Samuel A. Taylor, MD

Take-Home Points

• Cellular healing response differs between bony and soft tissue biceps tenodesis.
• Bony tenodesis incites an inflammatory healing response.
• Bony tenodesis healing occurs at the tendon-bone interface.
• Intrasseous bony fixation leads to tendon degeneration within the bone.
• Tendon-to-tendon tenodesis may result in regenerative tendon healing.

The long head of the biceps tendon (LHBT) is a well-established pain generator of the anterior shoulder^1,2 and may be surgically addressed in refractory cases.³ According to a recent study of 44,932 cases, biceps tenodesis rates increased 80% over just 3 years (2008-2011).⁴ Nevertheless, optimal tenodesis location and technique remain controversial. Proximal and distal tenodesis, including numerous soft-tissue and bony techniques, have been described.^5-7 Several studies have focused on the biomechanical strength of various fixation modalities.^8-14 These data highlight the ongoing evolution of our understanding of biceps-labrum complex (BLC) disease.

Over the years, tenodesis location has proved to be an important factor in outcomes.^3,15-20 Several recent studies have elucidated the role of the extra-articular LHBT and the limited capabilities of diagnostic arthroscopy.^15-17,20,21 Taylor and colleagues¹⁷ defined the bicipital tunnel as the extra-articular segment of LHBT and its fibro-osseous enclosure. The tunnel extends from the articular margin through the subpectoral region and can be divided into 3 zones: Zone 1 goes from the articular margin to the inferior margin of the subscapularis, zone 2 goes from the inferior margin of the subscapularis to the proximal margin of the pectoralis major tendon, and zone 3 is the subpectoral region. Zone 2 is often referred to as “no man’s land” for its relative invisibility from arthroscopy above and open exposure below.^17,21 Notably, a recent study reported a 47% prevalence of hidden tunnel lesions in patients with chronic BLC disease symptoms.¹⁸ Other studies have shown that standard proximal tenodesis methods often fail to address LHBT pathology in this area, leading to residual symptoms.^9,22 It is evident that tenodesis location and technique play important roles in patient outcomes. Sanders and colleagues¹⁶ found that the revision rate was significantly higher among patients who underwent biceps tenodesis without release of the bicipital tunnel sheath than among patients who underwent tenodesis with the release. Dr. O’Brien developed an alternative option: soft-tissue tenodesis with transfer of the LHBT to the conjoint tendon within the subdeltoid space.^23,24 This technique addresses intra-articular and extra-articular tunnel disease while mitigating the complications associated with bony tenodesis. Early and midterm studies have shown this to be an effective intervention for chronically symptomatic BLC disease.^25,26

Despite the abundance of literature on tenodesis techniques, no one has histologically evaluated the location-dependent healing and inflammatory responses. We conducted a study to determine the impact of tenodesis location on healing and inflammation in a rat model. We hypothesized that, compared with tendon-to-bone techniques, soft-tissue tenodesis would minimize inflammatory response and optimize healing.

Methods 

The study was approved by the Institutional Animal Care and Use Committee at the Hospital for Special Surgery. 

Animals

Biceps tenodesis was performed at 1 of 3 locations in 36 thirteen-week-old Sprague-Dawley rats (Charles River Laboratories). All rats were prepared for surgery by an experienced veterinary technician. Sedation was induced with isoflurane gas through a nose cone. 

Surgical Procedure

Animals were randomly assigned to 3 different tenodesis groups: tendon-to-bone in the bicipital groove (metaphyseal, M); tendon-to-bone in the subpectoral region (diaphyseal, D); and soft tissue-to-soft tissue transfer to the conjoint tendon (T). A standard deltopectoral approach was used to expose the biceps tendon. The tendon was tagged with a 5-0 polypropylene suture and tenotomized at the level of the bicipital groove (zone 1). All wounds were irrigated and closed with 4-0 nylon suture.

For animals undergoing tendon-to-bone metaphyseal tenodesis, a 0.045-mm Kirschner wire was used to drill bicortically into the intertubercular sulcus. Wire positioning distal to the physeal plate was confirmed with fluoroscopy. A locking stitch of 5-0 polypropylene suture was run along the free edge of the tendon. The tendon was then passed through the bone tunnel in an anterior-to-posterior direction, and the limbs of the suture were tied around the lateral cortex. 

The process was repeated for animals undergoing diaphyseal tenodesis; only the tenodesis location was different. The inferior border of the pectoralis major was identified, and a bicortical tunnel was made in the center of the diaphyseal bone. The tendon was then prepared and tenodesed to bone using the method already described.

In soft-tissue tenodesis, the conjoint tendon was identified and carefully dissected from surrounding tissues. The LHBT was then tenodesed to the attached conjoint tendon with interrupted simple stitches of 5-0 polypropylene suture.

The animals were allowed to bear weight on the operative limb immediately after surgery and without immobilization.

Specimen Harvest and Preparation

Four animals from each group were sacrificed at 6, 12, and 24 weeks. Harvested specimens were fixed in 10% neutral-buffered formalin solution. Bony specimens consisted of the upper half of the humerus and the tenodesed biceps tendon, and soft-tissue specimens consisted of the tenodesed LHBT-conjoint tendon complex. Bony specimens were decalcified in 10% ethylenediaminetetraacetic acid. All specimens were paraffin-embedded and sectioned at 7 microns.

Analysis of Cellularity

Sections were stained with hematoxylin-eosin. Overall cellularity at the tenodesis interface was quantified by averaging the nuclei count within 3 separate standardized ×20 magnification high power fields. Only nucleated cells were included in the cell count. Immunohistochemical staining with tenomodulin (Santa Cruz Laboratories, sc-49324) was performed to characterize the cell population at the interface. Deparaffinized sections underwent antigen retrieval with pronase for 30 minutes at 37°C and were incubated overnight with the anti-tenomodulin goat monoclonal antibody diluted to 1:200 in 1% phosphate-buffered saline. The prepared slides were then counterstained with methyl green. Specimens treated with tenomodulin were evaluated for presence or absence of a positive reaction at the tenodesis interface. 

Analysis of Inflammation

Inflammation at the interface was evaluated with the CD68 macrophage marker (ABcam, ab31630). Deparaffinized sections underwent antigen retrieval with pronase for 30 minutes at 37°C and were incubated overnight with anti-CD68 mouse monoclonal antibodies diluted to 1:200 in 1% phosphate-buffered saline. The prepared slides were then counterstained with neutral red. Inflammation was quantified by averaging the number of reactive cells within 3 separate standardized ×20 magnification high power fields.

Statistical Analysis

Descriptive statistics were calculated for cell and macrophage counts for each group at every time point. Two-way analysis of variance was used to compare the cell and macrophage counts between groups at each time point as well as the count differences within each group between time points. P values were Bonferroni-corrected to account for the multiple comparisons between groups. P < .05 was used to signify statistical significance.

Results

All 36 animals survived to their designated harvest time without complications. Twelve specimens were successfully harvested at 6 weeks and another 12 at 24 weeks. At 12 weeks, tenodesis failure occurred in 1 animal in group D, leaving 11 specimens for analysis.

Cellularity

At the 6-week harvest, 1 group T specimen was sectioned incorrectly and discarded, leaving 3 specimens for evaluation. Descriptive statistics for each group and each time point are listed in Table 1A. There were no significant differences in mean cellularity between the bony tenodesis groups at any time point (P = 1.000) (Table 1B).

At 6 weeks, both group M (P = .012) and group D (P = .021) showed significantly more cellularity than group T (Figure 1). The same was true for group M (P = .002) and group D (P = .001) at the 12-week harvest. There were no significant differences in cellularity between the 3 groups at 24 weeks. 

Within-group analysis revealed a trend of increasing cellularity at 12 weeks followed by a decrease at 24 weeks in all 3 groups (Table 2).

Group M showed a significant overall decrease in cellularity from 6 to 24 weeks (P = .035) and from 12 to 24 weeks (P = .004). The overall decrease in cell count from 6 to 24 weeks was not significant in group D (P = .124), whereas the decrease from 12 to 24 weeks was significant (P = .005). There were no significant differences in cellularity for group T between any of the time points.

Inflammatory Response 

During specimen processing, 1 group D specimen was severely degraded after pronase treatment, leaving 3 specimens for evaluation. Descriptive statistics for each group are listed in Table 3A.

At 6 weeks, mean CD68 cell count was significantly higher in group M than in group D (P = .011) and group T (P < .001) (Table 3B). Likewise, CD68 count was significantly higher in group D than in group T (P < .001). There were no differences in CD68 counts between the 2 bony tenodesis groups at 12 weeks (P = .486) or 24 weeks (P = .315). Both bony tenodesis groups, however, had persistently higher CD68 counts at 12 weeks when compared with group T (group M, P = .002; group D, P < .001). In these specimens, an inflammatory milieu characterized by a large accumulation of lymphocytes and giant cells was noted at the bone-tendon interface.

In comparison, inflammatory cells were scant at the tendon-tendon interface in group T specimens (Figure 2). There were no differences in CD68 reaction between the 3 tenodesis groups at 24 weeks. In all cases of tendon-to-bone tenodesis, no recognizable formed tendon was seen within the bone tunnel. Rather, all tendon-to-bone tenodeses were characterized by dense connective tissue at the bone surface, surrounded by an accumulation of macrophages.

Within-group analysis revealed a significant decrease in CD68 cells from 6 to 12 weeks and overall from 6 to 24 weeks in group M (Table 4). There was no significant change in CD68 cell counts between any time points within group D (P = 1.000) and between 6 and 12 weeks in group T (P = 1.000). Interestingly, the CD68 counts in group T showed an overall increase from 6 to 24 weeks (P = .019). The increase was even more significant from 12 to 24 weeks (P = .004).

Tissue-Specific Staining

At 6 weeks, antigen retrieval resulted in severe degradation of 2 group M specimens, 2 group D specimens, and 1 group T specimen. The most notable tenomodulin reaction occurred in group T at the 6- and 12-week harvests, with the 6-week group having the most robust reaction. There was scant reaction in this group at 24 weeks.

One group D specimen showed a positive reaction at 24 weeks. No reaction occurred in the remaining bony specimens across all time points (Figure 3).

Discussion

In this study, the healing response differed between bony and soft-tissue tenodesis techniques in a rat model. Tendon-to-bone tenodesis, both diaphyseal and metaphyseal, appeared to incite an inflammatory degenerative response, whereas tendon-to-tendon healing occurred in a more quiescent and perhaps even regenerative manner.

The early inflammatory response that occurred in the bony tenodesis groups is not unlike what occurs in fracture healing.²⁷ The reaction was even more robust at 12 weeks, signifying an ongoing inflammatory process. In this context, tendon degeneration may plausibly explain the consistent absence of mature tendon within the tunnels at all 3 time points. Some tendon degeneration may be explained by the vascular damage that occurred during surgery, but this damage was a constant factor in all 3 study groups. Interestingly, group M showed the highest early CD68 counts, consistent with this being the more biologically active region of bone.²⁸

Group T had significantly lower cell and macrophage counts throughout the study period, possibly indicating improved healing—an observation supported by a study in which the impact of macrophage depletion on bone-tendon interface healing was evaluated.²⁹ The authors found that, in suppressing macrophage activity, the morphologic and biomechanical properties at the healing interface were significantly improved.²⁹ These findings are consistent with Dr. O’Brien’s anecdotal experience with patients who previously underwent the biceps transfer; on second-look arthroscopy, there was complete seamless integration of tendon and conjoint tendon (Figure 4). 

 

Studies have found that the inflammatory process is closely associated with pain, and pain syndromes such as fibromyalgia.^30,31 Persistent inflammation, as seen in our bony tenodesis group, could explain the recalcitrant anterior shoulder pain that often occurs in patients after bony tenodesis of the LHBT.^2,6,19,32 

Studies have also suggested that osteoclasts at the bone-tendon interface—osteoclasts share a cell lineage with macrophages—may contribute to bone loss and tunnel widening.^33,34 Osteoclasts are expected at the bone tunnel, as fracture healing occurs at the bone-tendon interface. These osteoclasts could have contributed to the strong CD68 reaction in our bony tenodesis groups. However, CD68 historically has been described as the classic macrophage marker.³⁵ We specifically selected CD68 for this reason: Macrophages are the primary inflammatory cells involved in early healing and are key to the inflammatory process.³⁶

Results of the tenomodulin analysis suggested 2 different healing processes are occurring in the bony and tendon groups. Tenomodulin is a known tenocyte marker for developing and mature tendon in both rats and humans.^37,38 In our study, only group T had a positive tenomodulin reaction. Notably, the reaction occurred only at 6 and 12 weeks. This finding may indicate that a regenerative healing pattern becomes quiescent by 24 weeks. Indeed, it has been suggested that tenomodulin is a key regulator of tenocyte proliferation and tendon maturation.³⁹

The complete absence of tenomodulin reaction in our bony tenodesis groups in the setting of significant inflammation further supports our theory of tendon degeneration within the tunnel. One potential explanation for this finding may be that as the tendon heals to the surface of the bone, the intra-osseous tendon is no longer load-bearing and is resorbed by the body through an inflammatory response. This finding differs from those in previous studies, which have described viable tendon within the bone tunnel at all time points up to 26 weeks.⁴⁰ More recently, it has been suggested that callus formation at the external cortical tendon-bone interface is critical for healing and mechanical strength.^41,42 In addition, recent studies have found a predominantly fibroblastic healing process at the midtunnel, potentially leading to the formation of loose fibrovascular tissue at the tendon-bone interface.⁴³ These data, in concert with ours, call into question the rationale for performing intra-osseous tenodesis through bone tunnels.

