CC BY-NC-ND 4.0 · Rev Bras Ortop (Sao Paulo) 2020; 55(03): 329-338
DOI: 10.1055/s-0039-3402472
Artigo Original
Ombro e cotovelo
Sociedade Brasileira de Ortopedia e Traumatologia. Published by Thieme Revinter Publicações Ltda Rio de Janeiro, Brazil

Supraspinatus Muscle Tendon Lesion and Its Relationship with Long Head of the Biceps Lesion[*]

Article in several languages: português | English
1   Departamento de Ortopedia e Traumatologia, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brasil
,
Carina Cohen
1   Departamento de Ortopedia e Traumatologia, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brasil
,
Paulo Santoro Belangero
1   Departamento de Ortopedia e Traumatologia, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brasil
,
Alberto de Castro Pochini
1   Departamento de Ortopedia e Traumatologia, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brasil
,
Carlos Vicente Andreoli
1   Departamento de Ortopedia e Traumatologia, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brasil
,
Benno Ejnisman
1   Departamento de Ortopedia e Traumatologia, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brasil
› Author Affiliations
Further Information

Endereço para correspondência

Cassiano Diniz Carvalho
Rua Teixeira Santana 185, Fundinho, Uberlâ38400-196
Brasil   

Publication History

21 July 2018

05 February 2019

Publication Date:
27 February 2020 (online)

 

Abstract

Objective To identify the clinical, radiological, and arthroscopic correlation of long head of the biceps tendon injuries and their influence on pain when associated with rotator cuff injuries.

Methods Between April and December 2013, 50 patients were evaluated, including 38 (76%) women and 12 (24%) men, with a mean age of 65.1 years old. The patients were operated by the Shoulder and Elbow Group, Discipline of Sports Medicine, Orthopedics and Traumatology Department, Universidade Federal de São Paulo. The subjects underwent repair of the rotator cuff lesion with clinical, radiological and/or arthroscopic evidence of involvement of the long head of the biceps tendon.

Results An association between pain at palpation of the intertubercular groove of the humerus and high-grade partial lesions (partial rupture of the tendon affecting more than 50% of its structure) was observed at the arthroscopy (p = 0.003). There was also an association between the high-grade lesion of the long head of the biceps and injury to the supraspinatus muscle tendon (p < 0.05). For each centimeter of the supraspinatus muscle tendon injury, the patient presented a 1.7 higher probability of having a high-grade lesion at the long head of the biceps.

Conclusion Pain at the anterior shoulder region during palpation of the intertubercular groove of the humerus may be related to high-grade lesions to the long head of the biceps. Rotator cuff injury and its size are risk factors for high-grade injuries to the long head of the biceps tendon.


#

Introduction

Throughout history, the long head of the biceps (LHB) brachii tendon has been the subject of great controversy, being considered either a major source of shoulder pain or an insignificant structure.[1] Kessell and Watson[2] described it as an easy-to-blame but hard-to-condemn structure.

There is still no consensus on the true role of the LHB tendon in shoulder biomechanics. Nevertheless, its function, as well as its important role in static and dynamic stabilization, have been investigated by different authors.[3] Several authors have noted an important stabilizing role,[4] in addition to humeral head centralization at the secondary glenoid, as described by Pagnani.[5]

In 1934, biceps tendinitis was questioned by Codman,[6] who even doubted there was a tendinous inflammatory process, and considered that the pain was much more likely caused by supraspinatus muscle tendon injuries. Codman was unable to prove biceps involvement in any of his cases. From the 50’s, several authors considered biceps tendinitis an important cause of shoulder pain, and treated it with tenodesis.[2] [7] In 1950 DePalma[7] described degenerative tendon changes and their conservative and surgical treatment. In 2015, Godinho et al[8] described a new surgical technique for LHB tenodesis.

The LHB tendon is 9 cm long,[9] and it is divided into an intra-articular and an extra-articular portion; the extra-articular portion is fibrocartilaginous and slides on the intertubercular groove of the humerus. Such a division, however, is not 100% accurate. The humeral head moves as on a rail to the tendon, whereas the tendon does not move in relation to the bicipital groove.[2] [10] Therefore, the arm position dictates the relationship between the intra- and extra-articular portions. For instance, during arm adduction and extension, most of the tendon is intra-articular. In contrast, in extreme abduction, only a small part of the tendon is intra-articular.[1]

As such, LHB tendinopathy may arise from repeated friction, traction and glenohumeral rotation, which result in pressure and shear forces. Since the intertubercular groove is a constricted environment, it is usually affected by the inflammatory process.[11]

Diagnostic tests for LHB tendon injuries have limited clinical utility when applied alone.[12]

Today, magnetic resonance imaging (MRI) is the most used complementary test for LHB tendon injury diagnosis. Studies indicate that MRI sensitivity ranges from 52% to 69.8%, with 86% to 98% of specificity for complete lesions.[13] However, the arthroscopic evaluation is considered the gold standard for intra-articular LHB tendon injury diagnosis.[14]

Neviaser et al[15] observed a close relationship between LHB tendinopathy and rotator cuff injuries on arthrography and intraoperative observation of macroscopic changes.

The present study aimed to evaluate the clinical, radiological, and arthroscopic correlation of the LHB tendon lesions associated with rotator cuff injuries and their relationship with referred shoulder pain.


