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Quantitative analysis of attachment of the labrum to the glenoid fossa: a cadaveric study
J Orthop Sci (2015) 20:823–829 DOI 10.1007/s00776-015-0742-4
ORIGINAL ARTICLE
Quantitative analysis of attachment of the labrum to the glenoid fossa: a cadaveric study Masahito Yoshida1 · Hideyuki Goto1 · Masahiro Nozaki1 · Yasuhiro Nishimori1 · Tetsuya Takenaga1 · Atsunori Murase1 · Yuko Nagaya1 · Hirotaka Iguchi2 · Masaaki Kobayashi1 · Katsumasa Sugimoto3 · Takeshi Nishiyama4 · Takanobu Otsuka1
Received: 2 June 2014 / Accepted: 4 June 2015 / Published online: 14 July 2015 © The Japanese Orthopaedic Association 2015
Abstract Purpose This study investigated the direct and continuous attachment of the labrum to the glenoid fossa, including the fibrocartilaginous tissue, using image-analysis software and histology. Methods Twenty-six cadaveric shoulders (11 male, 15 female; mean age 80.1 years; age range 36–103 years) were used. The glenoid of each specimen was divided into six pie-slice-shaped pieces from the center perpendicular to the articular surface by radial incisions at the 2, 4, 6, 8, 10, and 12 o’clock positions. The general distribution of the labrum, including the fibrocartilage, was assessed in hematoxylin and eosin-, Safranin O- and Azan-Mallory-stained sections. The continuous length of attachment of the labrum to the glenoid was measured using image-analysis software. The width of attachment to the articular surface of the glenoid was assessed in each position. Results The labrum attached to both the articular surface and the neck of the glenoid in all shoulders (100 %) in the 4 and 6 o’clock positions. The mean length of the entire attachment to the glenoid was 4.6 mm (range 3.2–6.1 mm). The width of attachment from the bony edge of the glenoid to the edge of the labrum on the articular surface
* Hideyuki Goto hide‑[email protected]‑net.ne.jp 1
Department of Orthopedic Surgery, Graduate School of Medical Sciences, Nagoya City University, 1 Kawasumi, Mizuho‑cho, Mizuho‑ku, Nagoya, Aichi 467‑8601, Japan
2
Department of Arthroplastic Medicine, Graduate School of Medical Sciences, Nagoya City University, Nagoya, Japan
3
Nagoya Sports Clinic, Nagoya, Japan
4
Department of Public Health, Aichi Medical University, Nagakute, Japan
ranged from 0 to 4.3 mm. The length of the entire attachment of the labrum was shortest in the 2 o’clock position (p = 0.229). Additionally, the length of the entire attachment of the labrum was longest in the 4 o’clock position. The width of attachment to the articular surface of the glenoid was greatest in the 4 o’clock position (p < 0.01). Conclusion In the 4 and 6 o’clock positions, the labrum attached to both the articular surface and neck of the glenoid in all of the shoulders (100 %). The length of the entire attachment to the labrum, including the fibrocartilage, was shortest in the 2 o’clock position. The width of attachment to the articular surface of the glenoid was greatest in the 4 o’clock position (p < 0.01).
Introduction The glenoid labrum is a peripherally elevated tissue surrounding the edge of the glenoid fossa [1], which stabilizes the glenohumeral joint by adding depth to the glenoid cavity [2, 3]. Studies have demonstrated that the glenoid labrum consists of a circumferential fibrocartilaginous structure, which functions as connective tissue and acts as a part of the labrum itself [3–9]. Prodromos et al. demonstrated the presence of a fibrocartilaginous matrix within the labrum, which varied from being homogeneous to fibrous and contained chondrocytes in lacunae [9]. Ockert et al. investigated the size and morphology of this fibrocartilaginous part of the glenoid labrum, which mainly comprises collagen type II [8]. Given the regional difference of the labrum, there are some characteristic injuries such as Bankart lesions, superior labrum anterior and posterior (SLAP) lesions, reverse Bankart lesions, and circumferential detachment of the labrum. Bankart lesions, which involve exfoliation of the
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labrum from the glenoid in the anterior-inferior area, are major causes of recurrent dislocation of the shoulder and include the origin of the inferior glenohumeral ligament [2]. SLAP lesions, which involve labrum detachment from the superior area of the glenoid, are frequent in overhead athletes [1, 10, 11]. Reverse Bankart lesions are a major cause of posterior dislocation and are associated with detachment of the labrum in the posterior area of the glenoid [12, 13]. Successful outcomes of surgical repair for these injuries require a sound understanding of the anatomical variations of the labrum, which depend on the region. Several authors have described variations in the attachment, histology, and shape of the labrum depending on the location in the glenoid [3–5, 7, 14, 15]. A few previous studies have evaluated the length of attachment of the fibrous tissue of the labrum to the cartilage and the glenoid bone; however, these studies either approximated the length macroscopically or calculated the value as a straight line under light microscopy [6, 16, 17]. The present study investigated the direct and continuous length of the attachment of the labrum to the glenoid, which comprises fibrocartilaginous and fibrous tissues according to histological analysis. We hypothesized that the length of direct attachment of the labrum would demonstrate regional variations and that further diversity would be present in terms of the attachment of the labrum, including the fibrocartilaginous tissue, to the articular side of the glenoid.
