Growth in Bone Mass and SizeAre Racial and Gender Differences in Bone Mineral Density More Apparent than Real?
Ego Seeman and
M. D.
Austin and Repatriation Medical Centre
University of Melbourne
Melbourne, Australia 3084
Address correspondence and requests for reprints to: E. Seeman, M.D., Department of Endocrinology, Austin and Repatriation Centre, Heidelberg, Melbourne, 3084, Australia. E-mail:
ego{at}austin.unimelb.edu.au
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Introduction
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In this issue of JCEM, Gilsanz and
colleagues (1) (see page 1420) present data that give us insight into
the racial differences in bone mass, bone size, and bone mineral
density (BMD), which may partly contribute to the lower incidence of
fractures in blacks than in whites. The work is refreshing reading
because of the meticulous attention to study design and the resultant
credibility of the observations.
The investigators matched 80 black females and males with 80 whites of
the same gender, age, bone age, pubertal stage, height, and weight, and
report that: (i) blacks have higher volumetric apparent BMD of the
cancellous (trabecular) bone of the vertebral body; (ii) there are no
racial differences in femoral midshaft cortical thickness or its true
BMD; (iii) blacks have longer legs and a larger femoral midshaft
cross-sectional area, but shorter trunk length and vertebral height
(despite having the same vertebral cross sectional area).
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Apparent and true bone mineral density
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Many insights arise from this work, but few can be appreciated
unless the difference between "true" and "apparent" BMD is
understood. "True" (or material) BMD is the mass of a substance per
unit volume of its own uniform bulk; the true BMD of a
single trabecula, or the true BMD of cortical bone itselfdevoid of
its canals, canaliculae and spaces. Noninvasive methods such as dual
x-ray absorptiometry, measure "apparent" BMDthe mass of mineral
in a skeletal region, not all of which is bone. These regions
(eg. the vertebra or femur) are composed of mineral
fashioned into cortical bone and trabecular bone within a central
medullary cavity containing marrow.
The measurement provided by bone densitometry is commonly expressed as
an apparent bone mineral content (BMC, g) or as an areal apparent BMD
(g/cm2). "Areal" apparent BMD is derived by dividing
the regions BMC by its projected area in the coronal planethe
regions depth is not "seen" by the technology. Thus, bone size is
not taken into account in the apparent BMC measurement and only partly
taken into account in the areal apparent BMD measurementthe bigger
the bone, the higher the apparent BMC or areal apparent BMD.
The terms "apparent" and "areal" are almost universally dropped
from the literature for brevity and convenience, but at the price of
understanding that the size of the bone influenced the reported
"density" measurement. Larger bones in older children compared with
younger children, in blacks compared with whites, or males compared
with females, will be reported as having a higher (apparent) BMC or
(areal apparent) BMD, even though the amount of bone contained within
the periosteal envelope of the boneits volumetric BMDmay not be
higher (2, 3).
Quantitative computed tomography (QCT) measures volumetric BMD
(g/cm3)a measurement often mistakenly called "true"
BMD because it is volumetric. (Unstated, but implicit in the subtle
misuse of the word "true" is the unsubstantiated notion that this
is the better predictor of fracture than BMC or areal BMD.) QCT-derived
volumetric BMD is also an apparent BMD, or the amount of bone mineral
within a unit volume of bone, not all of which is mineral. Although
independent of external bone size, an increase in volumetric apparent
BMD during growth or a higher volumetric apparent density in blacks
than in whites, still tells us nothing about the morphological basis of
this increase in volumetric apparent BMD (3).
In trabecular bone, volumetric apparent BMD may increase during growth,
or it may be higher in blacks than in whites, in men than in women, in
any one or more of three ways: by increasing trabecular numbers, by
increasing trabecular thickness, or by increasing the true (material)
density of the trabeculae within this cubic volume of bone comprised of
trabecular mineral plates and sheets and marrow (Fig. 1
).

