The goal of this study is to clarify the development of the long head of the biceps brachii tendon (LHBT) and to verify the existence and development of the coracoglenoid ligament. Histological preparations of 22 human embryos (7-8 weeks of development) and 43 human fetuses (9-12 weeks of development) were studied bilaterally using a conventional optical microscope. The articular interzone gives rise to the LHBT, glenoid labrum, and articular capsule. During the fetal period, it was observed that in 50 cases (58%), the LHBT originated from both the glenoid labrum and the scapula, while in 36 cases (42%), it originated only from the glenoid labrum. The coracoglenoid ligament, first described by Sappey in 1867, is a constant structure that originates at the base of the coracoid process and projects toward the glenoid labrum zone, which is related to the origin of the LHBT. The coracoglenoid ligament was more easily identifiable in the 36 cases in which the LHBT originated only from the glenoid labrum. We suggest that the coracoglenoid ligament is a constant anatomical structure, is not derived from the articular interzone unlike the LHBT, and contributes to the fixation of the glenoid labrum in the scapula in cases in which the LHBT originated only from the glenoid labrum. We postulate that, when the LHBT is fixed only at the glenoid labrum, alterations in the coracoglenoid ligament could lead to a less sufficient attachment of the glenoid labrum to the scapula which could predispose to a superior labral lesion.

Keywords:
Shoulder ligament development, Biceps tendon, Coracoglenoid ligament, Human embryology, Glenoid labrum, Human development
1.
Abe, S., T. Nakamura, J.F. Rodriguez-Vazquez, G. Murakami, Y. Ide (2011) Early fetal development of the rotator interval region of the shoulder with special reference to topographical relationships among related tendons and ligaments. Surg Radiol Anat 33: 609-615.
2.
Aboul-Mahasen, L.M., S.A. Sadek (2002) Developmental morphological and histological studies on structures of the human fetal shoulder joint. Cells Tissues Organs 170: 1-20.
3.
Andersen, H. (1963) Histochemistry and development of the human shoulder and acromioclavicular joints with particular reference to the early development of the clavicle. Acta Anat (Basel) 55: 124-165.
4.
Audenaert, E.A., E.J. Barbaix, P. Van Hoonacker, B.M. Berghs (2008) Extraarticular variants of the long head of the biceps brachii: a reminder of embryology. J Shoulder Elbow Surg 17(1 suppl): 114S-117S.
5.
Bergman, R., A. Afifi, R. Miyauchi (2015) Illustrated Encyclopedia of Human Anatomic Variation: Opus I: Muscular System: Alphabetical Listing of Muscles: Biceps Brachii. http://www.anatomyatlases.org/AnatomicVariants/MuscularSystem/Text/B/02Biceps.shtml.
6.
Chen, J.W., J.L. Galloway (2014) The development of zebrafish tendon and ligament progenitors. Development 141: 2035-2045.
7.
Demondion, X., C. Maynou, B. Van Cortenbosch, K. Klein, X. Leroy, H. Mestdagh (2001) Relationship between the tendon of the long head of the biceps brachii muscle and the glenoid labrum (in French). Morphologie 85: 5-8.
8.
Dierickx, C., E. Ceccarelli, M. Conti, J. Vanlommel, A. Castagna (2009) Variations of the intra-articular portion of the long head of the biceps tendon: a classification of embryologically explained variations. J Shoulder Elbow Surg 18: 556-565.
9.
Edom-Vovard, F., D. Duprez (2004) Signals regulating tendon formation during chick embryonic development. Dev Dyn 229: 449-457.
10.
Egea, J.M., C. Melguizo, J. Prados, A. Aránega (2010) Capsular origin of the long head of the biceps brachii tendon: a clinical case. Rom J Morphol Embryol 51: 375-377.
11.
Fealy, S., S.A. Rodeo, E.F. Dicarlo, S.J. O'Brien (2000) The developmental anatomy of the neonatal glenohumeral joint. J Shoulder Elbow Surg 9: 217-222.
12.
Franco, J.C., T.P. Knapp, B.R. Mandelbaum (2005) Congenital absence of the long head of the biceps tendon. A case report. J Bone Joint Surg Am 87: 1584-1586.
13.
Gardner, E., D.J. Gray (1953) Prenatal development of the human shoulder and acromioclavicular joints. Am J Anat 92: 219-276.
14.
Gaskin, C.M., S.R. Golish, K.J. Blount, D.R. Diduch (2007) Anomalies of the long head of the biceps brachii tendon: clinical significance, MR arthrographic findings, and arthroscopic correlation in two patients. Skeletal Radiol 36: 785-789.
15.
Ghalayini, S.R., T.N. Board, M.S. Srinivasan (2007) Anatomic variations in the long head of biceps: contribution to shoulder dysfunction. Arthroscopy 23: 1012-1018.
16.
Gigis, P., C. Natsis, M. Polyzonis (1995) New aspects on the topography of the tendon of the long head of the biceps brachii muscle. One more stabilizer factor of the shoulder joint. Bull Assoc Anat (Nancy) 79: 9-11.
17.
Glueck, D.A., S.D. Mair, D.L. Johnson (2003) Shoulder instability with absence of the long head of the biceps tendon. Arthroscopy 19: 787-789.