Methods This study has been approved by the research ethics committee of Nagoya City University (no. 1060). Twentysix adult fresh cadaveric shoulders (11 male, 15 female; mean age 80.1 years; age range 36–103 years) were used for this study. Only those with no history of complaints or dysfunction were included. The skin, rotator cuff muscles, and coracoid process were resected from the scapula. The capsule, tendon of the long head of the biceps brachii, glenohumeral ligaments, and glenoid labrum were left intact. After macroscopic observation, all specimens were fixed in 10 % formaldehyde and decalcified with 10 % formic acid. The glenoid of each specimen was divided into six pie-slice-shaped pieces from the center of the glenoid perpendicular to the articular surface by radial incision at the 2, 4, 6, 8, 10, and 12 o’clock positions (Fig. 1a). The superior and inferior intersection of the long axis of the glenoid and the circumference of the glenoid circle were defined as the 12 o’clock and 6 o’clock position, respectively. The glenoid positions in this study were expressed as per the right shoulder. All the measurements were done for each section at the 2, 4, 6, 8, 10, and 12 o’clock positions. To identify the fibrous tissue of the labrum, hyaline
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Fig. 1 Tissue preparation. a The glenoid was divided into six pieslice-shaped pieces. b Cross-sectional area of the labrum and glenoid
cartilage, and fibrocartilaginous area (FCA), each specimen was embedded in paraffin (Fig. 1b) and stained with hematoxylin and eosin (H&E; Fig. 2a), Azan-Mallory (Fig. 2b), and Safranin-O (Fig. 2c). The general distribution of the labrum was assessed in sections stained with H&E, including the fibrocartilage. The outer edge between the fibrous labrum and capsule was defined by the density of elastic fibers in Azan-Mallory sections. The FCA and hyaline cartilage were defined by the staining density of Safranin-O. After assessing the differentiation between the FCA and the fibrous labrum tissues, both areas were measured on microscopic images using Image J version 1.40 software (National Institutes of Health, Rockville Pike, Bethesda, MD, USA; Fig. 3a). The direct length of the attachment of the labrum, including both fibrocartilaginous tissue and the fibrous labrum, to the glenoid was measured as a curved line using this software (Fig. 3b). The attachment sites of the labrum to the glenoid were determined histologically. The border between the layers of cartilage and bone tissues was distinguished, and the point of abrupt change was defined as the bony edge (arrowhead; Fig. 4a, b). The attachment of the labrum to the bony edge of the glenoid was observed under light microscopy at each position and classified into two morphological types. In the first, the labrum attachment extended beyond the bony edge of the glenoid and included not only the glenoid neck but also the articular surface (Fig. 4a). In the second, the attachment was found only within the glenoid neck and did not extend toward the articular surface of the glenohumeral joint (Fig. 4b). In addition, two of the three investigators assessed the histological attachment pattern of the labrum to the glenoid (that is, whether it extended to the articular surface of the glenoid). The length from the bony edge of the glenoid to the end of the labrum attachment to the articular surface was assessed as a straight line parallel to the surface (Fig. 5). When the attachment was limited only to the glenoid rim, its length was defined as 0 mm.
Quantitative analysis of attachment of the labrum to the glenoid fossa…
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Fig. 2 Methods of tissue staining. Photographic images of the histology of a cross-section of the glenoid in the 4 o’clock position. There was wide attachment between the labrum and the glenoid. a Hematoxylin and eosin (H&E), b Safranin-O, and c Azan-Mallory staining
Fig. 3 Histological specimen stained with Safranin-O. Labrum attachment to the glenoid in the 4 o’clock position. a The sizes of the fibrocartilaginous area (FCA) and fibrous labrum (FL) within the labrum were measured separately at each position from 12 to 10
o’clock, using Image J software; b the length of the entire labrum attachment (black arrow) to the glenoid was also measured by the same software. C capsule, G glenoid, AC articular cartilage, FCA fibrocartilage area, FL fibrous labrum
The intraobserver reliability was evaluated based on the correlation coefficients of two repeated measurements with an interval of 3 months. The mean length obtained from three measurements made by a single observer for each task was used in the analysis. Repeated-measures analysis of variance (ANOVA) was used to compare data from different regions of the labrum. Values of p < 0.05 were considered statistically significant. All analyses were performed using open-source statistical computing software (R package; http://www.r-project.org/).
anterior-superior position to 6.9 mm2 (2.4–13.6 mm2; SD, 2.4 mm2) in the posterior-inferior (8 o’clock) position. The ratio of the FCA to the entire labrum, including both fibrous and fibrocartilaginous tissue, ranged from 15.6 to 25.6 % in eachregion (Table 1). The mean length of attachment of the entire labrum was 4.6 mm (2.0–11.4 mm; SD, 1.6 mm). The attachment in the anterior-superior (2 o’clock) area was 3.2 mm (2.0–5.2 mm; SD, 0.8 mm), which was significantly shorter than in the other areas (p < 0.05; Fig. 6). The attachment in the anterior-inferior area (4 o’clock) was 6.1 mm (4.0– 11.4 mm; SD, 1.7 mm), which was significantly longer than in the other areas (p < 0.05; Fig. 6). The proportion in which the attachment reached the articular surface of the glenoid (type B) was 100 % in both the anterior-inferior (4 o’clock) and inferior (6 o’clock)
Results The mean size of the FCA ranged from 3.1 mm2 [0.6– 7.0 mm2; standard deviation (SD), 1.6 mm2] in the
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Fig. 4 Histological specimen stained with Safranin-O. Types of attachment of the labrum to the glenoid. a The attachment of the labrum (black arrow) to the glenoid in most locations in each shoulder extended to both the articular cartilage and the bony neck, including the bony edge of the scapula (black arrowhead). b The attach-
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ment of the labrum was limited to the bone of the glenoid neck. White line, the bony surface of the glenoid; white dotted line, perpendicular line to the bony surface of the glenoid from the bony edge of the glenoid
the edge of the labrum attachment to the articular surface ranged from 0 to 4.3 mm. A significant difference was found in the anterior-inferior (4 o’clock) and inferior (6 o’clock) regions compared with the others (12, 2, 8, and 10 o’clock; p < 0.01). Significant differences were also noted between the attachments in the anterior-inferior and inferior regions (p = 0.048; Fig. 8). The intraobserver correlation coefficients of repeated measurements for the length of attachment and the size of the labrum were 0.961 and 0.981, respectively, demonstrating excellent reproducibility.