#

Materials and Methods

A total of 56 patients were evaluated and operated on by a surgeon from the Shoulder and Elbow Group, Discipline of Sports Medicine, Orthopedics and Traumatology Department, Universidade Federal de São Paulo, São Paulo, Brazil, from April to December 2013. In total, 6 patients were excluded from the initial sample of 56 subjects. Among the excluded patients, two had incomplete MRI data, three had no intraoperative LHB tendon lesion, and one subject did not agree to sign the informed consent form (ICF). Of the remaining 50 patients, 38 (76%) were female and 12 (24%) were male, with a mean age of 65.1 years.

The inclusion criteria were patients with anterior shoulder pain submitted to rotator cuff injury repair and with clinical, radiological and/or arthroscopic evidence of LHB tendon involvement.

The exclusion criteria were patients who underwent rotator cuff lesion repair with no indication of tenotomy due to the lack of symptoms related to LHB lesion or absence of injury at the time of the arthroscopy, as well as patients with no rotator cuff lesion associated with LHB injury.

The patients were questioned and examined by specialists from the Brazilian Society of Shoulder and Elbow Surgery (Sociedade Brasileira de Cirurgia do Ombro e Cotovelo, SBCOC). The MRI scans were performed using the Achieva 1.5T (Philips, Amsterdam, Netherlands) scanner, and they were evaluated by two experienced surgeons, who were also SBCOC members, according to the same criteria specified in the data collection form; the Patte classification and rotator cuff lesion quantification in centimeters were used to define the degree of tendon retraction.

The patients were placed in the beach chair position, under general anesthesia and brachial plexus block, and submitted to arthroscopy for rotator cuff injury repair and intra- and extra-articular LHB tendon evaluation through macroscopic lesion analysis. With the scope at the posterior portal and the arthroscopic hook at the anterior portal, the LHB was dislocated inferiorly, bringing the extra-articular portion of the tendon into the joint.

The tip of the arthroscopic hook served as a measuring instrument to grade the thickness of the LHB lesion. The measurement was performed 1.5 cm from the labral insertion of the LHB tendon.

The MRI scans were performed using T1- and T2-weighted spin-echo techniques. The variables included LHB injury signs, presence and size of the rotator cuff lesion (Patte classification), and the presence of associated lesions, such as type-II superior labral tear from anterior to posterior (SLAP) lesion.

During surgery, macroscopic LHB tendon lesions, such as redness, fibrillation, flattening, partial injury, tendon dislocation, pulley injury, type-II SLAP lesion, and rotator cuff tendon injury, including the subscapularis muscle, which is directly related to LHB dislocation, were evaluated.

The study was approved by the Ethics in Research Committee at Hospital São Paulo and all patients signed the ICF.

The numerical variables were expressed as means and standard deviations (SDs), medians and quartiles (Qs), minimum and maximum values, whereas the categorical variables were expressed as absolute and relative frequencies.

The associations between pain and the physical tests, the MRI and the intraoperative findings were assessed by simple logistic regression models.

The analyses were performed using the Statistical Package for the Social Sciences (SPSS, SPSS, Inc., Chicago, IL, US) software, version 18, adopting a significance level of 5%.

The agreement and disagreement between LHB tendon injuries at the physical examination, MRI scans and arthroscopy, specifically high-grade partial LHB lesion and SLAP lesion, were evaluated using the McNemar nonparametric test, adopting a 5% significance level.


#

Results

The final sample consisted of 50 symptomatic patients who underwent rotator cuff lesion repair with symptoms and/or magnetic resonance imaging indicating LHB tendon involvement.

Symptom duration ranged from 2 to 240 months, and half of the patients had symptoms for at least 12 months. The right shoulder was affected in 70% of the subjects, and the affected limb was the dominant one for 72% of the patients.

At the physical examination, half of the patients had up to 160° (Q1 = 140° and Q3 = 180°) of active flexion range and up to 180° (Q1 = 170° and Q3 = 180°) of passive range. Pain at palpation of the LHB tendon at the humerus intertubercular groove was observed in 66% of the patients. In the special physical tests, 72% of the patients were positive for the O'Brien test, 78% were positive for the Palm Up test, and 40% were positive for the Yergason test.

The MRI showed that 92% of the patients had biceps tendinopathy, and 1 patient presented a total rupture (2.0%). Regarding the supraspinatus muscle tendon, 4% presented a partial bursal lesion; 4% had a partial intra-articular injury; and the remaining subjects presented total tendon injury, with tendon retraction ranging from 0.9 cm to 5 cm, with a median value of 2.9 cm.

The imaging evaluation also revealed that 42% of the patients presented infraspinatus muscle tendon injury; 32% had subscapularis muscle tendon injury; 14% presented LHB tendon dislocation; and 4% had type-II SLAP lesion.

During the arthroscopy, 60% of the patients had an LHB tendon lesion involving more than 50% of its thickness. The changes included redness in 88% of the patients ([Figure 1]); flattening in 54% ([Figure 2]); fibrillation in 86%; partial rupture in 60%; and biceps dislocation in 20% of the subjects.

Zoom Image
Fig. 1 Long head of the biceps (LHB) brachii tendon redness.
Zoom Image
Fig. 2 Long head of the biceps (LHB) brachii tendon flattening.

Other LHB tendon-related injuries were observed during the arthroscopy: 24% of the patients had subscapularis muscle tendon injury; 22% presented pulley injury; and 6% had type-II SLAP lesion.

[Table 1] shows the descriptive analyses of the numerical variables from the clinical evaluation, physical examination and radiological findings in our 50 patients.

