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J. Anat. (1997) 191, pp.

407416, with 6 gures Printed in the United Kingdom 407


Age-related changes in cortical porosity of the midshaft of
the human femur
S. A. FEIK, C. D. L. THOMAS AND J. G. CLEMENT
School of Dental Science, University of Melbourne, Victoria, Australia
(Accepted 8 July 1997)
:ns1r:c1
Complete cross-sections from the femoral midshaft of 180 individuals of known height and weight, aged
2197 y, from a modern Australian population were examined using automatic video image analysis to
quantify total subperiosteal porosity (TSPP). More specically, the aim was to investigate whether age
changes were similar in both sexes in (1) total subperiosteal area (TSPA), cortical area (CA) and medullary
area (MA), (2) intracortical porosity (ICP), and (3) the respective contributions to TSPP made by MA and
intracortical void area (ICVA). Our ndings indicated that both sexes showed a signicantly greater height
normalised TSPA in the 70s as compared with the 20s. Males had consistently larger bones with a greater
height normalised CA. In both sexes CA showed a tendency to increase till the 7th decade and then to
decline, more so in females. MA approximately trebled in females and doubled in males over the age range
studied. Although ICP also increased, from 46% in young adults to over 9% in the elderly, it showed a
signicant dierence between the sexes only in the 3rd decade, being greater in males at this stage. By
contrast, TSPP became signicantly greater in females (from that recorded in the 3rd decade) by the time
they reached the 50s, while in males this did not occur till the 80s. It increased from "25% in young adults
of both sexes to "50% in females and "37% in males in their 80s. However, in the elderly there was
great variability in both sexes in the appearance of bones from individuals of similar chronological age.
Some bones diered little from those in younger subjects, others showed greatly increased ICP, still others
displayed reduced cortical widths with low ICP. The femoral midshaft resembles other skeletal sites in that
age changes in TSPP are more marked in females than males.
Key words: Femur; age changes; porosity; medullary area; remodelling.
i N1robic1i oN
Age and sex dierences in the development of porosity
in bone are currently of great interest worldwide
because of the high prevalence of osteoporosis with its
associated risk of fracture (Melton, 1993). Australian
epidemiological data on osteoporosis resemble those
derived fromother urbanised populations in USAand
Europe (Seeman et al. 1993). Bone mineral density
(BMD) values are widely used to diagnose osteo-
porosis and to predict future fracture risk (Melton et
al. 1993; Kanis et al. 1994). These areal BMD values
are presented in g\cm# and take no account of bone
architecture. Since bone density is determined more
accurately by the relationship between bone organ
size and the amount of bone tissue contained within
Correspondence to Dr Sophie A. Feik, School of Dental Science, 711 Elizabeth St, Melbourne, Victoria 3000 Australia. Tel. : j61 3 9341
0445; fax:j61 3 9341 0339; e-mail : s.feik!dent.unimelb.edu.au
its periosteal surface (Seeman, 1995) quantitation of
these parameters becomes important when interpret-
ing observed bone mineral density changes with age.
With the advent of automated image analysis
techniques it has become possible to examine entire
cross-sections of bone to determine concurrently the
percentage area occupied by bone tissue and voids
within the bone perimeter. The authors have used this
method to examine the femoral midshaft and, al-
though this region is not usually implicated in
osteoporotic fractures, it has long been the subject of
numerous studies on bone ageing because of its
relative availability. It has also been shown recently
that reduced thickness of the femoral shaft cortex is
an independent predictor of hip fracture (Gluer et al.
1994). Hence a study of porosity changes at this site
might reasonably be expected to enhance under-
standing of femoral neck fractures.
In studies of porosity undertaken to date either
intracortical porosity (ICP) or, alternatively, changes
in medullary area (MA) and cortical width have been
determined in selected areas of bone cross-sections.
To our knowledge no studies of entire cross-sections
relating both ICP and MA to bone size have been
conducted, yet all 3 variables contribute to bone
density as dened above and thereby inuence bone
strength. The early studies of Jowsey (1960) and
Atkinson (1965) showed that ICP increased with age
but made no mention of sex dierences. An investi-
gation by Martin et al. (1980), albeit on men only,
similarly showed an increase with age, fromabout 9 to
18% between ages 40 and 90 y. Martin & Burr (1984),
on a small sample of 19 subjects, demonstrated no
signicant ICP dierences between males and females.