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Figure 1. Cartoon illustrating that volumetric trabecular
apparent bone mineral density (BMD) may increase in one or more of
three ways. The morphological basis of the increase is different, and
has different biological and perhaps biomechanical implications.
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The same mineral mass fashioned into greater trabecular numbers of half
the thickness results in a structure with more surface per unit mineral
mass than the same mineral mass fashioned into half the number of
trabeculae of double the thickness. Thinner trabeculae may be a
disadvantage at menopause when increased bone remodeling, a
surface-based phenomenon, may cause perforation of trabeculae. The same
mass fashioned with thicker trabeculae will have less surface per unit
volume, and so less surface available for remodeling to occur upon.
This is partly why bone remodeling may be slower with less of the
mineral mass "turned over" annually in blacks (4, 5, 6).
In a long bone such as the midshaft of the femur, volumetric apparent
BMD may be higher in blacks than in whites, or in men than in women in
two ways; for long bones of the same external dimensions, either the
cortex will be thicker (and the medullary cavity smaller) or the
cortical bone true BMD may be higher. True BMD of the bone remains
constant during life (7) or may increase in response to drug therapy
(8). During aging, increased intracortical porosity will reduce
cortical bone mass; apparent BMC will decrease but the true BMD of the
remaining cortical bone does not change (7). Figure 2
illustrates how intracortical porosity
increases with advancing age, while apparent BMD decreases. The decline
in apparent BMD is proportional to the increase in intracortical
porosity, but the true BMD of the remaining cortical bone is constant
(7). (QCT does not have the resolution to exclude canaliculi and canals
from the true BMD measurement. Thus, true BMD of cortical bone may be
underestimated when measured by QCT).

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Figure 2. In men and women, porosity (P), (the percentage of
cortical bone occupied by vascular cavities) increased with age.
Apparent mineral density (AMD) and ash weight per unit cortical bone
volume decreased with age and correlated with porosity. The true
mineral density (TMD)ash weight per unit volume of bone free of its
canals and resorption spaces remained unchanged with age (Laval-Jeantet
et al. Ref 7).
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Another level of complexity occurs during growth. Volumetric apparent
BMD not only depends on the amount of cortical and trabecular bone
contained within the periosteal surface of the bone during growth and
its true BMD. It also depends on the growth of the external size of the
bone relative to the accrual of bone taking place within the
growing bone. These processes are dissociated in time (because they are
regulated differently); at any age, size is nearer its peak adult value
than is the mineral accrued within it (9). Illness interrupting growth
may affect mineral accrual more than size (as size is nearer its peak),
contributing to reduced volumetric apparent BMD. At the age of 1213
yr, a time of increased fractures in children, growth in length and
mineral accrual are most dissociated (9).
So, if the growth in external size of the bone increases, apparent BMC
and areal apparent BMD increaseno surprisethe size of the bone is
increasing (upper panels, Fig. 3
) (10). However, if the increase in size
is matched by a proportional increase in the mass within its periosteal
envelope, volumetric apparent BMD remains constant during growth
(lower panels, fig. 3
). This appears to occur in long bones
such as the midshaft of the femur and the radius; volumetric apparent
BMD is independent of age during growth (10, 11). The
fascinating implication of this data is that the relative position of
an individuals long bone volumetric apparent BMD in the normal
distribution must be determined at birth, if not before!

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Figure 3. Areal and volumetric femoral shaft bone mineral
density (BMD) plotted against age for males and females. Lu et
al. (10). With permission.
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If growth in mineral mass contained within the periosteal surface of
the bone is proportionately more than the increase in its size,
volumetric apparent BMD increases. This occurs in the vertebral body.
As shown in Fig. 4
, volumetric apparent
BMD is constant until late puberty and then increases in boys and girls
by a similar amount (12) and probably because of increasing trabecular
thickness rather than numbers (4, 5, 13).

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Figure 4. Vertebral volumetric trabecular apparent bone
mineral density (BMD) in white and girls is similar before puberty and
independent of age until puberty when comparable increases occur. Drawn
from data in the legend of Fig. 2 , Gilsanz et al. (14).