Our study results, if confirmed in humans, will have significant clinical implications. If a similar effect can be confirmed in the human shoulder, one could argue that soft-tissue tenodesis may result in decreased postoperative shoulder pain. In addition, if tendon degeneration does occur within the intramedullary tunnel, surface fixation may be the better, safer alternative. Although older studies reported suboptimal strength with this type of fixation,^8,44 more recent studies have found surface fixation strength equivalent to screw fixation strength.^45,46 Such a shift in the treatment paradigm would obviate the need for violation of the humeral cortex, eliminating potential stress risers associated with screw fixation,⁴⁷ and effectively eliminating the risk of iatrogenic fracture.^48,49 It would be interesting to investigate what occurs histologically at the bone-tendon interface in surface fixation (ie, suture anchors). Would the inflammatory response at the surface be similar to the inflammatory intramedullary healing, or would it be similar to the quieter tendon-tendon healing? Answers to such questions have the potential to streamline the treatment algorithm for patients who require tenodesis.

Study Limitations

Our study had several limitations. First, as this was a basic science study using a rat model, its conclusions can only be extrapolated to humans. Second, given the nonspecific nature of the cellular analysis, we cannot draw any definitive conclusions about the cell population at the bone-tendon interface. For example, although tenomodulin is expressed by tenocytes, it is not an established specific marker for tenocytes and may be expressed by other fibroblastic cells. Still, our results provide insight into the local microenvironment and identify important differences between the tenodesis methods. Similarly, the complete absence of tendon within the bone tunnels suggests that an analysis of osteoclastic activity at the tenodesis interface may have been a valuable addition to the study. This finding, however, was unexpected, and we did not have the foresight to include it in our methods. A third limitation is that our fixation method essentially uses the suspension tenodesis method. This fixation method differs from the common fixation techniques used in the clinical setting. Testing of other fixation constructs would require a larger animal model. Furthermore, in suspension- type constructs, micromotion within the bone tunnel may independently elicit an inflammatory response. Inert suture was used in our fixation in order to reduce the risk of an iatrogenic inflammatory response. Last, it would have been valuable to perform a biomechanical analysis of the strength of each tenodesis construct. This was explored with our institution’s biomechanics team, but specimen size precluded successful analysis.

Conclusion

Our results indicated that, compared with tendon-to-tendon fixation, tendon-to-bone tenodesis produces a significantly greater inflammatory response at the tenodesis interface. An inflammatory milieu in the absence of tendon within the bony tunnel suggests intraosseous tendon degeneration. Tendon-to-tendon tenodesis, on the other hand, seems to limit the inflammatory response. In addition, a robust tenomodulin reaction in the early phases of tendon-to-tendon healing suggests regenerative healing. Our results showed a fundamental difference in the healing response between the 2 tenodesis methods. Further study is needed to evaluate the validity and applicability of our findings to the human patient population. Most important, our results underscore the need for more study to elucidate optimal tenodesis location and encourage orthopedic surgeons to reexamine current clinical practice patterns.

Take-Home Points

• Cellular healing response differs between bony and soft tissue biceps tenodesis.
• Bony tenodesis incites an inflammatory healing response.
• Bony tenodesis healing occurs at the tendon-bone interface.
• Intrasseous bony fixation leads to tendon degeneration within the bone.
• Tendon-to-tendon tenodesis may result in regenerative tendon healing.

The long head of the biceps tendon (LHBT) is a well-established pain generator of the anterior shoulder^1,2 and may be surgically addressed in refractory cases.³ According to a recent study of 44,932 cases, biceps tenodesis rates increased 80% over just 3 years (2008-2011).⁴ Nevertheless, optimal tenodesis location and technique remain controversial. Proximal and distal tenodesis, including numerous soft-tissue and bony techniques, have been described.^5-7 Several studies have focused on the biomechanical strength of various fixation modalities.^8-14 These data highlight the ongoing evolution of our understanding of biceps-labrum complex (BLC) disease.

Over the years, tenodesis location has proved to be an important factor in outcomes.^3,15-20 Several recent studies have elucidated the role of the extra-articular LHBT and the limited capabilities of diagnostic arthroscopy.^15-17,20,21 Taylor and colleagues¹⁷ defined the bicipital tunnel as the extra-articular segment of LHBT and its fibro-osseous enclosure. The tunnel extends from the articular margin through the subpectoral region and can be divided into 3 zones: Zone 1 goes from the articular margin to the inferior margin of the subscapularis, zone 2 goes from the inferior margin of the subscapularis to the proximal margin of the pectoralis major tendon, and zone 3 is the subpectoral region. Zone 2 is often referred to as “no man’s land” for its relative invisibility from arthroscopy above and open exposure below.^17,21 Notably, a recent study reported a 47% prevalence of hidden tunnel lesions in patients with chronic BLC disease symptoms.¹⁸ Other studies have shown that standard proximal tenodesis methods often fail to address LHBT pathology in this area, leading to residual symptoms.^9,22 It is evident that tenodesis location and technique play important roles in patient outcomes. Sanders and colleagues¹⁶ found that the revision rate was significantly higher among patients who underwent biceps tenodesis without release of the bicipital tunnel sheath than among patients who underwent tenodesis with the release. Dr. O’Brien developed an alternative option: soft-tissue tenodesis with transfer of the LHBT to the conjoint tendon within the subdeltoid space.^23,24 This technique addresses intra-articular and extra-articular tunnel disease while mitigating the complications associated with bony tenodesis. Early and midterm studies have shown this to be an effective intervention for chronically symptomatic BLC disease.^25,26

Despite the abundance of literature on tenodesis techniques, no one has histologically evaluated the location-dependent healing and inflammatory responses. We conducted a study to determine the impact of tenodesis location on healing and inflammation in a rat model. We hypothesized that, compared with tendon-to-bone techniques, soft-tissue tenodesis would minimize inflammatory response and optimize healing.

Methods 

The study was approved by the Institutional Animal Care and Use Committee at the Hospital for Special Surgery. 

Animals

Biceps tenodesis was performed at 1 of 3 locations in 36 thirteen-week-old Sprague-Dawley rats (Charles River Laboratories). All rats were prepared for surgery by an experienced veterinary technician. Sedation was induced with isoflurane gas through a nose cone. 

Surgical Procedure

Animals were randomly assigned to 3 different tenodesis groups: tendon-to-bone in the bicipital groove (metaphyseal, M); tendon-to-bone in the subpectoral region (diaphyseal, D); and soft tissue-to-soft tissue transfer to the conjoint tendon (T). A standard deltopectoral approach was used to expose the biceps tendon. The tendon was tagged with a 5-0 polypropylene suture and tenotomized at the level of the bicipital groove (zone 1). All wounds were irrigated and closed with 4-0 nylon suture.

For animals undergoing tendon-to-bone metaphyseal tenodesis, a 0.045-mm Kirschner wire was used to drill bicortically into the intertubercular sulcus. Wire positioning distal to the physeal plate was confirmed with fluoroscopy. A locking stitch of 5-0 polypropylene suture was run along the free edge of the tendon. The tendon was then passed through the bone tunnel in an anterior-to-posterior direction, and the limbs of the suture were tied around the lateral cortex. 

The process was repeated for animals undergoing diaphyseal tenodesis; only the tenodesis location was different. The inferior border of the pectoralis major was identified, and a bicortical tunnel was made in the center of the diaphyseal bone. The tendon was then prepared and tenodesed to bone using the method already described.

In soft-tissue tenodesis, the conjoint tendon was identified and carefully dissected from surrounding tissues. The LHBT was then tenodesed to the attached conjoint tendon with interrupted simple stitches of 5-0 polypropylene suture.

The animals were allowed to bear weight on the operative limb immediately after surgery and without immobilization.

Specimen Harvest and Preparation

Four animals from each group were sacrificed at 6, 12, and 24 weeks. Harvested specimens were fixed in 10% neutral-buffered formalin solution. Bony specimens consisted of the upper half of the humerus and the tenodesed biceps tendon, and soft-tissue specimens consisted of the tenodesed LHBT-conjoint tendon complex. Bony specimens were decalcified in 10% ethylenediaminetetraacetic acid. All specimens were paraffin-embedded and sectioned at 7 microns.

Analysis of Cellularity

Sections were stained with hematoxylin-eosin. Overall cellularity at the tenodesis interface was quantified by averaging the nuclei count within 3 separate standardized ×20 magnification high power fields. Only nucleated cells were included in the cell count. Immunohistochemical staining with tenomodulin (Santa Cruz Laboratories, sc-49324) was performed to characterize the cell population at the interface. Deparaffinized sections underwent antigen retrieval with pronase for 30 minutes at 37°C and were incubated overnight with the anti-tenomodulin goat monoclonal antibody diluted to 1:200 in 1% phosphate-buffered saline. The prepared slides were then counterstained with methyl green. Specimens treated with tenomodulin were evaluated for presence or absence of a positive reaction at the tenodesis interface. 

Analysis of Inflammation

Inflammation at the interface was evaluated with the CD68 macrophage marker (ABcam, ab31630). Deparaffinized sections underwent antigen retrieval with pronase for 30 minutes at 37°C and were incubated overnight with anti-CD68 mouse monoclonal antibodies diluted to 1:200 in 1% phosphate-buffered saline. The prepared slides were then counterstained with neutral red. Inflammation was quantified by averaging the number of reactive cells within 3 separate standardized ×20 magnification high power fields.

Statistical Analysis

Descriptive statistics were calculated for cell and macrophage counts for each group at every time point. Two-way analysis of variance was used to compare the cell and macrophage counts between groups at each time point as well as the count differences within each group between time points. P values were Bonferroni-corrected to account for the multiple comparisons between groups. P < .05 was used to signify statistical significance.

Results

All 36 animals survived to their designated harvest time without complications. Twelve specimens were successfully harvested at 6 weeks and another 12 at 24 weeks. At 12 weeks, tenodesis failure occurred in 1 animal in group D, leaving 11 specimens for analysis.

Cellularity

At the 6-week harvest, 1 group T specimen was sectioned incorrectly and discarded, leaving 3 specimens for evaluation. Descriptive statistics for each group and each time point are listed in Table 1A. There were no significant differences in mean cellularity between the bony tenodesis groups at any time point (P = 1.000) (Table 1B).

At 6 weeks, both group M (P = .012) and group D (P = .021) showed significantly more cellularity than group T (Figure 1). The same was true for group M (P = .002) and group D (P = .001) at the 12-week harvest. There were no significant differences in cellularity between the 3 groups at 24 weeks. 

Within-group analysis revealed a trend of increasing cellularity at 12 weeks followed by a decrease at 24 weeks in all 3 groups (Table 2).

Group M showed a significant overall decrease in cellularity from 6 to 24 weeks (P = .035) and from 12 to 24 weeks (P = .004). The overall decrease in cell count from 6 to 24 weeks was not significant in group D (P = .124), whereas the decrease from 12 to 24 weeks was significant (P = .005). There were no significant differences in cellularity for group T between any of the time points.

Inflammatory Response 

During specimen processing, 1 group D specimen was severely degraded after pronase treatment, leaving 3 specimens for evaluation. Descriptive statistics for each group are listed in Table 3A.

At 6 weeks, mean CD68 cell count was significantly higher in group M than in group D (P = .011) and group T (P < .001) (Table 3B). Likewise, CD68 count was significantly higher in group D than in group T (P < .001). There were no differences in CD68 counts between the 2 bony tenodesis groups at 12 weeks (P = .486) or 24 weeks (P = .315). Both bony tenodesis groups, however, had persistently higher CD68 counts at 12 weeks when compared with group T (group M, P = .002; group D, P < .001). In these specimens, an inflammatory milieu characterized by a large accumulation of lymphocytes and giant cells was noted at the bone-tendon interface.