Discussion Fig. 5 Histological specimen stained with Safranin-O. The labrum attachment to the glenoid in the 8 o’clock position. Measurement of the attachment of the labrum on the articular surface side (black arrow). From the bony edge of the glenoid (black arrow head), the average width of the attachment was determined in six positions. L, Labrum; white line, the bony surface of the glenoid; white dotted line, perpendicular line to the bony surface of the glenoid from the edge of the labrum attachment
areas, and the proportion in all other areas, with the exception of the superior (12 o’clock) area, was more than 80 % (Fig. 7). The length from the bony edge of the glenoid to
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The glenoid labrum has been defined as the fibrocartilaginous tissue positioned around the glenoid articular surface, consisting largely of collagen fibers [4, 7]. Several authors have demonstrated that fibrocartilage connects the fibrous tissue of the labrum with the bony tissue of the glenoid, and it has been considered to represent the labrum itself [3–9]. Prodromos et al. demonstrated that Safranin-O staining of the fibrocartilage for proteoglycans was mostly absent in the capsule and was intermediate between that of the fibrous capsule and the articular cartilage in the glenoid labrum [9]. Here, we used Safranin-O staining to evaluate the FCA connecting the articular cartilage of the glenoid with the fibrous
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Quantitative analysis of attachment of the labrum to the glenoid fossa… Table 1 Mean size of the fibrocartilage and fibrous labrum in each clockwise positions Location
Mean size of fibrocartilage (mm2)
Mean size of fibrous labrum (mm2)
Rate of fibrocatilgage in labrun (%)
Superior area (12 o’clock) Anterior-superior area (2 o’clock) Anterior-inferior area (4 o’clock) Inferior area (6 o’clock) Posterior-inferior area (8 o’clock)
5.5 ± 1.6 (3.2–9.3) 3.1 ± 1.6 (0.6–7.0) 6.8 ± 2.6 (2.9–127) 7.2 ± 2.9 (3.9–15.0) 6.9 ± 2.4 (2.4–13.6)
24.4 ± 6.8 (15.7–40) 21.3 ± 7.7 (11.7–38.9) 40.9 ± 20 (23.8–77.6) 39.9 ± 9.0 (24.6–58.5) 31.6 ± 8.6 (23.7–59.2)
22.5 (10.6–40) 15 (8.3–28.7) 17.6 (5.1–27.9) 20.3 (11.4–26.2) 26.9 (11.6–40)
Posterior-superior area (10 o’clock)
5.4 ± 2.3 (2.2–11.6)
30.7 ± 6.3 (22.5–43.2)
17.9 (8.2–30.2)
Fig. 6 Mean attachment of the labrum to the glenoid in each clockwise position. (*p < 0.05)
Fig. 7 Rate of attachment type of the labrum to articular cartilage and bony glenoid neck
tissue. In addition, we used Azan-Mallory staining to distinguish between the fibrous labrum and the capsule. The current study revealed the average distribution of the fibrocartilage within the entire labrum to be 19.6 % in the 12, 2, 4, 6, 8, and 10 o’clock positions. By contrast, Bain reported the average distribution of the fibrocartilage to be higher at 28 % in the 12, 2, 3, 4, 6, and 9 o’clock positions in a cadaveric study based on collage type IIlabeling of sections. This difference might have been due to
Fig. 8 Mean width of the attachment of the labrum on the articular surface of the glenoid in each clockwise position. The width of the attachment was significantly greater in the 4 and 6 o’clock positions than in the other positions (**p < 0.01) and significantly smaller at the 6 o’clock position than in the 4 o’clock position (*p < 0.05)
the different measurement techniques used, which mainly focused on proteoglycan staining with Safranin-O. In addition, the results of our study might have been affected by age-related histopathological changes of the glenoid labrum, which might cause the degeneration of the labrum [18, 19]. Degenerative changes to the labrum lead to a decrease in fibrocartilage, which includes proteoglycan, and an increase in the fibrous tissue of the labrum. Several studies have described variable morphology of the glenoid and the patterns of labrum attachment around the rim [3, 4, 5, 6, 7, 14, 15, 17]. Detrisac and Johnson classified several labrum shapes as normal anatomical variants [21]. Cooper et al. reported that the morphology of the labrum and capsule differed in its superior and inferior regions; they found that the inferior part of the labrum and capsule was usually a round, elevated, fibrous structure that was firmly attached to the glenoid, whereas the superior part of the labrum and capsule tended to be meniscal in appearance, more loosely attached to the glenoid, and mobile [5]. Itoigawa et al. reported that the rate of attachment of the anterior-inferior glenohumeral ligament-labrum
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complex (AIGHL-LC) to the articular cartilage and neck of the glenoid was 86.7 % in the 2 o’clock position and 88.3 % in the 4 o’clock position, using histological specimens stained with toluidine blue [17]. In our current study, the corresponding rates were 88.9 % in the 2 o’clock position and 100 % in the 4 o’clock position, respectively. The difference in these results might have been caused by the different staining method used for evaluating the fibrocartilaginous tissue. However, our results showed that the attachment of the labrum in the inferior parts (the 4, 6, and 8 o’clock positions) extended to the glenoid surface in more than 90 % of cases. These results are consistent with Cooper’s studies that showed wide attachment of the labrum in the inferior area of the glenoid. Huber et al. demonstrated that the width of attachment to the glenoid in each region ranged from 