Table 1

Variable

Average (standard deviation)

Median (1st quartile; 3rd quartile)

Range

minimum – maximum

Clinical evaluation

 Age (years)

65.1 (6.2)

65 (60; 69)

51–83

 Symptom duration (months)

30.7 (41.4)

12 (7; 36)

2–240

Physical exam

 Active flexion (°)

152.2 (31.7)

160 (140; 180)

80–180

 Passive flexion (°)

173.2 (13.8)

180 (170; 180)

110–180

Radiological evaluation: magnetic resonance imaging

 Size of the lesion at the supraspinatus muscle tendon (cm)

2.8 (1.2)

2.9 (1.5; 3.7)

0.9–5.0

[Table 2] shows the gender distribution, the dominance of the affected limb, and the categorical variables from the physical examination.

Table 2

Clinical evaluation

Gender

 Female

38 (76.0)

 Male

12 (24.0)

Affected shoulder

 Right

35 (70.0)

 Left

15 (30.0)

Dominant shoulder

 No

14 (28.0)

 Yes

36 (72.0)

Physical exam

Pain during humerus intertubercular groove palpation

 No

17 (34.0)

 Yes

33 (66.0)

O'Brien test

 Negative

14 (28.0)

 Positive

36 (72.0)

Palm Up test

 Negative

11 (22.0)

 Positive

39 (78.0)

Yergason test

 Negative

30 (60.0)

 Positive

20 (40.0)

[Table 3] shows the radiological evaluation (MRI) findings regarding the LHB tendon lesion, its dislocation in relation to the bicipital gutter, and associated rotator cuff injuries and SLAP lesion.

Table 3

Radiological evaluation: magnetic resonance imaging

Long head of the biceps (LHB) brachii lesion

 Total lesion

1 (2.0)

 Negative

3 (6.0)

 Positive

46 (92.0)

Infraspinatus muscle tendon lesion

 No

29 (58.0)

 Yes

21 (42.0)

Subscapularis muscle tendon lesion

 No

34 (68.0)

 Yes

16 (32.0)

Supraspinatus muscle tendon retraction

 I

8 (16.0)

 II

29 (58.0)

 III

9 (18.0)

 No

4 (8.0)

LHB dislocation

 No

43 (86.0)

 Yes

7 (14.0)

Superior labral tear from anterior to posterior (SLAP) lesion, type II

 No

48 (96.0)

 Yes

2 (4.0)

[Table 4] presents the morphological characteristics of the LHB tendon, its dislocation in relation to the bicipital gutter, and associated subscapularis muscle tendon injury and SLAP lesion observed during the arthroscopy.

Table 4

Surgical procedure: arthroscopy

Redness

 No

6 (12.0)

 Yes

44 (88.0)

Flattening

 No

23 (46.0)

 Yes

27 (54.0)

Fibrillation

 No

7 (14.0)

 Yes

43 (86.0)

Partial, high-grade long head of the biceps (LHB) brachii lesion

 No

20 (40.0)

 Yes

30 (60.0)

LHB dislocation

 No

40 (80.0)

 Yes

10 (20.0)

Subscapularis muscle tendon lesion

 No

38 (76.0)

 Yes

12 (24.0)

Pulley injury

 No

39 (78.0)

 Yes

11 (22.0)

Superior labral tear from anterior to posterior (SLAP) lesion, type II

 No

47 (94.0)

 Yes

3 (6.0)

Snyder classification of the SLAP lesion

 II

3 (6.0)

 No

47 (94.0)

There was an association between pain at palpation of the intertubercular groove of the humerus and high-grade partial LHB lesion (partial rupture affecting more than 50% of the LHB tendon – [Figures 3] and [4]) during the arthroscopy (p = 0.003). Patients with pain at palpation of the intertubercular groove of the humerus had an 83% probability of having a significant LHB lesion involving more than 50% of the thickness of the tendon. As such, the positive patients were 1.7 times more likely to develop a significant lesion, unlike the negative patients.

Zoom Image
Fig. 3 High-degree lesion at the long head of the biceps (LHB) brachii tendon, affecting over 50% of its thickness.
Zoom Image
Fig. 4 Proximal portion of the long head of the biceps (LHB) brachii tendon, with a lesion affecting over 50% of its thickness, after tenotomy.

There was no evidence of statistically significant associations between other special tests (Palm Up, O'Brien and Yergason) and high-grade partial LHB lesion (p > 0.05).

[Table 5] evaluates the associations between pain at palpation of the intertubercular groove of the humerus, special physical tests, magnetic resonance imaging findings and intraoperative findings.

Table 5

Pain during humerus intertubercular groove palpation

p-value

No

Yes

Physical exam

 O'Brien test

Negative (n = 14)

6 (42.9)

8 (57.1)

ns

Positive (n = 36)

11 (30.6)

25 (69.4)

 Palm Up test

Negative (n = 11)

6 (54.5)

5 (45.5)

ns

Positive (n = 39)

11 (28.2)

28 (71.8)

 Yergason test

Negative (n = 30)

12 (40.0)

18 (60.0)

ns

Positive (n = 20)

5 (25.0)

15 (75.0)

Magnetic resonance imaging

 LHB tendinopathy

No (n = 3)

1 (33.3)

2 (66.7)

ns

Yes (n = 46)

16 (34.8)

30 (65.2)

 Infraspinatus muscle tendon lesion

No (n = 29)

12 (41.4)

