Boundary Lubrication between the Tendon and the Pulley in the Finger*

UCHIYAMA, SHIGEHARU M.D.†; AMADIO, PETER C. M.D.†; ISHIKAWA, JUN-ICHI M.D.†; AN, KAI-NAN PH.D.†, ROCHESTER, MINNESOTA

Journal of Bone & Joint Surgery - American Volume:
Article
Abstract

The lubrication mechanism between the human flexor digitorum profundus tendon and the A2 pulley was investigated in vitro. The gliding resistance at the interface between the tendon and the pulley increased significantly after the tendon had been treated with a hyaluronidase solution. Alcian-blue staining of the surface of the tendon before and after it was treated with hyaluronidase suggested the presence of hyaluronate complex. Alcian blue-positive and hyaluronidase-sensitive materials, such as hyaluronate or proteoglycan, in the synovial membrane and the matrix of the tendon, may act as a boundary lubricant, facilitating the gliding and reducing the resistance between the tendon and the pulley. CLINICAL RELEVANCE: The use of intrasynovial tendon donor grafts, which appear to possess a boundary lubricant on their surface, may result in improved gliding of the tendon postoperatively, compared with more traditional grafts, such as the palmaris longus tendon, taken from extrasynovial sources.

Author Information

†Orthopedic Biomechanics Laboratory, Mayo Clinic and Mayo Foundation, 200 First Street, S.W., Rochester, Minnesota 55905. Please address requests for reprints to Dr. Amadio.

Article Outline

Frictional resistance occurs when the flexor tendon glides through its pulleys in the finger. A high level of friction can impede gliding of the tendon and may interfere with the results of repair of the flexor tendon4 or tendon-grafting22. Frictional resistance may limit motion after chronic or repetitive use, as in stenosing tenosynovitis. In order to minimize resistance and to prevent wearing of the surfaces of the tendon and the pulley, a lubrication mechanism must be present, as seen in diarthrodial joints12. The existence of a lubrication mechanism between the flexor tendon and the pulley was suggested by our finding that the resistance between the flexor profundus tendon and the A2 pulley was decreased and less sensitive to increasing load compared with the resistance between the palmaris longus tendon and the A2 pulley22. Some hypotheses about the lubrication between the tendon and the pulley have been reported2,21. In those studies, proteoglycan, fibronectin, and lipids were extracted from the synovial membrane of flexor tendons in chickens. Other studies have confirmed that intrasynovial tendon grafts have fewer adhesions and better motion than extrasynovial tendon grafts5,6,18. These observations have been related to a differential ability to synthesize proteoglycan and other matrix components1. However, the precise lubrication mechanisms at the tendon-pulley interface have yet to be studied. We investigated the hypothesis that a hyaluronate complex on or in the human flexor digitorum profundus tendon facilitates gliding and reduces the resistance between the tendon and the A2 pulley in vitro.

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Materials and Methods

The concept of measurement of friction and its application to the tendon-pulley unit have been verified and validated, as reported previously22,23.

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Biomechanical Testing

Thirty fresh-frozen index, ring, and long digits from thirty cadavera were used. Each specimen was dissected so as to leave only the A2 pulley with its osseous insertion and the flexor digitorum profundus tendon23. The tissues were thawed at room temperature immediately before testing. The specimen was mounted on a testing device, with the volar side up and the proximal side toward the actuator of the device22. With the arc of contact fixed at 50 degrees, the tendon was moved toward the actuator (flexion) with a velocity of 2.0 millimeters per second for a predetermined excursion, while load (tension of the tendon distal [F1] and proximal [F2] to the A2 pulley) and excursion were recorded at a sampling rate of ten hertz. This trial was repeated three times each for F1 loads of 0.98, 2.45, 4.9, 9.8, and 14.7 newtons. The specimens were randomly divided into three groups of ten each.

Four treatment protocols were used: (1) no treatment, (2) a wash with saline solution, (3) a soak in hyaluronidase solution (forty-four units per milliliter; source, bovine testes; 800 units per milligram dissolved in normal saline solution; ICN Biomedicals, Aurora, Ohio) at room temperature, and (4) a soak in saline solution at room temperature for two hours. Testing was carried out after each treatment protocol. The order of treatment varied among the three groups. The specimens in group 1 were tested before any treatment, after they had been washed with saline solution, and after they had been soaked in the hyaluronidase solution. The specimens in group 2 were tested before any treatment, after they had been soaked in the hyaluronidase solution, and after they had been washed with saline solution. The specimens in group 3 were tested twice before any treatment and tested after they had been soaked for two hours in saline solution.

