Human shoulder development is adapted to obstetrical constraints.

In humans, obstetrical difficulties arise from the large head and broad shoulders of the neonate relative to the maternal birth canal. Various characteristics of human cranial development, such as the relatively small head of neonates compared with adults and the delayed fusion of the metopic suture, have been suggested to reflect developmental adaptations to obstetrical constraints. On the other hand, it remains unknown whether the shoulders of humans also exhibit developmental features reflecting obstetrical adaptation. Here we address this question by tracking the development of shoulder width from fetal to adult stages in humans, chimpanzees, and Japanese macaques. Compared with nonhuman primates, shoulder development in humans follows a different trajectory, exhibiting reduced growth relative to trunk length before birth and enhanced growth after birth. This indicates that the perinatal developmental characteristics of the shoulders likely evolved to ease obstetrical difficulties such as shoulder dystocia in humans.

Heads, Shoulders, Elbows, Knees, and Toes: Modular Gdf5 Enhancers Control Different Joints in the Vertebrate Skeleton.

Synovial joints are crucial for support and locomotion in vertebrates, and are the frequent site of serious skeletal defects and degenerative diseases in humans. Growth and differentiation factor 5 (Gdf5) is one of the earliest markers of joint formation, is required for normal joint development in both mice and humans, and has been genetically linked to risk of common osteoarthritis in Eurasian populations. Here, we systematically survey the mouse Gdf5 gene for regulatory elements controlling expression in synovial joints. We identify separate regions of the locus that control expression in axial tissues, in proximal versus distal joints in the limbs, and in remarkably specific sub-sets of composite joints like the elbow. Predicted transcription factor binding sites within Gdf5 regulatory enhancers are required for expression in particular joints. The multiple enhancers that control Gdf5 expression in different joints are distributed over a hundred kilobases of DNA, including regions both upstream and downstream of Gdf5 coding exons. Functional rescue tests in mice confirm that the large flanking regions are required to restore normal joint formation and patterning. Orthologs of these enhancers are located throughout the large genomic region previously associated with common osteoarthritis risk in humans. The large array of modular enhancers for Gdf5 provide a new foundation for studying the spatial specificity of joint patterning in vertebrates, as well as new candidates for regulatory regions that may also influence osteoarthritis risk in human populations.

Ontogeny of modern human longitudinal body and transverse shoulder proportions.

OBJECTIVES: Whereas variation of modern human adult body size and shape has been widely studied in the context of ecogeographical clines, little is known about the differential growth patterns of transverse and longitudinal dimensions among human populations. Our study explored the ontogenetic variation of those body proportions in modern humans. METHODS: We compared results from four different approaches to study cross-sectional skeletal samples of Africans (n = 43), Amerindians (n = 69) and Europeans (n = 40) from 0 to 14 years of age. Clavicle, humerus, and femur intermetaphyseal lengths, and femoral distal metaphyseal breadth, were measured. Average ontogenetic trajectories were computed in order to compare the growth patterns of the three groups. RESULTS: Our findings demonstrated that the three geographical groups shared similar absolute and relative patterns of change with age for the four dimensions considered. Although interpopulation differences existed in transverse to longitudinal as well as in interlimb proportions, those differences did not seem to remain constant throughout ontogeny, similar to what has been shown for intralimb proportions. Growth rates of transverse shoulder proportions differed between populations from different regions after 10 years, whereas those for longitudinal proportions were very similar. CONCLUSIONS: The ontogeny of transverse shoulder proportions is more complex than what is observed for bi-iliac breadth, suggesting that transverse shoulder to limb proportions are not solely influenced by ecogeographical conditions. Our analysis demonstrates that methodologies that incorporate critical dimensions of body form could shed new light on human adaptation in both paleontological and neontological contexts.

Growth of the pectoral girdle in a sample of juveniles from the kellis 2 cemetery, Dakhleh Oasis, Egypt.