17 (58.6)

ns

Yes (n = 21)

5 (23.8)

16 (76.2)

 Subscapularis muscle tendon lesion

No (n = 34)

13 (38.2)

21 (61.8)

ns

Yes (n = 16)

4 (25.0)

12 (75.0)

 LHB dislocation

No (n = 43)

14 (32.6)

29 (67.4)

ns

Yes (n = 7)

3 (42.9)

4 (57.1)

 SLAP lesion

No (n = 48)

17 (35.4)

31 (64.6)

ns

Yes (n = 2)

0 (0.0)

2 (100.0)

Intraoperative

 Redness

No (n = 6)

4 (66.7)

2 (33.3)

ns

Yes (n = 44)

13 (29.5)

31 (70.5)

 Flattening

No (n = 23)

7 (30.4)

16 (69.6)

ns

Yes (n = 27)

10 (37.0)

17 (63.0)

 Fibrillation

No (n = 7)

3 (42.9)

4 (57.1)

ns

Yes (n = 43)

14 (32.6)

29 (67.4)

 Partial, high-grade LHB lesion

No (n = 20)

12 (60.0)

8 (40.0)

0.003

Yes (n = 30)

5 (16.7)

25 (83.3)

 LHB dislocation

No (n = 40)

13 (32.5)

27 (67.5)

ns

Yes (n = 10)

4 (40.0)

6 (60.0)

 Subscapularis muscle tendon lesion

No (n = 38)

13 (34.2)

25 (65.8)

ns

Yes (n = 12)

4 (33.3)

8 (66.7)

 Pulley injury

No (n = 39)

13 (33.3)

26 (66.7)

ns

Yes (n = 11)

4 (36.4)

7 (63.6)

 SLAP lesion

No (n = 47)

16 (34.0)

31 (66.0)

ns

Yes (n = 3)

1 (33.3)

2 (66.7)

In this specific group of patients, all of them presenting supraspinatus muscle tendon injury and some degree of LHB tendon injury, high-grade LHB lesion was directly related to the size of the supraspinatus tendon lesion (p < 0.05); for each centimeter of supraspinatus muscle tendon injury, the risk of having a high-grade LHB lesion was 1.7 higher. Thus, in patients with supraspinatus muscle tendon injuries that are 1 cm and 3 cm long, the chance of having a significant LHB lesion is 41.4% and 67.1% respectively.

[Table 6] shows the associations between LHB tendinopathy on the MRI and physical examination tests and intraoperative findings; there was no evidence of association between tendinopathy on the MRI and the analyzed variables (p > 0.05). However, there was an association between subscapularis muscle tendon injury on the MRI and LHB dislocation during the arthroscopy (p < 0.001). It is noteworthy that the probability of an individual with total subscapularis muscle tendon injury to present intraoperative LHB dislocation is of 91%, corresponding to a 55-fold increased risk in patients with this lesion.

Table 6

LHB lesion at MRI

p-value

No (n = 3)

Yes (n = 47)

Physical exam

 Pain during humerus intertubercular groove palpation

No

1 (33.3)

16 (34.0)

ns

Yes

2 (66.7)

31 (66.0)

 O'Brien test

Negative

2 (66.7)

12 (25.5)

ns

Positive

1 (33.3)

35 (74.5)

 Palm Up test

Negative

0 (0.0)

11 (23.4)

ns

Positive

3 (100.0)

36 (76.6)

 Yergason test

Negative

2 (66.7)

28 (59.6)

ns

Positive

1 (33.3)

19 (40.4)

Intraoperative

 Redness

No

1 (33.3)

5 (10.6)

ns

Yes

2 (66.7)

42 (89.4)

 Flattening

No

1 (33.3)

22 (46.8)

ns

Yes

2 (66.7)

25 (53.2)

 Fibrillation

No

0 (0.0)

7 (14.9)

ns

Yes

3 (100.0)

40 (85.1)

 Partial, high-grade LHB lesion

No

1 (33.3)

19 (40.4)

ns

Yes

2 (66.7)

28 (59.6)

 LHB dislocation

No

2 (66.7)

38 (80.9)

ns

Yes

1 (33.3)

9 (19.1)

 Subscapularis muscle tendon lesion

No

1 (33.3)

37 (78.7)

ns

Yes

2 (66.7)

10 (21.3)

 Pulley injury

No

1 (33.3)

38 (80.9)

ns

Yes

2 (66.7)

9 (19.1)

 SLAP lesion

No

3 (100.0)

44 (93.6)

ns

Yes

0 (0.0)

3 (6.4)

 Snyder classification of the SLAP lesion

II

0 (0.0)

3 (6.4)

ns

No

3 (100.0)

44 (93.6)

The McNemar test was applied to evaluate the agreement between the physical examination tests and the characteristics of the lesions on the MRI and intraoperatively observed during the arthroscopy. We observed that palpation of the intertubercular groove of the humerus is a good test to detect high-grade LHB tendon lesions. Similarly, the MRI agreed with the arthroscopy for SLAP lesions and LHB dislocation.


#

Discussion

Patients with LHB tendon disease often complain of pain at the anterior shoulder region, especially at the humerus intertubercular groove. The symptoms may be difficult to distinguish from those of other shoulder disorders, especially rotator cuff injuries.[16]

Despite the lack of statistical significance, there was a similar positivity between the Palm Up test and the intraoperative presence of high-grade LHB tendon injury (78% and 60% respectively). Bennett et al[17] reported that the Palm Up test has a high sensitivity (90%) for macroscopic LHB tendon lesions; although to a lesser extent, such high sensitivity was also observed in the present study.