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To summarize, (i) areal apparent BMD, as measured noninvasively, is
confounded by bone size; increasing areal apparent BMD during growth or
higher areal apparent BMD in one individual compared with another may
be the result of greater size; (ii) if size is constant, increasing
areal or volumetric apparent BMD may be the result of increasing
cortical thickness, trabecular number or thickness, or increasing true
(material) density of these structures; (iii) if size and accrual are
both increasing, apparent volumetric BMD depends on their
relative changes. Thus, when we speak of higher BMD in
blacks than whites, in men than women, what do we really mean? Now to
the work.
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Racial and gender differences in vertebral volumetric trabecular
apparent BMD
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A glance at the figures in the paper by Gilsanz and colleagues on
page 1420, shows that before puberty there were no racial or gender
differences in volumetric apparent BMD of the trabecular bone of the
vertebral body (1). Thus, by inference, before puberty, trabecular
number, thickness, and their true (material) BMD do not differ by race
or gender. Racial differences emerged at puberty; vertebral volumetric
trabecular apparent BMD was approximately 250260 mg/cm3
in Tanner stage 1 in blacks, whites, males, and females, increasing by
approximately 40 mg/cm3 in white females and males and by
approximately 80 mg/cm3 in black females and males by
Tanner stage 5. However, within a race, the increases in boys and girls
during puberty were no different. Gilsanz and colleagues have reported
this race-specific, but gender-independent effect of puberty in two
previous studies (12, 14). Aaron and colleagues (15) have reported no
difference in trabecular number and thickness in white males and
females in young adulthood.
So, in young adulthood, peak vertebral volumetric trabecular apparent
BMD is higher in black than in white men, and is higher in black than
in white women, but is no different in women and men of the same race.
Han et al. (4, 5) report that blacks have thicker trabeculae
than whites, not greater numbers. This has not been found in other
studies, perhaps in part because of sample size considerations and
morphological differences in African blacks and American blacks (6, 13, 16, 17). Whether the true BMD of trabeculae themselves is higher in
blacks is unknown. QCT does not have the resolution to determine true
BMD of a single trabecula. However, there is histomorphometric data
supporting this possibility (16).
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Racial and gender differences in femoral midshaft cortical
thickness and true BMD
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Neither the width of the cortical bone of the mid-shaft of the
femur, nor its true BMD (determined by QCT) differed in blacks and
whites. However, the periosteal diameter of the shaft was greater in
blacks. Although the cortical width was the same, the amount of
cortical bone was greater (apparent BMC was greater) because the
circumference of the bone was greater in blacks. This greater bone mass
was placed further from the central shaft axis, conferring greater
resistance to bending in blacks than whites (18).
Cortical width is determined by the growth of the endocortical surface
relative to the periosteal surface. Periosteal expansion
must be greater than endocortical expansion during growth, otherwise
cortical width would not increase as the bone grows in length and
diameter. However, cortical width was the same in blacks and whites,
despite blacks having a bigger bone, suggesting that medullary
expansion during growth must have been greater in blacks.
Alternatively, as the direction of endocortical growth changes from
expansion to contraction at puberty (19), the similar cortical width
could have been the result of less endocortical contraction at puberty
in blacks. Endocortical contraction did appear to occur in this study
by Gilsanz and colleagues, but the changes were not significant.
These surfaces behave differently because they are regulated
differently. An understanding of the hormonal regulators of periosteal
and endocortical growth and remodeling in blacks and whites, and in men
and women may contribute to the development of new drugs that increase
periosteal growth (increasing the bending strength of cortical bone),
increase endocortical apposition (increasing cortical thickness), or
reduce endocortical resorption (preventing cortical thinning) (20).
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Racial and gender differences in upper and lower body segment
lengths
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Despite being matched for height, blacks had longer legs and
shorter trunks than whites, longer femurs, and shorter vertebrae than
whites. So, longitudinal growth of the femur must have been more rapid
in blacks, while longitudinal vertebral growth must have been slower.