OBJECTIVES: This study investigates growth patterns in the scapula and clavicle in a cross-sectional juvenile skeletal sample ranging from 20 weeks gestation to 8.5 years of age from the Kellis 2 cemetery, Dakhleh Oasis, Egypt. The primary goal is to quantify growth patterns and growth velocities in the scapula and clavicle to better understand the development of the pectoral girdle. METHODS: A series of low-order polynomial regression models was used to examine growth curves in clavicle diaphyseal length, scapular height, and scapular width. Incremental growth and relative percent increase were examined among successive age groups as a proxy measure of growth velocity. Scapular body proportions were assessed with the scapular index and compared across age groups using a Kruskal-Wallis test with post-hoc tests. RESULTS: A third-order polynomial best describes growth in clavicle diaphyseal length and scapular height, and a second-order polynomial best describes growth in scapular width. Growth velocity patterns are similar among clavicle diaphyseal length, scapular height, and scapular width particularly from birth until the end of early childhood. Clavicle diaphyseal length decelerates during middle childhood while scapular height and width accelerate during this time. With increasing age, the scapular body proportionately increases more in height than in width. The relatively narrow scapular body characteristic of adult scapulae is first evident during early childhood. CONCLUSIONS: Changes in scapular body shape during ontogeny may be a reflection of the greater alterations taking place in the integrated morphology of the pectoral girdle during the biomechanical shift from crawling to bipedalism. Am. J. Hum. Biol. 28:636-645, 2016. © 2016 Wiley Periodicals, Inc.

Integration of the mammalian shoulder girdle within populations and over evolutionary time.

Morphological integration has the potential to link morphological variation within populations with morphological evolution among species. This study begins to investigate this link by comparing integration among shoulder girdle elements (e.g. scapular blade, glenoid, coracoid, etc.) during the origin and evolution of therian mammals, and within modern bat, opossum and mouse populations. In this study, correlations among skeletal elements and patterns of allometry are used as proxies for integration. Results suggest that shoulder girdle elements tended to vary and evolve independently during the origin of mammals and subsequent radiation of placentals, consistent with the elements' distinct developmental and evolutionary origins. This finding suggests that skeletal element correlations, and therefore integration, can be conserved over large taxonomic and temporal scales. However, marsupials display a different pattern in which shoulder girdle elements tend to be more integrated, with the exception of the coracoid. This finding is consistent with a shift in the pattern of skeletal element integration coincident with the appearance of the marsupial mode of reproduction. This finding provides further evidence that development can play a significant role in the establishment of patterns of skeletal element correlation and that patterns of skeletal element correlation can themselves evolve when faced with sufficient selective pressures.

Sport-specific musculoskeletal growth and postural control in female artistic gymnasts: a 12 month cohort study.

Female gymnasts have been evidenced to experience sport-specific growth, of which broad shoulders and narrow hips are common characteristics. In addition to being a central component of handstand performance, postural control mechanisms, including whole-body and lumbo-pelvic stability, have been identified as risk factors for overuse spinal pathology. The study aimed to develop a fundamental understanding of musculoskeletal growth and postural control responses of female artistic gymnasts in order to extend longitudinal insights into overuse spinal pathology risk. Whole-body anthropometric measures were collected for 12 competitive female gymnasts (age at recruitment: nine to 15 years) at three time points across a 12 month period. Musculoskeletal growth was partially defined as the rate of bicristal-to-biacromial breadth ratio development, and informed shoulder- and pelvis-dominant growth sub-groups. Kinematic and kinetic indicators of postural control were determined for a total of 700 handstand trials. The shoulder-dominant (gymnastics-specific) growth group was found to have significantly greater biomechanical risk for general stability (p < 0.001) than the pelvis-dominant group. Significantly greater lumbo-pelvic risk was demonstrated for the pelvis-dominant group (p < 0.001). Extended idiosyncratic examination of proportional sport-specific growth measures alongside multi-faceted risk monitoring was advocated for the effective development of future overuse pathology prevention protocols.

Chondrogenesis and ossification of the lissamphibian pectoral girdle.

Knowledge of amphibian shoulder development is requisite for further understanding of gnathostome pectoral girdle evolution. Fish and amniotes share few pectoral girdle elements, but modern amphibians exhibit a unique combination of traits that bridge the morphological gap between these two groups. I analyzed patterns of chondrogenesis, ossification, and bone histology of the pectoral girdles of two anuran species (Xenopus laevis and Bombina orientalis) and two urodele species (Ambystoma mexicanum and Desmognathus aeneus) to provide new insight into the evolution of the tetrapod pectoral girdle. Comparisons reveal the following: 1) variation in the pattern of chondrogenesis among the anuran species analyzed correlates to variation in adult pectoral girdle morphology; 2) morphologically similar pectoral skeletons do not necessarily have similar patterns of bone histology; and 3) the urodele and anuran pectoral girdles included herein share a common morphology despite differences in patterns of chondrogenesis.