4.6 mm (1.9 mm on the articular side) in the posterior region to 10.7 mm (4.7 mm on the articular side) in the inferior region [5]. Itoigawa reported values of 4.7 mm (1.6 mm on the articular side) in the anterior-superior (2 o’clock) direction and 8.4 mm (3.0 mm on the articular side) in the anterior-inferior (4 o’clock) direction [17]. These studies divided the original attachment into two parts and evaluated them as straight lines using calipers or digital calipers. By contrast, the attachment in our current study ranged from 3.2 mm (0.9 mm on the articular side) in the anterior-superior (2 o’clock) position to 6.0 mm (2.5 mm on the articular side) in the anterior-inferior (4 o’clock) position, giving relatively shorter lengths at each position. This variation was attributed to the different measurement techniques used in the two studies. Our measurement is not macroscopic, but microscopic, based on histological differences between the labrum, cartilage and fibrous tissues. Additionally, we measured the attachment as a curved and continuous line and defined the labrum as a complex of fibrous tissue and the FCA. In the anterior-superior area, the length of the labrum attachment was significantly shorter in the 2 o’clock position than in the other positions, although it was present in all cases. This result was consistent with previous reports demonstrating that the labrum in this area was attached more narrowly. Williams demonstrated that there are some normal variations in the anterior-superior glenoid quadrant, such as a cord-like MGHL and no anterior-superior labral tissue and sublabral foramen. These normal variations could have some effects on our results. Moreover, in the clinical case of anterior-superior labrum detachment, its narrow width attachment should be taken into consideration [22, 23]. We also measured the length of attachment between the bony edge of the glenoid and the medial edge of the labrum, including the fibrocartilage tissue, although this distance was evaluated as a straight line, as in other studies. Huber et al. demonstrated that the widths of attachment of the fibrous tissue of the labrum to the cartilaginous tissue on the glenoid
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surface in the anterior-superior and anterior-inferior positions were 2.4 mm and 4.0 mm, respectively. Itoigawa reported values of 1.6 mm and 3.0 mm at the same positions. Our current results, 0.9 mm in the anterior-superior (2 o’clock) area and 2.5 mm in the anterior-inferior (4 o’clock) area, were shorter than those reported in the previous studies. From these results, in the case of anterior-superior labrum detachment, the suture anchor might be inserted within 1 mm from the bony edge of the glenoid. For its anterior-inferior detachment of the labrum, such as a Bankart lesion, a minimum of one anchor might be inserted on the articular surface of the glenoid 2–3 mm away from the bony edge. Labrum repair with suture anchor methods is increasingly common for injuries such as SLAP, Bankart, and reverse Bankart lesions. The chief aim is to fix the detached tissue around the edge of the glenoid bone by a suture anchor. Moreover, if surgeons perform an anatomical repair, they should take the length and morphology of attachment between the bone of the scapula and the labrum, depending on each region, into consideration. For the detachment of the labrum in the anterior-inferior, inferior and posterior-inferior area, it might be reasonable to insert the suture anchor on the articular side of the glenoid for anatomical reattachment of the labrum in these regions. Generally, in cases of labrum detachment, the fibrocartilage could be damaged. In these cases, although the connection between the fibrous labrum and glenoid bone can be repaired with suture anchors, histological insertion of the labrum, including the fibrocartilage, cannot be duplicated. Biological approaches might be considered such as tissue engineering, utilizing biomaterials and cells that would be able to reproduce the fibrocartilage between the labrum and the glenoid bone. Limitations Some limitations need to be kept in mind when interpreting the present findings. First, the number of specimens examined was small. Second, the age of the donors was relatively high, so the possible effects of degenerative changes on the results must be considered. Moreover, males and females were considered as one group in this study, which may have an effect on the length of the attachment of the labrum and the area of FCA.
Conclusions The length of the entire attachment of the labrum, including fibrocartilaginous tissue, was shortest in the 2 o’clock position. In all shoulders, the labrum attached to both the articular surface and the neck of the glenoid in the 4 and 6 o’clock positions. In addition, the width of its attachment to
Quantitative analysis of attachment of the labrum to the glenoid fossa…
the articular surface on the glenoid was greatest at the 4 and 6 o’clock positions. Acknowledgments The authors sincerely appreciate the support provided to us for the histological specimen preparation by the late Mr. Fujii and Mrs. Kawai from the Department of Pathology and Molecular Diagnosis at Nagoya City University Graduate School of Medical Science. We also acknowledge the assistance of Matthew Miller from the Department of Bioengineering and Orthopedic Surgery, University of Pittsburgh. Conflict of interest The authors declare that they have no conflict of interest.
