e176(1) C OPYRIGHT Ó 2014

BY

T HE J OURNAL

OF

B ONE

AND J OINT

S URGERY, I NCORPORATED

Exhibit Selection

The Biceps Tendon: From Proximal to Distal AAOS Exhibit Selection David Y. Ding, MD, Garret Garofolo, BS, Dylan Lowe, MD, Eric J. Strauss, MD, and Laith M. Jazrawi, MD Investigation conducted at New York University Hospital for Joint Diseases, New York, NY

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he function of the long head of the biceps tendon (LHB) in shoulder glenohumeral biomechanics is unclear. However, there is agreement that the biceps can develop tendinopathy resulting in pain over the anterior aspect of the shoulder, specifically in the bicipital groove1,2. With recent advancements in arthroscopy and more detailed imaging, selection of appropriate management for proximal biceps disorders is important. Compared with this proximal component, the anatomy, epidemiology, and underlying pathophysiology of the distal component of the biceps tendon are less well understood. Although distal biceps rupture has a low annual incidence, approximately 1.2 per 100,000 persons3, it can lead to substantial morbidity. The emerging understanding of the clinical importance of distal biceps ruptures and the effectiveness of distal biceps repair are the focal points for the increased attention to this topic. Patients are unique individuals who may be best suited for a specific treatment depending on their age, activity level, and goals. The ideal repair would be one that is anatomic, permits early motion, and has low surgical morbidity and minimal complications. Our review provides an overview of the anatomic, biomechanical, and clinical literature that fully encompasses the biceps brachii from origin to insertion with an emphasis on treatment indications, surgical approaches, fixation techniques, and clinical outcomes.

The Proximal Aspect of the Biceps Tendon Anatomy he LHB arises from the superior glenoid labrum and supraglenoid tubercle. This proximal, intra-articular portion of the biceps tendon has an asymmetric network of sensory

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sympathetic nerve fibers, predominantly near its origin, and is a primary pain generator in the anterior aspect of the shoulder4. The reflection pulley—composed of fibers from the superior glenohumeral ligament, coracohumeral ligament, and superior aspect of the subscapularis tendon—functions to stabilize the biceps tendon as it advances through the bicipital groove5 (Fig. 1). As the LHB enters the bicipital groove (located between the lesser and greater tuberosities), it is maintained there by the transverse humeral ligament, formed mostly of fibers from the subscapularis tendon6. Anatomic variants are common for the LHB. In the landmark article by Vangsness et al.7, the origin of the biceps tendon is described as having four possible variants. Other authors have attempted to characterize the many variations of the intra-articular portion of the LHB. Kanatli et al. found seven types of biceps tendon morphology during arthroscopic evaluation8. One variant—the pulley type—had clinical importance as it was associated with a substantial increase in labral pathology (Fig. 2). They hypothesized that the pulleytype variant produced a double-pulley effect that provided countertraction to the proximal portion of the tendon, increasing anterolateral traction on the superior labral complex and leading to more labral pathology. Pathophysiology Although some authors believe that the biceps tendon has little impact on shoulder function9, others have found substantial contributions to anterior stabilization and depression of the humeral head10,11. They theorized that in the absence of an intact LHB, excessive glenohumeral motion may lead to early-onset

Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

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http://dx.doi.org/10.2106/JBJS.N.00032

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Fig. 1

Illustration (left) of the biceps pulley with corresponding proton density-weighted saline solution MR arthrograms and bandsaw sagittal sections of a cadaver specimen through the medial (Fig. 1-A), middle (Fig. 1-B), and lateral (Fig. 1-C) portions of the rotator interval. SGHL = superior glenohumeral ligament, BT = biceps tendon, CHL = coracohumeral ligament, MCHL = medial coracohumeral ligament, LCHL = lateral coracohumeral ligament, and RIC = rotator interval capsule.