The positivity on the O'Brien test was of 72%. Only 4% of the tests were positive for SLAP injury on the MRI. At the intraoperative evaluation, however, 6% of the patients presented with this lesion. The McNemar test assessed the agreement between physical examination, MRI and arthroscopy findings. It showed a discrepancy between O'Brien's positivity and both MRI and arthroscopy, demonstrating that this isolated test is not suitable for SLAP lesion diagnosis.[18] However, the incidence of SLAP lesion on the MRI and arthroscopy showed a statistically significant agreement.

The literature is controversial regarding the ability of the O'Brien test alone to detect SLAP injuries. Ben Kibler et al[12] demonstrated that it has a moderate sensitivity (61%), which is consistent with the results found by Godinho et al,[19] who observed a sensitivity of 66.7%. This test is not able to reproduce the peel back movement that occurs in the LHB to trigger the symptoms. Nonetheless, the O'Brien test has a moderate ability to diagnose SLAP lesions,[16] which was not consistent with our results. On the other hand, another authors concluded that this test is not a sensitive diagnostic indicator and observed a high incidence of false-positive patients, possibly due to associated shoulder injuries (rotator cuff injury, for example).[20] [21]

No single test is sufficient for SLAP lesion diagnosis. A combination of the available tests can increase the efficiency of lesion identification, although the result of this association is insignificant when compared to any test applied alone.[18]

In total, 40% of the patients had a positive result in the Yergason test. However, only 20% of the patients had LHB tendon dislocation on the arthroscopy, and 14% were diagnosed with it on the MRI. Similarly, the McNemar test showed a disagreement between the Yergason test and the incidence of lesions on both the MRI and arthroscopy, demonstrating that this isolated test is not suitable for LHB dislocation diagnosis. However, lesion incidence on the MRI and arthroscopy presented a statistically significant agreement.

Consistent with our results on the Yergason test, Ben Kibler et al[12] demonstrated that it has high specificity and low sensitivity, being more accurate to rule out a lesion than to detect it.

Taylor et al[22] observed that palpation of the intertubercular groove of the humerus and the O'Brien test have high sensitivity (97.8% and 95.7% respectively). On the other hand, the Palm Up and Yergason tests are very specific (86.7% and 97.9% respectively), but present low sensitivity. Therefore, when the O'Brien test and humerus intertubercular groove palpation are negative, we can safely exclude the presence of an extra-articular LHB lesion.

Analyzing our results regarding the special tests previously described, as well as data found in the literature, we observed that tests applied together are more successful in the diagnosis than the tests applied alone.[18]

Long head of the biceps tendon injuries are complex and multifactorial. They are didactically defined as biceps-labral complex lesions, which are divided in labral LHB insertion lesions (SLAP lesions); intra-articular tendon body and tendon pulley lesions; and extra-articular lesions at the humerus intertubercular groove. Given this interaction between regions that could harbor painful injuries to the LHB tendon, a set of three tests has been proposed to increase the diagnostic accuracy compared to the isolated tests. The following associated tests were proposed: humerus intertubercular groove palpation; the throwing test (with the arm abducted at 90°, the elbow flexed at 90° and maximum external rotation, the patient initiates a throwing motion against a resistance imposed by the examiner); and the O'Brien test.[18] [22]

The MRI is the most common tool to diagnose intra-articular LHB tendon lesions. In our study, the MRI was positive in 92% of the patients, and 59.6% of them had a high-grade LHB lesion (affecting more than 50% of the tendon). There was a 90% agreement between the MRI and arthroscopy when redness, flattening and high-grade partial injury were considered as macroscopic signs of injury.

In contrast, Malavolta et al[23] observed a moderate sensitivity (67%) and a high specificity (98%) on the MRI. These authors only evaluated total LHB tendon ruptures, whereas we also considered inflammatory signs and partial injuries, which may explain the higher incidence of positive tests.

Mohtadi et al[13] observed a lower prevalence of diagnosis on the MRI and a lower agreement between the MRI and the arthroscopy, of 66% and 37.7% respectively. We attributed this disagreement to the fact that the population evaluated in our study was older (mean age of 65.1 years versus 46.2 years in the study by Mohtadi et al[13]), considering that the incidence of LHB tendon injuries associated with rotator cuff injuries increases with age.

The only statistically significant correlation between the physical examination and the arthroscopic evaluation found in our study was pain at palpation of the intertubercular groove of the humerus, which was observed in 83% of the patients with lesions affecting more than 50% of the LHB tendon thickness. Partial injury is the most common indication for tenotomy and tenodesis.[24] Accordingly, surgeons must be prepared for a possible LHB tendon procedure if the suspicion on the physical examination is confirmed during surgery.

Current histological studies have questioned whether alterations observed in imaging scans and arthroscopy can really characterize LHB inflammation. Streit et al[25] concluded that anterior shoulder pain does not appear to be related to an inflammatory process at the extra-articular portion of the LHB tendon in most cases. Of the 26 patients evaluated, only 2 presented histological alterations consistent with chronic inflammation, and none had histological alterations characteristic of an acute inflammatory process.

