ELSEVlER
Journal of Orthopaedic Research Journal of Orthopaedic Research 21 (2003) 162-166
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Gliding properties of the long head of the biceps brachii G. Heers, S.W. O'Driscoll, A.M. Halder, C. Zhao, N. Mura, L.J. Berglund, M.E. Zobitz, K.-N. An * Biomechanics Luborutory, Diuision of Orthopedic Reseurch, Muyo Clinic Rochester, 200 First Street, Southwest, Rochester, M N 55905, USA
Abstract To elucidate the role of mechanical forces that resist motion of the long head of the biceps brachii, the gliding resistance of the tendon during abduction and adduction was measured. Nine human cadaveric glenohumeral joints were obtained (mean age 68 years, range 47-84). A testing device was developed to simulate glenohumeral abduction and adduction motion. Gliding resistance was calculated as the force differential on the proximal and distal ends of the biceps brachii at five glenohumeral angles (15", 30°, 45", 60" and 75"). The average gliding resistance in abduction at 15", 30", 45", 60" and 75" for a 4.9 N load was 0.41, 0.40, 0.36, 0.32 and 0.28 N, respectively. At these same angles, but during adduction motion, the force on the proximal tendon end was either identical or less than the distal tendon end (p > 0.46) indicating a lack of resistance and even a phenomena of "negative" resistance in which some other force overcame the friction. The difference in gliding resistance between abduction and adduction was significant 0, < 0.05). The results indicate that forces opposing biceps tendon gliding are more complicated than sinlply due to friction. Tendon deformation inside the bicipital groove produces a direction-dependent effect due to a mechanism of elastic recoil. Understanding forces that are absorbed by the tendon during active motion may provide insight into pathological changes that develop inside and around the tendon. 0 2002 Orthopaedic Research Society. Published by Elsevier Science Ltd. All rights reserved. Kevnvords: Biceps tendon; Friction; Mechanical forces; Bicipital groove
Introduction Rupture of the long head of the biceps brachii is one of the most common tendon ruptures in the human body [ 5 ] . These tendon ruptures are thought to occur on the basis of preceding degenerative lesions [2,12]. Some authors believe that the pathology seen in the biceps is directly related to its close relationship with the rotator cuff [7,8]. As they both pass under the coracoacromial arch, both the cuff and tendon can be involved in the impingement syndrome. However, pathology of the long head of the biceps tendon is also observed without associated cuff lesions [16]. Similar to the wrist tendons, the biceps tendon passes through a fibro-osseus tunnel, which instigates mechanical forces that oppose tendon gliding. The gliding resistance within the bicipital groove
may play a role in the development of these secondary changes in the tendon [10,12]. Although the morphology and mechanical properties of the biceps tendon [3,6] and the bicipital groove [I] have been described, there is no report describing the forces resisting motion of the long head of the biceps brachii in the intertubercular groove during glenohumeral motion. Characterizing the fundamental gliding properties is necessary in order to differentiate changes that develop with pathological alterations to the long head of the biceps brachii. The purpose of this study was to determine the forces that resist motion of the biceps tendon in the bicipital groove during abduction and adduction motions of the glenohumeral joint.
Materials and methods *Corresponding author. Tel.: + 1-507-5381717/2842262; fax: + 1507-284-5392. E-mud riddress:
[email protected] (K.-N. An).