osteoarthritis. Nevertheless, Berlemann et al. reviewed fifteen patients who had undergone tenodesis of the LHB and found only slight upward migration of the humeral head on postoperative radiographs, which was without clinical importance in any case12. LHB pathology includes a spectrum of conditions from inflammatory tendinitis to degenerative tendinosis. SLAP (superior labrum from anterior to posterior) tears may involve the biceps anchor13. Biceps instability often occurs in conjunction with rotator cuff tears, especially those involving the subscapularis tendon14. This instability causes continued trauma to the biceps tendon as it subluxates or dislocates, resulting in LHB ruptures15. Pulley tears are also associated with LHB instability and can occur as a result of acute trauma, chronic repetitive

microtrauma, or age-related degeneration5. Rarely, primary tendinitis is seen; this involves isolated inflammatory changes to the tendon with no associated pathologic disorders of the shoulder16. Diagnosis Physical Examination

Pain from the LHB is commonly located over the bicipital groove on the anterior aspect of the shoulder2,17. This pain can be differentiated from shoulder pain by performing provocative tests such as the Speed and Yergason tests18. A positive result on these tests is pain over the anterior aspect of the shoulder that is consistent with the location of the symptomatology near the

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Imaging

Shoulder radiographs should be made for initial evaluation of osseous anatomic causes of shoulder pain. If further imaging proves necessary, ultrasonography is cost-effective and useful for detecting rupture and subluxation or dislocation of the biceps. However, it has poor sensitivity (49%) in detecting partial ruptures and biceps tendinitis21. Better visualization of the LHB occurs with MRI (magnetic resonance imaging), which can also detect other abnormal shoulder pathology (e.g., rotator cuff and SLAP tears). With the addition of intra-articular contrast, MR arthrography offers the best means of identifying subtle patterns of LHB instability22 (Fig. 3). The ligamentous biceps pulley is often difficult to visualize on standard MRI but can be seen on axial images of high-resolution MR arthrography. Management Nonoperative Treatment Fig. 2 8

The pulley type variant described by Kanatli et al. has a double-pulley effect providing counter-traction to the proximal portion of the tendon, increasing anterolateral traction on the superior labral complex and leading to more labral pathology.

bicipital groove. Biceps instability often presents with clicking or snapping in the anterior aspect of the shoulder as well as tenderness to palpation on full abduction and external rotation of the arm19. Baumann et al. reviewed 1007 diagnostic arthroscopies and showed a 7.1% prevalence of isolated biceps pulley tears20. The O’Brien test (sensitivity = 67%, specificity = 64%) and Speed test (sensitivity = 67%, specificity = 61%) were the most sensitive and specific tests for pulley tears. Even so, these tests are commonly positive for LHB pathologies of various types and do not uniquely identify pulley injuries. SLAP tears may involve the biceps anchor and may also cause these tests to be positive. After an LHB rupture, ecchymosis can be seen in the proximal aspect of the arm, and a Popeye deformity can be seen in this area in slender individuals.

The initial treatments for LHB tendinitis or a SLAP tear is conservative management of symptoms. Rest and NSAIDs (nonsteroidal anti-inflammatory drugs) can be combined with physical therapy to manage early-stage LHB disease. If severe inflammation of the tendon sheath is resistant to those therapies, corticosteroid injections can be directed into the bicipital groove23. Ultrasonography can be used to substantially improve injection accuracy24,25 and to avoid intratendinous injection and potential iatrogenic tendon rupture26. Operative Treatment

Operative repair of type-II SLAP tears has been controversial. The argument in favor of repair has centered on its ability to restore the anatomic balance of the shoulder. Clinically, however, the benefits of a repair are not as straightforward. In a small study, Boileau et al. demonstrated the effectiveness of biceps tenodesis (satisfaction rate, 93%) compared with SLAP repair (satisfaction rate, 40%)27 in a cohort in which the mean age was thirty-seven years in the repair group compared with fifty-two years in the tenodesis group. The current evidence regarding type-II SLAP tears is that younger, overhead athletes

Fig. 3

3-T T2-weighted axial MRI showing the LHB lying in the bicipital groove (left) and medially subluxated as a result of a subscapularis tendon (SSc) rupture.