Lower limb growth before puberty is growth hormone-dependent and
procedes at a constant velocity before puberty while spine length is
accelerating (Fig. 5
) (21); both the
deceleration in limb growth and acceleration in trunk growth are partly
estrogen dependent, even in males (22, 23). Hypogonadism produces
longer leg length and shorter trunk length.

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Figure 5. The tempo of growth (centimeter/year) in femur
length and trunk length differ, the former decelerates at puberty, the
latter accelerates. Adapted from Tupman et al. (21).
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Men have longer legs than women because epiphyseal fusion occurs later.
They enter puberty 2 yr later, and their pubertal growth spurt reaches
a higher peak velocity and continues longer (24). Whether adrenarche
and puberty occur at different chronological ages in blacks than whites
is uncertain. Whether the tempo of prepubertal and pubertal
longitudinal and circumferential growth of the axial and appendicular
skeleton is different in blacks and whites is uncertain. Whether using
methods for determining bone age and pubertal staging developed in
white children is appropriate for evaluating nonwhite races is
questionable. There is some evidence of earlier skeletal maturation in
blacks (25).
Thus, blacks have longer legs and shorter trunks than whites, Asians
have longer trunks and shorter legs than whites, Hispanics have similar
body proportions as whites, but they are shorter. Men have longer legs
than women, but differ less in their trunk length (26, 27). Thus, we
all look at each other with less obliquity when we sit than when we
stand. Differing regional sensitivity to sex hormones and growth
hormone or IGF-1 could partly account for these racial differences. To
speculate, if long bone epiphyses and vertebral growth are less
sensitive to estrogen in blacks, this might explain the longer legs and
shorter trunk lengths. Could greater sensitivity to estrogens in Asians
account for their shorter legs and longer trunks than whites or blacks?
These hypotheses are yet to be tested and may not be entirely
unprecedented; there is evidence of differing sensitivity to
parathyroid hormone in blacks and whites (28).
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Racial and gender differences in BMD: more apparent than
real?
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Gender and racial differences in areal apparent BMD, reported
using single and dual photon or x-ray absorptiometry, are partly, but
not entirely, the result of confounding by bone size and body size.
When size is taken into account many racial differences in areal
apparent BMD diminish or disappear (29, 30). The longer legs in men
than women, and in blacks than whites, produces the correspondingly
higher proximal femoral apparent BMC and areal apparent BMD. The
shorter trunk length in blacks would make the vertebral areal apparent
BMD less than in whites were it not for the higher
trabecular volumetric apparent BMD in blacks (because of their thicker
trabeculae). Trunk length is similar in women and men, but men have
wider vertebrae, producing the higher spine apparent BMC and areal
apparent BMD, but volumetric apparent BMD is the samethe amount of
bone in the bone is the same in men and women. The shorter legs in
Asians will result in the lower apparent BMC or areal apparent BMD and
a shorter hip axis length (which is purportedly associated with a lower
hip fracture risk) (31). The need for locally developed controls in the
use of bone densitometry rather than the manufacturers reference
ranges is obvious.
Thus, the effect of size on BMD has misled us in many ways (3). The
most compelling morphological evidence of higher BMD in blacks is the
data supporting greater trabecular thickness at the spine and iliac
crest (1, 4, 5, 13). Cortical thickness was no greater in blacks in the
study by Gilsanz et al. (1), but there was more bone placed
further from the central axis of the femur. There is little convincing
evidence that either cortical thickness or its true BMD is higher in
blacks when careful matching for external bone size is done. Men and
women have the same peak volumetric apparent BMD at the completion of
growth; the higher apparent BMC or areal apparent BMD are the result of
differences in bone size. Most of the literature reporting racial and
gender differences in areal BMD is not convincing because bone and body
size is not adequately taken into account, and when taken into account,
is adjusted for by statistical methods using height, weight, or body
mass index. These are poor surrogates for the actual size of the bone
being measured, particularly given that racial and gender differences
in body segment lengths will produce over- or underestimates depending
on which regions and races are compared.
