The idea that primary bone microstructure may reflect bone formation rate was suggested by Amprino (1947) and is a general finding that has been reported by Currey (2002), Stover et al. (1992) and others (de Ricqlès et al., 1991; Mori et al., 2003). This relationship has been demonstrated experimentally in mallard duck limb bones by Castanet et al. (1996) and de Margerie et al. (2002). de Margerie et al. (2004) advanced these studies by examining growth rates and associated bone tissue types (‘laminar’, ‘longitudinal’, ‘reticular’ or ‘radial’ fibrolamellar) in transverse sections in growing king penguin limb bones (i.e., humerus, radius, femur, tibiotarsus). They showed that the highest growth rates were associated with ‘radial’ microarchitecture of fibrolamellar bone, where vascular cavities in the woven network are aligned radially. Additionally, there seems to be a greater tendency for the microstructure of slower growing bone to be aligned in the longitudinal direction, especially if growth is greater in that direction. For example, Petrtyl et al. (1996) speculate that the longitudinal orientation of the canals in the primary bone tissue of the human femoral diaphysis is a consequence of longitudinal shifting of the periosteum against the bone surface. Similar interpretations have been suggested for the longitudinal primary vascular canals in the slow-growing long bones of alligators (Lee, 2004).
Click here to see the study of de Margerie et al. (2004)
When considering potential evidence of bone adaptation in the three-dimensional vascular patterns of bone it is important to ask whether or not the vessels are within primary bone or secondary bone. This important distinction, which distinguishes unremodeled from remodeled bone, is not yet reliable in micro-level computerized tomographic images because the current state of this technology does not provide sufficient resolution (Cooper et al., 2006; Pazzaglia et al., 2010). Nevertheless, when considering vascular architecture in primary bone this possibility should be considered: preferred vascular orientation in bone may simply be a product of programmed development expressed as different rates of osteogenesis within and between skeletal elements. Alternatively, the regional nanostructural anisotropy (i.e., predominant CFO) of the bone matrix that surrounds the vessels can be independent of rates of osteogenesis. This matrix anisotropy can be enhanced, and may be dramatically different, between regions exposed to different mechanical loads during matrix formation. As noted, prevalent/predominant strain characteristics that appear to be most clearly linked with the production of these variations include specific strain modes (i.e. tension, compression and shear). In this case, it is the ‘adaptability’ of CFO, not the vascular orientation that is relatively more important in producing the apparent CFO differences. Prospective experimental studies, although limited, support an important causal role for strain mode in this context (Boskey et al., 1999; Puustjarvi et al., 1999; Takano et al., 1999). In this interpretation, predominant CFO may be more strongly influenced by load history, which contrasts with situations where three-dimensional arrangement of vessels (e.g., preferred orientations) may be more strongly influenced by the rate of osteogenesis. The point here is that in some cases osteogenesis can result in bone histology that could fool investigators into thinking that they have detected accommodations/adaptations to load history. Again, this issue is typically a consideration in cases where osteon formation is scarce or absent; more examples and discussion on this topic can be found in Skedros and Hunt (2004), Schneider et al. (2007), and Pazzaglia et al. (2007).
Amprino R. 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement. Arch. Biol. 58:315-330.
Boskey AL, Wright TM, Blank RD. 1999. Collagen and bone strength. J. Bone Miner. Res. 14:330-335.
Castanet J, Grandin A, Abourachid A, de Ricqlès A. 1996. [Expression of growth dynamic in the structure of the periosteal bone in the mallard, Anas platyrhynchos]. C R Acad Sci III 319:301-308.
Cooper D, Thomason C, Clement J, Hallgrimsson B. 2006. Three-dimensional microcomputed tomography imaging of basic multicellular unit-related resorption spaces in human cortical bone. Anat Rec A Discov Mol Cell Evol Biol 288:806-816.
Currey JD. 2002. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press.
de Margerie E. 2002. Laminar bone as an adaptation to torsional loads in flapping flight. J. Anat. 201:521-526.
de Margerie E, Robin JP, Verrier D, Cubo J, Groscolas R, Castanet J. 2004. Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). J Exp Biol 207:869-879.
de Ricqlès A, Meunier FJ, Castanet L, Francillon-Vieillot H. 1991. Comparative microstructure of bone. In: Hall BK, editor. Bone. Boca Raton, FL: CRC Press. p 1-78.
Lee AH. 2004. Histological organization and its relationship to function in the femur of Alligator mississippiensis. J. Anat. 204:197-207.
Mori R, Kodaka T, Sano T, Yamagishi N, Asari M, Naito Y. 2003. Comparative histology of the laminar bone between young calves and foals. Cells Tissues Organs 175:43-50.
Pazzaglia UE, Bonaspetti G, Rodella LF, Ranchetti F, Azzola F. 2007. Design, morphometry and development of the secondary osteonal system in the femoral shaft of the rabbit. J Anat 211:303-312.
Pazzaglia UE, Zarattini G, Giacomini D, Rodella L, Menti AM, Feltrin G. 2010. Morphometric analysis of the canal system of cortical bone: An experimental study in the rabbit femur carried out with standard histology and micro-CT. Anat Histol Embryol 39:17-26.
Petrtýl M, Hert J, Fiala P. 1996. Spatial organization of Haversian bone in man. J. Biomech. 29:161-169.
Puustjarvi K, Nieminen J, Rasanen T, Hyttinen M, Helminen HJ, Kroger H, Huuskonen J, Alhava E, Kovanen V. 1999. Do more highly organized collagen fibrils increase bone mechanical strength in loss of mineral density after one-year running training? J Bone Miner Res 14:321-329.
Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, Muller R. 2007. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 22:1557-1570.
Skedros JG, Hunt KJ. 2004. Does the degree of laminarity mediate site-specific differences in collagen fiber orientation in primary bone? An evaluation in the turkey ulna diaphysis. J. Anat. 205:121-134.
Stover SM, Pool RR, Martin RB, Morgan JP. 1992. Histological features of the dorsal cortex of the third metacarpal bone mid-diaphysis during postnatal growth in thoroughbred horses. J Anat 181:455-469.
Takano Y, Turner CH, Owan I, Martin RB, Lau ST, Forwood MR, Burr DB. 1999. Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution. J Orthop Res 17:59-66.