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Fig. 4-A

Fig. 4-B

Figs. 4-A and 4-B Biceps tenodesis performed with use of a mini-open incision. Fig. 4-A The exposure of the bicipital groove involves retraction of the deltoid and pectoralis muscles superolaterally and retraction of the short head of the biceps brachii and coracobrachialis muscles medially. Vigorous medial retraction should be avoided to protect the musculocutaneous nerve. Fig. 4-B A unicortical drill hole slightly larger than the LHB diameter is made at the distal aspect of the bicipital groove.

who report a distinct traumatic event may improve if treated with repair of the tear but older patients with lower expectations perform better with minimal intervention. A biceps tenotomy involves cutting the LHB at its origin near the superior labrum, maintaining the integrity of the labral ring. Arthroscopic biceps tenotomy is an option for partial ruptures, ruptures associated with a subscapularis tear, and longitudinal ruptures that result in poor tendon gliding, medial subluxation, or disruption of the pulley2,19. Despite possible residual Popeye deformity and fatigue weakness28, a tenotomy is an effective and reproducible technique to relieve shoulder pain due to LHB pathology29. There is minimal surgical morbidity and activity restrictions are not required during rehabilitation. In younger, more active individuals, a tenotomy can potentially lead to decreased strength and pain with repeated activity, making tenodesis rather than tenotomy a preferred option. Tenodesis involves reattachment of the LHB to either soft tissue or the proximal aspect of the humerus to prevent retraction. Selected more frequently in younger, active patients, biceps tenodesis affords improved cosmesis and restores the proper length-tension relationship. It can be performed by means of either arthroscopy30-32 or a mini-open procedure (Figs. 4-A and 4-B). The disadvantages of tenodesis compared with tenotomy involve a longer surgical procedure, increased surgical morbidity, and lifting restrictions during patient rehabilitation. A variety of reattachment sites for biceps tenodesis have been described, including the coracoid, lesser tuberosity, transverse humeral ligament, pectoralis major tendon, and bicipital groove. The

current controversy involves the location of tenodesis within the bicipital groove. The LHB can be fixed suprapectorally33,34 at the entrance to the bicipital groove or subpectorally35,36 under the superior border of the pectoralis major tendon. Those who favor subpectoral biceps tenodesis over suprapectoral tenodesis argue that removal of the tendon removes a pain generator within the intertubercular groove. Fixation superior to or within the bicipital groove can lead to persistent tenosynovitis of the biceps sheath, resulting in an increased revision rate37. Lutton et al.36 reported that tenodesis of the biceps in the upper half of the bicipital groove led to persistent pain in 40% of the patients in their series at six months of follow-up. Although a tenotomy is technically easier to perform, advocates of biceps tenodesis claim improved function and cosmesis when the length-tension relationship is restored. Slenker et al. performed a systematic review of sixteen studies with a total of 699 tenotomy procedures and 433 tenodesis procedures. Both procedures had similarly excellent results (74% for tenotomy compared with 77% for tenodesis), but tenodesis resulted in a much lower rate of Popeye deformity (8% compared with 43%)38. The rate of residual bicipital pain was 24% in the tenodesis group compared with 19% in the tenotomy group. On the basis of the limited studies available, biceps tenotomy is recommended for more sedentary, obese older patients who are not concerned with cosmesis and have lower physical demands. Many biceps tenodesis methods have been described. These include unicortical or bicortical button fixation (Fig. 5), interference screw fixation, keyhole fixation to bone, suture

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Fig. 5

Figs. 5-A and 5-B Bicortical button fixation of the long head of the biceps. Fig. 5-A The cortical button is loaded after whipstitching the tendon by passing a free suture through the ipsilateral button hole away from the tendon and back through the contralateral hole toward the tendon. This is repeated with the other free suture end. Fig. 5-B Final fixation showing the cortical button on the posterior aspect of the humerus and the whipstitched LHB shuttled through the humerus and then tied down with suture.