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Analysis of Data

The average difference between the F2 and F1 loads for the whole excursion was considered to be the gliding resistance between the tendon and the pulley for that trial. The first trial was considered preconditioning14. The average of the second and third trials at each load were used for analysis. For the specimens in group 3, the gliding resistance measured before treatment was compared with that measured after the tendon had been subjected to a two-hour soak in saline solution to determine if this had an effect on the gliding resistance. A paired t test was used for the comparison, with a Bonferroni correction of p < 0.01 (0.05/5) to maintain the over-all protection level.

With use of ten independent t tests (five loads for two groups), the difference between the gliding resistance after the first treatment (that is, no treatment) and that after the second treatment for groups 1 and 2 (a wash with saline solution and a soak in the hyaluronidase solution, respectively) was compared with the difference between the gliding resistance after the first treatment (that is, no treatment) and that after the second treatment (also no treatment) for group 3. The difference between the gliding resistance after the second treatment and that after the third treatment for groups 1 and 2 (a soak in the hyaluronidase solution and a wash with saline solution after a soak in the hyaluronidase, respectively) was also compared with the difference between the gliding resistance after the second treatment and that after the third treatment (a soak in saline solution) for group 3. Bonferroni corrections of p < 0.005 (0.05/10) were used to maintain the over-all protection level.

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Staining with Alcian Blue

Ten flexor digitorum profundus tendons and five palmaris longus tendons were dissected from the fingers of five cadavera. The flexor digitorum profundus tendons were washed in saline solution, after which five were soaked in the hyaluronidase solution and five were not. All ten were stained with alcian blue (1 per cent solution in 1 per cent acetic acid) for twenty minutes at room temperature, as were the five palmaris longus tendons, which had been washed with saline solution but not soaked in the hyaluronidase solution.

Alcian blue stain is a reagent commonly used for the detection of proteoglycan, including hyaluronate3,8,10,14,26. The staining intensity of the surface of the tendon was evaluated visually and was considered simply to be more than, less than, or roughly similar to that of the other specimens. A greater staining intensity was considered indicative of a greater quantity of proteoglycan. The grading was based on the assessment of the investigators. No specific blinded testing was done to determine the reliability and the repeatability of the grading method.

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Scanning Electron Microscopy

Five flexor digitorum profundus tendons from five cadavera were studied with scanning electron microscopy. Each tendon was cut axially into radial and ulnar parts. One part of each tendon was treated with the hyaluronidase solution and the other was not so treated. Specimens from the surface of each tendon were observed with scanning electron microscopy to determine if there was obvious damage to the collagen-fiber structure after the treatment with hyaluronidase. Broken or irregular fibers were considered abnormal, and the fibers in a specimen were graded simply as more irregular than, less irregular than, or roughly similar to those in the other specimens. The grading was based on the assessment of the investigators. No specific blinded testing was done to determine the reliability and the repeatability of the grading method.

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Results

The curve pattern of the F1 and F2 loads after the tendons had been either washed with saline solution or soaked in the hyaluronidase solution was unchanged from the normal pattern (before treatment), but the curves of the F2 load were shifted upward (indicating increased force), parallel to the normal curve, for the tendons that had been treated with hyaluronidase (Figs. 1-A, 1-B, and 1-C). Regardless of the order of the treatment protocols, only the tendons that had been soaked in the hyaluronidase solution had a significant increase in the gliding resistance (Figs. 2-A and 2-B).

The surfaces of the flexor digitorum profundus tendons that had not been soaked in the hyaluronidase solution were strongly stained by alcian blue, whereas the surfaces of the palmaris longus tendons were unstained or minimally stained. The intensity of staining was decreased on the surfaces of the flexor digitorum profundus tendons that had been soaked in the hyaluronidase solution (Fig. 3).

On scanning electron microscopy of the tendons that had not been soaked in the hyaluronidase solution, the synovial membrane was intact at some locations and worn away at others, where subintima collagen fibers could be seen. There was no obvious damage to the collagen-fiber arrangement on the surfaces of the tendons that had been treated with hyaluronidase (Figs. 4-A and 4-B.

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Discussion

Because we found no difference in the gliding resistance after the tendons had been soaked in saline solution for two hours but had not been treated with hyaluronidase (group 3), we believe that our findings are the result of changes in a hyaluronidase-sensitive substance on the surface of the tendon and not to autolysis. As washing of the tendon in saline solution did not remove this substance, we believe that the substance is probably bound to the surface.