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Where are we? Where do we need to be? How do we get there?
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The work presented in JCEM by Gilsanz and colleagues is
meritorious by virtue of the questions it answers and by the questions
arising from its scholarship. The inference made from this work and
other studies, is that the higher vertebral volumetric trabecular
apparent BMD established during growth in blacks may be partly
responsible for the lower spine fracture incidence in black than white
women. This is certainly plausible, but there is no direct experimental
evidence showing a correlation between the incidence of vertebral
fractures and trabecular numbers or thickness in any race or either
gender. There is also no experimental evidence showing that the racial
or gender differences in vertebral fractures rates are explained by
racial or gender difference in any morphological characteristic. The
placement of the femoral midshaft cortical bone further from the
central shaft axis in blacks than whites, and in men than women, may
confer greater resistance to bending. Whether the lower appendicular
fracture rates in blacks than whites, and males than females is
attributable to these differences in bone size has not been tested by
showing a correlation between hip fracture rates and the
cross-sectional area of bone in blacks, whites, men, or women. Nor is
there evidence that racial or gender differences in hip fracture rates
are explained by corresponding racial or gender differences in bone
size or bone geometry. This work is yet to be done.
Bone fragility has its seed sown earlyduring growth and development,
and perhaps during the 9 months before birth. There is much more to
growth than final height, and much more to bone than its BMD. Skeletal
growth is region- surface-, gender- and race-specific. Bone size
proceeds more rapidly than its mineral accrual, appendicular growth is
more rapid than axial growth, periosteal surfaces grow more rapidly
than endocortical surfaces and, at puberty, in different directions, so
that bone size is nearer completion of growth than the mineral accrued
within it. To understand the pathogenetic mechanisms responsible for
the differing growth and aging of the skeleton in men and women, in
blacks, whites, Asians, and other racial/ethnic groups, to understand
the effects of exercise, dietary calcium intake, hormone deficiency,
and excess, think surface and structure. What is the structural basis
for an increase or decrease in BMD? What genetic and environmental
factors contribute to the race specific, but gender independent,
increase in trabecular thickness at puberty? What regulates
longitudinal growth of axial and appendicular skeletons in men and
women of different races? What factors regulate the absolute and
relative rates of periosteal and endocortical modeling (growth) and
remodeling, and so, cortical thickness? If cortical thickness is
greater in blacks than whites or greater in men than women, is this the
result of reduced endocortical expansion (relative to periosteal
expansion) before puberty or greater endocortical contraction during
puberty? Is the sensitivity to sex steroids, growth hormone or IGF-1
different in blacks? What is the basis for the secular trends in leg
length and trunk length that vary by race, gender, and epoch
(32, 33, 34, 35).
Noninvasive methods of measuring bone mass have made many important
contributions to the study of the definition, epidemiology, detection,
pathogenesis, prevention, and treatment of osteoporosis and to fracture
risk prediction. However, the techniques summate the changes on the
mineralized surfaces of a three-dimensional world into one or two
ossified dimensions, creating flaws in the way we conceptualize the
skeleton, in the way we develop our thinking and in the way we direct
our research. The structural changes underlying the increase in BMD
during growth are not conveyed by the imagery of density. The failure
to appreciate the macro- and micro-architectural basis of a regions
volumetric apparent BMD ensures that any structural differences
responsible for racial and gender differences in fracture rates will
not even be thought about, much less identified and studied (3). A
better understanding of the pathogenesis of osteoporosis can be gained
by the comparative study of the genetic and environmental factors
influencing the surface specific skeletal growth in size and mineral
accrual of the axial and appendicular in men and women of different
races.
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Acknowledgments
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I would like to thank my colleagues Drs. G. Jerums and D.
Roberts, Austin and Repatriation Medical Centre, University of
Melbourne, Melbourne, Australia, and Professor A. M. Parfitt,
University of Arkansas, city Arkansas, for their constructive
criticisms of the manuscript.
Received February 5, 1998.
Accepted February 9, 1998.
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