Postcranial skeletal pneumaticity: a case study in the use of quantitative microCT to assess vertebral structure in birds

Abstract

Limb elements in birds have been characterized as exhibiting a reduction in trabecular bone, thinner cortices and decreased bending strength when pneumatized, yet it is unclear if these characteristics generalize to the axial skeleton. Thin section techniques, the traditional gold standard for bone structure studies, have most commonly been applied to the study of avian bone. This destructive technique, however, makes it subsequently impossible to use the same samples in experimental testing systems that allow researchers to correlate structure with the mechanical properties of the bone. Micro-computed tomography ( µ CT), a non-destructive X-ray imaging technique, can be used to assess the effect of pneumatization on vertebral cortical and trabecular bone through virtual extraction and structural quantification of each tissue type. We conducted a preliminary investigation of the application of µ CT methods to the study of cortical and trabecular bone structure in a small sample of pneumatic and apneumatic thoracic vertebrae. The sample consisted of two similar-sized anatids, Aix sponsa ( n = 7) and Oxyura jamaicensis ( n = 5). Volumes of interest were created that contoured (outlined) the boundaries of the ventral cortical bone shell, the trabecular compartment and the whole centrum (cortical bone + trabecular bone), and allowed independent structural analysis of each volume of interest. Results indicated that bone volume fraction of the whole centrum was significantly higher in the apneumatic O. jamaicensis than in the pneumatized A. sponsa ( A. sponsa = 36%, O. jamaicensis = 48%, P < 0.05). In contrast, trabecular bone volume fraction was similar between the two species. The ventral cortical bone shell was approximately 23% thinner ( P < 0.05) in A. sponsa (0.133 mm) compared with apneumatic O. jamaicensis (0.172 mm). This case study demonstrates that µ CT is a powerful non-destructive imaging technique that may be applied to the three-dimensional study of avian bone. The preliminary results suggest that pneumatic and apneumatic vertebrae of comparably sized avian species differ in relative bone volume, with the largest difference apparent at the level of the cortex, and not within trabecular bone. The presence of relatively thin cortices in pneumatic vertebrae is consistent with previous studies contrasting diaphyseal cortical bone between pneumatic and apneumatic long bones. Methodological issues related to this and any comparative µ CT study of bone structure are discussed.

Evolution of archosaurian body plans: skeletal adaptations of an air‐sac‐based breathing apparatus in birds and other archosaurs

“…Whereas explicit scaling studies have yet to be performed regarding the impact of whole-body postcranial skeletal pneu-matization, basic physics dictates that an air-filled volume will have a lower mass (as a function of reduced density) than an equal sized volume filled with marrow. A growing number of studies have also documented that the cortex of pneumatic bone is thinner relative to that observed in apneumatic bone (Currey and Alexander, '85;Cubo and Casinos, 2000;Fajardo et al, 2007), suggesting another mechanism by which bone specific volume-mass relationships may be altered in the context of pneumatization. Hence, in a volume constant model, the lower mass of an airfilled element would require less energy to move through the environment during normal activities such as locomotion, assuming that the structural/ mechanical integrity of an air-filled bone is sufficient to withstand physiological loads (e.g., joint-and ground-reaction forces, site-specific tendon and ligament forces) generated during life.…”

Lumbar Vertebral Body Bone Microstructural Scaling in Small to Medium‐Sized Strepsirhines

“…Two volumes of interest (VOIs) were created to characterize the whole vertebral body's (vb) (1) trabecular bone (Tb) and (2) cortical bone (Ct) shell using image analysis tools associated with the scanner. The protocol described below generally follows Fajardo et al (2007a). Each lCT scan produced a three-dimensional stack that could be viewed slice by slice.…”

“…In the vbVOI, the following three-dimensional trabecular bone structural and fabric properties (Table 2) were measured without any model assumptions (Parfitt et al, 1983;Guldberg et al, 2003) or concern for caveats related to measurements in two dimensional sections (i.e., stereology, Underwood, 1970;Weibel, 1979Weibel, , 1980: trabecular bone volume (Tb.BV), trabecular bone volume fraction (Tb.BV/TV), structure model index (Tb.SMI) (Hildebrand and Ruegsegger, 1997a), trabecular number (Tb.N) (Hildebrand et al, 1999), trabecular thickness (Tb.Th) (Hildebrand and Rü egsegger, 1997b), trabecular separation (Tb.Sp) (Hildebrand et al, 1999), connectivity density (Tb.Conn.D), and the degree of anisotropy (Laib et al, 2000;Fajardo et al, 2007a). This degree of anisotropy (DA) method has been described previously (Laib et al, 2000;Fajardo et al, 2007a).…”

Vertebral Pneumatization

“…Besides birds [6] and dinosaurs [4] pneumatization of vertebral bodies is very rare and even intraosseous gas or trapped gas in vertebral cysts is uncommon. Less than 15 human cases were found in the literature over the last 15 years involving pneumatization at the cervical level [5,10,14,15,17,19,20] and most were less than 5 mm in size.…”