anchor fixation, and suture fixation to adjacent tissue32,39,40. The gold standard in terms of fixation strength is interference screws (Fig. 6), which are biomechanically superior to suture anchors41 and bone tunnels42. Kusma et al. analyzed the mechanical properties resulting from five common fixation methods and showed that interference screws provided a significant advantage in primary fixation strength and cyclic displacement43. Bicortical button fixation can also be used as an alternative because of its equivalent pull-out strength and minimal drill size. The Distal Aspect of the Biceps Tendon Anatomy ntil recently, the distal aspect of the biceps tendon was believed to be a singular, flat, paratenon-lined, extrasynovial structure that wrapped around the bicipital tuberosity and attached to the ulnar aspect of the tuberosity44-46. However, recent cadaveric studies47 have identified a normal variant, present in 40% to 60% of individuals, which possesses two distinct tendinous insertions, both of which are continuations of their respective long and short heads. The anatomic footprint comprises approximately 64% of the length of the tuberosity (21 mm) and approximately 10% of the width of the tuberosity (7 mm)48,49. The lacertus fibrosus is a three-layer aponeurosis that encompasses the biceps tendon at the level of the musculotendinous junction and helps prevent proximal retraction after a distal biceps tendon rupture46-48.

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Pathophysiology Distal biceps rupture typically occurs as a result of an overwhelming eccentric load applied to a previously flexed elbow. This sudden overpowering force results in an acute avulsion of the distal tendon stump from the bicipital tuberosity47,50. Most often, distal biceps ruptures occur in the dominant arm (86%) of men thirty to fifty51 years of age with a history of tobacco use3,52. Corticosteroid and tobacco use are implicated in bilateral distal biceps ruptures53. The combination of physiological

ischemia, potential focal osseous irregularities of the radial tuberosity49, and the oblique biomechanical force exerted by medial translation of the lacertus fibrosus during flexion of pronated forearm predisposes the tendon to rupture46,54,55. Diagnosis Physical Examination

Distal biceps tendon injuries represent a spectrum of disease from tendinitis to partial-thickness ruptures to complete ruptures. Patients who present within four weeks of a complete distal biceps rupture are considered to have an acute injury. These patients usually describe a sudden, painful ‘‘popping’’ sensation, which is associated with antecubital pain, loss of function, and weakness in flexion and supination. Depending on the duration of time since the rupture, ecchymosis and swelling may be minimal or nonexistent. Partial ruptures are usually identified by deep antecubital pain exacerbated by resisted supination. Chronic complete ruptures are typically categorized as ruptures that are more than four weeks old. These patients usually lack pain and swelling but report decreased supination strength and fatigue and have an identifiable ‘‘reverse Popeye sign’’ caused by proximal retraction of the tendon stump. Palpation of the radial tuberosity or displaced tendon stump can cause pain. In the ‘‘hook test’’ described by O’Driscoll et al., the patient fully supinates the forearm and passively flexes the elbow to form a 90° angle. The examiner then places an index finger deeply to ‘‘hook’’ the lateral edge of the biceps tendon56. The contralateral, uninjured arm is useful as a control. A negative test is when the examiner can hook the tendon without pain, and a positive test is the absence of a cord-like biceps tendon under which the examiner may hook a finger. Imaging

Distal biceps rupture is predominantly a clinical diagnosis; however, additional imaging may rule out other pathology. Radiographs are commonly negative50. Occasionally, osseous

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avulsion of the radial tuberosity can be seen. MRI can differentiate complete and partial ruptures from tendinosis as well as identify the rupture location and amount of retraction57-59 (Fig. 7). Although MRI is the gold standard, ultrasonography is less expensive and can utilize the contralateral arm for comparison. As ultrasonography is very operator-dependent, further studies are needed to evaluate the accuracy of ultrasonography as the sole diagnostic instrument. Management Nonoperative

Traditionally, distal biceps ruptures were managed nonoperatively to avoid the morbidity that would result from the extensive dissection required to provide adequate surgical exposure60. Conservative treatment remained the preferred treatment until 198561, when it was shown that nonoperative treatment yielded 30% and 40% reductions in flexion and supination strength, respectively. Studies by Chillemi et al.62 and Hetsroni et al.63 echoed those results, with operatively treated patients having better subjective and objective functional outcomes. Currently, nonoperative management is reserved for lowdemand, sedentary patients and those with substantial medical comorbidities64-66. Operative

Fig. 6

Interference screw fixation. The biceps tendon is sized, and a hole 0.5 to 1 mm larger than the interference screw is reamed. The tendon is then pushed to the bottom of the bone socket. Finally, the anchor is advanced into the socket.