18.
Hyman, J.L., R.F. Warren (2001) Extra-articular origin of biceps brachii. Arthroscopy 17: E29.
19.
Kardon, G. (1998) Muscle and tendon morphogenesis in the avian hind limb. Development 125: 4019-4032.
20.
Kolts, I., L.C. Busch, H. Tomusk, A. Arend, A. Eller, M. Merila, M. Russlies (2000) Anatomy of the coracohumeral and coracoglenoidal ligaments. Ann Anat 182: 563-566.
21.
Koplas, M.C., C.S. Winalski, W.H. Ulmer, M. Recht (2009) Bilateral congenital absence of the long head of the biceps tendon. Skeletal Radiol 38: 715-719.
22.
Lapner, P.L., M.A. Lapner, H.K. Uhthoff (2010) The anatomy of the superior labrum and biceps origin in the fetal shoulder. Clin Anat 23: 821-828.
23.
Lorda-Diez, C.I., J.A. García-Porrero, J.M. Hurlé, J.A. Montero (2014) Decorin gene expression in the differentiation of the skeletal connective tissues of the developing limb. Gene Expr Patterns 15: 52-60.
24.
Macalister, A. (1867) Notes on an instance of irregularity in the muscles around the shoulder joint. J Anat Physiol 1: 316-319.
25.
Macalister, A. (1875) Additional observations on muscular anomalies in human anatomy (third series), with a catalogue of the principal muscular variations hitherto published.” Trans Roy Irish Acad 25: 80-84.
26.
MacDonald, P.B. (1998) Congenital anomaly of the biceps tendon and anatomy within the shoulder joint. Arthroscopy 14: 741-742.
27.
MacManus, J., R.W. Mowry (1968) Técnica histológica. Madrid, Atika.
28.
Mariani, P.P., A. Bellelli, C. Botticella (1997) Arthroscopic absence of the long head of the biceps tendon. Arthroscopy 13: 499-501.
29.
Morgan, C.D., S.S. Burkhart, M. Palmeri, M. Gillespie (1998) Type II SLAP lesions: three subtypes and their relationships to superior instability and rotator cuff tears. Arthroscopy 14: 553-565.
30.
Neale, R.M. (1937) The alleged transmigration of the long tendon of the biceps brachii. Anat Rec 67: 205-218.
31.
O'Rahilly, R., F. Müller (2001) Human Embryology & Teratology. New York, Wiley-Liss.
32.
O'Rahilly, R., F. Müller (2010) Developmental stages in human embryos: revised and new measurements. Cells Tissues Organs 192: 73-84.
33.
Pal, G.P., R.H. Bhatt, V.S. Patel (1991) Relationship between the tendon of the long head of biceps brachii and the glenoidal labrum in humans. Anat Rec 229: 278-280.
34.
Pouliart, N., K. Somers, S. Eid, O. Gagey (2007) Variations in the superior capsuloligamentous complex and description of a new ligament. J Shoulder Elbow Surg 16: 821-836.
35.
Richards, D.P., M. Schwartz (2003) Anomalous intraarticular origin of the long head of biceps brachii. Clin J Sport Med 13: 122-124.
36.
Rouvière, H., A. Delmas (2005) Anatomía humana descriptiva, Topografía y funcional. Barcelona, Masson.
37.
Sappey, P.C. (1867) Traité d'anatomie descriptive. Paris, Delayahe.
38.
Standring, S. (2008) Gray's Anatomy: The Anatomical Basis of Clinical Practice. New York, Churchill Livingstone-Elsevier.
39.
Terminologia Anatomica (2011) Federative International Programme for Anatomical Terminology, International Federation of Associations of Anatomists. Stuttgart, Thieme.
40.
Tuoheti, Y., E. Itoi, H. Minagawa, N. Yamamoto, H. Saito, N. Seki, K. Okada, Y. Shimada, H. Abe (2005) Attachment types of the long head of the biceps tendon to the glenoid labrum and their relationships with the glenohumeral ligaments. Arthroscopy 21: 1242-1249.
41.
Vangsness, C.T., S.S. Jorgenson, T. Watson, D.L. Johnson (1994) The origin of the long head of the biceps from the scapula and glenoid labrum. An anatomical study of 100 shoulders. J Bone Joint Surg Br 76: 951-954.
42.
Wahl, C.J., J.D. MacGillivray (2007) Three congenital variations in the long head of the biceps tendon: a review of pathoanatomic considerations and case reports. J Shoulder Elbow Surg 16: e25-e30.
43.
Weinstabl, R., H. Hertz, W. Firbas (1986) Connection of the ligamentum coracoglenoidale with the muscular pectoralis minor (in German). Acta Anat (Basel) 125: 126-131.
44.
Welcker, H. (1878) Die Einwanderung der Bicepssehne in das Schultergelenk. Nebst Notizen über Ligamentum interarticulare humeri und Ligamentum teres femoris. Arch Anat Physiol 1: 20-42.
45.
Yeh, L., R. Pedowitz, S. Kwak, P. Haghighi, C. Muhle, D. Trudell, D. Resnick (1999) Intracapsular origin of the long head of the biceps tendon. Skeletal Radiol 28: 178-181.
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