There may be hyaluronate and other alcian blue-positive, hyaluronidase-sensitive materials on the surface of the flexor digitorum profundus tendon either in a complex with fibronectin or as a part of the proteoglycan of the synovial membrane or the surface of the tendon2,19,21. Proteoglycan may also be present between collagen-fiber bundles on the volar part of the tendon, as a result of adaptive differentiation of the fibrocytes into cartilaginous cells in response to repetitive compression11,13,24. These substances may play a role in the surface lubrication of the tendon-pulley interaction. At lower loads, there was no significant increase in the gliding resistance of tendons that had been treated with hyaluronidase; this may have been because a fluid film of saline solution acted as a lubricant between the tendon and the pulley. As the load increased, an increase in the gliding resistance became evident. The higher loads that we used were similar to those that have been noted in tendons moving actively without resistance17. Thus, we believe that these loads may be more representative of the in vivo conditions than the lower loads were. We hypothesize that the fluid film may have been squeezed out of the tendon-pulley interface under high loads, after which direct contact became the dominant interaction. Under these conditions, any potential lubricant bound to the surface of the tendon, such as hyaluronate or proteoglycan, may act to reduce the frictional resistance as a boundary lubricant. We believe that our findings support the hypothesis that treatment with hyaluronidase removed these surface lubricants and therefore increased the gliding resistance.

The gliding resistance at the tendon-pulley interface may depend on the surface conditions18, macroscopic shape2, or compression properties of the tendon and the pulley. This is evidenced by the shapes of the curves for the F2 loads (Fig. 1-A, 1-B and 1-C); a peak of resistance was associated with a change in the cross-sectional profile of the flexor digitorum profundus tendon as it moved beneath the A2 pulley23. Because the force pattern as a function of excursion of the tendon did not change even after treatment with hyaluronidase, we believe that a change in the surface conditions was responsible for the increase in gliding resistance that we observed. If the compression properties or the shape of the tendon had changed substantially, we would have expected a change not only in the magnitude of force but also in the pattern of force.

Several limitations of this study should be mentioned. The tendons were washed with saline solution to remove synovial fluid from their surface so that the hyaluronidase could react only to any hyaluronate that was chemically combined or included on the surface. However, it was unclear how much synovial fluid was present before and after the tendons were washed. We believe that most of the synovial fluid was washed away by this procedure20. Although there was a tendency for the gliding resistance to increase after the tendons had been washed, no significant difference was detected. This suggests that the synovial fluid may have a coating effect, which may have partially blocked the action of hyaluronidase on the tendons that were not washed before they were treated with this enzyme. Although washing with saline solution did not increase the gliding resistance significantly in our study, given the wide standard deviations many more specimens would need to be examined to test the hypothesis that washing causes a significant difference in the measured resistance. Our sample size of ten in each group was sufficient to provide roughly an 80 per cent chance of detecting a difference of one standard deviation. With standard deviations of 100 per cent of the mean and more, our sample size does not have the statistical power to test for the presence of a difference in the range of 50 per cent or less. Approximately forty specimens would be needed to produce an 80 per cent chance of detecting a difference of this size (that is, one-half of the standard deviation).

We do not know exactly what the hyaluronidase dissolved in the tendon, or the quantity that it dissolved, as the implications of hyaluronidase digestion are unclear and the specificity of the hyaluronidase preparation can be questioned. This may explain the relatively large standard deviations in the gliding resistance of the tendons that had been treated with hyaluronidase. Of course, we cannot rule out completely the possibility that the collagen-fiber structure on the surface of the tendon was damaged by treatment with hyaluronidase and that this contributed to the increase in the gliding resistance that we observed. However, we believe that such an effect would have been negligible because no obvious damage was seen with scanning electron microscopy, and treatment with hyaluronidase is not thought to affect the biomechanical properties of the collagen network substantially16.

Finally, there are other potential lubricants in the synovial fluid or the synovial membrane as well as lubrication mechanisms other than boundary lubrication. This study did not rule out the possibility that other lubrication mechanisms were involved in the reduction of the resistance between the tendon and the pulley.

The superior gliding ability of intrasynovial tendons, such as the flexor digitorum profundus, compared with that of extrasynovial tendons, has been the subject of much recent research. Intrasynovial tendon grafts have been shown to have less early necrosis, better intrinsic healing, fewer adhesions, and better gliding ability1,5,6,18 than extrasynovial grafts. Tenocyte metabolism appears to differ between intrasynovial and extrasynovial tendons1. In this study, we explored another possible difference, surface lubrication. Our observations suggest that, in addition to the potential factors previously elucidated, there also is a difference in surface lubrication. We, as well as others1,5,6,18, believe that intrasynovial tendon grafts have better gliding abilities than extrasynovial tendon grafts; we believe that one contributing factor is a difference in surface lubrication.

*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding sources were the Mayo Foundation and National Institutes of Health Grant AR17172.

Investigation performed at the Orthopedic Biomechanics Laboratory, Mayo Clinic and Mayo Foundation, Rochester

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