In comparison, inflammatory cells were scant at the tendon-tendon interface in group T specimens (Figure 2). There were no differences in CD68 reaction between the 3 tenodesis groups at 24 weeks. In all cases of tendon-to-bone tenodesis, no recognizable formed tendon was seen within the bone tunnel. Rather, all tendon-to-bone tenodeses were characterized by dense connective tissue at the bone surface, surrounded by an accumulation of macrophages.

Within-group analysis revealed a significant decrease in CD68 cells from 6 to 12 weeks and overall from 6 to 24 weeks in group M (Table 4). There was no significant change in CD68 cell counts between any time points within group D (P = 1.000) and between 6 and 12 weeks in group T (P = 1.000). Interestingly, the CD68 counts in group T showed an overall increase from 6 to 24 weeks (P = .019). The increase was even more significant from 12 to 24 weeks (P = .004).

Tissue-Specific Staining

At 6 weeks, antigen retrieval resulted in severe degradation of 2 group M specimens, 2 group D specimens, and 1 group T specimen. The most notable tenomodulin reaction occurred in group T at the 6- and 12-week harvests, with the 6-week group having the most robust reaction. There was scant reaction in this group at 24 weeks.

One group D specimen showed a positive reaction at 24 weeks. No reaction occurred in the remaining bony specimens across all time points (Figure 3).

Discussion

In this study, the healing response differed between bony and soft-tissue tenodesis techniques in a rat model. Tendon-to-bone tenodesis, both diaphyseal and metaphyseal, appeared to incite an inflammatory degenerative response, whereas tendon-to-tendon healing occurred in a more quiescent and perhaps even regenerative manner.

The early inflammatory response that occurred in the bony tenodesis groups is not unlike what occurs in fracture healing.²⁷ The reaction was even more robust at 12 weeks, signifying an ongoing inflammatory process. In this context, tendon degeneration may plausibly explain the consistent absence of mature tendon within the tunnels at all 3 time points. Some tendon degeneration may be explained by the vascular damage that occurred during surgery, but this damage was a constant factor in all 3 study groups. Interestingly, group M showed the highest early CD68 counts, consistent with this being the more biologically active region of bone.²⁸

Group T had significantly lower cell and macrophage counts throughout the study period, possibly indicating improved healing—an observation supported by a study in which the impact of macrophage depletion on bone-tendon interface healing was evaluated.²⁹ The authors found that, in suppressing macrophage activity, the morphologic and biomechanical properties at the healing interface were significantly improved.²⁹ These findings are consistent with Dr. O’Brien’s anecdotal experience with patients who previously underwent the biceps transfer; on second-look arthroscopy, there was complete seamless integration of tendon and conjoint tendon (Figure 4). 

 

Studies have found that the inflammatory process is closely associated with pain, and pain syndromes such as fibromyalgia.^30,31 Persistent inflammation, as seen in our bony tenodesis group, could explain the recalcitrant anterior shoulder pain that often occurs in patients after bony tenodesis of the LHBT.^2,6,19,32 

Studies have also suggested that osteoclasts at the bone-tendon interface—osteoclasts share a cell lineage with macrophages—may contribute to bone loss and tunnel widening.^33,34 Osteoclasts are expected at the bone tunnel, as fracture healing occurs at the bone-tendon interface. These osteoclasts could have contributed to the strong CD68 reaction in our bony tenodesis groups. However, CD68 historically has been described as the classic macrophage marker.³⁵ We specifically selected CD68 for this reason: Macrophages are the primary inflammatory cells involved in early healing and are key to the inflammatory process.³⁶

Results of the tenomodulin analysis suggested 2 different healing processes are occurring in the bony and tendon groups. Tenomodulin is a known tenocyte marker for developing and mature tendon in both rats and humans.^37,38 In our study, only group T had a positive tenomodulin reaction. Notably, the reaction occurred only at 6 and 12 weeks. This finding may indicate that a regenerative healing pattern becomes quiescent by 24 weeks. Indeed, it has been suggested that tenomodulin is a key regulator of tenocyte proliferation and tendon maturation.³⁹

The complete absence of tenomodulin reaction in our bony tenodesis groups in the setting of significant inflammation further supports our theory of tendon degeneration within the tunnel. One potential explanation for this finding may be that as the tendon heals to the surface of the bone, the intra-osseous tendon is no longer load-bearing and is resorbed by the body through an inflammatory response. This finding differs from those in previous studies, which have described viable tendon within the bone tunnel at all time points up to 26 weeks.⁴⁰ More recently, it has been suggested that callus formation at the external cortical tendon-bone interface is critical for healing and mechanical strength.^41,42 In addition, recent studies have found a predominantly fibroblastic healing process at the midtunnel, potentially leading to the formation of loose fibrovascular tissue at the tendon-bone interface.⁴³ These data, in concert with ours, call into question the rationale for performing intra-osseous tenodesis through bone tunnels.

Our study results, if confirmed in humans, will have significant clinical implications. If a similar effect can be confirmed in the human shoulder, one could argue that soft-tissue tenodesis may result in decreased postoperative shoulder pain. In addition, if tendon degeneration does occur within the intramedullary tunnel, surface fixation may be the better, safer alternative. Although older studies reported suboptimal strength with this type of fixation,^8,44 more recent studies have found surface fixation strength equivalent to screw fixation strength.^45,46 Such a shift in the treatment paradigm would obviate the need for violation of the humeral cortex, eliminating potential stress risers associated with screw fixation,⁴⁷ and effectively eliminating the risk of iatrogenic fracture.^48,49 It would be interesting to investigate what occurs histologically at the bone-tendon interface in surface fixation (ie, suture anchors). Would the inflammatory response at the surface be similar to the inflammatory intramedullary healing, or would it be similar to the quieter tendon-tendon healing? Answers to such questions have the potential to streamline the treatment algorithm for patients who require tenodesis.

Study Limitations

Our study had several limitations. First, as this was a basic science study using a rat model, its conclusions can only be extrapolated to humans. Second, given the nonspecific nature of the cellular analysis, we cannot draw any definitive conclusions about the cell population at the bone-tendon interface. For example, although tenomodulin is expressed by tenocytes, it is not an established specific marker for tenocytes and may be expressed by other fibroblastic cells. Still, our results provide insight into the local microenvironment and identify important differences between the tenodesis methods. Similarly, the complete absence of tendon within the bone tunnels suggests that an analysis of osteoclastic activity at the tenodesis interface may have been a valuable addition to the study. This finding, however, was unexpected, and we did not have the foresight to include it in our methods. A third limitation is that our fixation method essentially uses the suspension tenodesis method. This fixation method differs from the common fixation techniques used in the clinical setting. Testing of other fixation constructs would require a larger animal model. Furthermore, in suspension- type constructs, micromotion within the bone tunnel may independently elicit an inflammatory response. Inert suture was used in our fixation in order to reduce the risk of an iatrogenic inflammatory response. Last, it would have been valuable to perform a biomechanical analysis of the strength of each tenodesis construct. This was explored with our institution’s biomechanics team, but specimen size precluded successful analysis.

Conclusion

Our results indicated that, compared with tendon-to-tendon fixation, tendon-to-bone tenodesis produces a significantly greater inflammatory response at the tenodesis interface. An inflammatory milieu in the absence of tendon within the bony tunnel suggests intraosseous tendon degeneration. Tendon-to-tendon tenodesis, on the other hand, seems to limit the inflammatory response. In addition, a robust tenomodulin reaction in the early phases of tendon-to-tendon healing suggests regenerative healing. Our results showed a fundamental difference in the healing response between the 2 tenodesis methods. Further study is needed to evaluate the validity and applicability of our findings to the human patient population. Most important, our results underscore the need for more study to elucidate optimal tenodesis location and encourage orthopedic surgeons to reexamine current clinical practice patterns.

Take-Home Points

• Cellular healing response differs between bony and soft tissue biceps tenodesis.
• Bony tenodesis incites an inflammatory healing response.
• Bony tenodesis healing occurs at the tendon-bone interface.
• Intrasseous bony fixation leads to tendon degeneration within the bone.
• Tendon-to-tendon tenodesis may result in regenerative tendon healing.

The long head of the biceps tendon (LHBT) is a well-established pain generator of the anterior shoulder^1,2 and may be surgically addressed in refractory cases.³ According to a recent study of 44,932 cases, biceps tenodesis rates increased 80% over just 3 years (2008-2011).⁴ Nevertheless, optimal tenodesis location and technique remain controversial. Proximal and distal tenodesis, including numerous soft-tissue and bony techniques, have been described.^5-7 Several studies have focused on the biomechanical strength of various fixation modalities.^8-14 These data highlight the ongoing evolution of our understanding of biceps-labrum complex (BLC) disease.

Over the years, tenodesis location has proved to be an important factor in outcomes.^3,15-20 Several recent studies have elucidated the role of the extra-articular LHBT and the limited capabilities of diagnostic arthroscopy.^15-17,20,21 Taylor and colleagues¹⁷ defined the bicipital tunnel as the extra-articular segment of LHBT and its fibro-osseous enclosure. The tunnel extends from the articular margin through the subpectoral region and can be divided into 3 zones: Zone 1 goes from the articular margin to the inferior margin of the subscapularis, zone 2 goes from the inferior margin of the subscapularis to the proximal margin of the pectoralis major tendon, and zone 3 is the subpectoral region. Zone 2 is often referred to as “no man’s land” for its relative invisibility from arthroscopy above and open exposure below.^17,21 Notably, a recent study reported a 47% prevalence of hidden tunnel lesions in patients with chronic BLC disease symptoms.¹⁸ Other studies have shown that standard proximal tenodesis methods often fail to address LHBT pathology in this area, leading to residual symptoms.^9,22 It is evident that tenodesis location and technique play important roles in patient outcomes. Sanders and colleagues¹⁶ found that the revision rate was significantly higher among patients who underwent biceps tenodesis without release of the bicipital tunnel sheath than among patients who underwent tenodesis with the release. Dr. O’Brien developed an alternative option: soft-tissue tenodesis with transfer of the LHBT to the conjoint tendon within the subdeltoid space.^23,24 This technique addresses intra-articular and extra-articular tunnel disease while mitigating the complications associated with bony tenodesis. Early and midterm studies have shown this to be an effective intervention for chronically symptomatic BLC disease.^25,26

Despite the abundance of literature on tenodesis techniques, no one has histologically evaluated the location-dependent healing and inflammatory responses. We conducted a study to determine the impact of tenodesis location on healing and inflammation in a rat model. We hypothesized that, compared with tendon-to-bone techniques, soft-tissue tenodesis would minimize inflammatory response and optimize healing.

Methods 

The study was approved by the Institutional Animal Care and Use Committee at the Hospital for Special Surgery. 

Animals

Biceps tenodesis was performed at 1 of 3 locations in 36 thirteen-week-old Sprague-Dawley rats (Charles River Laboratories). All rats were prepared for surgery by an experienced veterinary technician. Sedation was induced with isoflurane gas through a nose cone. 

Surgical Procedure

Animals were randomly assigned to 3 different tenodesis groups: tendon-to-bone in the bicipital groove (metaphyseal, M); tendon-to-bone in the subpectoral region (diaphyseal, D); and soft tissue-to-soft tissue transfer to the conjoint tendon (T). A standard deltopectoral approach was used to expose the biceps tendon. The tendon was tagged with a 5-0 polypropylene suture and tenotomized at the level of the bicipital groove (zone 1). All wounds were irrigated and closed with 4-0 nylon suture.

For animals undergoing tendon-to-bone metaphyseal tenodesis, a 0.045-mm Kirschner wire was used to drill bicortically into the intertubercular sulcus. Wire positioning distal to the physeal plate was confirmed with fluoroscopy. A locking stitch of 5-0 polypropylene suture was run along the free edge of the tendon. The tendon was then passed through the bone tunnel in an anterior-to-posterior direction, and the limbs of the suture were tied around the lateral cortex. 

The process was repeated for animals undergoing diaphyseal tenodesis; only the tenodesis location was different. The inferior border of the pectoralis major was identified, and a bicortical tunnel was made in the center of the diaphyseal bone. The tendon was then prepared and tenodesed to bone using the method already described.

In soft-tissue tenodesis, the conjoint tendon was identified and carefully dissected from surrounding tissues. The LHBT was then tenodesed to the attached conjoint tendon with interrupted simple stitches of 5-0 polypropylene suture.

The animals were allowed to bear weight on the operative limb immediately after surgery and without immobilization.