Previous reports from our laboratory have described a method for calculating resistance of human finger tendons gliding through the finger pulley [14,15]. In contrast to this analog of a moving cable on a fixed mechanical pulley, the long head of the biceps tendon passively
0736-0266/03/$ - see front matter 0 2002 Orthopaedic Research Society. Published by Elsevier Science Ltd. All rights reserved PIT: SO7 3 6 - 0 2 6 6 ( 02)OO 1 0 3 - 1
G Heers c't a1 I Journal of Orthopaedic Research 21 (2003j I 6 2 I66 slides on the rotating humeral head [4]. Therefore, it was necessary to develop a method of rotating the humeral head, while permitting the biceps tendon to passively slide on the humeral head and through the bicipital groove. Specimen preparation For the measurements of gliding resistance between the biceps tendon and the humeral head nine shoulders from nine fresh frozen cadaver shoulders with no radiological evidence of glenohumeral osteoarthritis were obtained (mean age 68 years, range 47-84). Neither the tendon nor the rotator cuff had any macroscopic signs of degeneration. An X-ray of the bicipital groove was taken by supporting the humerus in a ringstand and directing the central beam parallel to the coronal axis of the humerus and angled 15" [l]. Specimens containing bony spurs within the groove were excluded from the study. All soft tissues were removed, except for the biceps tendon-muscle complex. The biceps tendon was cut near its myotendinous junction. The location of the tendon on the humeral head and at the entrance to the bicipital groove was marked with waterproof ink. The glenoid was detached from the scapula and cemented into an aluminum fixture (Fig. I). The distal humerus was removed and a fiberglass rod was cemented in the medullary canal. During dissection the specimen was moistened with physiologic saline solution to prevent dehydration. Testing upparatus The prepared specimen was mounted on the testing device (Fig. I). A fiberglass rod in the medullary canal was connected to a drive mechanism, which could abduct and adduct the humerus. A load transducer was connected to each end of the biceps tendon. The distal load transducer was connected by a cable to a 4.9 N weight aligned with the physiological line of action. The proximal end of the biceps tendon was cut from the glenoid and sutured to a second load transducer. The superior tip of the glenoid was removed and the proximal load transducer was fixed relative to the mounted glenoid to allow the proximal tendon to follow a physiological course.
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corresponds to an average arm abduction of 150" [I I]. Following abduction motion, the direction was reversed and the humerus was adducted. Testing was done with the tendon running over the apex of the humeral head, which corresponds to external rotation [13]. A loading condition of 4.9 N on the biceps tendon was chosen based on EMG data, which suggest a light muscle activity during external rotation [I71 and based on an estimated force generation of 55 N [9] by the biceps muscle. The analog outputs of the two load cells were sampled at a rate of 30 Hz. The accuracy and reliability of the two load transducers has already been reported [15]. T o determine repeatability of the measurements each trial was repeated three times. To prevent the tendon from drying out continuous saline irrigation was provided by an infusion set at a rate of 30 drips per minute. Additional testing After testing the cadaver specimens, the data suggested an unanticipated directional dependence of the gliding resistance. Three additional tests were then performed to determine if the shape of the bicipital groove or the viscoelastic properties of the tendon affected the gliding resistance.
1. We removed the humerus and replaced it with a smooth plastic cylinder to provide a uniform surface for the tendon to glide over, without the lateral constraints of the bicipital groove. For this test the tendon would not twist as it does in the groove. 2. The humerus was removed and replaced with a smooth plastic cylinder and the tendon was replaced with a plastic coated string. This configuration demonstrated the ideal frictional interaction between a belt and pulley and the simplified representation of the tendonhumeral head interaction. 3. Using a cadaver humerus, the biceps tendon was replaced with a plastic coated string. The string would not compress as the bicipital groove narrowed nor is there a tendency for it to rotate. Therefore, it represents a pure gliding through the bicipital groove. Data analysis
Testing protocol The humerus was moved on a metal track up to 90" (abduction) from a starting position corresponding to hanging arm position. The rate of motion was prescribed at 6" per second by the computer-controlled drive mechanism. The term "abduction" in the current study is used to describe elevation of the humerus, and the abduction angle refers to glenohumeral motion only. A glenohumeral motion of 90"
The difference in measured force between the distal and proximal load transducers is the gliding resistance [14,15]. Therefore, in abduction direction the gliding resistance would be calculated as distal tendon force minus proximal tendon force. For adduction, the gliding resistance would be proximal tendon force minus distal tendon force. The difference between the proximal and distal force measurements and the gliding resistance between abduction and adduction at five
Fig. 1. Experimental set-up. The humerus is attached to a computer-controlled drive mechanism, which moves on a metal track up to 90". The outputs of the load transducers at the proximal and distal ends of the tendon are recorded during motion.