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829 10. Andrews JR, Carson WG Jr, McLeod WD. Glenoid labrum tears related to the long head of the biceps. Am J Sports Med. 1985;13((5):337–41. 11. Burkhart SS, Morgan C. SLAP lesions in the overhead athlete. Orthop Clin North Am. 2001;32(3):431–41. 12. Bigliani LU, Pollock RG, McIlveen SJ, Endrizzi DP, Flatow EL. Shift of the posteroinferior aspect of the capsule for recurrent posterior glenohumeral instability. J Bone Joint Surg Am. 1995;77(7):1011–20. 13. Kim SH, Ha KI, Park JH, Kim YM, Lee YS, Lee JY, Yoo JC. Arthroscopic posterior labral repair and capsular shift for traumatic unidirectional recurrent posterior subluxation of the shoulder. J Bone Joint Surg Am. 2003;85(8):1479–87. 14. Eberly VC, McMahon PJ, Lee TQ. Variation in the glenoid origin of the anteroinferior glenohumeral capsulolabrum. Clin Orthop Relat Res. 2002;400:26–31. 15. Uhthoff HK, Piscopo M. Anterior capsular redundancy of the shoulder: congenital or traumatic? An embryological study. J Bone Joint Surg Br. 1985;67(3):363–6. 16. Bain GI, Galley IJ, Singh C, Carter C, Eng K. Anatomic study of the superior glenoid labrum. Clin Anat. 2013;26(3):367–76. 17. Itoigawa Y, Itoi E, Sakoma Y, Yamamoto N, Sano H, Kaneko K. Attachment of the anteroinferior glenohumeral ligament– labrum complex to the glenoid: an anatomic study. Arthroscopy. 2012;28(11):1628–33. 18. Pfahler M, Haraida S, Shulz C, Anetzberger H, Refior HJ, Bauer GS, Bigliani LU. Age-related changes of the glenoid labrum in normal shoulders. J Shoulder Elb Surg. 2003;12(1):40–52. 19. Plate JF, Bates CM, Mannava S, Smith TL, Jorgensen MJ, Register TC, Stehle JR, High KP, Shively CA, Kaplan JR, Saul KR, Tuohy CJ. Age-related degenerative functional, radiographic, and histological changes of the shoulder in nonhuman primates. J Shoulder Elbow Surg. 2013;22(8):1019–29. 20. Moseley HF, Overgaard B. The anterior capsular mechanism in recurrent anterior dislocation of the shoulder. J Bone Joint Surg Br. 1962;44(4):913–27. 21. Detrisac DA, Johnson LL. Arthroscopic shoulder anatomy; surgical and pathological implications. Thorofare, NJ. 1986:Slack;69–89. 22. Williams MM, Snyder SJ, Buford D Jr. The Buford complex— the “cord-like” middle glenohumeral ligament and absent anterosuperior labrum complex: a normal anatomic capsulolabral variant. Arthroscopy. 1994;10(3):241–7. 23. Ilahi OA, Labbe MR, Cosculluela P. Variants of the anterosuperior glenoid labrum and associated pathology. Arthroscopy. 2002;18(8):882–6.
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ORIGINAL ARTICLE
Quantitative analysis of attachment of the labrum to the glenoid fossa: a cadaveric study Masahito Yoshida1 · Hideyuki Goto1 · Masahiro Nozaki1 · Yasuhiro Nishimori1 · Tetsuya Takenaga1 · Atsunori Murase1 · Yuko Nagaya1 · Hirotaka Iguchi2 · Masaaki Kobayashi1 · Katsumasa Sugimoto3 · Takeshi Nishiyama4 · Takanobu Otsuka1
Received: 2 June 2014 / Accepted: 4 June 2015 / Published online: 14 July 2015 © The Japanese Orthopaedic Association 2015
Abstract Purpose This study investigated the direct and continuous attachment of the labrum to the glenoid fossa, including the fibrocartilaginous tissue, using image-analysis software and histology. Methods Twenty-six cadaveric shoulders (11 male, 15 female; mean age 80.1 years; age range 36–103 years) were used. The glenoid of each specimen was divided into six pie-slice-shaped pieces from the center perpendicular to the articular surface by radial incisions at the 2, 4, 6, 8, 10, and 12 o’clock positions. The general distribution of the labrum, including the fibrocartilage, was assessed in hematoxylin and eosin-, Safranin O- and Azan-Mallory-stained sections. The continuous length of attachment of the labrum to the glenoid was measured using image-analysis software. The width of attachment to the articular surface of the glenoid was assessed in each position. Results The labrum attached to both the articular surface and the neck of the glenoid in all shoulders (100 %) in the 4 and 6 o’clock positions. The mean length of the entire attachment to the glenoid was 4.6 mm (range 3.2–6.1 mm). The width of attachment from the bony edge of the glenoid to the edge of the labrum on the articular surface
* Hideyuki Goto hide‑[email protected]‑net.ne.jp 1
Department of Orthopedic Surgery, Graduate School of Medical Sciences, Nagoya City University, 1 Kawasumi, Mizuho‑cho, Mizuho‑ku, Nagoya, Aichi 467‑8601, Japan
2
Department of Arthroplastic Medicine, Graduate School of Medical Sciences, Nagoya City University, Nagoya, Japan
3
Nagoya Sports Clinic, Nagoya, Japan
4
Department of Public Health, Aichi Medical University, Nagakute, Japan
ranged from 0 to 4.3 mm. The length of the entire attachment of the labrum was shortest in the 2 o’clock position (p = 0.229). Additionally, the length of the entire attachment of the labrum was longest in the 4 o’clock position. The width of attachment to the articular surface of the glenoid was greatest in the 4 o’clock position (p < 0.01). Conclusion In the 4 and 6 o’clock positions, the labrum attached to both the articular surface and neck of the glenoid in all of the shoulders (100 %). The length of the entire attachment to the labrum, including the fibrocartilage, was shortest in the 2 o’clock position. The width of attachment to the articular surface of the glenoid was greatest in the 4 o’clock position (p < 0.01).
Introduction The glenoid labrum is a peripherally elevated tissue surrounding the edge of the glenoid fossa [1], which stabilizes the glenohumeral joint by adding depth to the glenoid cavity [2, 3]. Studies have demonstrated that the glenoid labrum consists of a circumferential fibrocartilaginous structure, which functions as connective tissue and acts as a part of the labrum itself [3–9]. Prodromos et al. demonstrated the presence of a fibrocartilaginous matrix within the labrum, which varied from being homogeneous to fibrous and contained chondrocytes in lacunae [9]. Ockert et al. investigated the size and morphology of this fibrocartilaginous part of the glenoid labrum, which mainly comprises collagen type II [8]. Given the regional difference of the labrum, there are some characteristic injuries such as Bankart lesions, superior labrum anterior and posterior (SLAP) lesions, reverse Bankart lesions, and circumferential detachment of the labrum. Bankart lesions, which involve exfoliation of the
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labrum from the glenoid in the anterior-inferior area, are major causes of recurrent dislocation of the shoulder and include the origin of the inferior glenohumeral ligament [2]. SLAP lesions, which involve labrum detachment from the superior area of the glenoid, are frequent in overhead athletes [1, 10, 11]. Reverse Bankart lesions are a major cause of posterior dislocation and are associated with detachment of the labrum in the posterior area of the glenoid [12, 13]. Successful outcomes of surgical repair for these injuries require a sound understanding of the anatomical variations of the labrum, which depend on the region. Several authors have described variations in the attachment, histology, and shape of the labrum depending on the location in the glenoid [3–5, 7, 14, 15]. A few previous studies have evaluated the length of attachment of the fibrous tissue of the labrum to the cartilage and the glenoid bone; however, these studies either approximated the length macroscopically or calculated the value as a straight line under light microscopy [6, 16, 17]. The present study investigated the direct and continuous length of the attachment of the labrum to the glenoid, which comprises fibrocartilaginous and fibrous tissues according to histological analysis. We hypothesized that the length of direct attachment of the labrum would demonstrate regional variations and that further diversity would be present in terms of the attachment of the labrum, including the fibrocartilaginous tissue, to the articular side of the glenoid.
