Histomorphometry Of Human Cortical Bone Applications To Age Estimation
ALEXANDER G. ROBLING SAM D. STOUT
INTRODUCTION
Quantitative bone histology (histomorpho-metry) has been used to estimate age at death for nearly a century, the first published report of which appeared in 1911 (Balthazard and Lebrun, 1911). Bone histomorphometry offers a powerful tool to the skeletal biologist, and its application to age estimation in modern, historic, and prehistoric populations has been met with encouraging results. These successes can be enhanced by incorporating several recently elucidated factors affecting reliability and accuracy into histological age estimates. Such factors include sex and population variability, adequate sampling techniques—including reference sample composition, choice of skeletal element, and topographic sampling procedure—and the effects of pathological conditions and the biomechanical loading environment. Indeed, proper use of histomorphometric age estimation techniques requires an understanding of the effect of these intrinsic and extrinsic factors on derived age estimates. This chapter reviews the physiologic basis for histomorphometric age-estimation techniques,
the histomorphology of cortical bone and its relation to age estimation, some factors known to affect derived estimates, and finally, considers future directions in the field. Appendix A provides working examples of two techniques commonly used for histomorphometric age estimation and includes labeled schematic diagrams for both examples. Appendix B profiles selected age estimation techniques.
THE PHYSIOLOGIC BASIS FOR HISTOMORPHOMETRIC AGE ESTIMATION TECHNIQUES: BONE MODELING AND REMODELING
Development of the adult skeleton is achieved by growth, modeling, and remodeling. Growth and modeling are two processes that work in concert in the normal growing individual and thus will be considered together. In long bones, growth increases bone length and diameter (both internal and external) as specified by the genetic program of the organism. This baseline architecture is modified by the modeling process, which sculpts the bone's size, shape,
Biological Anthropology of the Human Skeleton, Second Edition. Edited by M. Anne Katzenberg and Shelley R. Saunders Copyright # 2008 John Wiley & Sons, Inc.
and curvature to optimally sustain the mechanical loads typically borne by that bone. The separate effects of growth and modeling are apparent in the limb bones of paralyzed, growing children and animals, which usually lack significant bone curvature, develop subnormal cortical thickness, and exhibit a roughly circular cross section. Modeling adjusts bone architecture and mass via modeling drifts, which add bone to some surfaces and remove it from others. Modeling drifts move bone through tissue space (Fig. 5.1) and can simultaneously increase or decrease the cross section's size by selectively inhibiting or promoting cellular activity at the resorptive and appositional surfaces accordingly. In the normal developing skeleton, growth and modeling result in the production of organized, parallel sheets of primary lamellar bone— circumferential and endosteal lamellae— typically visible in diaphyseal cross sections (Fig. 5.2a). Some circumferential and endosteal lamellae deposited early in the developmental period are removed or "modeled out" as the bone drifts. Thus, the adult cortex comprises a collection of lamellae exhibiting an array of different ages. Their mean age, however, is always less than the individual's chronological age. The circumferential and endosteal lamellae deposited during modeling provide the canvas on which discrete units of cortical remodeling leave their mark (see below).
Once skeletal maturity is reached, modeling reduces to a trivial level compared with that
Figure 5.1 (A): During development, modeling drifts in the middle third of the sixth rib remove bone from the internally facing surfaces and deposit bone on the externally facing surfaces. As the rib drifts laterally, the formation surfaces outpace the resorptive surfaces, and the rib gains cross-sectional area. Note that none of the tissue present in the young rib (a) is present in the adult rib (c); it has been completely "modeled out." (B): Enlarged view of the drifting rib cortex (trabeculae have been removed for clarity). The younger bone (lamellae) is darker, and the older bone is lighter. The cross section thus comprises a mosaic of different aged lamellae. (C): The same drifting rib cortex illustrated in B. The stippled region represents the size and position of the rib cortex at time 1 (arbitrarily designated as age 6 in the figure). A year later (shaded silhouette), some cortex that was present at age 6 is still present (region exhibiting both stippling and shading). However, nearly half of the cortical bone present at age 7 did not exist in the same rib just one year earlier. Bone modeling is a dynamic process in the growing skeleton that regularly and rapidly alters the size, shape, relative position, and age of bone tissue.