The association between rotator cuff injuries and LHB tendon injuries is well known in the medical literature,[15] and although several studies confirm their anatomical relationship, only a few are devoted to a more detailed investigation.[26] The literature reports that the association between these 2 lesions ranges from 78.5% in a smaller sample (n = 28)[24] to 22% in a larger sample (n = 207) as observed by Braum et al.[27]

Lafosse et al[21] observed a strong relationship between LHB lesion and rotator cuff injury size. Thus, our study corroborates the literature and adds a risk relationship not yet described between these two variables. We observed that, for every centimeter of supraspinatus muscle tendon injury, the patient has a 1.7-fold greater risk of developing a high-grade LHB tendon lesion. The incidence ranges from 41.4% to 67.1% for 1- and 3-cm lesions respectively.

The patients who underwent biceps surgery concurrently with rotator cuff lesion repair had better outcomes compared to those submitted to the isolated cuff repair.[28] Chechia et al[29] demonstrated a 93.4% satisfaction rate in patients undergoing rotator cuff repair associated with LHB tenodesis. Ikemoto et al[30] observed better results in patients submitted to tenodesis associated with tenotomy compared to those who underwent isolated tenotomy, noting that the latter also presented satisfactory results.

The present study had limitations regarding its sample, even though a 50-patient population is compatible with the Brazilian literature. For a test power of 50% and 90%, a sample of 208 and 300 patients respectively would be required. Other limiting factors were the absence of a control group with patients without LHB tendon lesions, and the fact that this was a specific population, composed mostly of female patients with a mean age of 65.1 years.

The fact that we did not find significant associations between the variables does not mean that they do not exist; in reality, the sample size may have been responsible for the non-significance in the analyses.


#
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Conflito de interesses

Os autores declaram não haver conflito de interesses.

* Work performed at the Orthopedics and Traumatology Department, Centro de Traumatologia do Esporte (CETE), Escola Paulista de Medicina, Universidade Federal de São Paulo (Unifesp), São Paulo, SP, Brazil.


  • Referências

  • 1 Rockwood Jr. Charles A. , Matsen 3rd, Frederick A. The shoulder. 4th ed. Philadelphia: Saunders Elsevier; 2009
  • 2 Kessel L, Watson M. The painful arc syndrome. Clinical classification as a guide to management. J Bone Joint Surg Br 1977; 59 (02) 166-172
  • 3 Itoi E, Kuechle DK, Newman SR, Morrey BF, An KN. Stabilising function of the biceps in stable and unstable shoulders. J Bone Joint Surg Br 1993; 75 (04) 546-550
  • 4 Warner JJ, McMahon PJ. The role of the long head of the biceps brachii in superior stability of the glenohumeral joint. J Bone Joint Surg Am 1995; 77 (03) 366-372
  • 5 Pagnani MJ, Deng XH, Warren RF, Torzilli PA, O'Brien SJ. Role of the long head of the biceps brachii in glenohumeral stability: a biomechanical study in cadavera. J Shoulder Elbow Surg 1996; 5 (04) 255-262
  • 6 Codman EA. The Shoulder. Boston: Thomas Todd; 1934
  • 7 DePalma AF. Surgery of the shoulder. Philadelphia: JB Lippincott; 1950
  • 8 Godinho GG, Mesquita FA, França FdeO, Freitas JM. “ROCAMBOLE-LIKE” biceps tenodesis: technique and results. Rev Bras Ortop 2015; 46 (06) 691-696
  • 9 Enad JG. Bifurcate origin of the long head of the biceps tendon. Arthroscopy 2004; 20 (10) 1081-1083
  • 10 Logal RJ. Rupture of the long tendon of the biceps brachii muscle. Clin Orthop Relat Res 1976; (121) 217-221
  • 11 Raney EB, Thankam FG, Dilisio MF, Agrawal DK. Pain and the pathogenesis of biceps tendinopathy. Am J Transl Res 2017; 9 (06) 2668-2683