Evaluation of shoulder balance in the normal adolescent population and its correlation with radiological parameters.

A descriptive clinical study in healthy adolescents was done to evaluate the clinical shoulder balance and analyze the correlation between clinical and radiological parameters which are currently used to evaluate shoulder balance. In addition to trunk shift and rib hump, shoulder balance is one of the criteria that are used to evaluate the outcomes in spinal deformity surgery. Several methods have been proposed to evaluate the shoulder balance in scoliotic patients; however, there is no uniformity to these methods in the current literature. Patients who applied to pediatric clinic without musculoskeletal pathology formed the patient population. Volunteers were asked to fill out a questionnaire assessing shoulder balance perception and had their clinical photograph taken simultaneously with a P-A chest X-ray. The clinical shoulder balance was evaluated through analysis of the clinical photograph. The X-rays were used to evaluate the radiological shoulder balance. The evaluated parameters included coracoid height difference (CHD), clavicular angle (CA), the clavicle-rib cage intersection difference (CRID), clavicular tilt angle difference (CTAD), and T1-tilt. The study group was composed of 48 male and 43 female patients with an average age of 13.6 +/- 2.1 (10-18) years. In the questionnaire, all patients stated that their shoulders were level. The digital photographs revealed that only 17(18.7%) adolescents had absolutely level shoulders. The average height difference between shoulders was 7.5 +/- 5.8 mm. The average CHD was 6.9 +/- 5.8 mm, average CA was 2.2 +/- 1.7 degrees , average CRID was 4.8 +/- 3.6 mm, average CTAD was 4 +/- 3.2 degrees , and average T1-tilt was 1.3 +/- 1.4 degrees . CHD, CA, and CRID demonstrated high correlation with clinical pictures, whereas CTAD demonstrated moderate and T1-tilt demonstrated only mild correlation. The radiological parameters used to evaluate the shoulder balance correlate with the clinical appearance. Contrary to popular belief, shoulder balance in healthy adolescents often does not exist.

Is prism adaptation "for" growth?

The assumption that prism adaptation mechanisms evolved for developmental plasticity was questioned by analyzing natural transformations (magnification, rotation, displacement) of the arm and shoulder. Accommodating ordinary movement was found to be a closer match to prisms than transformations caused by growth. In addition, overlap between equations of movement and growth may point to a distal function of adaptation that is very general.

Growth of the pectoral girdle of the Leopard frog, Rana pipiens (Anura: Ranidae).

This article describes the growth of the anuran pectoral girdle of Rana pipiens and compares skeletal development of the shoulder to that of long bones. The pectoral girdle chondrifies as two halves, each adjacent to a developing humerus. In each, the scapula and coracoid form as single foci of condensed chondrocytes that fuse, creating a cartilaginous glenoid bridge articulating with the humerus. Based on histological sections, both the dermal clavicle and cleithrum begin to ossify at approximately the same time as the periosteum forms around the endochondral bones. The dermal and endochondral bones of the girdle form immobile joints with neighboring girdle elements; however, the cellular organization and growth pattern of the scapula and coracoid closely resemble those of a long bone. Similar to a long bone epiphysis, distal margins of both endochondral elements have zones of hyaline, stratified, and hypertrophic cartilages. As a result, fused elements of the girdle can grow without altering the glenoid articulation with the humerus. Comparisons of anuran long bone and pectoral girdle growth suggest that different bones can have similar histology and development regardless of adult morphology.

Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of didelphids and remarks on the origin of the therian scapula.

The development of the scapula was studied in embryonic and postnatal specimens of Monodelphis domestica and perinatal specimens of Philander opossum, Caluromys philander, and Sminthopsis virginiae using histological sections and 3D reconstructions. Additionally, macerated skeletons of postnatal M. domestica were examined. This study focused on the detachment of the scapulocoracoid from the sternum and on the acquisition of a supraspinous fossa, a supraspinatus muscle, and a scapular spine, all these events associated with the origin of the therian shoulder girdle. In none of the specimens is there a continuity of the cartilaginous scapulocoracoid with the sternum, even though the structures are in close proximity, especially in S. virginiae. At birth, the first rib laterally presents a pronounced boss that probably contacts the humerus during certain movements. Only the acromial portion of the scapular spine, which originates from the anterior margin of the scapular blade, is preformed in cartilage. The other portion is formed by appositional bone ("Zuwachsknochen"), which expands from the perichondral ossification of the scapula into an intermuscular aponeurosis between the supra- and infraspinous muscles. This intermuscular aponeurosis inserts more or less in the middle of the lateral surface of the developing scapula. Thus, the floor of the supraspinous fossa is present from the beginning of scapular development, simultaneously with the infraspinous fossa. The homology of the therian spine with the anterior border of the sauropsid and monotreme scapula is questioned. We consider the dorsal portion (as opposed to the ventral or acromial portion) of the scapular spine a neomorphic structure of therian mammals.