Figure 5.1 (A): During development, modeling drifts in the middle third of the sixth rib remove bone from the internally facing surfaces and deposit bone on the externally facing surfaces. As the rib drifts laterally, the formation surfaces outpace the resorptive surfaces, and the rib gains cross-sectional area. Note that none of the tissue present in the young rib (a) is present in the adult rib (c); it has been completely "modeled out." (B): Enlarged view of the drifting rib cortex (trabeculae have been removed for clarity). The younger bone (lamellae) is darker, and the older bone is lighter. The cross section thus comprises a mosaic of different aged lamellae. (C): The same drifting rib cortex illustrated in B. The stippled region represents the size and position of the rib cortex at time 1 (arbitrarily designated as age 6 in the figure). A year later (shaded silhouette), some cortex that was present at age 6 is still present (region exhibiting both stippling and shading). However, nearly half of the cortical bone present at age 7 did not exist in the same rib just one year earlier. Bone modeling is a dynamic process in the growing skeleton that regularly and rapidly alters the size, shape, relative position, and age of bone tissue.
Figure 5.2 (a) Undecalcified cross section of a tibial diaphysis illustrating cortical histomorphology. Cross (f) = circumferential (primary) lamellar bone. Solid arrow = type I (common) osteons. Feathered arrow = type II osteon. Darts (+«) = osteon fragments. Asterisk (*) = resorptive bay. Open arrow (O) = drifting osteon. Open point (>) = primary osteon. Closed point (>) = primary vascular canal (non-Haversian canal). (b) Microradiograph from an ulnar diaphysis illustrating a double-zonal osteon (center). Note that the arrest line (lighter ring) follows the contours of the centripetal lamellae and osteocyte lacunae.
Figure 5.2 (a) Undecalcified cross section of a tibial diaphysis illustrating cortical histomorphology. Cross (f) = circumferential (primary) lamellar bone. Solid arrow = type I (common) osteons. Feathered arrow = type II osteon. Darts (+«) = osteon fragments. Asterisk (*) = resorptive bay. Open arrow (O) = drifting osteon. Open point (>) = primary osteon. Closed point (>) = primary vascular canal (non-Haversian canal). (b) Microradiograph from an ulnar diaphysis illustrating a double-zonal osteon (center). Note that the arrest line (lighter ring) follows the contours of the centripetal lamellae and osteocyte lacunae.
which occurs during development. Renewed modeling in the adult skeleton can occur, however, in some disease states and in cases where the mechanical loading environment has been altered radically. These observations are relevant to those using histomorphometric techniques to estimate age because renewed adult modeling, in the absence of a concurrent increase in remodeling, will decrease the mean tissue age and ultimately result in age estimates lower than actual age.
Unlike modeling, which involves either resorption or formation (but not both) at a locus, bone remodeling always follows an activation ! resorption ! formation sequence at a locus (Fig. 5.3). Remodeling removes and replaces discrete, measurable "packets" of bone. These packets, or bone structural units (BSUs), form the basis for most histomorpho-metric age estimation techniques. Within the cortex of bone, BSUs comprise secondary osteons.
- Figure 5.3 (top) Longitudinal view of a BMU moving through tissue space from right to left. (bottom) Schematic illustrations of an evolving osteon corresponding to selected transverse sections of the longitudinal system depicted above. [Redrawn after Stout (1989).]
Bone is remodeled by a complex arrangement of cells, collectively called the basic multicellular unit (BMU). Intracortical BMUs tunnel through long bone diaphyses in a nearly longitudinal orientation (Hert et al. 1994). The leading region of the BMU is lined with osteoclasts—specialized cells capable of bone resorption. The diameter of the tunnel excavated by osteoclasts, which typically reaches roughly 250-300 mm, defines the cross-sectional size of the osteon that will form in its wake. A histological section that transects the resorptive phase of a BMU (the cutting cone) will exhibit a cavity with rough, scalloped edges (Howship's lacunae), known as a resorptive bay (Figs. 5.2a and 5.3). Howship's lacunae are characteristic of all actively resorbing bone surfaces.
Following closely behind the osteoclasts is a group of mononuclear cells. The exact function of these cells remains unclear (Eriksen and Langdahl, 1995). Mononuclear cells line the resorptive bay during the reversal phase (the period between resorption and formation). It is likely that they smooth off the scalloped periphery of the resorptive bay in preparation for the deposition of a reversal line—a thin, mineral-deficient, sulfur-rich layer of matrix that separates an osteon from surrounding interstitial lamellae (Schaffler et al., 1987). An appreciation of reversal lines is particularly important in applying histomorphometric age estimation techniques because their presence can be used to differentiate secondary osteons (a product of remodeling) from primary osteons (a product of modeling).
Behind the mononuclear cells, rows of osteo-blasts adhere to the reversal zone and deposit layers of osteoid (unmineralized bone matrix) centripetally. The size of the remodeling space constricts as more concentric osteonal lamellae are deposited and mineralized. At a specified point, deposition ceases leaving a Haversian canal in the center.
Post a comment