Methods This study has been approved by the research ethics committee of Nagoya City University (no. 1060). Twentysix adult fresh cadaveric shoulders (11 male, 15 female; mean age 80.1 years; age range 36–103 years) were used for this study. Only those with no history of complaints or dysfunction were included. The skin, rotator cuff muscles, and coracoid process were resected from the scapula. The capsule, tendon of the long head of the biceps brachii, glenohumeral ligaments, and glenoid labrum were left intact. After macroscopic observation, all specimens were fixed in 10 % formaldehyde and decalcified with 10 % formic acid. The glenoid of each specimen was divided into six pie-slice-shaped pieces from the center of the glenoid perpendicular to the articular surface by radial incision at the 2, 4, 6, 8, 10, and 12 o’clock positions (Fig. 1a). The superior and inferior intersection of the long axis of the glenoid and the circumference of the glenoid circle were defined as the 12 o’clock and 6 o’clock position, respectively. The glenoid positions in this study were expressed as per the right shoulder. All the measurements were done for each section at the 2, 4, 6, 8, 10, and 12 o’clock positions. To identify the fibrous tissue of the labrum, hyaline
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Fig. 1 Tissue preparation. a The glenoid was divided into six pieslice-shaped pieces. b Cross-sectional area of the labrum and glenoid
cartilage, and fibrocartilaginous area (FCA), each specimen was embedded in paraffin (Fig. 1b) and stained with hematoxylin and eosin (H&E; Fig. 2a), Azan-Mallory (Fig. 2b), and Safranin-O (Fig. 2c). The general distribution of the labrum was assessed in sections stained with H&E, including the fibrocartilage. The outer edge between the fibrous labrum and capsule was defined by the density of elastic fibers in Azan-Mallory sections. The FCA and hyaline cartilage were defined by the staining density of Safranin-O. After assessing the differentiation between the FCA and the fibrous labrum tissues, both areas were measured on microscopic images using Image J version 1.40 software (National Institutes of Health, Rockville Pike, Bethesda, MD, USA; Fig. 3a). The direct length of the attachment of the labrum, including both fibrocartilaginous tissue and the fibrous labrum, to the glenoid was measured as a curved line using this software (Fig. 3b). The attachment sites of the labrum to the glenoid were determined histologically. The border between the layers of cartilage and bone tissues was distinguished, and the point of abrupt change was defined as the bony edge (arrowhead; Fig. 4a, b). The attachment of the labrum to the bony edge of the glenoid was observed under light microscopy at each position and classified into two morphological types. In the first, the labrum attachment extended beyond the bony edge of the glenoid and included not only the glenoid neck but also the articular surface (Fig. 4a). In the second, the attachment was found only within the glenoid neck and did not extend toward the articular surface of the glenohumeral joint (Fig. 4b). In addition, two of the three investigators assessed the histological attachment pattern of the labrum to the glenoid (that is, whether it extended to the articular surface of the glenoid). The length from the bony edge of the glenoid to the end of the labrum attachment to the articular surface was assessed as a straight line parallel to the surface (Fig. 5). When the attachment was limited only to the glenoid rim, its length was defined as 0 mm.
Quantitative analysis of attachment of the labrum to the glenoid fossa…
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Fig. 2 Methods of tissue staining. Photographic images of the histology of a cross-section of the glenoid in the 4 o’clock position. There was wide attachment between the labrum and the glenoid. a Hematoxylin and eosin (H&E), b Safranin-O, and c Azan-Mallory staining
Fig. 3 Histological specimen stained with Safranin-O. Labrum attachment to the glenoid in the 4 o’clock position. a The sizes of the fibrocartilaginous area (FCA) and fibrous labrum (FL) within the labrum were measured separately at each position from 12 to 10
o’clock, using Image J software; b the length of the entire labrum attachment (black arrow) to the glenoid was also measured by the same software. C capsule, G glenoid, AC articular cartilage, FCA fibrocartilage area, FL fibrous labrum
The intraobserver reliability was evaluated based on the correlation coefficients of two repeated measurements with an interval of 3 months. The mean length obtained from three measurements made by a single observer for each task was used in the analysis. Repeated-measures analysis of variance (ANOVA) was used to compare data from different regions of the labrum. Values of p < 0.05 were considered statistically significant. All analyses were performed using open-source statistical computing software (R package; http://www.r-project.org/).
