Interindividual Variation in Functionally Adapted Trait Sets Is Established During Postnatal Growth and Predictable Based on Bone Robustness

Abstract

Adults acquire unique sets of morphological and tissue-quality bone traits that are predictable based on robustness and deterministic of strength and fragility. How and when individual trait sets arise during growth has not been established. Longitudinal structural changes of the metacarpal diaphysis were measured for boys and girls from 3 mo to 8 yr of age using hand radiographs obtained from the Bolton-Brush collection. Robustness varied approximately 2-fold among boys and girls, and individual values were established by 2 yr of age, indicating that genetic and environmental factors controlling the relationship between growth in width and growth in length were established early during postnatal growth. Significant negative correlations between robustness and relative cortical area and a significant positive correlation between robustness and a novel measure capturing the efficiency of growth indicated that coordination of the subperiosteal and endocortical surfaces was responsible for this population acquiring a narrow range of trait sets that was predictable based on robustness. Boys and girls with robust diaphyses had proportionally thinner cortices to minimize mass, whereas children with slender diaphyses had proportionally thicker cortices to maximize stiffness. Girls had more slender metacarpals with proportionally thicker cortices compared with boys at all prepubertal ages. Although postnatal growth patterns varied in fundamentally different ways with sex and robustness, the dependence of trait sets on robustness indicated that children sustained variants affecting subperiosteal growth because they shared a common biological factor regulating functional adaptation. Considering the natural variation in acquired trait sets may help identify determinants of fracture risk, because age-related bone loss and gain will affect slender and robust structures differently.