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

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.

On the homology of the shoulder girdle in turtles.

The shoulder girdle in turtles is encapsulated in the shell and has a triradiate morphology. Due to its unique configuration among amniotes, many theories have been proposed about the skeletal identities of the projections for the past two centuries. Although the dorsal ramus represents the scapular blade, the ventral two rami remain uncertain. In particular, the ventrorostral process has been compared to a clavicle, an acromion, and a procoracoid based on its morphology, its connectivity to the rest of the skeleton and to muscles, as well as with its ossification center, cell lineage, and gene expression. In making these comparisons, the shoulder girdle skeleton of anurans has often been used as a reference. This review traces the history of the debate on the homology of the shoulder girdle in turtles. And based on the integrative aspects of developmental biology, comparative morphology, and paleontology, we suggest acromion and procoracoid identities for the two ventral processes.

Origin of the unique morphology of the shoulder girdle in turtles.

The shoulder girdle of turtles has a triradiate morphology. Although its dorsal process represents the scapular blade, the skeletal identities of the two ventral processes remain uncertain. To elucidate the question, developmental patterns of the girdles were compared between Chinese soft-shelled turtles, chickens, and mice. Despite the morphological diversity of adults, the initial primordia of the shoulder girdles showed similar morphological patterns. The ventral two processes developed from the anlagen comparable to those of the acromion and the coracoid in other amniotes. The developmental pattern of the acromion is very similar among embryos, whereas that of the coracoid in mammals differs from that in non-mammals, implying that coracoids are not homologous between non-mammals and mammals. Therefore, amniotes have retained the ancestral pattern of the girdle anlage, and the shoulder girdle of turtles has been achieved through a transformation of the pattern in the late ontogenic period.

Sprengel's deformity and spinal dysraphism: connecting the shoulder and the spine.

BACKGROUND AND PURPOSE: Sprengel's deformity, a rare congenital malformation of the scapula, may be observed in combination with spinal dysraphism. The co-occurrence of these malformations suggests an unknown shared etiology. Therefore, we reviewed the medical records of eight children presenting with both malformations and performed a review of the literature. PATIENTS AND METHODS: Databases from four university medical centers were searched for children presenting between 1992 and 2012 with spinal dysraphism and a Sprengel's deformity. CONCLUSION: The combination of spinal dysraphism and Sprengel's deformity is rare, and is associated with segmentation defects of the spine and ribs. Although the etiology of both spinal dysraphism and Sprengel's deformity remains unclear, all deformities of the spine, ribs, and shoulder might result from a common genetic defect affecting somitogenesis.

Early fetal development of the rotator interval region of the shoulder with special reference to topographical relationships among related tendons and ligaments.

PURPOSE: There is a little information on the early fetal development of the rotator interval region of the shoulder, particularly with regard to whether topographical relationships among the ligaments and tendons change during development. METHODS: We examined the histological sections (transverse or frontal) of right or left shoulder in 20 mid-term human fetuses (7-15 weeks of gestation). RESULTS: The biceps tendon had an accompanying bursa-like cavity before the joint cavitation. The bursa for the tendon remained open to the joint cavity until 12 weeks. When reaching the glenoid, the biceps tendon involved and carried mesenchymal tissue around the coracoid process (the future coracohumeral ligament) toward the infraspinatus tendon. Until 10 weeks, the primitive glenohumeral ligament was established as simple collateral ligaments on the inner or humeral side of the rotator cuff tendons and the biceps long tendon. However, the subscapularis tendon crossed, attached to, and reformed the upper structure of the superior glenohumeral ligament. CONCLUSIONS: The early development of the coracohumeral ligament suggests that it is a primitive and basic structure. However, we hypothesize that mechanical demands from the subscapularis tendon and biceps long tendon are likely to change the primitive form of the rotator interval to the adult morphology, including the superior glenohumeral ligament. The significant modification evident during early fetal development suggests that anatomical reconstruction after rotator cuff tears should not be based on the "ideal" anatomy, especially that of the superior glenohumeral ligament, but on individual requirements.

The anatomy of the superior labrum and biceps origin in the fetal shoulder.

The presence of a sublabral recess has been observed in adult shoulders. It is unclear whether this occurrence is a developmental variation or is acquired. The primary objective of the study was to determine if a cleft exists between the superior labrum and the superior cartilaginous glenoid anlage during the second trimester. The secondary objective was to define the origin of the long head of the biceps in the human fetus in the second trimester. Shoulders of 11 fetuses, 11-20 weeks old, were sectioned in the coronal plane. The superior labrum was observed to be continuous with the superior glenoid anlage, and a cleft was not observed at any stage of development. The biceps tendon originated from the superior labrum and the superior glenoid tubercle anlage in all specimens. Fibers extending in the direction of superior glenoid tubercle anlage were always very prominent.