anterior-superior position to 6.9 mm2 (2.4–13.6 mm2; SD, 2.4 mm2) in the posterior-inferior (8 o’clock) position. The ratio of the FCA to the entire labrum, including both fibrous and fibrocartilaginous tissue, ranged from 15.6 to 25.6 % in eachregion (Table 1). The mean length of attachment of the entire labrum was 4.6 mm (2.0–11.4 mm; SD, 1.6 mm). The attachment in the anterior-superior (2 o’clock) area was 3.2 mm (2.0–5.2 mm; SD, 0.8 mm), which was significantly shorter than in the other areas (p < 0.05; Fig. 6). The attachment in the anterior-inferior area (4 o’clock) was 6.1 mm (4.0– 11.4 mm; SD, 1.7 mm), which was significantly longer than in the other areas (p < 0.05; Fig. 6). The proportion in which the attachment reached the articular surface of the glenoid (type B) was 100 % in both the anterior-inferior (4 o’clock) and inferior (6 o’clock)
Results The mean size of the FCA ranged from 3.1 mm2 [0.6– 7.0 mm2; standard deviation (SD), 1.6 mm2] in the
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Fig. 4 Histological specimen stained with Safranin-O. Types of attachment of the labrum to the glenoid. a The attachment of the labrum (black arrow) to the glenoid in most locations in each shoulder extended to both the articular cartilage and the bony neck, including the bony edge of the scapula (black arrowhead). b The attach-
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ment of the labrum was limited to the bone of the glenoid neck. White line, the bony surface of the glenoid; white dotted line, perpendicular line to the bony surface of the glenoid from the bony edge of the glenoid
the edge of the labrum attachment to the articular surface ranged from 0 to 4.3 mm. A significant difference was found in the anterior-inferior (4 o’clock) and inferior (6 o’clock) regions compared with the others (12, 2, 8, and 10 o’clock; p < 0.01). Significant differences were also noted between the attachments in the anterior-inferior and inferior regions (p = 0.048; Fig. 8). The intraobserver correlation coefficients of repeated measurements for the length of attachment and the size of the labrum were 0.961 and 0.981, respectively, demonstrating excellent reproducibility.
Discussion Fig. 5 Histological specimen stained with Safranin-O. The labrum attachment to the glenoid in the 8 o’clock position. Measurement of the attachment of the labrum on the articular surface side (black arrow). From the bony edge of the glenoid (black arrow head), the average width of the attachment was determined in six positions. L, Labrum; white line, the bony surface of the glenoid; white dotted line, perpendicular line to the bony surface of the glenoid from the edge of the labrum attachment
areas, and the proportion in all other areas, with the exception of the superior (12 o’clock) area, was more than 80 % (Fig. 7). The length from the bony edge of the glenoid to
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The glenoid labrum has been defined as the fibrocartilaginous tissue positioned around the glenoid articular surface, consisting largely of collagen fibers [4, 7]. Several authors have demonstrated that fibrocartilage connects the fibrous tissue of the labrum with the bony tissue of the glenoid, and it has been considered to represent the labrum itself [3–9]. Prodromos et al. demonstrated that Safranin-O staining of the fibrocartilage for proteoglycans was mostly absent in the capsule and was intermediate between that of the fibrous capsule and the articular cartilage in the glenoid labrum [9]. Here, we used Safranin-O staining to evaluate the FCA connecting the articular cartilage of the glenoid with the fibrous
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Quantitative analysis of attachment of the labrum to the glenoid fossa… Table 1 Mean size of the fibrocartilage and fibrous labrum in each clockwise positions Location
Mean size of fibrocartilage (mm2)
Mean size of fibrous labrum (mm2)
Rate of fibrocatilgage in labrun (%)
Superior area (12 o’clock) Anterior-superior area (2 o’clock) Anterior-inferior area (4 o’clock) Inferior area (6 o’clock) Posterior-inferior area (8 o’clock)
5.5 ± 1.6 (3.2–9.3) 3.1 ± 1.6 (0.6–7.0) 6.8 ± 2.6 (2.9–127) 7.2 ± 2.9 (3.9–15.0) 6.9 ± 2.4 (2.4–13.6)
24.4 ± 6.8 (15.7–40) 21.3 ± 7.7 (11.7–38.9) 40.9 ± 20 (23.8–77.6) 39.9 ± 9.0 (24.6–58.5) 31.6 ± 8.6 (23.7–59.2)
22.5 (10.6–40) 15 (8.3–28.7) 17.6 (5.1–27.9) 20.3 (11.4–26.2) 26.9 (11.6–40)
Posterior-superior area (10 o’clock)
5.4 ± 2.3 (2.2–11.6)
30.7 ± 6.3 (22.5–43.2)
17.9 (8.2–30.2)
Fig. 6 Mean attachment of the labrum to the glenoid in each clockwise position. (*p < 0.05)
Fig. 7 Rate of attachment type of the labrum to articular cartilage and bony glenoid neck
tissue. In addition, we used Azan-Mallory staining to distinguish between the fibrous labrum and the capsule. The current study revealed the average distribution of the fibrocartilage within the entire labrum to be 19.6 % in the 12, 2, 4, 6, 8, and 10 o’clock positions. By contrast, Bain reported the average distribution of the fibrocartilage to be higher at 28 % in the 12, 2, 3, 4, 6, and 9 o’clock positions in a cadaveric study based on collage type IIlabeling of sections. This difference might have been due to
Fig. 8 Mean width of the attachment of the labrum on the articular surface of the glenoid in each clockwise position. The width of the attachment was significantly greater in the 4 and 6 o’clock positions than in the other positions (**p < 0.01) and significantly smaller at the 6 o’clock position than in the 4 o’clock position (*p < 0.05)
the different measurement techniques used, which mainly focused on proteoglycan staining with Safranin-O. In addition, the results of our study might have been affected by age-related histopathological changes of the glenoid labrum, which might cause the degeneration of the labrum [18, 19]. Degenerative changes to the labrum lead to a decrease in fibrocartilage, which includes proteoglycan, and an increase in the fibrous tissue of the labrum. Several studies have described variable morphology of the glenoid and the patterns of labrum attachment around the rim [3, 4, 5, 6, 7, 14, 15, 17]. Detrisac and Johnson classified several labrum shapes as normal anatomical variants [21]. Cooper et al. reported that the morphology of the labrum and capsule differed in its superior and inferior regions; they found that the inferior part of the labrum and capsule was usually a round, elevated, fibrous structure that was firmly attached to the glenoid, whereas the superior part of the labrum and capsule tended to be meniscal in appearance, more loosely attached to the glenoid, and mobile [5]. Itoigawa et al. reported that the rate of attachment of the anterior-inferior glenohumeral ligament-labrum