Specimen Harvest and Preparation

Four animals from each group were sacrificed at 6, 12, and 24 weeks. Harvested specimens were fixed in 10% neutral-buffered formalin solution. Bony specimens consisted of the upper half of the humerus and the tenodesed biceps tendon, and soft-tissue specimens consisted of the tenodesed LHBT-conjoint tendon complex. Bony specimens were decalcified in 10% ethylenediaminetetraacetic acid. All specimens were paraffin-embedded and sectioned at 7 microns.

Analysis of Cellularity

Sections were stained with hematoxylin-eosin. Overall cellularity at the tenodesis interface was quantified by averaging the nuclei count within 3 separate standardized ×20 magnification high power fields. Only nucleated cells were included in the cell count. Immunohistochemical staining with tenomodulin (Santa Cruz Laboratories, sc-49324) was performed to characterize the cell population at the interface. Deparaffinized sections underwent antigen retrieval with pronase for 30 minutes at 37°C and were incubated overnight with the anti-tenomodulin goat monoclonal antibody diluted to 1:200 in 1% phosphate-buffered saline. The prepared slides were then counterstained with methyl green. Specimens treated with tenomodulin were evaluated for presence or absence of a positive reaction at the tenodesis interface. 

Analysis of Inflammation

Inflammation at the interface was evaluated with the CD68 macrophage marker (ABcam, ab31630). Deparaffinized sections underwent antigen retrieval with pronase for 30 minutes at 37°C and were incubated overnight with anti-CD68 mouse monoclonal antibodies diluted to 1:200 in 1% phosphate-buffered saline. The prepared slides were then counterstained with neutral red. Inflammation was quantified by averaging the number of reactive cells within 3 separate standardized ×20 magnification high power fields.

Statistical Analysis

Descriptive statistics were calculated for cell and macrophage counts for each group at every time point. Two-way analysis of variance was used to compare the cell and macrophage counts between groups at each time point as well as the count differences within each group between time points. P values were Bonferroni-corrected to account for the multiple comparisons between groups. P < .05 was used to signify statistical significance.

Results

All 36 animals survived to their designated harvest time without complications. Twelve specimens were successfully harvested at 6 weeks and another 12 at 24 weeks. At 12 weeks, tenodesis failure occurred in 1 animal in group D, leaving 11 specimens for analysis.

Cellularity

At the 6-week harvest, 1 group T specimen was sectioned incorrectly and discarded, leaving 3 specimens for evaluation. Descriptive statistics for each group and each time point are listed in Table 1A. There were no significant differences in mean cellularity between the bony tenodesis groups at any time point (P = 1.000) (Table 1B).

At 6 weeks, both group M (P = .012) and group D (P = .021) showed significantly more cellularity than group T (Figure 1). The same was true for group M (P = .002) and group D (P = .001) at the 12-week harvest. There were no significant differences in cellularity between the 3 groups at 24 weeks. 

Within-group analysis revealed a trend of increasing cellularity at 12 weeks followed by a decrease at 24 weeks in all 3 groups (Table 2).

Group M showed a significant overall decrease in cellularity from 6 to 24 weeks (P = .035) and from 12 to 24 weeks (P = .004). The overall decrease in cell count from 6 to 24 weeks was not significant in group D (P = .124), whereas the decrease from 12 to 24 weeks was significant (P = .005). There were no significant differences in cellularity for group T between any of the time points.

Inflammatory Response 

During specimen processing, 1 group D specimen was severely degraded after pronase treatment, leaving 3 specimens for evaluation. Descriptive statistics for each group are listed in Table 3A.

At 6 weeks, mean CD68 cell count was significantly higher in group M than in group D (P = .011) and group T (P < .001) (Table 3B). Likewise, CD68 count was significantly higher in group D than in group T (P < .001). There were no differences in CD68 counts between the 2 bony tenodesis groups at 12 weeks (P = .486) or 24 weeks (P = .315). Both bony tenodesis groups, however, had persistently higher CD68 counts at 12 weeks when compared with group T (group M, P = .002; group D, P < .001). In these specimens, an inflammatory milieu characterized by a large accumulation of lymphocytes and giant cells was noted at the bone-tendon interface.

In comparison, inflammatory cells were scant at the tendon-tendon interface in group T specimens (Figure 2). There were no differences in CD68 reaction between the 3 tenodesis groups at 24 weeks. In all cases of tendon-to-bone tenodesis, no recognizable formed tendon was seen within the bone tunnel. Rather, all tendon-to-bone tenodeses were characterized by dense connective tissue at the bone surface, surrounded by an accumulation of macrophages.

Within-group analysis revealed a significant decrease in CD68 cells from 6 to 12 weeks and overall from 6 to 24 weeks in group M (Table 4). There was no significant change in CD68 cell counts between any time points within group D (P = 1.000) and between 6 and 12 weeks in group T (P = 1.000). Interestingly, the CD68 counts in group T showed an overall increase from 6 to 24 weeks (P = .019). The increase was even more significant from 12 to 24 weeks (P = .004).

Tissue-Specific Staining

At 6 weeks, antigen retrieval resulted in severe degradation of 2 group M specimens, 2 group D specimens, and 1 group T specimen. The most notable tenomodulin reaction occurred in group T at the 6- and 12-week harvests, with the 6-week group having the most robust reaction. There was scant reaction in this group at 24 weeks.

One group D specimen showed a positive reaction at 24 weeks. No reaction occurred in the remaining bony specimens across all time points (Figure 3).

Discussion

In this study, the healing response differed between bony and soft-tissue tenodesis techniques in a rat model. Tendon-to-bone tenodesis, both diaphyseal and metaphyseal, appeared to incite an inflammatory degenerative response, whereas tendon-to-tendon healing occurred in a more quiescent and perhaps even regenerative manner.

The early inflammatory response that occurred in the bony tenodesis groups is not unlike what occurs in fracture healing.²⁷ The reaction was even more robust at 12 weeks, signifying an ongoing inflammatory process. In this context, tendon degeneration may plausibly explain the consistent absence of mature tendon within the tunnels at all 3 time points. Some tendon degeneration may be explained by the vascular damage that occurred during surgery, but this damage was a constant factor in all 3 study groups. Interestingly, group M showed the highest early CD68 counts, consistent with this being the more biologically active region of bone.²⁸

Group T had significantly lower cell and macrophage counts throughout the study period, possibly indicating improved healing—an observation supported by a study in which the impact of macrophage depletion on bone-tendon interface healing was evaluated.²⁹ The authors found that, in suppressing macrophage activity, the morphologic and biomechanical properties at the healing interface were significantly improved.²⁹ These findings are consistent with Dr. O’Brien’s anecdotal experience with patients who previously underwent the biceps transfer; on second-look arthroscopy, there was complete seamless integration of tendon and conjoint tendon (Figure 4). 

 

Studies have found that the inflammatory process is closely associated with pain, and pain syndromes such as fibromyalgia.^30,31 Persistent inflammation, as seen in our bony tenodesis group, could explain the recalcitrant anterior shoulder pain that often occurs in patients after bony tenodesis of the LHBT.^2,6,19,32 

Studies have also suggested that osteoclasts at the bone-tendon interface—osteoclasts share a cell lineage with macrophages—may contribute to bone loss and tunnel widening.^33,34 Osteoclasts are expected at the bone tunnel, as fracture healing occurs at the bone-tendon interface. These osteoclasts could have contributed to the strong CD68 reaction in our bony tenodesis groups. However, CD68 historically has been described as the classic macrophage marker.³⁵ We specifically selected CD68 for this reason: Macrophages are the primary inflammatory cells involved in early healing and are key to the inflammatory process.³⁶

Results of the tenomodulin analysis suggested 2 different healing processes are occurring in the bony and tendon groups. Tenomodulin is a known tenocyte marker for developing and mature tendon in both rats and humans.^37,38 In our study, only group T had a positive tenomodulin reaction. Notably, the reaction occurred only at 6 and 12 weeks. This finding may indicate that a regenerative healing pattern becomes quiescent by 24 weeks. Indeed, it has been suggested that tenomodulin is a key regulator of tenocyte proliferation and tendon maturation.³⁹

The complete absence of tenomodulin reaction in our bony tenodesis groups in the setting of significant inflammation further supports our theory of tendon degeneration within the tunnel. One potential explanation for this finding may be that as the tendon heals to the surface of the bone, the intra-osseous tendon is no longer load-bearing and is resorbed by the body through an inflammatory response. This finding differs from those in previous studies, which have described viable tendon within the bone tunnel at all time points up to 26 weeks.⁴⁰ More recently, it has been suggested that callus formation at the external cortical tendon-bone interface is critical for healing and mechanical strength.^41,42 In addition, recent studies have found a predominantly fibroblastic healing process at the midtunnel, potentially leading to the formation of loose fibrovascular tissue at the tendon-bone interface.⁴³ These data, in concert with ours, call into question the rationale for performing intra-osseous tenodesis through bone tunnels.

Our study results, if confirmed in humans, will have significant clinical implications. If a similar effect can be confirmed in the human shoulder, one could argue that soft-tissue tenodesis may result in decreased postoperative shoulder pain. In addition, if tendon degeneration does occur within the intramedullary tunnel, surface fixation may be the better, safer alternative. Although older studies reported suboptimal strength with this type of fixation,^8,44 more recent studies have found surface fixation strength equivalent to screw fixation strength.^45,46 Such a shift in the treatment paradigm would obviate the need for violation of the humeral cortex, eliminating potential stress risers associated with screw fixation,⁴⁷ and effectively eliminating the risk of iatrogenic fracture.^48,49 It would be interesting to investigate what occurs histologically at the bone-tendon interface in surface fixation (ie, suture anchors). Would the inflammatory response at the surface be similar to the inflammatory intramedullary healing, or would it be similar to the quieter tendon-tendon healing? Answers to such questions have the potential to streamline the treatment algorithm for patients who require tenodesis.

Study Limitations

Our study had several limitations. First, as this was a basic science study using a rat model, its conclusions can only be extrapolated to humans. Second, given the nonspecific nature of the cellular analysis, we cannot draw any definitive conclusions about the cell population at the bone-tendon interface. For example, although tenomodulin is expressed by tenocytes, it is not an established specific marker for tenocytes and may be expressed by other fibroblastic cells. Still, our results provide insight into the local microenvironment and identify important differences between the tenodesis methods. Similarly, the complete absence of tendon within the bone tunnels suggests that an analysis of osteoclastic activity at the tenodesis interface may have been a valuable addition to the study. This finding, however, was unexpected, and we did not have the foresight to include it in our methods. A third limitation is that our fixation method essentially uses the suspension tenodesis method. This fixation method differs from the common fixation techniques used in the clinical setting. Testing of other fixation constructs would require a larger animal model. Furthermore, in suspension- type constructs, micromotion within the bone tunnel may independently elicit an inflammatory response. Inert suture was used in our fixation in order to reduce the risk of an iatrogenic inflammatory response. Last, it would have been valuable to perform a biomechanical analysis of the strength of each tenodesis construct. This was explored with our institution’s biomechanics team, but specimen size precluded successful analysis.

Conclusion

Our results indicated that, compared with tendon-to-tendon fixation, tendon-to-bone tenodesis produces a significantly greater inflammatory response at the tenodesis interface. An inflammatory milieu in the absence of tendon within the bony tunnel suggests intraosseous tendon degeneration. Tendon-to-tendon tenodesis, on the other hand, seems to limit the inflammatory response. In addition, a robust tenomodulin reaction in the early phases of tendon-to-tendon healing suggests regenerative healing. Our results showed a fundamental difference in the healing response between the 2 tenodesis methods. Further study is needed to evaluate the validity and applicability of our findings to the human patient population. Most important, our results underscore the need for more study to elucidate optimal tenodesis location and encourage orthopedic surgeons to reexamine current clinical practice patterns.

Pathology of the biceps-labrum complex (BLC) can be an important source of shoulder pain. Discussion of pathoanatomy, imaging, and surgical intervention is facilitated by distinguishing the anatomical zones of the BLC: inside, junction, and bicipital tunnel (extra-articular), parts of which cannot be visualized with standard diagnostic arthroscopy.

The recent literature indicates that bicipital tunnel lesions are common and perhaps overlooked. Systematic reviews suggest improvement in outcomes of BLC operations when the bicipital tunnel is decompressed. Higher-level clinical and basic science studies are needed to fully elucidate the role of the bicipital tunnel, but it is evident that a comprehensive physical examination and an understanding of the limits of advanced imaging are necessary to correctly diagnose and treat BLC-related shoulder pain.