[Effect of muscular dysfunction on the development of shoulder joint in children with Erb's paralysis]. / Vliianie myschechnoi disfunktsii na razvitie plechevogo sustava u detei pri paraliche Erba

In order to evaluate the disturbances of development of the shoulder joint in children with Erb's paralysis the authors conducted an X-ray examination of the shoulder girdle and the shoulder in the anterior-posterior projection. The assessment of the functional state of the muscles of the shoulder girdle was made with the aid of clinical EMG. It was established that there was a retardation of growth and ossification of the radial head of the humerus on the affected side, a decrease in the longitudinal and cross-sectional sizes of the humerus, a retardation in the development of the joint scopular cavity, disorders in spacial interrelationship in the components of the shoulder joint and internal rotation of the shoulder joint. The structural and anatomical changes in the components of the shoulder joint are associated with disorders of the neurotrophic processes in the bone tissue and the muscular dysbalance.

The developing shoulder has a limited capacity to recover after a short duration of neonatal paralysis.

Mechanical stimuli are required for the proper development of the musculoskeletal system. Removal of muscle forces during fetal or early post-natal timepoints impairs the formation of bone, tendon, and their attachment (the enthesis). The goal of the current study was to examine the capacity of the shoulder to recover after a short duration of neonatal rotator cuff paralysis, a condition mimicking the clinical condition neonatal brachial plexus palsy. We asked if reapplication of muscle load to a transiently paralyzed muscle would allow for full recovery of tissue properties. CD-1 mice were injected with botulinum toxin A to paralyze the supraspinatus muscle from birth through 2 weeks and subsequently allowed to recover. The biomechanics of the enthesis was determined using tensile testing and the morphology of the shoulder joint was determined using microcomputed tomography and histology. A recovery period of at least 10 weeks was required to achieve control properties, demonstrating a limited capacity of the shoulder to recover after only two weeks of muscle paralysis. Although care must be taken when extrapolating results from an animal model to the human condition, the results of the current study imply that treatment of neonatal brachial plexus palsy should be aggressive, as even short periods of paralysis could lead to long-term deficiencies in enthesis biomechanics and shoulder morphology.

Newborn shoulder width: a prospective study of 2222 consecutive measurements.

OBJECTIVES: To relate maternal and infant characteristics to newborn shoulder width and to evaluate the predictive value of newborn shoulder width measurement in cases of shoulder dystocia. DESIGN: Newborn shoulder width was systematically measured at birth during a period of 18 months. SETTING: Department of Obstetrics and Gynaecology of Saint-Antoine University Hospital, Paris, France. POPULATION: A total of 2222 newborn shoulder width measurements were performed and 22 cases of true shoulder dystocia occurred during the study period. METHODS: Newborn shoulder width measurements were reviewed and correlated with maternal age, parity, nonpregnant weight, weight gain during pregnancy, height, race, fasting glucose and one hour glucose levels, gestational age, birthweight and sex of the neonate. A receiver-operating characteristics curve was constructed to evaluate newborn shoulder width as a test for predicting shoulder dystocia. RESULTS: The mean newborn shoulder width was 122.06 mm (10.50 SD). Stepwise multiple regression showed that newborn shoulder width was significantly associated with birthweight (P < 0.001), parity (P = 0.04), and nonpregnant weight (P = 0.04). We estimated that the best cut off for shoulder dystocia prediction was a newborn shoulder width measurement with a low false positive rate (< 10%) in association with a high sensitivity rate. Therefore, newborn shoulder width measurement > or = 140 mm was selected. This measurement should have a low sensitivity of 27.27%, a specificity of 91.82%, a positive predictive value of 4.02%, and a negative predictive value of 99.01% for shoulder dystocia prediction. Nevertheless, birthweight > or = 4000 g should have a better predictive value retrospectively for shoulder dystocia. CONCLUSIONS: Newborn shoulder width measurement, which is strongly correlated with birthweight, still remains a poor predictor for shoulder dystocia, even when this evaluation is correct antenatally.