  • 12 Ben Kibler W, Sciascia AD, Hester P, Dome D, Jacobs C. Clinical utility of traditional and new tests in the diagnosis of biceps tendon injuries and superior labrum anterior and posterior lesions in the shoulder. Am J Sports Med 2009; 37 (09) 1840-1847
  • 13 Mohtadi NG, Vellet AD, Clark ML. , et al. A prospective, double-blind comparison of magnetic resonance imaging and arthroscopy in the evaluation of patients presenting with shoulder pain. J Shoulder Elbow Surg 2004; 13 (03) 258-265
  • 14 Anbar A, Emad Y, Zeinhom F, Ragab Y. Shoulder arthroscopy remains superior to direct MR arthrography for diagnosis of subtle rotator interval lesions. Eur J Orthop Surg Traumatol 2015; 25 (04) 689-697
  • 15 Neviaser TJ, Neviaser RJ, Neviaser JS, Neviaser JS. The four-in-one arthroplasty for the painful arc syndrome. Clin Orthop Relat Res 1982; (163) 107-112
  • 16 Ejnisman B, Monteiro GC, Andreoli CV, de Castro Pochini A. Disorder of the long head of the biceps tendon. Br J Sports Med 2010; 44 (05) 347-354
  • 17 Bennett WF. Specificity of the Speed's test: arthroscopic technique for evaluating the biceps tendon at the level of the bicipital groove. Arthroscopy 1998; 14 (08) 789-796
  • 18 Taylor SA, Newman AM, Dawson C. , et al. The “3-Pack” Examination is critical for comprehensive evaluation of the Biceps Labrum Complex and the Bicipital Tunnel: a prospective study. Arthroscopy 2017; 33 (01) 28-38
  • 19 Godinho GG, Freitas JM, França FO, Lopes AA, Milazzo AJ, Dal Zotto C. Efficiency of the evaluation, clinical (O'Brien test) and imaging (Arthro-MRI) methods in the diagnosis of shoulder SLAP lesions. Rev Bras Ortop 2006; 41 (11/12): 461-466
  • 20 Stetson WB, Templin K. The crank test, the O'Brien test, and routine magnetic resonance imaging scans in the diagnosis of labral tears. Am J Sports Med 2002; 30 (06) 806-809
  • 21 Lafosse L, Reiland Y, Baier GP, Toussaint B, Jost B. Anterior and posterior instability of the long head of the biceps tendon in rotator cuff tears: a new classification based on arthroscopic observations. Arthroscopy 2007; 23 (01) 73-80
  • 22 Taylor SA, Khair MM, Gulotta LV. , et al. Diagnostic glenohumeral arthroscopy fails to fully evaluate the biceps-labral complex. Arthroscopy 2015; 31 (02) 215-224
  • 23 Malavolta EA, Assunção JH, Guglielmetti CL, de Souza FF, Gracitelli ME, Ferreira Neto AA. Accuracy of preoperative MRI in the diagnosis of disorders of the long head of the biceps tendon. Eur J Radiol 2015; 84 (11) 2250-2254
  • 24 Creech MJ, Yeung M, Denkers M, Simunovic N, Athwal GS, Ayeni OR. Surgical indications for long head biceps tenodesis: a systematic review. Knee Surg Sports Traumatol Arthrosc 2016; 24 (07) 2156-2166
  • 25 Streit JJ, Shishani Y, Rodgers M, Gobezie R. Tendinopathy of the long head of the biceps tendon: histopathologic analysis of the extra-articular biceps tendon and tenosynovium. Open Access J Sports Med 2015; 6: 63-70
  • 26 Redondo-Alonso L, Chamorro-Moriana G, Jiménez-Rejano JJ, López-Tarrida P, Ridao-Fernández C. Relationship between chronic pathologies of the supraspinatus tendon and the long head of the biceps tendon: systematic review. BMC Musculoskelet Disord 2014; 15: 377
  • 27 Braun S, Horan MP, Elser F, Millett PJ. Lesions of the biceps pulley. Am J Sports Med 2011; 39 (04) 790-795
  • 28 Watson ST, Robbins CB, Bedi A, Carpenter JE, Gagnier JJ, Miller BS. Comparison of outcomes 1 year after Rotator Cuff Repair with and without concomitant biceps surgery. Arthroscopy 2017; 33 (11) 1928-1936
  • 29 Checchia SL, Doneux PS, Miyazaki AN. , et al. Biceps tenodesis associated with arthroscopic repair of rotator cuff tears. J Shoulder Elbow Surg 2005; 14 (02) 138-144
  • 30 Ikemoto RY, Pileggi PE, Murachovsky J. , et al. Tenotomy with or without tenodesis of the long head of the biceps for arthroscopic repair of the rotator cuff. Rev Bras Ortop 2015; 47 (06) 736-740

