Development of the human shoulder joint during the embryonic and early fetal stages: anatomical considerations for clinical practice

Abstract

Although several studies have been published regarding the morphology and anatomical variations of the human shoulder joint, most have dealt with adult individuals. Those looking into the development of the joint have been focused on specific structures or have observed specimens in advanced gestational stages. The goal of this paper is to perform a complete analysis of the embryonic and early fetal development of the elements in the shoulder joint, and to clarify some contradictory data in the literature. In our study, serial sections of 32 human embryos (Carnegie stages 16-23) and 26 fetuses (9-13 weeks) were analyzed. The chondrogenic anlagen of the humerus and the medial border of the scapula can be observed from as early as Carnegie stage 17, whereas that of the rest of the scapula appears at stage 18. The osteogenic process begins in week 10 for the humeral head and week 11 for the scapula. At stage 19 the interzone becomes apparent, which will form the glenohumeral joint. In the next stage the glenohumeral joint will begin delaminating and exhibiting a looser central band. Denser lateral bands will join the humeral head (caput humeri) and the margins of the articular surface of the scapula, thus forming the glenoid labrum, which can be fully appreciated by stage 22. In 24-mm embryos (stage 21) we can observe, for the first time, the long head of the biceps tendon (which is already inserted in the glenoid labrum by week 9), and the intertubercular sulcus, whose depth is apparent since week 12. Regarding ligamentous structures, the coracohumeral ligament is observed at the end of Carnegie stage 23, whereas the primitive glenohumeral ligament already appeared in week 10. The results of this study provide a detailed description of the morphogenesis, origin and chronological order of appearance of the main intrinsic structures of the human shoulder joint during late embryonic and early fetal development. We expect these results to help explain several functional aspects of the shoulder joint, and to clarify some contradictory data in the literature regarding this complex anatomical and biomechanical structure, helping future researchers in their efforts.

Shoulder girdle formation and positioning during embryonic and early fetal human development

“…Mekonen et al detected the scapula (shoulder blade) at CS17 in histological sections [29]. Hita-Contreras et al observed the chondrogenic anlagen at the medial border of the scapula from as early as CS17, whereas the scapula body appeared at CS18 [10]. We first detected the scapula body at CS17 with the coracoid and humeral head at CS18 on PCX-CT images, consistent with recent histological studies.…”

“…In this study, the connection of the body and coracoid could not be confirmed at CS18 because of the resolution of the PCX-CT image. Hita-Contreras et al observed three outgrowths of the mesenchymal condensation with an irregular shape corresponding to the body of the scapula, future coracoid process, and large mass of the humerus, acromion, and spine of the scapula [10]. The authors, however, did not mention whether these three outgrowths were connected.…”

“…Blechschmidt, Müller and O’Rahilly, and O’Rahilly et al also noted the axial position of the scapula [ 6 – 9 ]. Recent studies have primarily described the morphogenesis of the shoulder joint (between the scapula and humerus) [ 10 ]. Moreover, specific structures such as the glenoid labrum, the long head (caput longum) of the biceps tendon [ 11 ] and the rotator interval [ 12 ] have also been described in detail.…”

Rotator cable in pathological shoulders: comparison with normal anatomy in a cadaveric study

“…Most of the concerns address the anterior part of the cable that ends in the region of the rotator interval, interweaving with the coracohumeral and superior glenohumeral ligaments (Choo et al 2014; Kask et al 2008; Kolts et al 2000; Pouliart et al 2007). Embryological studies report only that the development of the glenohumeral joint capsule occurs during Carnegie stages 22–23 (Aboul-Mahasen and Sadek 2002; Fealy et al 2000; Hita-Contreras et al 2017). However, as it has been reported in macroscopic (Burkhart et al 1993; Rahu et al 2016) and microscopic (Fallon et al 2002) studies, and as we confirmed in normal and pathological specimens, rotator cables form a functional complex with the supra- and infraspinatus muscles.…”

Genetics of scapula and pelvis development: An evolutionary perspective

“…Recent analysis by Hita-Contreras et al (2018) has shown that this mesenchymal condensation has multiple outgrowths: one each for the scapular body, coracoid process, and the acromion and spine. These findings agree with Capellini et al (2010) assessment using 3D Optimal Projection Tomography of the boundaries of Sox9 expression, a marker of mesenchymal condensation formation.…”