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complex (AIGHL-LC) to the articular cartilage and neck of the glenoid was 86.7 % in the 2 o’clock position and 88.3 % in the 4 o’clock position, using histological specimens stained with toluidine blue [17]. In our current study, the corresponding rates were 88.9 % in the 2 o’clock position and 100 % in the 4 o’clock position, respectively. The difference in these results might have been caused by the different staining method used for evaluating the fibrocartilaginous tissue. However, our results showed that the attachment of the labrum in the inferior parts (the 4, 6, and 8 o’clock positions) extended to the glenoid surface in more than 90 % of cases. These results are consistent with Cooper’s studies that showed wide attachment of the labrum in the inferior area of the glenoid. Huber et al. demonstrated that the width of attachment to the glenoid in each region ranged from 4.6 mm (1.9 mm on the articular side) in the posterior region to 10.7 mm (4.7 mm on the articular side) in the inferior region [5]. Itoigawa reported values of 4.7 mm (1.6 mm on the articular side) in the anterior-superior (2 o’clock) direction and 8.4 mm (3.0 mm on the articular side) in the anterior-inferior (4 o’clock) direction [17]. These studies divided the original attachment into two parts and evaluated them as straight lines using calipers or digital calipers. By contrast, the attachment in our current study ranged from 3.2 mm (0.9 mm on the articular side) in the anterior-superior (2 o’clock) position to 6.0 mm (2.5 mm on the articular side) in the anterior-inferior (4 o’clock) position, giving relatively shorter lengths at each position. This variation was attributed to the different measurement techniques used in the two studies. Our measurement is not macroscopic, but microscopic, based on histological differences between the labrum, cartilage and fibrous tissues. Additionally, we measured the attachment as a curved and continuous line and defined the labrum as a complex of fibrous tissue and the FCA. In the anterior-superior area, the length of the labrum attachment was significantly shorter in the 2 o’clock position than in the other positions, although it was present in all cases. This result was consistent with previous reports demonstrating that the labrum in this area was attached more narrowly. Williams demonstrated that there are some normal variations in the anterior-superior glenoid quadrant, such as a cord-like MGHL and no anterior-superior labral tissue and sublabral foramen. These normal variations could have some effects on our results. Moreover, in the clinical case of anterior-superior labrum detachment, its narrow width attachment should be taken into consideration [22, 23]. We also measured the length of attachment between the bony edge of the glenoid and the medial edge of the labrum, including the fibrocartilage tissue, although this distance was evaluated as a straight line, as in other studies. Huber et al. demonstrated that the widths of attachment of the fibrous tissue of the labrum to the cartilaginous tissue on the glenoid
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surface in the anterior-superior and anterior-inferior positions were 2.4 mm and 4.0 mm, respectively. Itoigawa reported values of 1.6 mm and 3.0 mm at the same positions. Our current results, 0.9 mm in the anterior-superior (2 o’clock) area and 2.5 mm in the anterior-inferior (4 o’clock) area, were shorter than those reported in the previous studies. From these results, in the case of anterior-superior labrum detachment, the suture anchor might be inserted within 1 mm from the bony edge of the glenoid. For its anterior-inferior detachment of the labrum, such as a Bankart lesion, a minimum of one anchor might be inserted on the articular surface of the glenoid 2–3 mm away from the bony edge. Labrum repair with suture anchor methods is increasingly common for injuries such as SLAP, Bankart, and reverse Bankart lesions. The chief aim is to fix the detached tissue around the edge of the glenoid bone by a suture anchor. Moreover, if surgeons perform an anatomical repair, they should take the length and morphology of attachment between the bone of the scapula and the labrum, depending on each region, into consideration. For the detachment of the labrum in the anterior-inferior, inferior and posterior-inferior area, it might be reasonable to insert the suture anchor on the articular side of the glenoid for anatomical reattachment of the labrum in these regions. Generally, in cases of labrum detachment, the fibrocartilage could be damaged. In these cases, although the connection between the fibrous labrum and glenoid bone can be repaired with suture anchors, histological insertion of the labrum, including the fibrocartilage, cannot be duplicated. Biological approaches might be considered such as tissue engineering, utilizing biomaterials and cells that would be able to reproduce the fibrocartilage between the labrum and the glenoid bone. Limitations Some limitations need to be kept in mind when interpreting the present findings. First, the number of specimens examined was small. Second, the age of the donors was relatively high, so the possible effects of degenerative changes on the results must be considered. Moreover, males and females were considered as one group in this study, which may have an effect on the length of the attachment of the labrum and the area of FCA.
Conclusions The length of the entire attachment of the labrum, including fibrocartilaginous tissue, was shortest in the 2 o’clock position. In all shoulders, the labrum attached to both the articular surface and the neck of the glenoid in the 4 and 6 o’clock positions. In addition, the width of its attachment to
Quantitative analysis of attachment of the labrum to the glenoid fossa…
the articular surface on the glenoid was greatest at the 4 and 6 o’clock positions. Acknowledgments The authors sincerely appreciate the support provided to us for the histological specimen preparation by the late Mr. Fujii and Mrs. Kawai from the Department of Pathology and Molecular Diagnosis at Nagoya City University Graduate School of Medical Science. We also acknowledge the assistance of Matthew Miller from the Department of Bioengineering and Orthopedic Surgery, University of Pittsburgh. Conflict of interest The authors declare that they have no conflict of interest.
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