Anatomy of Biceps-Labrum Complex

The long head of the biceps tendon (LHBT) and the glenoid labrum work as an interdependent functional unit, the biceps-labrum complex (BLC). The BLC is divided into 3 distinct anatomical zones: inside, junction, and bicipital tunnel.^1,2

Inside

The inside includes the superior labrum and biceps attachment. The LHBT most commonly originates in the superior labrum.^3-5 Vangsness and colleagues³ described 4 types of LHBT origins: Type I biceps attaches solely to the posterior labrum, type II predominantly posterior, type III equally to the anterior and posterior labrum, and type IV mostly to the anterior labrum. The LHBT can also originate in the supraglenoid tubercle or the inferior border of the supraspinatus.^3,6

Junction

Junction is the intra-articular segment of the LHBT and the biceps pulley. The LHBT traverses the glenohumeral joint en route to the extra-articular bicipital tunnel.² The LHBT is enveloped in synovium that extends into part of the bicipital tunnel.² The intra-articular segment of the LHBT is about 25 mm in length⁷ and has a diameter of 5 mm to 6 mm.⁸

A cadaveric study found that the average length of the LHBT that can be arthroscopically visualized at rest is 35.6 mm, or only 40% of the total length of the LHBT with respect to the proximal margin of the pectoralis major tendon.¹ When the LHBT was pulled into the joint, more tendon (another 14 mm) was visualized.¹ Therefore, diagnostic arthroscopy of the glenohumeral joint visualizes about 50% of the LHBT.⁹The morphology of the LHBT varies by location. The intra-articular portion of the LHBT is wide and flat, whereas the extra-articular portion is round.⁸ The tendon becomes smoother and more avascular as it exits the joint to promote gliding within its sheath in the bicipital groove.¹⁰ The proximal LHBT receives its vascular supply from superior labrum tributaries, and distally the LHBT is supplied by ascending branches of the anterior humeral circumflex artery.⁴ There is a hypovascular zone, created by this dual blood supply, about 12 mm to 30 mm from the LHBT origin, predisposing the tendon to rupture or fray in this region.¹¹The LHBT makes a 30° turn into the biceps pulley system as it exits the glenohumeral joint. The fibrous pulley system that stabilizes the LHBT in this region has contributions from the coracohumeral ligament, the superior glenohumeral ligament, and the supraspinatus tendon.^12-14

The floor of the pulley consists of the superior glenohumeral ligament with reinforcing fibers from the superior border of the subscapularis tendon.¹⁵ The roof consists of the coracohumeral ligament fibers with supraspinatus fibers contributing posteriorly (Figure 1).¹²

Bicipital Tunnel

The bicipital tunnel, the third portion of the BLC, remains largely hidden from standard diagnostic glenohumeral arthroscopy. The bicipital tunnel is an extra-articular, closed space that constrains the LHBT from the articular margin through the subpectoral region.²

The bicipital tunnel itself can be divided into 3 zones (Figure 2).²

Zone 1 is the traditional bicipital groove or “bony groove” that extends from the articular margin to the distal margin of the subscapularis tendon. The floor consists of a deep osseous groove covered by a continuation of subscapularis tendon fibers and periosteum.²Zone 2, “no man’s land,” extends from the distal margin of the subscapularis tendon to the proximal margin of the pectoralis major (PMPM). The LHBT in this zone cannot be visualized during a pull test at arthroscopy, yet lesions commonly occur here.¹ Zones 1 and 2 have a similar histology and contain synovium.²Zone 3 is the subpectoral region distal to the PMPM. Fibers of the latissimus dorsi form the flat floor of zone 3, and the pectoralis major inserts lateral to the LHBT on the humerus in this zone. The synovium encapsulating the LHBT in zones 1 and 2 rarely extends past the PMPM. Taylor and colleagues² found a higher percentage of unoccupied tunnel space in zone 3 than in zones 1 and 2, which results in a “functional bottleneck” between zones 2 and 3 represented by the PMPM.

 

Pathoanatomy

BLC lesions may occur in isolation or concomitantly across multiple anatomical zones. In a series of 277 chronically symptomatic shoulders that underwent transfer of the LHBT to the conjoint tendon with subdeltoid arthroscopy, Taylor and colleagues¹ found 47% incidence of bicipital tunnel lesions, 44% incidence of junctional lesions, and 35% incidence of inside lesions. In their series, 37% of patients had concomitant lesions involving more than 1 anatomical zone.

Inside Lesions

Inside lesions involve the superior labrum, the LHBT origin, or both. Superior labrum anterior-posterior (SLAP) tears are included as inside BLC lesions. Snyder and colleagues¹⁶ originally identified 4 broad categories of SLAP tears, but Powell and colleagues¹⁷ described up to 10 variations. Type II lesions, which are the most common, destabilize the biceps anchor.

Dynamic incarceration of the biceps between the humeral head and the glenoid labrum is another inside lesion that can be identified during routine diagnostic glenohumeral arthroscopy. The arthroscopic active compression test, as described by Verma and colleagues,¹⁸ can be used during surgery to demonstrate incarceration of the biceps tendon.

Medial biceps chondromalacia, attritional chondral wear along the anteromedial aspect of the humeral head, occurs secondary to a windshield wiper effect of the LHBT in the setting of an incarcerating LHBT or may be associated with destabilization of the biceps pulley.

Junctional Lesions

Junctional lesions, which include lesions that affect the intra-articular LHBT, can be visualized during routine glenohumeral arthroscopy. They include partial and complete biceps tears, biceps pulley lesions, and junctional biceps chondromalacia.

Biceps pulley injuries and/or tears of the upper subscapularis tendon can destabilize the biceps as it exits the joint, and this destabilization may result in medial subluxation of the tendon and the aforementioned medial biceps chondromalacia.^10,19 Junctional biceps chondromalacia is attritional chondral wear of the humeral head from abnormal tracking of the LHBT deep to the LHBT near the articular margin.

Recently elucidated is the limited ability of diagnostic glenohumeral arthroscopy to fully identify the extent of BLC pathology.^1,20-22 Gilmer and colleagues²⁰ found that diagnostic arthroscopy identified only 67% of biceps pathology and underestimated its extent in 56% of patients in their series. Similarly, Moon and colleagues²¹ found that 79% of proximal LHBT tears propagated distally into the bicipital tunnel and were incompletely visualized with standard arthroscopy.

Bicipital Tunnel Lesions

Recent evidence indicates that the bicipital tunnel is a closed space that often conceals space-occupying lesions, including scar, synovitis, loose bodies, and osteophytes, which can become trapped in the tunnel. The functional bottleneck between zones 2 and 3 of the bicipital tunnel explains the aggregation of loose bodies in this region.² Similarly, as the percentage of free space within the bicipital tunnel increases, space-occupying lesions (eg scar, loose bodies, osteophytes) may exude a compressive and/or abrasive force within zones 1 and 2, but not as commonly within zone 3.²

Physical Examination of Biceps-Labrum Complex

Accurate diagnosis of BLC disease is crucial in selecting an optimal intervention, but challenging. Beyond identifying biceps pathology, specific examination maneuvers may help distinguish between lesions of the intra-articular BLC and lesions of the extra-articular bicipital tunnel.²³

Traditional examination maneuvers for biceps-related shoulder pain include the Speed test, the full can test, and the Yergason test.^24,25 For the Speed test, the patient forward-flexes the shoulder to 60° to 90°, extends the arm at the elbow, and supinates the forearm. The clinician applies a downward force as the patient resists. The reported sensitivity of the Speed test ranges from 37% to 63%, and specificity is 60% to 88%.^25,26 In the full can test, with the patient’s arm in the plane of the scapula, the shoulder abducted to 90°, and the forearm in neutral rotation, a downward force is applied against resistance. Sensitivity of the full can test is 60% to 67%, and specificity is 76% to 84%.²⁴ The Yergason test is performed with the patient’s arm at his or her side, the elbow flexed to 90°, and the forearm pronated. The patient supinates the forearm against the clinician’s resistance. Sensitivity of the Yergason test is 19% to 32%, and specificity is 70% to 100%.^25,26 The Yergason test has a positive predictive value of 92% for bicipital tunnel disease.

O’Brien and colleagues^23,26 introduced a “3-pack” physical examination designed to elicit BLC symptoms. In this examination, the LHBT is palpated along its course within the bicipital tunnel. Reproduction of the patient’s pain by palpation had a sensitivity of 98% for bicipital tunnel disease but was less specific (70%). Gill and colleagues²⁷ reported low sensitivity (53%) and low specificity (54%) for biceps palpation, and they used arthroscopy as a gold standard. Since then, multiple studies have demonstrated that glenohumeral arthroscopy fails to identify lesions concealed within the bicipital tunnel.^20-22The second part of the 3-pack examination is the active compression test. A downward force is applied as the patient resists with his or her arm forward-flexed to 90° and adducted 10° to 15° with the thumb pointing downward.²⁸ This action is repeated with the humerus externally rotated and the forearm supinated. A positive test is indicated by reproduction of symptoms with the thumb down, and elimination or reduction of symptoms with the palm up. Test sensitivity is 88% to 96%, and specificity is 46% to 64% for BLC lesions, but for bicipital tunnel disease sensitivity is higher (96%), and the negative predictive value is 93%.²⁶The third component of the 3-pack examination is the throwing test. A late-cocking throwing position is re-created with the shoulder externally rotated and abducted to 90° and the elbow flexed to 90°. The patient steps forward with the contralateral leg and moves into the acceleration phase of throwing while the clinician provides isometric resistance. If this maneuver reproduces pain, the test is positive. As Taylor and colleagues²⁶ reported, the throwing test has sensitivity of 73% to 77% and specificity of 65% to 79% for BLC pathology. This test has moderate sensitivity and negative predictive value for bicipital tunnel disease but may be the only positive test on physical examination in the setting of LHBT instability.

 

Imaging of Biceps-Labrum Complex

Plain anteroposterior, lateral, and axillary radiographs of the shoulder should be obtained for all patients having an orthopedic examination for shoulder pain. Magnetic resonance imaging (MRI) and ultrasound are the advanced modalities most commonly used for diagnostic imaging. These modalities should be considered in conjunction with, not in place of, a comprehensive history and physical examination.

The literature suggests MRI fails to accurately detect many LHBT lesions (Table).^29-37

MRI has sensitivity of 9% to 89% for LHBT pathology^29-37 and 38% to 98% for SLAP pathology.^35,38-41 The wide range of reported sensitivity and specificity might be attributed to the varying criteria for what constitutes a BLC lesion. Some authors include biceps chondromalacia, dynamic incarceration of LHBT, and extra-articular bicipital tunnel lesions, while others historically have included only intra-articular LHBT lesions that can be directly visualized arthroscopically.

In their retrospective review of 277 shoulders with chronic refractory BLC symptoms treated with subdeltoid transfer of the LHBT to the conjoint tendon, Taylor and colleagues³⁰ reported MRI was more sensitive for inside BLC lesions than for junctional or bicipital tunnel lesions (77% vs 43% and 50%, respectively).

Treatment Options for Biceps-Labrum Complex Lesions

A diagnosis of BLC disease warrants a trial of conservative (nonoperative) management for at least 3 months. Many patients improve with activity modification, use of oral anti-inflammatory medication, and structured physical therapy focused on dynamic stabilizers and range of motion. If pain persists, local anesthetic and corticosteroid can be injected under ultrasound guidance into the bicipital tunnel; this injection has the advantage of being both diagnostic and therapeutic. Hashiuchi and colleagues⁴² found ultrasound-guided injections are 87% successful in achieving intra-sheath placement (injections without ultrasound guidance are only 27% successful).

If the 3-month trial of conservative management fails, surgical intervention should be considered. The goal in treating BLC pain is to maximize clinical function and alleviate pain in a predictable manner while minimizing technical demands and morbidity. A singular solution has not been identified. Furthermore, 3 systematic reviews failed to identify a difference between the most commonly used techniques, biceps tenodesis and tenotomy.^43-45 These reviews grouped all tenotomy procedures together and compared them with all tenodesis procedures. A limitation of these systematic reviews is that they did not differentiate tenodesis techniques. We prefer to classify techniques according to whether or not they decompress zones 1 and 2 of the bicipital tunnel.

Bicipital Tunnel Nondecompressing Techniques

Release of the biceps tendon, a biceps tenotomy, is a simple procedure that potentially avoids open surgery and provides patients with a quick return to activity. Disadvantages of tenotomy include cosmetic (Popeye) deformity after surgery, potential cramping and fatigue, and biomechanical changes in the humeral head,^46-48 particularly among patients younger than 65 years. High rates of revision after tenotomy have been reported.^43,49 Incomplete retraction of the LHBT and/or residual synovium may be responsible for refractory pain following biceps tenotomy.⁴⁹ We hypothesize that failure of tenotomy may be related to unaddressed bicipital tunnel disease.

