Richard A. Lazenby

Methodological considerations for analyzing trabecular architecture: an example from the primate hand

Micro‐computed tomographic analyses of trabecular bone architecture have been used to clarify the link between positional behavior and skeletal anatomy in primates. However, there are methodological decisions associated with quantifying and comparing trabecular anatomy across taxa that vary greatly in body size and morphology that can affect characterizations of trabecular architecture, such as choice of the volume of interest (VOI) size and location. The potential effects of these decisions may be amplified in small, irregular‐shaped bones of the hands and feet that have more complex external morphology and more heterogeneous trabecular structure compared to, for example, the spherical epiphysis of the femoral head. In this study we investigate the effects of changes in VOI size and location on standard trabecular parameters in two bones of the hand, the capitate and third metacarpal, in a diverse sample of nonhuman primates that vary greatly in morphology, body mass and positional behavior. Results demonstrate that changes in VOI location and, to a lesser extent, changes in VOI size had a dramatic affect on many trabecular parameters, especially trabecular connectivity and structure (rods vs. plates), degree of anisotropy, and the primary orientation of the trabeculae. Although previous research has shown that some trabecular parameters are susceptible to slight variations in methodology (e.g. VOI location, scan resolution), this study provides a quantification of these effects in hand bones of a diverse sample of primates. An a priori understanding of the inherent biases created by the choice of VOI size and particularly location is critical to robust trabecular analysis and functional interpretation, especially in small bones with complex arthroses.

Scaling VOI size in 3D μCT studies of trabecular bone: a test of the over-sampling hypothesis.

For comparative 3D microCT studies of trabecular bone, the use of a volume of interest (VOI) scaled to body size may avoid over-sampling the trabecular mass in smaller versus larger-bodied taxa and comparison of regions that are not functionally homologous (Fajardo and Müller: Am J Phys Anthropol 115 (2001) 327-336), though the influence on quantitative analyses using scaled versus nonscaled VOIs remains poorly characterized. We compare trabecular architectural properties reflecting mass, organization, and orientation from three volumes of interest (large, scaled, and small) obtained from the distal first metacarpal in a sample of Homo (n = 10) and Pan (n = 12). We test the null hypotheses that neither absolute VOI size, nor scaling of the VOI to metacarpal size as a proxy for body size, biases intraspecific analyses nor impacts the detection of interspecific differences. These hypotheses were only partially supported. While certain properties (e.g., bone volume fraction or trabecular thickness) were not affected by varying VOI size within taxa, others were significantly impacted (e.g., intersection surface, connectivity, and structure). In comparing large versus scaled VOIs, we found that the large VOI inflated the number and/or magnitude of significant differences between Homo and Pan. In summary, our results support the use of scaled VOIs in studies of trabecular architecture.

Second metacarpal midshaft geometry in an historic cemetery sample.

Study of bone mass at the second metacarpal midshaft has contributed to our understanding of skeletal growth and aging within and between populations and has relied extensively on noninvasive techniques and in particular radiogrammetric data. This study reports age, sex, and side variation in size and shape data acquired from direct measurement of cross-sections obtained from a large (n = 356), homogeneous skeletal sample. Correlation analysis and three-way ANOVA of size-adjusted data confirm general impressions of patterned variation in this element: males have absolutely but not necessarily relatively larger bones than females; the right side is larger than the left, though a larger than expected proportion (approximately 25%) of left metacarpals exhibits greater values than the right; and bone mass but not strength (in males) declines with age. Contrary to the widely accepted assumption of circularity for this location, direct measurement of cross-sectional geometry confirms previous biplanar radiogrammetric conclusions regarding the noncircularity of the second metacarpal midshaft and identifies a significant difference between males and females, with the latter having a more cylindrical diaphysis. Deviation of the axes of maximum and minimum bending strength associated with noncircularity suggests a distribution of bone mass to resist bending moments perpendicular to the distal palmar arch, though this conclusion awaits more robust study of the functional anatomy of the metacarpal diaphysis.