Operative management is strongly advocated in young, active, healthy individuals who wish to return to full participation in life and activities. Sarda et al. recently reviewed twenty-four patients treated with distal biceps repair who had attained their maximum recovery. They reported complete recovery of flexion and supination strength with return of full elbow range of motion in all but two patients, who lacked 10° of full extension67. Initially, surgeons debated whether to reattach the tendon to the bicipital tuberosity (anatomic repair) or to the brachialis or lacertus fibrosus (nonanatomic repair)68. Rantanen and Orava performed a meta-analysis of 147 cases showing that 90% of anatomic repairs yielded good to excellent results at three years compared with only 60% of nonanatomic repairs. Nonoperative treatment had the poorest outcome, with only 14% yielding good-toexcellent results69. Furthermore, Klonz et al.70 showed poorer supination strength after nonanatomic repairs (42% to 56% of the strength on the contralateral side) compared with anatomic repairs (91% of the strength on the contralateral side). With new minimally invasive implants and improved understanding of the surgical anatomy, several studies71-73 have demonstrated the benefit of using a single-incision approach to perform a distal biceps repair. There are currently two singleincision approaches used to repair a distal biceps rupture: a longitudinal S-shaped incision (Henry technique) and a short transverse incision (limited antecubital incision)71,74. The postoperative complications most commonly seen with singleincision anterior approaches are neurological, with neurapraxia involving the lateral antebrachial cutaneous nerve being the most common followed by the median nerve and the radial nerve (including the posterior interosseous nerve)65,70-72,74-76. The lateral antebrachial cutaneous nerve can be protected with careful

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Fig. 7

T2-weighted MRI showing complete rupture of the distal aspect of the biceps tendon (arrowhead), with the tendon end retracted approximately 1.4 cm into the upper arm. Note the intact lacertus fibrosus (white arrow), which can prevent proximal retraction of the tendon.

dissection and the posterior interosseous nerve can be protected with forearm supination, minimizing iatrogenic nerve injury71,74. Sotereanos et al.77 evaluated the single-incision anterior approach in sixteen patients. Eight patients were considered to have an acute injury (less than six weeks) and experienced full recovery of flexion and supination strength. The other eight patients were deemed to have a chronic injury (greater than six weeks) and experienced deficits in flexion and supination strength averaging 14% and 16%, respectively. Balabaud et al.71 observed similar positive results in a series of nine patients. Despite the overall good results, complications are common. In a meta-analysis of 165 distal biceps repairs, Chavan et al.78 reported an overall complication rate of 18%, with most of these (13%) being transient lateral antebrachial cutaneous nerve neurapraxia. The two-incision technique combines an anterior incision with a posterolateral incision to the radial tuberosity. The anterior incision is used to identify the tendon stump, and the posterior incision is used to identify the posterior-ulnar ‘‘true anatomic’’ aspect of the radial tuberosity79. Cadaveric studies have shown that it is extremely difficult to reliably repair the tendon to its anatomic footprint through an isolated anterior approach80. When using a two-incision approach, the posterior incision involves dissecting or splitting the supinator, which

may injure the posterior interosseous nerve; in addition, there is a potential risk of heterotopic ossification resulting from injury to the interosseous membrane52,61,65,75,81-83. Several studies utilizing the two-incision approach have documented promising results. D’Alessandro et al.52 evaluated ten patients by means of self-reported outcomes and isokinetic testing; the mean reported outcome was 9.75 out of 10. An interesting finding in that study as well as the study by Leighton et al.82 was the restoration of normal flexion strength and endurance when the surgical procedure was performed on the nondominant arm but a 25% loss in supination strength when the dominant arm was treated. Karunakar et al.81 evaluated twenty patients and also noted reduced range of motion of the forearm (in four patients), supination strength (in ten), and flexion strength (in three) even though all twenty patients reported good or excellent results on self-reported questionnaires. Although the two-incision technique yields good subjective results, the complication rate is high (16% to 31%)84. Reported complications include persistent anterior elbow pain (8%), sensory nerve paresthesia of the lateral antebrachial cutaneous nerve or superficial radial nerve (10%), heterotopic ossification (6%), restricted forearm rotation (4%), posterior interosseous nerve palsy (2%), and rerupture (2%).

