain of chronic pain in the proximal anterior shoulder. The pain can extend down the arm into the muscle belly of the biceps or radiate to the deltoid insertion. It is less likely to radiate into the neck or distally beyond the biceps. Typically, patients have no history of major trauma. They tend to be young or middle-aged and have a history of repetitive overhead activity. The pain is less intense at rest and worse with use. There is disagreement regarding night pain associated with biceps tendinitis: Neviaser stated that there is significant night pain, whereas Simon stated that nocturnal exacerbation is common. In our experience all painful conditions of the shoulder are worse at night, possibly because of compression loading and the supine position placing the shoulder at or below the level of the heart.
Bicipital symptoms are often seen in patients who participate in sports. Any activity at or above shoulder level brings the tuberosities, the bicipital groove, the biceps tendon, and the rotator cuff into close proximity and potentially in direct contact with the anterior acromion, the coracoacromial ligament, and the anterior edge of the glenoid. This can lead to trauma to the intervening biceps tendon.
Biceps instability is most commonly seen in throwing athletes. A palpable snap or pop is often felt at certain positions in the arc of rotation. The patient complains again of pain in the front of the shoulder. This pain is usually reproduced when the arm is raised to 90 degrees.
Patients with rupture of their biceps tendon sometimes also report an audible pop in the shoulder followed by acute onset of pain. The patient then often notes a change in contour of the arm and formation of ecchymosis over the next several days.
Calcific tendinitis in the distal part of the LHBT can also clinically manifest as anterior shoulder pain in young and middle-aged adults. The duration and severity of this pain varies.
Superior labral injuries and injuries to the biceps-labral complex can occur in isolation or in parallel with any of the above conditions. Overhead athletes may report pain during throwing, serving, or other overhead activity, but a paucity of pain at rest. In more severe injuries throwers may report a “dead arm” and the inability to throw.
Physical Examination
Clinical evaluation of the superior labrum and biceps-labral complex can be challenging due to relatively poor specificity for a number of clinical tests. Many of the tests described below for evaluating the biceps can also be utilized to test the superior labrum. However, multiple maneuvers can be performed in isolation and in combination with other tests to specifically evaluate the superior labrum. The original and modified O’Driscoll dynamic labral shear test is performed by stabilizing the scapula, placing the humerus in the location that evokes symptoms, and then applying a compressive and shear load.
The active compression test—commonly known as O’Brien’s test—evaluates the superior labrum and can help distinguish pain emanating from the superior labrum from pain from the acromioclavicular joint. The test is performed by placing the shoulder in 90 degrees of forward flexion, 10 to 15 degrees of adduction and internal rotation, and applying a downward force. This maneuver is then repeated with the arm in external rotation. The test is considered positive for labral pathology if the first maneuver caused pain localized deep in the shoulder and the second maneuver (the arm in external rotation) resulted in less pain. O’Brien and colleagues have extended the original active compression test to include the “three-pack” physical examination of the biceps-labral complex. This consists of (1) palpation of the bicipital tunnel, (2) an active compression test, and (3) a throwing test that consists of placing the arm in 90 degrees of abduction and the elbow in 90 degrees of flexion and then passively placing the arm in external rotation, thus simulating a throwing motion. The three-pack examination can be used in conjunction with diagnostic or therapeutic injections into the glenohumeral joint to diagnose or rule out symptomatic biceps-labral complex lesions.
Physical examination can reveal point tenderness in the bicipital groove. With the arm in 10 degrees of internal rotation, the biceps tendon faces directly anterior and sits 7 cm distal to the acromion ( Fig. 17-26 ). This point tenderness would be expected to move as the arm is rotated and the position of the bicipital groove changes. Tenderness from subdeltoid bursitis can also localize to the anterior shoulder but is generally more diffuse and should not travel with arm rotation. In our opinion this tenderness in motion is the most specific test for bicipital lesions. It does not however differentiate biceps instability from tendinitis. Many authors have suggested that the biceps tendon can be manipulated and, in the presence of instability, can be felt subluxating out of the groove. In our opinion what is perceived by the examiner as the biceps tendon subluxating may in fact be muscle bundles of the deltoid rolling against the humerus. Palpable subluxation might therefore be an inaccurate test for biceps instability.