Low Bone Mass in Past and Present Aboriginal Populations

A slight and gradual loss of bone mass is characteristic of all aging primates, if they live long enough (Garn, 1970; Burr, 1980). Nevertheless, the observation of reduced bone mass among ancestral human skeletal remains is limited to relatively recent populations. Since the domestication of plants roughly 12,000 years ago, skeletal remains from disparate parts of the world have occasionally shown low bone mass. Perhaps earlier populations did not suffer age-related bone loss because they died at young ages (Pfeiffer, 1990), or perhaps their diet or lifestyle facilitated effective bone maintenance. Past human populations were more dependent on local natural resources and their own physical labor for subsistence, a cultural pattern maintained by only a few geographically isolated aboriginal groups today. These “anthropological populations” have been portrayed as natural paradigms whose dietary habits might be studied as representations of our species’ natural “set point” for nutritional requirements, and against which we might evaluate modern regimens and their biological consequences (Eaton et al., 1988; Eaton and Nelson, 1991).

Second metacarpal cross‐sectional geometry: Rehabilitating a circular argument

Radiogrammetry of the second metacarpal has long served as a measure of normal and abnormal bone growth and aging, functional asymmetry, and fracture risk in osteoporosis. The method relies on algebraic interpretation (circular or elliptical models) of uni‐ or biplanar radiographic images. This paper tests the conformance of these models with actual measures of metacarpal geometric variation in a sample of 356 bones from an historic archaeological sample. Both the circular and elliptical models significantly over‐estimate actual values for all variables (e.g., total area (3.05% and 9.42%, respectively) and cortical area (7.25% and 12.25%), bending rigidity about the mediolateral (13.88% and 20.92%) and anteroposterior axes (17.35% for the elliptical model). The greater degree of systematic bias found for the elliptical model is contrary to results of an earlier study (Lazenby, 1997), and suggests that sample composition can influence the method error associated with a particular approach. The import of radiogrammetric bias will depend on the degree of shape variation among samples compared (e.g., left vs right, male vs female, etc.), which in most cases cannot be predetermined. Consequently, reduced major axis equations were derived from regressing actual on estimated values for total area (TA), cortical area (CA) and two measures of bending rigidity (Ix, Iy) in order to permit adjustment for radiogrammetric error associated with these algebraic models. Application of these formulae to a hold‐out sample showed no significant differences between actual and predicted values. Am. J. Hum. Biol. 10:747–756, 1998.

A three-dimensional microcomputed tomographic study of site-specific variation in trabecular microarchitecture in the human second metacarpal

Variation in trabecular microarchitecture is widely accepted as being regulated by both functional (mechanical loading) and genetic parameters, although the relative influence of each is unclear. Studies reporting inter‐site differences in trabecular morphology (volume, number and structure) reveal a complex interaction at the gene–environment interface. We report inter‐ and intra‐site variation in trabecular anatomy using a novel model of contralateral (left vs right) and ipsilateral (head vs base) comparisons for the human second metacarpal in a sample of n = 29 historically known 19th century EuroCanadians. Measures of bone volume fraction, structure model index, connectivity, trabecular number, spacing and thickness as well as degree of anisotropy were obtained from 5‐mm volumes of interest using three‐dimensional microcomputed tomography. We hypothesized that: (i) the more diverse loading environment of metacarpal heads should produce a more robust trabecular architecture than corresponding bases within sides and (ii) the ipsilateral differences between epiphyses will be larger on the right side than on the left side, as a function of handedness. Analysis of covariance (Side × Epiphysis) with Age as covariate revealed a clear dichotomy between labile and constrained architectures within and among anatomical sites. The predicted variation in loading was accommodated by changes in trabecular volume, whereas trabecular structure did not vary significantly by side or by epiphysis within sides. Age was a significant covariate only for females. We conclude that environmental and genetic regulation of bone adaptation may act through distinct pathways and local anatomies to ensure an integrated lattice of sufficient mass to meet normal functional demands.

Circumferential variation in human second metacarpal cortical thickness: Sex, age, and mechanical factors

Variation in cortical thickness (CT) in four quadrants of the human second metacarpal was investigated in a sample (100 males and 72 females, skeletal age 20 to 50+ years) from a 19th‐century cemetery. Both left and right elements were studied (total N = 344). Multivariate analysis of covariance (MANCOVA) (for age, sex, and side, controlling for absolute size) was used to test the hypothesis of equality of thickness in the dorsal, palmar, medial, and lateral quadrants. Differences in regional CT posits localized regulation of resorption and formation adapting bone shape to functional loads, with implications for activity‐modulation of skeletal senescence. The palmar cortex was found to be uniformly thicker in both sexes and both sides, and at all ages (young, middle, and old adult); the medial, lateral, and dorsal cortices did not differ significantly. Patterns of age‐related loss occurring preferentially at the endocortical surface differed between men and women, with women showing significant declines across all age groups for all quadrants, and males only small decrements after middle age. The greater CT in the palmar quadrant corresponds to the region of maximum compressive strain in the second metacarpal for functions involving full flexion (grasping). Although the palmar cortex is thicker at all ages, women lose mass in that quadrant at the same rate as in other quadrants, suggesting that function does not offer protection against endocrinologically‐mediated depletion of bone mass (postmenopausal osteopenia). Anat Rec 267:154–158, 2002.