Genetic and biomechanical determinants of glenoid version: implications for glenoid implant placement in shoulder arthroplasty.

SUMMARY: The universally accepted method of measuring glenoid version to determine proper alignment of the glenoid component during total shoulder arthroplasty does not account for the complex and variable relationship of the glenoid vault with the scapular body. Existing evidence indicates that the glenoid and the scapular body development are controlled by independent genetic and biomechanical factors. This raises the question: How relevant is the relationship of the glenoid face to the scapular body? This review paper integrates our present understanding of the genetics of scapular development and congenital and neuromuscular conditions to generate insights into scapular morphology and biomechanics. Glenoid version as traditionally defined may have limited relevance when positioning the glenoid component during total shoulder arthroplasty. Further studies of soft-tissue and muscular balance are needed to fully understand the consequences of variations in glenoid version. LEVEL OF EVIDENCE: Review.

Variations of the intra-articular portion of the long head of the biceps tendon: a classification of embryologically explained variations.

BACKGROUND: Although the intra-articular portion of the long head of the biceps (LHB) usually runs free, different types of fusions with the inferior surface of the capsule are known to be possible. Anatomic variations of this part of the LHB have been previously described and were nearly always considered to be innocent. MATERIALS AND METHODS: Out of 2 populations of 1500 arthroscopies each, we collected prospectively and retrospectively all possible variations of the proximal portion of the LHB. RESULTS: We included 57 cases (1.91%) of this total population in an attempt to describe the complete range of these form variants: the simple vinculum or pulley-like sling, the partial or complete mesotenon between biceps and capsule, the complete adherent LHB, the double-tendon origin, the reversed-type split-tendon, and the complete absence of the LHB. We suggest a classification of 12 variations of the intra-articular portion of the LHB. DISCUSSION: By taking into account an extensive literature review, we suggest that these conditions are congenital and consider them as a result of partial detachment from the mesothelial or synovial fusion with the inferior surface of the capsule. The incidence of these variants and their associated pathologies are investigated. CONCLUSION: By offering this new classification and a physiopathologic hypothesis, we try to explain why some of these anatomic variants may also acquire a pathologic significance.

Arthroscopic study of the shoulder joint in fetuses.

PURPOSE: The purpose of this study was to macroscopically examine the fetal shoulder joint using arthroscopy. We attempted to identify and describe the specific characteristics of the fetal shoulder joint, how it evolves during the last few weeks of intrauterine development, and any possible variations with regard to the adult shoulder. TYPE OF STUDY: Observational anatomic case series. METHODS: We used 20 frozen fetuses with a gestational age of 24 to 40 +/- 2 weeks, obtained from spontaneous abortions. Examination was performed with standard arthroscopic surgical equipment, using a 2.7-mm optical lens. Whenever possible, we tried to use the standard arthroscopic portals. Images were obtained for comparison with the adult shoulder. RESULTS: The arthroscopic images of the fetal glenohumeral joint are similar to those of an adult shoulder, with the only differences being those related to the stage of development. In this study we observed no so-called bare spot in the glenoid cavity such as has been described in treatises on the adult shoulder joint. The arthroscopic images of the anterosuperior region of the fetal joint show more highly defined structures than in the adult shoulder, especially the coracohumeral and glenohumeral ligaments. CONCLUSIONS: To our knowledge, this is the first arthroscopic study to target the fetal shoulder joint. The results indicate minimal differences when compared with the adult shoulder joint; for some structures, particularly in the anterosuperior region, the anatomy observed was easier to discern than what is observed in adult shoulder arthroscopy. CLINICAL RELEVANCE: Our study obtained clear images of virgin shoulder joints that had never been subjected to deterioration from wear or other distorting forces. The clarity of these images is useful for locating and identifying structures in the adult shoulder.

Histological studies of the glenoid labrum from fetal life to old age.

To help to resolve the controversy regarding the composition of the glenoid labrum, thirty-eight shoulders from cadavera were examined grossly and histologically. We used specimens for individuals of different ages so that we could determine what changes occur as a result of aging. In children and adults, the labrum appeared to be fibrocartilaginous tissue. The labrum was a separate anatomical structure that could be distinguished from the fibrous capsule of the shoulder. Neonatal labra were composed of primitive mesenchymal tissue containing only few chondrocytes that modulated into fibrocartilage in the first few years of life. Neonatal labra contained no elastin, whereas specimens from adults had rare elastin fibers. The labrum was sparsely vascularized throughout its substance, with no particular pattern of distribution. Vascularity decreased with increasing age of the individual.