G Heers et al I Jouinal of Orthopueu'rc Rewarrh 21 (2003) 162-166
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different glenohumeral angles ( 1 S", 30", 45", 60", and 75") were compared statistically using a paired t-test. Over thc different glenohurnera1 angles the gliding resistance for abduction and adduction were compared separately using analysis of variance. A statistical significance of x = 0.05 was used. The data at the starting position (0") and the final position (90" of abduction) were excluded, as they would also include the transition between static and dynamic resistance.
Results In all nine specimens there was a force differential between the proximal and distal tendon ends. The intraspecimen variability was low with an average standard deviation among the three trials of 0.02 N . During abduction, that is the proximal part of the tendon is moving into the bicipital groove, the mean gliding resistance gradually decreased from 0.40 N at 15" abduction to 0.39 N at 30", 0.35 N at 45", 0.31 N at 60", and 0.27 N at 75" (Fig. 2). The gliding resistance during abduction was not significantly different at the different angles (p = 0.24). In the adduction direction, that is the proximal part of the tendon is moving out of the groove into its original position, a "negative" gliding resistance, or force in the direction of gliding was calculated in all of the specimens for many of the glenohumeral positions. Although the relative gliding motion was reversed, at all adduction angles the force on the proximal tendon end was either identical or less than the distal tendon ends (p > 0.46). The mean gliding resistances were 0.01 N, -0.07 N, -0.1 1 N, -0.12 N , and -0.05 N at 75", 60", 45", 30", and I 5", respectively. There was no significant difference in gliding resistance among the different arm positions (p = 0.17). Comparing gliding resistance between abduction and adduction showed a significantly higher gliding resistance at all arm positions in the abduction direction (p < 0.001) (Table 1). 5.2,
5.01
T
I
t
Table 1 Results of gliding resistance Angle
Abduction
Adduction
p-value
15 30 45 60 75
0.40 (0.1 1 ) 0.39 (0.14) 0.35 (0.15) 0.31 (0.14) 0.27 (0.16)
-0.05 -0.12 -0.11 -0.07 0.01
p < 0.05 p < 0.05 p < 0.05 p < 0.05 p < 0.05
(0.12) (0.10) (0.08) (0.1 1) (0.15)
Values expressed in Newtons as mean (standard dekiation). Statistical comparison indicates abduction versus adduction.
6.5
+Trial 1
+- Trial 2 -A-
Trial 3
Distal Force Transducer
5.5
5 0
._.__..--._..___..
2
~
Y
Abduction
4.5
3.5 4 0
15
30
45
60
75
Glenohumeral Angle (degrees)
Fig. 3. Force at proximal tendon end for simulations of tendonhumeral head interaction. Trial 1 : humeral head replacement, no biologic groove, biological tendon; trial 2: humeral head replacement, no biologic groove, biceps tendon replacement: trial 3: biologic head. biologic groove, tendon replacement. Since the distal tendon force transducer recorded the 4.9 N attached weight in both abduction and adduction, it is shown as a single dotted line.
The results of the additional tests (Fig. 3) differed from the cadaver tests. Although the gliding resistance was not identical among the three trials performed due to the different materials used in each test, the proximal load transducer read a lower force than did the distal load transducer in abduction. In the reverse direction (adduction) the proximal load transducer read a higher force than the distal load transducer.
Proximal Force (Abduclion)
Discussion 4.4
4.2
,
0
15 30 45 60 75 Glenohumeral Angle (degrees)
7
90
Fig. 2. Force at proximal tendon end at five glenohumeral angles. Since the distal tendon transducer recorded the 4.9 N attached weight in both abduction and adduction, it is shown as a single dotted line. In abduction motion the proximal force was always less then the distal force. In adduction motion the distal force is greater or similar to the proximal force.