Endereço para correspondência

Cassiano Diniz Carvalho
Rua Teixeira Santana 185, Fundinho, Uberlâ38400-196
Brasil   

  • Referências

  • 1 Rockwood Jr. Charles A. , Matsen 3rd, Frederick A. The shoulder. 4th ed. Philadelphia: Saunders Elsevier; 2009
  • 2 Kessel L, Watson M. The painful arc syndrome. Clinical classification as a guide to management. J Bone Joint Surg Br 1977; 59 (02) 166-172
  • 3 Itoi E, Kuechle DK, Newman SR, Morrey BF, An KN. Stabilising function of the biceps in stable and unstable shoulders. J Bone Joint Surg Br 1993; 75 (04) 546-550
  • 4 Warner JJ, McMahon PJ. The role of the long head of the biceps brachii in superior stability of the glenohumeral joint. J Bone Joint Surg Am 1995; 77 (03) 366-372
  • 5 Pagnani MJ, Deng XH, Warren RF, Torzilli PA, O'Brien SJ. Role of the long head of the biceps brachii in glenohumeral stability: a biomechanical study in cadavera. J Shoulder Elbow Surg 1996; 5 (04) 255-262
  • 6 Codman EA. The Shoulder. Boston: Thomas Todd; 1934
  • 7 DePalma AF. Surgery of the shoulder. Philadelphia: JB Lippincott; 1950
  • 8 Godinho GG, Mesquita FA, França FdeO, Freitas JM. “ROCAMBOLE-LIKE” biceps tenodesis: technique and results. Rev Bras Ortop 2015; 46 (06) 691-696
  • 9 Enad JG. Bifurcate origin of the long head of the biceps tendon. Arthroscopy 2004; 20 (10) 1081-1083
  • 10 Logal RJ. Rupture of the long tendon of the biceps brachii muscle. Clin Orthop Relat Res 1976; (121) 217-221
  • 11 Raney EB, Thankam FG, Dilisio MF, Agrawal DK. Pain and the pathogenesis of biceps tendinopathy. Am J Transl Res 2017; 9 (06) 2668-2683
  • 12 Ben Kibler W, Sciascia AD, Hester P, Dome D, Jacobs C. Clinical utility of traditional and new tests in the diagnosis of biceps tendon injuries and superior labrum anterior and posterior lesions in the shoulder. Am J Sports Med 2009; 37 (09) 1840-1847
  • 13 Mohtadi NG, Vellet AD, Clark ML. , et al. A prospective, double-blind comparison of magnetic resonance imaging and arthroscopy in the evaluation of patients presenting with shoulder pain. J Shoulder Elbow Surg 2004; 13 (03) 258-265
  • 14 Anbar A, Emad Y, Zeinhom F, Ragab Y. Shoulder arthroscopy remains superior to direct MR arthrography for diagnosis of subtle rotator interval lesions. Eur J Orthop Surg Traumatol 2015; 25 (04) 689-697
  • 15 Neviaser TJ, Neviaser RJ, Neviaser JS, Neviaser JS. The four-in-one arthroplasty for the painful arc syndrome. Clin Orthop Relat Res 1982; (163) 107-112
  • 16 Ejnisman B, Monteiro GC, Andreoli CV, de Castro Pochini A. Disorder of the long head of the biceps tendon. Br J Sports Med 2010; 44 (05) 347-354
  • 17 Bennett WF. Specificity of the Speed's test: arthroscopic technique for evaluating the biceps tendon at the level of the bicipital groove. Arthroscopy 1998; 14 (08) 789-796
  • 18 Taylor SA, Newman AM, Dawson C. , et al. The “3-Pack” Examination is critical for comprehensive evaluation of the Biceps Labrum Complex and the Bicipital Tunnel: a prospective study. Arthroscopy 2017; 33 (01) 28-38
  • 19 Godinho GG, Freitas JM, França FO, Lopes AA, Milazzo AJ, Dal Zotto C. Efficiency of the evaluation, clinical (O'Brien test) and imaging (Arthro-MRI) methods in the diagnosis of shoulder SLAP lesions. Rev Bras Ortop 2006; 41 (11/12): 461-466
  • 20 Stetson WB, Templin K. The crank test, the O'Brien test, and routine magnetic resonance imaging scans in the diagnosis of labral tears. Am J Sports Med 2002; 30 (06) 806-809
  • 21 Lafosse L, Reiland Y, Baier GP, Toussaint B, Jost B. Anterior and posterior instability of the long head of the biceps tendon in rotator cuff tears: a new classification based on arthroscopic observations. Arthroscopy 2007; 23 (01) 73-80
  • 22 Taylor SA, Khair MM, Gulotta LV. , et al. Diagnostic glenohumeral arthroscopy fails to fully evaluate the biceps-labral complex. Arthroscopy 2015; 31 (02) 215-224
  • 23 Malavolta EA, Assunção JH, Guglielmetti CL, de Souza FF, Gracitelli ME, Ferreira Neto AA. Accuracy of preoperative MRI in the diagnosis of disorders of the long head of the biceps tendon. Eur J Radiol 2015; 84 (11) 2250-2254
  • 24 Creech MJ, Yeung M, Denkers M, Simunovic N, Athwal GS, Ayeni OR. Surgical indications for long head biceps tenodesis: a systematic review. Knee Surg Sports Traumatol Arthrosc 2016; 24 (07) 2156-2166
  • 25 Streit JJ, Shishani Y, Rodgers M, Gobezie R. Tendinopathy of the long head of the biceps tendon: histopathologic analysis of the extra-articular biceps tendon and tenosynovium. Open Access J Sports Med 2015; 6: 63-70
  • 26 Redondo-Alonso L, Chamorro-Moriana G, Jiménez-Rejano JJ, López-Tarrida P, Ridao-Fernández C. Relationship between chronic pathologies of the supraspinatus tendon and the long head of the biceps tendon: systematic review. BMC Musculoskelet Disord 2014; 15: 377
  • 27 Braun S, Horan MP, Elser F, Millett PJ. Lesions of the biceps pulley. Am J Sports Med 2011; 39 (04) 790-795
  • 28 Watson ST, Robbins CB, Bedi A, Carpenter JE, Gagnier JJ, Miller BS. Comparison of outcomes 1 year after Rotator Cuff Repair with and without concomitant biceps surgery. Arthroscopy 2017; 33 (11) 1928-1936
  • 29 Checchia SL, Doneux PS, Miyazaki AN. , et al. Biceps tenodesis associated with arthroscopic repair of rotator cuff tears. J Shoulder Elbow Surg 2005; 14 (02) 138-144
  • 30 Ikemoto RY, Pileggi PE, Murachovsky J. , et al. Tenotomy with or without tenodesis of the long head of the biceps for arthroscopic repair of the rotator cuff. Rev Bras Ortop 2015; 47 (06) 736-740

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Fig. 1 Hiperemia do tendão da cabeça longa do bíceps (CLB).
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Fig. 2 Achatamento do tendão da cabeça longa do bíceps (CLB).
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Fig. 3 Lesão de alto grau do tendão da cabeça longa do bíceps (CLB) acometendo mais de 50% da espessura do tendão.
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Fig. 4 Porção proximal do tendão da cabeça longa do bíceps (CLB) acometendo mais de 50% da espessura do tendão após tenotomia.
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Fig. 1 Long head of the biceps (LHB) brachii tendon redness.
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Fig. 2 Long head of the biceps (LHB) brachii tendon flattening.
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Fig. 3 High-degree lesion at the long head of the biceps (LHB) brachii tendon, affecting over 50% of its thickness.
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Fig. 4 Proximal portion of the long head of the biceps (LHB) brachii tendon, with a lesion affecting over 50% of its thickness, after tenotomy.