Proximal nondecompressing tenodesis techniques may be performed either on soft tissue in the interval or rotator cuff or on bone at the articular margin or within zone 1 of the bicipital tunnel.^50-52 These techniques can be performed with standard glenohumeral arthroscopy and generally are fast and well tolerated and have limited operative morbidity. Advantages of these techniques over simple tenotomy are lower rates of cosmetic deformity and lower rates of cramping and fatigue pain, likely resulting from maintenance of the muscle tension relationship of the LHBT. Disadvantages of proximal tenodesis techniques include introduction of hardware for bony fixation, longer postoperative rehabilitation to protect repairs, and failure to address hidden bicipital tunnel disease. Furthermore, the rate of stiffness in patients who undergo proximal tenodesis without decompression of the bicipital tunnel may be as high as 18%.⁵³

Bicipital Tunnel Decompressing Techniques

Surgical techniques that decompress the bicipital tunnel include proximal techniques that release the bicipital sheath within zones 1 and 2 of the bicipital tunnel (to the level of the proximal margin of the pectoralis major tendon) and certain arthroscopic suprapectoral techniques,⁵⁴ open subpectoral tenodeses,^55-57 and arthroscopic transfer of the LHBT to the conjoint tendon.^58,59

Open subpectoral tenodesis techniques have the advantage of maintaining the length-tension relationship of the LHBT and preventing Popeye deformity. However, these techniques require making an incision near the axilla, which may introduce an unnecessary source of infection. Furthermore, open subpectoral tenodesis requires drilling the humerus and placing a screw for bony fixation of the LHBT, which can create a risk of neurovascular injury, given the proximity of neurovascular structures,^60-62 and humeral shaft fracture, particularly in athletes.^63,64Our preferred method is transfer of the LHBT to the conjoint tendon (Figure 3).⁵⁹

The subdeltoid space is a large, relatively avascular fascial plane bounded superiorly by the acromion and coracoacromial ligament, medially by the coracoid and conjoint tendon, inferiorly by the musculotendinous insertion of the pectoralis major, and laterally by the border of the humerus.⁶⁵ After the LHBT is released from the superior labrum, it is transferred to the subdeltoid space and sutured to the conjoint tendon in side-to-side fashion with nonabsorbable sutures.^58,59 This technique allows for isometric tensioning of the LHBT, which preserves the strength of the biceps muscle, and fixation of soft tissue to soft tissue obviates the need for bone tunnels, mitigating fracture risk. A histologic study that compared healing between LHBT tenodesis with bone and soft-tissue transfer to the conjoint tendon found a more robust response of tenomodulin in the soft-tissue transfer, suggesting tendon regeneration in this technique.⁶⁶ Perhaps the most significant advantage is the ability of this approach to effectively decompress the bicipital tunnel. Early-term results were promising, and recent midterm results demonstrated durability of clinical outcomes.^58,59Sanders and colleagues⁴⁹ compared revision rates of biceps procedures and found a 6.8% rate for techniques that released the biceps sheath and a 20.6% rate for operations in which the sheath was not released. Subsequent meta-analysis of 30 studies (1881 patients) found improved Constant scores in the cohort that underwent bicipital tunnel decompression in comparison with the cohort that did not have the bicipital tunnel decompressed, but there was no significant difference in UCLA (University of California Los Angeles) scores between cohorts.67 

In light of recent literature that confirms the prevalence of bicipital tunnel lesions that have been overlooked, and the power of physical examination, we have proposed an evidence-based approach to diagnosing and managing BLC disease (Figure 4).

 

Am J Orthop. 2016;45(7):E503-E511. Copyright Frontline Medical Communications Inc. 2016. All rights reserved.

Pathology of the biceps-labrum complex (BLC) can be an important source of shoulder pain. Discussion of pathoanatomy, imaging, and surgical intervention is facilitated by distinguishing the anatomical zones of the BLC: inside, junction, and bicipital tunnel (extra-articular), parts of which cannot be visualized with standard diagnostic arthroscopy.

The recent literature indicates that bicipital tunnel lesions are common and perhaps overlooked. Systematic reviews suggest improvement in outcomes of BLC operations when the bicipital tunnel is decompressed. Higher-level clinical and basic science studies are needed to fully elucidate the role of the bicipital tunnel, but it is evident that a comprehensive physical examination and an understanding of the limits of advanced imaging are necessary to correctly diagnose and treat BLC-related shoulder pain.

Anatomy of Biceps-Labrum Complex

The long head of the biceps tendon (LHBT) and the glenoid labrum work as an interdependent functional unit, the biceps-labrum complex (BLC). The BLC is divided into 3 distinct anatomical zones: inside, junction, and bicipital tunnel.^1,2

Inside

The inside includes the superior labrum and biceps attachment. The LHBT most commonly originates in the superior labrum.^3-5 Vangsness and colleagues³ described 4 types of LHBT origins: Type I biceps attaches solely to the posterior labrum, type II predominantly posterior, type III equally to the anterior and posterior labrum, and type IV mostly to the anterior labrum. The LHBT can also originate in the supraglenoid tubercle or the inferior border of the supraspinatus.^3,6

Junction

Junction is the intra-articular segment of the LHBT and the biceps pulley. The LHBT traverses the glenohumeral joint en route to the extra-articular bicipital tunnel.² The LHBT is enveloped in synovium that extends into part of the bicipital tunnel.² The intra-articular segment of the LHBT is about 25 mm in length⁷ and has a diameter of 5 mm to 6 mm.⁸

A cadaveric study found that the average length of the LHBT that can be arthroscopically visualized at rest is 35.6 mm, or only 40% of the total length of the LHBT with respect to the proximal margin of the pectoralis major tendon.¹ When the LHBT was pulled into the joint, more tendon (another 14 mm) was visualized.¹ Therefore, diagnostic arthroscopy of the glenohumeral joint visualizes about 50% of the LHBT.⁹The morphology of the LHBT varies by location. The intra-articular portion of the LHBT is wide and flat, whereas the extra-articular portion is round.⁸ The tendon becomes smoother and more avascular as it exits the joint to promote gliding within its sheath in the bicipital groove.¹⁰ The proximal LHBT receives its vascular supply from superior labrum tributaries, and distally the LHBT is supplied by ascending branches of the anterior humeral circumflex artery.⁴ There is a hypovascular zone, created by this dual blood supply, about 12 mm to 30 mm from the LHBT origin, predisposing the tendon to rupture or fray in this region.¹¹The LHBT makes a 30° turn into the biceps pulley system as it exits the glenohumeral joint. The fibrous pulley system that stabilizes the LHBT in this region has contributions from the coracohumeral ligament, the superior glenohumeral ligament, and the supraspinatus tendon.^12-14

The floor of the pulley consists of the superior glenohumeral ligament with reinforcing fibers from the superior border of the subscapularis tendon.¹⁵ The roof consists of the coracohumeral ligament fibers with supraspinatus fibers contributing posteriorly (Figure 1).¹²

Bicipital Tunnel

The bicipital tunnel, the third portion of the BLC, remains largely hidden from standard diagnostic glenohumeral arthroscopy. The bicipital tunnel is an extra-articular, closed space that constrains the LHBT from the articular margin through the subpectoral region.²

The bicipital tunnel itself can be divided into 3 zones (Figure 2).²

Zone 1 is the traditional bicipital groove or “bony groove” that extends from the articular margin to the distal margin of the subscapularis tendon. The floor consists of a deep osseous groove covered by a continuation of subscapularis tendon fibers and periosteum.²Zone 2, “no man’s land,” extends from the distal margin of the subscapularis tendon to the proximal margin of the pectoralis major (PMPM). The LHBT in this zone cannot be visualized during a pull test at arthroscopy, yet lesions commonly occur here.¹ Zones 1 and 2 have a similar histology and contain synovium.²Zone 3 is the subpectoral region distal to the PMPM. Fibers of the latissimus dorsi form the flat floor of zone 3, and the pectoralis major inserts lateral to the LHBT on the humerus in this zone. The synovium encapsulating the LHBT in zones 1 and 2 rarely extends past the PMPM. Taylor and colleagues² found a higher percentage of unoccupied tunnel space in zone 3 than in zones 1 and 2, which results in a “functional bottleneck” between zones 2 and 3 represented by the PMPM.

 

Pathoanatomy

BLC lesions may occur in isolation or concomitantly across multiple anatomical zones. In a series of 277 chronically symptomatic shoulders that underwent transfer of the LHBT to the conjoint tendon with subdeltoid arthroscopy, Taylor and colleagues¹ found 47% incidence of bicipital tunnel lesions, 44% incidence of junctional lesions, and 35% incidence of inside lesions. In their series, 37% of patients had concomitant lesions involving more than 1 anatomical zone.

Inside Lesions

Inside lesions involve the superior labrum, the LHBT origin, or both. Superior labrum anterior-posterior (SLAP) tears are included as inside BLC lesions. Snyder and colleagues¹⁶ originally identified 4 broad categories of SLAP tears, but Powell and colleagues¹⁷ described up to 10 variations. Type II lesions, which are the most common, destabilize the biceps anchor.

Dynamic incarceration of the biceps between the humeral head and the glenoid labrum is another inside lesion that can be identified during routine diagnostic glenohumeral arthroscopy. The arthroscopic active compression test, as described by Verma and colleagues,¹⁸ can be used during surgery to demonstrate incarceration of the biceps tendon.

Medial biceps chondromalacia, attritional chondral wear along the anteromedial aspect of the humeral head, occurs secondary to a windshield wiper effect of the LHBT in the setting of an incarcerating LHBT or may be associated with destabilization of the biceps pulley.

Junctional Lesions

Junctional lesions, which include lesions that affect the intra-articular LHBT, can be visualized during routine glenohumeral arthroscopy. They include partial and complete biceps tears, biceps pulley lesions, and junctional biceps chondromalacia.

Biceps pulley injuries and/or tears of the upper subscapularis tendon can destabilize the biceps as it exits the joint, and this destabilization may result in medial subluxation of the tendon and the aforementioned medial biceps chondromalacia.^10,19 Junctional biceps chondromalacia is attritional chondral wear of the humeral head from abnormal tracking of the LHBT deep to the LHBT near the articular margin.

Recently elucidated is the limited ability of diagnostic glenohumeral arthroscopy to fully identify the extent of BLC pathology.^1,20-22 Gilmer and colleagues²⁰ found that diagnostic arthroscopy identified only 67% of biceps pathology and underestimated its extent in 56% of patients in their series. Similarly, Moon and colleagues²¹ found that 79% of proximal LHBT tears propagated distally into the bicipital tunnel and were incompletely visualized with standard arthroscopy.

Bicipital Tunnel Lesions

Recent evidence indicates that the bicipital tunnel is a closed space that often conceals space-occupying lesions, including scar, synovitis, loose bodies, and osteophytes, which can become trapped in the tunnel. The functional bottleneck between zones 2 and 3 of the bicipital tunnel explains the aggregation of loose bodies in this region.² Similarly, as the percentage of free space within the bicipital tunnel increases, space-occupying lesions (eg scar, loose bodies, osteophytes) may exude a compressive and/or abrasive force within zones 1 and 2, but not as commonly within zone 3.²

Physical Examination of Biceps-Labrum Complex

Accurate diagnosis of BLC disease is crucial in selecting an optimal intervention, but challenging. Beyond identifying biceps pathology, specific examination maneuvers may help distinguish between lesions of the intra-articular BLC and lesions of the extra-articular bicipital tunnel.²³

Traditional examination maneuvers for biceps-related shoulder pain include the Speed test, the full can test, and the Yergason test.^24,25 For the Speed test, the patient forward-flexes the shoulder to 60° to 90°, extends the arm at the elbow, and supinates the forearm. The clinician applies a downward force as the patient resists. The reported sensitivity of the Speed test ranges from 37% to 63%, and specificity is 60% to 88%.^25,26 In the full can test, with the patient’s arm in the plane of the scapula, the shoulder abducted to 90°, and the forearm in neutral rotation, a downward force is applied against resistance. Sensitivity of the full can test is 60% to 67%, and specificity is 76% to 84%.²⁴ The Yergason test is performed with the patient’s arm at his or her side, the elbow flexed to 90°, and the forearm pronated. The patient supinates the forearm against the clinician’s resistance. Sensitivity of the Yergason test is 19% to 32%, and specificity is 70% to 100%.^25,26 The Yergason test has a positive predictive value of 92% for bicipital tunnel disease.