Anterior capsular redundancy of the shoulder: congenital or traumatic? An embryological study.

A study of the attachment of the joint capsule to the scapula, and of the shape of the humeral head, has been carried out in 52 fetal and embryonic shoulders. In 77% of cases the anterior capsule was attached to the labrum or close to it; in the remaining 23% it was inserted into the neck of the scapula, so creating a pouch. In all 52 specimens the humeral head was spherical. It was concluded that the pouched and redundant anterior capsule sometimes seen during surgery for recurrent dislocation of the shoulder, may not be traumatic in origin, but could be a developmental variant.

Injuries to the glenoid labrum, including slap lesions.

The glenoid labrum of the shoulder has extensive anatomic variation but appears to be important for contributing to shoulder stability and for increasing the depth of contact between the glenoid labrum and the humeral head. Tears of the labrum are commonly seen in association with other pathologic entities, such as instability and rotator cuff tears, and treatment of the labral pathology may be incidental to treatment of the other more significant pathology. However, conditions isolated to the labrum do occur and can be a significant source of shoulder problems. Effective treatment of these lesions may result in significant improvement in the patient's symptoms. Labral lesions are difficult to diagnose, and special diagnostic studies and, frequently, arthroscopy are required. The recently described SLAP lesion is an uncommon but significant cause of shoulder disability that generally requires arthroscopic diagnosis. The arthroscopic treatment of this lesion depends on the type of SLAP lesion present. Recent techniques have permitted arthroscopic stabilization of the biceps labral detachment and type II SLAP lesions.

Recurrent anterior dislocation of shoulder joint.

111 patients with fresh dislocation of shoulder joint were treated with modified Putti-Platt procedure. Of these, 17 had recurrent anterior dislocation. 13 patients were followed up on the average for 25 years. According to Rowe criteria, 10 patients (76.9%) showed excellent results, 2 (15.4%) good, and (7.7%) fair. No recurrence and restriction of external rotation were found. Clinical experience and fetal investigation on congenital factors of recurrent shoulder dislocation were described.

Development of the supraspinatus tendon-to-bone insertion: localized expression of extracellular matrix and growth factor genes.

The adult healing response of the rotator cuff tendon-to-bone insertion site differs from the ordered process of insertion site development. Healing is characterized by disorganized scar and a lack of fibrocartilage formation, in contrast to the well organized fibrocartilaginous transition which forms during the normal development of the tendon-to-bone insertion. The purpose of this study was to localize the expression of a number of extracellular matrix and growth factor genes during insertion site development in order to guide future strategies for augmenting adult rotator cuff healing. The rotator cuff was morphologically distinct at 13.5 dpc (days postconception). Neo-tendon was evident as a condensation of cells adjacent to bone. The interface between tendon and bone did not form into a mature fibrocartilaginous insertion until 21-days postnatally, based upon the appearance of four distinct zones with a mineralized humeral head. Fibroblasts of the supraspinatus tendon expressed type I collagen at all timepoints. Type II collagen was first expressed by chondrocytes in the fibrocartilage and mineralized fibrocartilage at 7 days and persisted in the mineralized fibrocartilage at 56 days. Type X collagen was first expressed by the chondrocytes in the mineralized fibrocartilage at 14 days and persisted in the mineralized fibrocartilage at 56 days. A shift from TGF-beta3 to TGF-beta1 expression occurred at 15.5 dpc.

The developmental anatomy of the neonatal glenohumeral joint.

The embryologic development of the capsular ligaments, synovial lining, rotator cuff, and bony structures of the shoulder is incompletely understood. The purpose of this study is to report the gross and microscopic anatomy of the developing glenohumeral joint on the basis of dissections of fetal shoulder specimens. After Institutional Review Board approval from our hospital, 51 shoulders in 37 fetal specimens were obtained from cases of fetal demise. The gestation time of these specimens ranged from 9 to 40 weeks. The morphology of the capsule, labrum, and associated ligaments were studied by dissection under a dissecting microscope. High-resolution radiographs were made, and sections were processed for routine histology. There was noted to be minimal variation in the shape and slope of the acromion. The coracoid was much larger in relation to the shoulder than in the mature shoulder. The coracoacromial ligament was grossly evident at this stage of development, with distinct anterolateral and posteromedial bands in this ligament. The inferior glenohumeral ligament was seen as a prominent thickening in the capsule, whereas the middle and superior glenohumeral ligaments were thinner and more difficult to identify as distinct structures. Upon histologic examination, the inferior glenohumeral ligament was seen to consist of several layers of organized collagen fibers. The inferior glenohumeral ligament inserted into the labrum and margin of the glenoid. The capsule was much thinner in the region superior to the inferior glenohumeral ligament. A rotator interval capsular defect was often present, and the coracohumeral ligament was seen as a distinct structure as early as 15 weeks. A bare spot in the glenoid was not observed. This study indicates that some of the important functional elements of the structure of the mature human shoulder are present early in development, including the glenohumeral and coracohumeral ligaments. The coracoacromial ligament plays a significant role in the formation of the coracoacromial arch in the neonatal shoulder. The presence of a capsular rotator interval indicates that this aspect of capsular anatomy is congenital.