Osteometric variation in the Inuit second metacarpal: a test of Allen's Rule

Bergmanns and Allens Rules predict a relationship between climate and morphology as a thermoregulatory adaptation. These ecogeographic principles predict/explain change in the ratio of body surface area to body mass in hot and cold climates. With regard to Allens Rule we would expect short and relatively broad limb proportions. Such adaptation should be observable in skeletal architecture. This paper provides a test of Allens Rule using osteometric data for the second metacarpal from the Sadlermiut of Southampton Island, Northwest Territories, Canada. Following adjustment for body size, ANOVA by sample and sex shows the Sadlermiut second metacarpal to be shorter, wider at the base and deeper at the distal metacarpophalangeal joint, in comparison to an historic sample of European settlers. This pattern of difference suggests an Inuit hand with a thermally adapted morphology, viz. a large mass relative to surface area. Copyright

Bone loss, traditional diet, and cold adaptation in Arctic populations

North American Inuit and Inupiat (“Eskimo”) populations have been described as having a lower bone mass relative to Caucasians as a consequence of their traditional high‐protein “acid‐ash” diet. However, this bone buffering mechanism has also been implicated as a risk factor for osteoporosis in industrialized Caucasian populations, and one recent study has found a positive association between dietary protein, and bone mass in premenopausal women. The original studies documenting the Eskimo‐Caucasian difference in aging bone loss do not consider the consequences of population variation in body composition, in particular lean body mass (LBM), which correlates with bone mass. The possibility also exists that the original reference sample may be exceptional rather than normative for bone mineral density (BMD). Regression analysis was conducted on published age‐ and sex‐specific cohort means for BMD, and bone mineral content adjusted for estimates of LBM for the original Eskimo‐Caucasian comparisons, and for an additional Caucasian sample from Belgium. Significant differences were found between all groups, including Belgians, and the Wisconsin sample for BMD, supporting the notion of the latter having exceptional bone quality when measured as BMD. When adjusted for LBM, the Eskimo samples are distinct in pattern and magnitude of aging bone loss relative to Caucasians, supporting the hypothesis of real inter‐population differences. However, given the current ambiguity surrounding the “protein‐calcium buffering” model, an alternative explanation is offered. It is hypothesized that the accelerated bone loss among the Inuit and Inupiat reflects higher production and utilization of the thyroid hormones, T4 and T3, as a mechanism of cold adaptation through enhanced nonshivering thermogenesis. Am. J. Hum. Biol. 9:329–341, 1997.

Trabecular architecture in the thumb of Pan and Homo: implications for investigating hand use, loading, and hand preference in the fossil record

OBJECTIVES Humans display an 85-95% cross-cultural right-hand bias in skilled tasks, which is considered a derived behavior because such a high frequency is not reported in wild non-human primates. Handedness is generally considered to be an evolutionary byproduct of selection for manual dexterity and augmented visuo-cognitive capabilities within the context of complex stone tool manufacture/use. Testing this hypothesis requires an understanding of when appreciable levels of right dominant behavior entered the fossil record. Because bone remodels in vivo, skeletal asymmetries are thought to reflect greater mechanical loading on the dominant side, but incomplete preservation of external morphology and ambiguities about past loading environments complicate interpretations. We test if internal trabecular bone is capable of providing additional information by analyzing the thumb of Homo sapiens and Pan. MATERIALS AND METHODS We assess trabecular structure at the distal head and proximal base of paired (left/right) first metacarpals using micro-CT scans of Homo sapiens (n = 14) and Pan (n = 9). Throughout each epiphysis we quantify average and local bone volume fraction (BV/TV), degree of anisotropy (DA), and elastic modulus (E) to address bone volume patterning and directional asymmetry. RESULTS We find a right directional asymmetry in H. sapiens consistent with population-level handedness, but also report a left directional asymmetry in Pan that may be the result of postural and/or locomotor loading. CONCLUSION We conclude that trabecular bone is capable of detecting right/left directional asymmetry, but suggest coupling studies of internal structure with analyses of other skeletal elements and cortical bone prior to applications in the fossil record.