O’Brien and colleagues^23,26 introduced a “3-pack” physical examination designed to elicit BLC symptoms. In this examination, the LHBT is palpated along its course within the bicipital tunnel. Reproduction of the patient’s pain by palpation had a sensitivity of 98% for bicipital tunnel disease but was less specific (70%). Gill and colleagues²⁷ reported low sensitivity (53%) and low specificity (54%) for biceps palpation, and they used arthroscopy as a gold standard. Since then, multiple studies have demonstrated that glenohumeral arthroscopy fails to identify lesions concealed within the bicipital tunnel.^20-22The second part of the 3-pack examination is the active compression test. A downward force is applied as the patient resists with his or her arm forward-flexed to 90° and adducted 10° to 15° with the thumb pointing downward.²⁸ This action is repeated with the humerus externally rotated and the forearm supinated. A positive test is indicated by reproduction of symptoms with the thumb down, and elimination or reduction of symptoms with the palm up. Test sensitivity is 88% to 96%, and specificity is 46% to 64% for BLC lesions, but for bicipital tunnel disease sensitivity is higher (96%), and the negative predictive value is 93%.²⁶The third component of the 3-pack examination is the throwing test. A late-cocking throwing position is re-created with the shoulder externally rotated and abducted to 90° and the elbow flexed to 90°. The patient steps forward with the contralateral leg and moves into the acceleration phase of throwing while the clinician provides isometric resistance. If this maneuver reproduces pain, the test is positive. As Taylor and colleagues²⁶ reported, the throwing test has sensitivity of 73% to 77% and specificity of 65% to 79% for BLC pathology. This test has moderate sensitivity and negative predictive value for bicipital tunnel disease but may be the only positive test on physical examination in the setting of LHBT instability.

 

Imaging of Biceps-Labrum Complex

Plain anteroposterior, lateral, and axillary radiographs of the shoulder should be obtained for all patients having an orthopedic examination for shoulder pain. Magnetic resonance imaging (MRI) and ultrasound are the advanced modalities most commonly used for diagnostic imaging. These modalities should be considered in conjunction with, not in place of, a comprehensive history and physical examination.

The literature suggests MRI fails to accurately detect many LHBT lesions (Table).^29-37

MRI has sensitivity of 9% to 89% for LHBT pathology^29-37 and 38% to 98% for SLAP pathology.^35,38-41 The wide range of reported sensitivity and specificity might be attributed to the varying criteria for what constitutes a BLC lesion. Some authors include biceps chondromalacia, dynamic incarceration of LHBT, and extra-articular bicipital tunnel lesions, while others historically have included only intra-articular LHBT lesions that can be directly visualized arthroscopically.

In their retrospective review of 277 shoulders with chronic refractory BLC symptoms treated with subdeltoid transfer of the LHBT to the conjoint tendon, Taylor and colleagues³⁰ reported MRI was more sensitive for inside BLC lesions than for junctional or bicipital tunnel lesions (77% vs 43% and 50%, respectively).

Treatment Options for Biceps-Labrum Complex Lesions

A diagnosis of BLC disease warrants a trial of conservative (nonoperative) management for at least 3 months. Many patients improve with activity modification, use of oral anti-inflammatory medication, and structured physical therapy focused on dynamic stabilizers and range of motion. If pain persists, local anesthetic and corticosteroid can be injected under ultrasound guidance into the bicipital tunnel; this injection has the advantage of being both diagnostic and therapeutic. Hashiuchi and colleagues⁴² found ultrasound-guided injections are 87% successful in achieving intra-sheath placement (injections without ultrasound guidance are only 27% successful).

If the 3-month trial of conservative management fails, surgical intervention should be considered. The goal in treating BLC pain is to maximize clinical function and alleviate pain in a predictable manner while minimizing technical demands and morbidity. A singular solution has not been identified. Furthermore, 3 systematic reviews failed to identify a difference between the most commonly used techniques, biceps tenodesis and tenotomy.^43-45 These reviews grouped all tenotomy procedures together and compared them with all tenodesis procedures. A limitation of these systematic reviews is that they did not differentiate tenodesis techniques. We prefer to classify techniques according to whether or not they decompress zones 1 and 2 of the bicipital tunnel.

Bicipital Tunnel Nondecompressing Techniques

Release of the biceps tendon, a biceps tenotomy, is a simple procedure that potentially avoids open surgery and provides patients with a quick return to activity. Disadvantages of tenotomy include cosmetic (Popeye) deformity after surgery, potential cramping and fatigue, and biomechanical changes in the humeral head,^46-48 particularly among patients younger than 65 years. High rates of revision after tenotomy have been reported.^43,49 Incomplete retraction of the LHBT and/or residual synovium may be responsible for refractory pain following biceps tenotomy.⁴⁹ We hypothesize that failure of tenotomy may be related to unaddressed bicipital tunnel disease.

Proximal nondecompressing tenodesis techniques may be performed either on soft tissue in the interval or rotator cuff or on bone at the articular margin or within zone 1 of the bicipital tunnel.^50-52 These techniques can be performed with standard glenohumeral arthroscopy and generally are fast and well tolerated and have limited operative morbidity. Advantages of these techniques over simple tenotomy are lower rates of cosmetic deformity and lower rates of cramping and fatigue pain, likely resulting from maintenance of the muscle tension relationship of the LHBT. Disadvantages of proximal tenodesis techniques include introduction of hardware for bony fixation, longer postoperative rehabilitation to protect repairs, and failure to address hidden bicipital tunnel disease. Furthermore, the rate of stiffness in patients who undergo proximal tenodesis without decompression of the bicipital tunnel may be as high as 18%.⁵³

Bicipital Tunnel Decompressing Techniques

Surgical techniques that decompress the bicipital tunnel include proximal techniques that release the bicipital sheath within zones 1 and 2 of the bicipital tunnel (to the level of the proximal margin of the pectoralis major tendon) and certain arthroscopic suprapectoral techniques,⁵⁴ open subpectoral tenodeses,^55-57 and arthroscopic transfer of the LHBT to the conjoint tendon.^58,59

Open subpectoral tenodesis techniques have the advantage of maintaining the length-tension relationship of the LHBT and preventing Popeye deformity. However, these techniques require making an incision near the axilla, which may introduce an unnecessary source of infection. Furthermore, open subpectoral tenodesis requires drilling the humerus and placing a screw for bony fixation of the LHBT, which can create a risk of neurovascular injury, given the proximity of neurovascular structures,^60-62 and humeral shaft fracture, particularly in athletes.^63,64Our preferred method is transfer of the LHBT to the conjoint tendon (Figure 3).⁵⁹

The subdeltoid space is a large, relatively avascular fascial plane bounded superiorly by the acromion and coracoacromial ligament, medially by the coracoid and conjoint tendon, inferiorly by the musculotendinous insertion of the pectoralis major, and laterally by the border of the humerus.⁶⁵ After the LHBT is released from the superior labrum, it is transferred to the subdeltoid space and sutured to the conjoint tendon in side-to-side fashion with nonabsorbable sutures.^58,59 This technique allows for isometric tensioning of the LHBT, which preserves the strength of the biceps muscle, and fixation of soft tissue to soft tissue obviates the need for bone tunnels, mitigating fracture risk. A histologic study that compared healing between LHBT tenodesis with bone and soft-tissue transfer to the conjoint tendon found a more robust response of tenomodulin in the soft-tissue transfer, suggesting tendon regeneration in this technique.⁶⁶ Perhaps the most significant advantage is the ability of this approach to effectively decompress the bicipital tunnel. Early-term results were promising, and recent midterm results demonstrated durability of clinical outcomes.^58,59Sanders and colleagues⁴⁹ compared revision rates of biceps procedures and found a 6.8% rate for techniques that released the biceps sheath and a 20.6% rate for operations in which the sheath was not released. Subsequent meta-analysis of 30 studies (1881 patients) found improved Constant scores in the cohort that underwent bicipital tunnel decompression in comparison with the cohort that did not have the bicipital tunnel decompressed, but there was no significant difference in UCLA (University of California Los Angeles) scores between cohorts.67 

In light of recent literature that confirms the prevalence of bicipital tunnel lesions that have been overlooked, and the power of physical examination, we have proposed an evidence-based approach to diagnosing and managing BLC disease (Figure 4).

 

Am J Orthop. 2016;45(7):E503-E511. Copyright Frontline Medical Communications Inc. 2016. All rights reserved.

Pathology of the biceps-labrum complex (BLC) can be an important source of shoulder pain. Discussion of pathoanatomy, imaging, and surgical intervention is facilitated by distinguishing the anatomical zones of the BLC: inside, junction, and bicipital tunnel (extra-articular), parts of which cannot be visualized with standard diagnostic arthroscopy.

The recent literature indicates that bicipital tunnel lesions are common and perhaps overlooked. Systematic reviews suggest improvement in outcomes of BLC operations when the bicipital tunnel is decompressed. Higher-level clinical and basic science studies are needed to fully elucidate the role of the bicipital tunnel, but it is evident that a comprehensive physical examination and an understanding of the limits of advanced imaging are necessary to correctly diagnose and treat BLC-related shoulder pain.

Anatomy of Biceps-Labrum Complex

The long head of the biceps tendon (LHBT) and the glenoid labrum work as an interdependent functional unit, the biceps-labrum complex (BLC). The BLC is divided into 3 distinct anatomical zones: inside, junction, and bicipital tunnel.^1,2

Inside

The inside includes the superior labrum and biceps attachment. The LHBT most commonly originates in the superior labrum.^3-5 Vangsness and colleagues³ described 4 types of LHBT origins: Type I biceps attaches solely to the posterior labrum, type II predominantly posterior, type III equally to the anterior and posterior labrum, and type IV mostly to the anterior labrum. The LHBT can also originate in the supraglenoid tubercle or the inferior border of the supraspinatus.^3,6

Junction

Junction is the intra-articular segment of the LHBT and the biceps pulley. The LHBT traverses the glenohumeral joint en route to the extra-articular bicipital tunnel.² The LHBT is enveloped in synovium that extends into part of the bicipital tunnel.² The intra-articular segment of the LHBT is about 25 mm in length⁷ and has a diameter of 5 mm to 6 mm.⁸

A cadaveric study found that the average length of the LHBT that can be arthroscopically visualized at rest is 35.6 mm, or only 40% of the total length of the LHBT with respect to the proximal margin of the pectoralis major tendon.¹ When the LHBT was pulled into the joint, more tendon (another 14 mm) was visualized.¹ Therefore, diagnostic arthroscopy of the glenohumeral joint visualizes about 50% of the LHBT.⁹The morphology of the LHBT varies by location. The intra-articular portion of the LHBT is wide and flat, whereas the extra-articular portion is round.⁸ The tendon becomes smoother and more avascular as it exits the joint to promote gliding within its sheath in the bicipital groove.¹⁰ The proximal LHBT receives its vascular supply from superior labrum tributaries, and distally the LHBT is supplied by ascending branches of the anterior humeral circumflex artery.⁴ There is a hypovascular zone, created by this dual blood supply, about 12 mm to 30 mm from the LHBT origin, predisposing the tendon to rupture or fray in this region.¹¹The LHBT makes a 30° turn into the biceps pulley system as it exits the glenohumeral joint. The fibrous pulley system that stabilizes the LHBT in this region has contributions from the coracohumeral ligament, the superior glenohumeral ligament, and the supraspinatus tendon.^12-14

The floor of the pulley consists of the superior glenohumeral ligament with reinforcing fibers from the superior border of the subscapularis tendon.¹⁵ The roof consists of the coracohumeral ligament fibers with supraspinatus fibers contributing posteriorly (Figure 1).¹²

Bicipital Tunnel

The bicipital tunnel, the third portion of the BLC, remains largely hidden from standard diagnostic glenohumeral arthroscopy. The bicipital tunnel is an extra-articular, closed space that constrains the LHBT from the articular margin through the subpectoral region.²

The bicipital tunnel itself can be divided into 3 zones (Figure 2).²

Zone 1 is the traditional bicipital groove or “bony groove” that extends from the articular margin to the distal margin of the subscapularis tendon. The floor consists of a deep osseous groove covered by a continuation of subscapularis tendon fibers and periosteum.²Zone 2, “no man’s land,” extends from the distal margin of the subscapularis tendon to the proximal margin of the pectoralis major (PMPM). The LHBT in this zone cannot be visualized during a pull test at arthroscopy, yet lesions commonly occur here.¹ Zones 1 and 2 have a similar histology and contain synovium.²Zone 3 is the subpectoral region distal to the PMPM. Fibers of the latissimus dorsi form the flat floor of zone 3, and the pectoralis major inserts lateral to the LHBT on the humerus in this zone. The synovium encapsulating the LHBT in zones 1 and 2 rarely extends past the PMPM. Taylor and colleagues² found a higher percentage of unoccupied tunnel space in zone 3 than in zones 1 and 2, which results in a “functional bottleneck” between zones 2 and 3 represented by the PMPM.