Developmental morphological and histological studies on structures of the human fetal shoulder joint.

In the present work, morphological changes in the interior structures of the developing human shoulder joint were studied at different prenatal ages (9, 12, 16, 23 and 40 weeks) and were compared with the same structures in the adult joint. It was found that the shoulder joint had gone through important developmental changes during the 12th week of the prenatal life and it is assumed that genetic factors operative during this stage of development were more important than mechanical factors. A subsequent development of the intracapsular glenohumeral ligaments was present at the 16th week. The glenoid labrum, the biceps tendon and the three glenohumeral ligaments formed a complete ring around the glenoid fossa which constituted a functional unit, which seemed to have a role in stabilizing the joint. In the present work, histological prenatal studies were done on sagittal and radial sections from the glenoid fossa and its associated structures and the results were compared with the same structures in adults. At a crown-rump length of 30 mm (9 weeks), intermingling of the collagen fibres of the superior labrum and the biceps tendon was observed and the superior labrum could be considered as an extension of the biceps tendon. While the superior and inferior parts of the labrum appeared fibrous, the posterior labrum appeared as a primitive cellular condensation. At the 12th week, it became a fibrocellular structure and changed to a fibrocartilaginous structure at the 16th week. But until full term, no definitive fibrocartilage was found due to its hypercellularity compared to the adult. It was found that at all ages, the capsule was formed of cellular and fibrous elements, its collagenous content was progressively increased with age and at full term, it became generally fibrous but was still different compared to adults. In all stages of development, the synovial tissue of different regions of the same joint exhibited marked variations in thickness, vascularity, cellular density and collagenous content. It lined the capsule, surrounded the biceps tendon and reflected on the labrum. Its cell density as well as their vascular and collagenous contents were progressively increased with age. At full term, the synovial tissue was thickest at its inferior reflection and forming large folds. The synovial tissue lining the capsule was thinner than the synovial tissue at its reflection from the labrum, many villi and processes arising from it and projecting into the joint cavity.

The formation of human synovial joint cavities: a possible role for hyaluronan and CD44 in altered interzone cohesion.

During fetal development, cavitation occurs within the primitive skeleton along planes destined to become the articular surfaces of synovial joints. A histochemical study of human fetal limbs was undertaken to identify the cell types involved in this cavitation and the possible role of interactions between cells and extracellular matrix. Cryostat sections were stained with antibodies to CD68, factor VIII related antigen, prolyl hydroxylase, beta 1 integrin, VCAM-1, proliferating cell nuclear antigen, chondroitin-4 sulphate, chondroitin-6-sulphate, hyaluronan synthase and CD44. Similar sections were reacted for uridine diphosphoglucose dehydrogenase (UDPGD) and acid phosphatase activity. Hyaluronan was demonstrated using an aggrecan core protein hyaluronan binding region probe. Macrophages were present prior to cavitation in the periphery of joint interzones but not at the presumptive joint line in the central interzone. Fibroblastic cells were present throughout. Absence of local VCAM-1 expression indicated that cavitation was temporally distinct from full fibroblast-like synoviocyte differentiation. CD44 was expressed by interzone cells at all stages. Staining for hyaluronan and hyaluronan synthase, but not chondroitin sulphates was present in the interzone before and at the time of cavitation. UDPGD activity was increased in a narrow band of cells at the presumptive joint line prior to cavitation. These findings suggest that joint cavitation is dependent on the behaviour of fibroblastic cells and/or adjacent chondrocytes, rather than macrophages. Since UDPGD activity is involved in hyaluronan synthesis, it is proposed that joint cavitation is facilitated by a rise in local hyaluronan concentration in an area of tissue where cohesion is dependent on the interaction between cellular CD44 and extracellular hyaluronan. As proposed by Toole et al. (1984) such a local rise in hyaluronan concentration may lead to a switch from intercellular cohesion to dissociation, leading to tissue cavitation.