Our hypothesis was that the normal biceps tendon moving through the bicipital groove in a lubricated environment should only be resisted by frictional forces between the tendon and the bone. In terms of our experiment we expected that during abduction, the distal end of the tendon would measure a greater force than the proximal due to friction resisting the relative tendon motion. With adduction, the motion would be resisted in the opposite direction and the proximal tendon would
G. Heers et al. I Journal of Orthopaedic Research 21 (2003) 162-166
measure greater loading. However, we only observed the anticipated outcome during abduction. During passive adduction the distal tendon maintained a higher or equal force than the proximal tendon end. Thus, the sum of the forces acting in adduction was working in the same direction as the tendon motion, which contradicts what is expected of a purely frictional force. These findings might be explained by the interaction between the geometry of the tendon and the bicipital groove. A consistent difference in shape was noted between the proximal and middle portions of the tendon [6]. The tendon is flatter as it progresses over the humeral head and more triangular in the bicipital groove. In abduction, the flat proximal part of the tendon enters the bicipital groove, which is hourglass shaped [3], whereas the triangular middle part of the tendon moves distally. With abduction motion the tendon deforms in order to follow the shape of the groove. Meanwhile, in adduction the proximal portion of the tendon regains its original shape as it exits the groove. We believe that this elastic recoil of the tendon accounts for additional force on the tendon during gliding. During tendon gliding into the groove, the resistance to deformation acts in the same way as the frictional forces, thus increasing the overall gliding resistance while during adduction the elastic recoil and gliding friction work in opposite directions. The directional-dependent resistance to gliding was confirmed by replacing the tendon with a plastic coated string that had a much higher stiffness and more consistent geometry than the tendon, and therefore would not exhibit the elastic recoil effect. The gliding resistance of the plastic cord followed expected trends, with friction opposing the direction of gliding. In addition, we replaced the humeral head with a cylinder to eliminate the geometry effect of the bicipital groove. Once again the results demonstrated that friction opposed the direction of gliding. Therefore, we confirmed that during tendon gliding, friction between surfaces and energy storage during tendon deformation affects the gliding resistance. Since this is an in vitro study, we are unable to exactly replicate the in vivo environment in which the biceps tendon is surrounded by synovial fluid. We took care to prevent tendon dehydration by providing a continuous saline irrigation of the tendon during the testing process. Although joint fluid might have reduced the frictional component observed with tendon motion, it is likely that the relative relationship between the elastic forces and the frictional forces would remain. Another limitation to the study is that we tested only one rate of tendon gliding (6" per second of abduction/ adduction) and only one position of humeral rotation. A higher rate of tendon gliding would occur during rapid glenohumeral motion, such as baseball pitching. Our rate of motion, however, was sufficient to examine the
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tendon during continuous motion, as we did not observe any evidence of irregular stick-slip phenomena. The selection of only one position of humeral rotation was made to provide a simple model for understanding the gliding mechanism of the biceps tendon. In external rotation the course of the tendon is straight over the apex of the humeral head [13] and the excursion of the tendon into the bicipital groove is greatest. For internal rotation the resistance might be increased. Applying lower and higher loading to the tendon (1, 2, 10 and 15 N, data not shown) revealed a linear relationship between loading and resistance and the phenomenon described in this study was consistent. This study demonstrated that the gliding resistance between the biceps tendon and bicipital groove was more complicated that expected. A directional-dependent resistance to gliding motion of the biceps tendon was observed that is likely due to a combination of surface friction and elastic deformation and recoil. Although these forces are small compared with normal tensile demands placed on the tendon, they may not necessarily be insignificant over repeated cycles, especially when tendon pathology is present. Future studies looking at the development of pathological changes inside and around the tendon should recognize that the biceps tendon undergoes this cyclical deformation and account for the intrafibrous strains that will be imposed.
Acknowledgement
This study was supported by the Mayo Foundation.
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