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To our knowledge, only one prospective, randomized controlled trial comparing single and two-incision repair techniques has been performed to date; it demonstrated no significant differences in outcomes between the techniques85. However, that study by Grewal et al., while underpowered with respect to complications, did show a marked difference in the rate of transient neurapraxia of the lateral antebrachial cutaneous nerve: 40% in the single-incision group compared with 7% in the two-incision group. Chavan et al.78 performed a systematic review that included 165 distal biceps rupture repairs utilizing a single incision and 142 utilizing two incisions. Unsatisfactory results were significantly more common in the two-incision group (31%) than in the single-incision group (6%), due primarily to decreased forearm rotation or

supination strength. It is thought that this loss of strength was caused by robust dissection between the radius and ulna leading to denervation of or damage to the supinator75,86. Complication rates were similar in the two groups (18% for a single incision and 16% for two incisions); however, the singleincision group had a higher rate of nerve injury (12%) whereas the two incision group had more frequent loss of forearm rotation (9%). This reiterates the increased risk of transient neurapraxia of the lateral antebrachial cutaneous nerve with the single-incision technique, likely secondary to intraoperative tissue retraction. The commonly used methods of fixation are bone tunnels, suture anchors87, cortical buttons65 (Fig. 8), and interference screws88.

Fig. 8

Figs. 8-A through 8-D Cortical button repair of a distal biceps rupture. Fig. 8-A We prefer a transverse incision 2 cm distal to the elbow crease. Fig. 8-B The cortical button is loaded after whipstitching the tendon by passing a free suture end through the ipsilateral button hole away from the tendon and back through the contralateral hole toward the tendon. Fig. 8-C This is repeated with the other free suture end. Fig. 8-D The tendon is then docked in a bone tunnel, and the button is flipped onto the opposite cortex.

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Outcomes Biomechanical Outcomes

The classic Boyd and Anderson technique utilized bone tunnels89. However, the popularity of the single-incision technique has coincided with increasing use of minimally invasive fixation techniques such as suture anchors, cortical buttons, and interference screws. To date, the most comprehensive study examining the biomechanical properties of distal biceps tendon repairs is that of Mazzocca et al.90. They observed that virtually all fixation devices were capable of withstanding tensile forces similar to those withstood by the native tendon, which fails at 210 to 221 N91,92. However, cortical button fixation yielded superior pull-out strength (440 to 584 N)90,93-95, up to three times that for bone tunnels and twice that for suture anchors. As a result, the stronger cortical button repair may allow earlier postoperative elbow motion. Chronic Distal Biceps Ruptures

In chronic distal biceps ruptures, the combination of muscle atrophy and shortening, distal tendon retraction, and fibrosis makes primary anatomic reattachment of the tendon challenging. Especially in cases in which the lacertus fibrosus is also ruptured, the distal aspect of the biceps tendon retracts proximally. If the excursion of the tendon is not adequate for an anatomic repair, a nonanatomic tenodesis to the brachialis muscle restores elbow flexion strength but does not restore supination strength70. Primary repair of a chronic distal biceps rupture is possible if the excursion of the tendon permits repair with the arm

in 70° of flexion96. However, the authors of previous studies have recommended the use of allograft when anatomic repair cannot be achieved. Recent studies have shown successful restoration of strength and elbow range of motion with allograft use. In what we believe to be the largest case series to date, Snir et al. reviewed twenty distal biceps ruptures that underwent delayed reconstruction, primarily with use of Achilles allograft; all yielded satisfactory results, almost full return of strength, and no limitation in elbow motion97. Other studies have shown similar successful reconstruction with use of Achilles96,98,99, semitendinosus100,101, and fascia lata102,103 allograft as well as hamstring autograft104,105. n

David Y. Ding, MD Garret Garofolo, BS Dylan Lowe, MD Eric J. Strauss, MD Laith M. Jazrawi, MD Department of Orthopaedic Surgery, New York University Hospital for Joint Diseases, 301 East 17th Street, New York, NY 10003. E-mail address for D.Y. Ding: [email protected]. E-mail address for D. Lowe: [email protected]. E-mail address for E.J. Strauss: [email protected]. E-mail address for L.M. Jazrawi: [email protected]

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