 

Pathoanatomy

BLC lesions may occur in isolation or concomitantly across multiple anatomical zones. In a series of 277 chronically symptomatic shoulders that underwent transfer of the LHBT to the conjoint tendon with subdeltoid arthroscopy, Taylor and colleagues¹ found 47% incidence of bicipital tunnel lesions, 44% incidence of junctional lesions, and 35% incidence of inside lesions. In their series, 37% of patients had concomitant lesions involving more than 1 anatomical zone.

Inside Lesions

Inside lesions involve the superior labrum, the LHBT origin, or both. Superior labrum anterior-posterior (SLAP) tears are included as inside BLC lesions. Snyder and colleagues¹⁶ originally identified 4 broad categories of SLAP tears, but Powell and colleagues¹⁷ described up to 10 variations. Type II lesions, which are the most common, destabilize the biceps anchor.

Dynamic incarceration of the biceps between the humeral head and the glenoid labrum is another inside lesion that can be identified during routine diagnostic glenohumeral arthroscopy. The arthroscopic active compression test, as described by Verma and colleagues,¹⁸ can be used during surgery to demonstrate incarceration of the biceps tendon.

Medial biceps chondromalacia, attritional chondral wear along the anteromedial aspect of the humeral head, occurs secondary to a windshield wiper effect of the LHBT in the setting of an incarcerating LHBT or may be associated with destabilization of the biceps pulley.

Junctional Lesions

Junctional lesions, which include lesions that affect the intra-articular LHBT, can be visualized during routine glenohumeral arthroscopy. They include partial and complete biceps tears, biceps pulley lesions, and junctional biceps chondromalacia.

Biceps pulley injuries and/or tears of the upper subscapularis tendon can destabilize the biceps as it exits the joint, and this destabilization may result in medial subluxation of the tendon and the aforementioned medial biceps chondromalacia.^10,19 Junctional biceps chondromalacia is attritional chondral wear of the humeral head from abnormal tracking of the LHBT deep to the LHBT near the articular margin.

Recently elucidated is the limited ability of diagnostic glenohumeral arthroscopy to fully identify the extent of BLC pathology.^1,20-22 Gilmer and colleagues²⁰ found that diagnostic arthroscopy identified only 67% of biceps pathology and underestimated its extent in 56% of patients in their series. Similarly, Moon and colleagues²¹ found that 79% of proximal LHBT tears propagated distally into the bicipital tunnel and were incompletely visualized with standard arthroscopy.

Bicipital Tunnel Lesions

Recent evidence indicates that the bicipital tunnel is a closed space that often conceals space-occupying lesions, including scar, synovitis, loose bodies, and osteophytes, which can become trapped in the tunnel. The functional bottleneck between zones 2 and 3 of the bicipital tunnel explains the aggregation of loose bodies in this region.² Similarly, as the percentage of free space within the bicipital tunnel increases, space-occupying lesions (eg scar, loose bodies, osteophytes) may exude a compressive and/or abrasive force within zones 1 and 2, but not as commonly within zone 3.²

Physical Examination of Biceps-Labrum Complex

Accurate diagnosis of BLC disease is crucial in selecting an optimal intervention, but challenging. Beyond identifying biceps pathology, specific examination maneuvers may help distinguish between lesions of the intra-articular BLC and lesions of the extra-articular bicipital tunnel.²³

Traditional examination maneuvers for biceps-related shoulder pain include the Speed test, the full can test, and the Yergason test.^24,25 For the Speed test, the patient forward-flexes the shoulder to 60° to 90°, extends the arm at the elbow, and supinates the forearm. The clinician applies a downward force as the patient resists. The reported sensitivity of the Speed test ranges from 37% to 63%, and specificity is 60% to 88%.^25,26 In the full can test, with the patient’s arm in the plane of the scapula, the shoulder abducted to 90°, and the forearm in neutral rotation, a downward force is applied against resistance. Sensitivity of the full can test is 60% to 67%, and specificity is 76% to 84%.²⁴ The Yergason test is performed with the patient’s arm at his or her side, the elbow flexed to 90°, and the forearm pronated. The patient supinates the forearm against the clinician’s resistance. Sensitivity of the Yergason test is 19% to 32%, and specificity is 70% to 100%.^25,26 The Yergason test has a positive predictive value of 92% for bicipital tunnel disease.

O’Brien and colleagues^23,26 introduced a “3-pack” physical examination designed to elicit BLC symptoms. In this examination, the LHBT is palpated along its course within the bicipital tunnel. Reproduction of the patient’s pain by palpation had a sensitivity of 98% for bicipital tunnel disease but was less specific (70%). Gill and colleagues²⁷ reported low sensitivity (53%) and low specificity (54%) for biceps palpation, and they used arthroscopy as a gold standard. Since then, multiple studies have demonstrated that glenohumeral arthroscopy fails to identify lesions concealed within the bicipital tunnel.^20-22The second part of the 3-pack examination is the active compression test. A downward force is applied as the patient resists with his or her arm forward-flexed to 90° and adducted 10° to 15° with the thumb pointing downward.²⁸ This action is repeated with the humerus externally rotated and the forearm supinated. A positive test is indicated by reproduction of symptoms with the thumb down, and elimination or reduction of symptoms with the palm up. Test sensitivity is 88% to 96%, and specificity is 46% to 64% for BLC lesions, but for bicipital tunnel disease sensitivity is higher (96%), and the negative predictive value is 93%.²⁶The third component of the 3-pack examination is the throwing test. A late-cocking throwing position is re-created with the shoulder externally rotated and abducted to 90° and the elbow flexed to 90°. The patient steps forward with the contralateral leg and moves into the acceleration phase of throwing while the clinician provides isometric resistance. If this maneuver reproduces pain, the test is positive. As Taylor and colleagues²⁶ reported, the throwing test has sensitivity of 73% to 77% and specificity of 65% to 79% for BLC pathology. This test has moderate sensitivity and negative predictive value for bicipital tunnel disease but may be the only positive test on physical examination in the setting of LHBT instability.

 

Imaging of Biceps-Labrum Complex

Plain anteroposterior, lateral, and axillary radiographs of the shoulder should be obtained for all patients having an orthopedic examination for shoulder pain. Magnetic resonance imaging (MRI) and ultrasound are the advanced modalities most commonly used for diagnostic imaging. These modalities should be considered in conjunction with, not in place of, a comprehensive history and physical examination.

The literature suggests MRI fails to accurately detect many LHBT lesions (Table).^29-37

MRI has sensitivity of 9% to 89% for LHBT pathology^29-37 and 38% to 98% for SLAP pathology.^35,38-41 The wide range of reported sensitivity and specificity might be attributed to the varying criteria for what constitutes a BLC lesion. Some authors include biceps chondromalacia, dynamic incarceration of LHBT, and extra-articular bicipital tunnel lesions, while others historically have included only intra-articular LHBT lesions that can be directly visualized arthroscopically.

In their retrospective review of 277 shoulders with chronic refractory BLC symptoms treated with subdeltoid transfer of the LHBT to the conjoint tendon, Taylor and colleagues³⁰ reported MRI was more sensitive for inside BLC lesions than for junctional or bicipital tunnel lesions (77% vs 43% and 50%, respectively).

Treatment Options for Biceps-Labrum Complex Lesions

A diagnosis of BLC disease warrants a trial of conservative (nonoperative) management for at least 3 months. Many patients improve with activity modification, use of oral anti-inflammatory medication, and structured physical therapy focused on dynamic stabilizers and range of motion. If pain persists, local anesthetic and corticosteroid can be injected under ultrasound guidance into the bicipital tunnel; this injection has the advantage of being both diagnostic and therapeutic. Hashiuchi and colleagues⁴² found ultrasound-guided injections are 87% successful in achieving intra-sheath placement (injections without ultrasound guidance are only 27% successful).

If the 3-month trial of conservative management fails, surgical intervention should be considered. The goal in treating BLC pain is to maximize clinical function and alleviate pain in a predictable manner while minimizing technical demands and morbidity. A singular solution has not been identified. Furthermore, 3 systematic reviews failed to identify a difference between the most commonly used techniques, biceps tenodesis and tenotomy.^43-45 These reviews grouped all tenotomy procedures together and compared them with all tenodesis procedures. A limitation of these systematic reviews is that they did not differentiate tenodesis techniques. We prefer to classify techniques according to whether or not they decompress zones 1 and 2 of the bicipital tunnel.

Bicipital Tunnel Nondecompressing Techniques

Release of the biceps tendon, a biceps tenotomy, is a simple procedure that potentially avoids open surgery and provides patients with a quick return to activity. Disadvantages of tenotomy include cosmetic (Popeye) deformity after surgery, potential cramping and fatigue, and biomechanical changes in the humeral head,^46-48 particularly among patients younger than 65 years. High rates of revision after tenotomy have been reported.^43,49 Incomplete retraction of the LHBT and/or residual synovium may be responsible for refractory pain following biceps tenotomy.⁴⁹ We hypothesize that failure of tenotomy may be related to unaddressed bicipital tunnel disease.

Proximal nondecompressing tenodesis techniques may be performed either on soft tissue in the interval or rotator cuff or on bone at the articular margin or within zone 1 of the bicipital tunnel.^50-52 These techniques can be performed with standard glenohumeral arthroscopy and generally are fast and well tolerated and have limited operative morbidity. Advantages of these techniques over simple tenotomy are lower rates of cosmetic deformity and lower rates of cramping and fatigue pain, likely resulting from maintenance of the muscle tension relationship of the LHBT. Disadvantages of proximal tenodesis techniques include introduction of hardware for bony fixation, longer postoperative rehabilitation to protect repairs, and failure to address hidden bicipital tunnel disease. Furthermore, the rate of stiffness in patients who undergo proximal tenodesis without decompression of the bicipital tunnel may be as high as 18%.⁵³

Bicipital Tunnel Decompressing Techniques

Surgical techniques that decompress the bicipital tunnel include proximal techniques that release the bicipital sheath within zones 1 and 2 of the bicipital tunnel (to the level of the proximal margin of the pectoralis major tendon) and certain arthroscopic suprapectoral techniques,⁵⁴ open subpectoral tenodeses,^55-57 and arthroscopic transfer of the LHBT to the conjoint tendon.^58,59

Open subpectoral tenodesis techniques have the advantage of maintaining the length-tension relationship of the LHBT and preventing Popeye deformity. However, these techniques require making an incision near the axilla, which may introduce an unnecessary source of infection. Furthermore, open subpectoral tenodesis requires drilling the humerus and placing a screw for bony fixation of the LHBT, which can create a risk of neurovascular injury, given the proximity of neurovascular structures,^60-62 and humeral shaft fracture, particularly in athletes.^63,64Our preferred method is transfer of the LHBT to the conjoint tendon (Figure 3).⁵⁹

The subdeltoid space is a large, relatively avascular fascial plane bounded superiorly by the acromion and coracoacromial ligament, medially by the coracoid and conjoint tendon, inferiorly by the musculotendinous insertion of the pectoralis major, and laterally by the border of the humerus.⁶⁵ After the LHBT is released from the superior labrum, it is transferred to the subdeltoid space and sutured to the conjoint tendon in side-to-side fashion with nonabsorbable sutures.^58,59 This technique allows for isometric tensioning of the LHBT, which preserves the strength of the biceps muscle, and fixation of soft tissue to soft tissue obviates the need for bone tunnels, mitigating fracture risk. A histologic study that compared healing between LHBT tenodesis with bone and soft-tissue transfer to the conjoint tendon found a more robust response of tenomodulin in the soft-tissue transfer, suggesting tendon regeneration in this technique.⁶⁶ Perhaps the most significant advantage is the ability of this approach to effectively decompress the bicipital tunnel. Early-term results were promising, and recent midterm results demonstrated durability of clinical outcomes.^58,59Sanders and colleagues⁴⁹ compared revision rates of biceps procedures and found a 6.8% rate for techniques that released the biceps sheath and a 20.6% rate for operations in which the sheath was not released. Subsequent meta-analysis of 30 studies (1881 patients) found improved Constant scores in the cohort that underwent bicipital tunnel decompression in comparison with the cohort that did not have the bicipital tunnel decompressed, but there was no significant difference in UCLA (University of California Los Angeles) scores between cohorts.67 

In light of recent literature that confirms the prevalence of bicipital tunnel lesions that have been overlooked, and the power of physical examination, we have proposed an evidence-based approach to diagnosing and managing BLC disease (Figure 4).

 

Am J Orthop. 2016;45(7):E503-E511. Copyright Frontline Medical Communications Inc. 2016. All rights reserved.