Differential growth and development of the upper and lower human thorax

Abstract

The difficulties in quantifying the 3D form and spatial relationships of the skeletal components of the ribcage present a barrier to studies of the growth of the thoracic skeleton. Thus, most studies to date have relied on traditional measurements such as distances and indices from single or few ribs. It is currently known that adult-like thoracic shape is achieved early, by the end of the second postnatal year, with the circular cross-section of the newborn thorax transforming into the ovoid shape of adults; and that the ribs become inclined such that their anterior borders come to lie inferior to their posterior. Here we present a study that revisits growth changes using geometric morphometrics applied to extensive landmark data taken from the ribcage. We digitized 402 (semi) landmarks on 3D reconstructions to assess growth changes in 27 computed tomography-scanned modern humans representing newborns to adults of both sexes. Our analyses show a curved ontogenetic trajectory, resulting from different ontogenetic growth allometries of upper and lower thoracic units. Adult thoracic morphology is achieved later than predicted, by diverse modifications in different anatomical regions during different ontogenetic stages. Besides a marked increase in antero-posterior dimensions, there is an increase in medio-lateral dimensions of the upper thorax, relative to the lower thorax. This transforms the pyramidal infant thorax into the barrel-shaped one of adults. Rib descent is produced by complex changes in 3D curvature. Developmental differences between upper and lower thoracic regions relate to differential timings and rates of maturation of the respiratory and digestive systems, the spine and the locomotor system. Our findings are relevant to understanding how changes in the relative rates of growth of these systems and structures impacted on the development and evolution of modern human body shape.

Figure 1. 3D landmarks.

Landmarks (red) and sliding semilandmarks (blue) used to describe the thoracic skeleton; newborn subject in frontal (a) and lateral (b) view.

Figure 2. Ontogenetic increase of thoracic size.

Changes in centroid size in males and females. X-axis shows age in years, y-axis shows centroid size.

Figure 3. Principal components analysis in shape space.

3D Scatterplots of principal components of shape with 95% confidence intervals of the adults (red ellipses) (a) PC1 versus PC2, (b) PC1 versus PC3. Note that 95% of the adult range in (a) excludes not only all group 1 subjects but also almost half of group 2. (b) The adult range includes most of group 2 and excludes most of group 1. Group mean markers are slightly enlarged and semitransparent.

Figure 4. Principal components analysis in Procrustes form space.

Form space ontogenetic shape trajectory. The growth allometry is curved in form space. A line between the enlarged semitransparent dots representing the means of the three age groups illustrates this change of orientation in growth allometry. Different projections of the ontogenetic shape trajectory show (A) PC1-PC2 and (B) PC1-PC3. The warped ribcage models show frontal views of the smallest (youngest) specimen (C) and the largest individual (G). The green transformation grid (x-y plane) shows relative upper thoracic expansion and lower thorax contraction during growth from C to G. The lateral views show shape changes from the smallest (D) to the largest individual (H) and demonstrate the complex changes in rib orientation, axial and lateral curvature. These ae more pronounced in the upper thorax (orange and red TPS grid) than in the lower (violet TPS grid) during growth. Note how the lower thoracic spine and the relative elongation of the lower ribs both contribute the lower thoracic shape changes. Superior views show the realtively strongly medio-laterally expanded thorax of the smallest (E) and the realtivley deeper chest in the largest (I). This view also shows that the posterior-most structure in the smallest individuals is the spine while in the largest it is the bilateral posterior projection of the ribcage lateral to the angulus costae (invagination of the vertebral spine). The frontal views in F) and J) illustrate the changes in thoracic shape represented by PC3 which are a considerable component of the differences between the means of group 2 (blue) and group 3 (red). These changes likely reflect growth of stature during later ontogeny.

Figure 5. Mean shapes of age groups.

Group 1 (green), 2 (blue) and 3 (red) in frontal (a-b), left lateral (d–f), superior (g-i) and inferior (j-l) views.

Figure 6. Procrustes registered means of age groups.

Group 1 (green) and 2 (blue) (a,d,g,j), age groups 2 (blue) and 3 (red) (b,e,h,k), and of all three age groups in frontal (a-b), left lateral (d–f), superior (g-i) and inferior (j-l) views.