Cortical width loss in conjunction with ICP has been
considered in a few studies (Atkinson, 1965; Thomp-
son, 1980). Thompson concluded that males and
females had similar patterns of intracortical bone loss
but the patterns of cortical width loss were dissimilar
between the sexes, with only the females demon-
strating a signicant decline in cortical width values
with age. He attributed gender anomalies in some of
his results to inadequate numbers of subjects in the
younger cohorts. The problems of sampling small
cohorts and limited areas of femoral cross-sections,
which apply to all the studies cited above, are
compounded by Arnolds (1970) observation that
porosity distribution is not uniform around the shaft.
It is much greater endosteally and in the anterior and
posterior regions (Martin & Burr, 1984). Diculties
such as these have prompted a number of investigators
to state that the results of their studies need
verication.
The aim of this study was to compare ageing trends
in total subperiosteal porosity (TSPP) in men and
women from a large sample of cadavers in a
contemporary Australian population. Complete fem-
oral cross-sections were examined to determine
whether age changes were similar in both sexes in (1)
total subperiosteal area (TSPA), cortical area (CA)
and medullary area (MA), (2) intracortical porosity
(ICP), and (3) the respective contributions to total
subperiosteal porosity (TSPP) made by MA and
intracortical void area (ICVA).
x:1rri :is :Nb xr1nobs
Bone specimens (nl180) were collected at the
Victorian Institute of Forensic Medicine, Melbourne,
Australia, from people who had died suddenly with
no known diseases directly aecting their bones. The
sample was almost exclusively Anglo-Celtic, as judged
by the names. Information on the age, sex, supine
length, weight and, in almost every case, the cause of
death was available. Collection of specimens from
both sexes representing each year from21 to 100 y was
attempted. Details of the sample are included as part
of Figure 2. Specimens 24 cm in length were sawn by
mortuary sta from the midshaft of either femur and
xed in 70% ethanol. No attempt was made to record
the orientation of the specimens. The specimens were
cleaned manually and transverse sections, 110200 m
thick, were obtained using a Leitz 1600 sawing
microtome.
Macroscopic measurements
Images of the bone sections were acquired using a
monochrome, 700 line resolution video camera (Dage-
MTI Model 65, Michigan City, Indiana, USA) tted
with a 50 mm focal length macro lens and a video
digitiser (PIP-512, Matrox Ltd, Dorval, Quebec,
Canada). The programs used were Bioscan Optimas
V4.02 image processing software (Bioscan, Edmonds,
Washington, USA) and Microsoft Excel V5.0. The
system was calibrated by acquiring and measuring an
image of a scale with divisions of 0.1 mm (stage
micrometer no. 310345. Wild, Heerbrugg, Switzer-
land). TSPA and CA (as total foreground) were
automatically acquired and MA calculated from these
measurements.
Microradiography and microscopic measurements
For radiomicrography, planoparallel sections (100p5
m) were obtained by lapping the sawed sections on
1200 grade wet and dry carborundum paper using a
custom built hand-lapping tool. The sections were
radiomicrographed using a Matchlett Laboratories
OEG x-ray tube with a copper target operated at
25 kV and 10 mA. The lm used was Kodak SO-343
at a distance of 195 mmfromthe target. An aluminium
step wedge was radiomicrographed with each section.
The radiomicrographs were mounted on glass slides
and masked with black tape to dene the borders and
exclude extraneous light. An array of contiguous
monochrome images from entire cross-sections was
recorded by tiling on a computer-controlled X-Y
stage (Lang Electronics MCC 11\12\13-JS-RS 232)
tted to a Leitz Dialux 20 microscope. The camera
used was a 3-chip colour video camera with a
resolution of 768 by 486 pixels (Sony DXC-930P). The
408 S. A. Feik, C. D. L. Thomas and J. G. Clement
video digitiser and computer were the same as
described above. The eld of viewof the camera, using
a i1 microscope objective (Leitz PL 1\0.04), was
"3 mmi2 mm and most sections were contained
within a rectangle 30 mmi35 mm, thus approxi-
mately 180 frames (tiles) were needed per specimen.
Frame boundaries matched to a precision of 0.1 m.
Within each tile, bone tissue and voids were isolated
by thresholding (conversion to a 2-level image with
grey levels above a xed reference value becoming
white and those below being set to black) and their
areas measured.
For each tiled specimen, the microscopically mea-
sured cortical bone area (summed bone area j
summed void area) was compared with the macro-
scopically measured bone area; the average dierence
between these measurements was 2.8%. The former
measurement was used for all subsequent calculations.
Tiling of a number of sections was repeated both by
the same and a dierent operator. The intra- and
interoperator coecients of variation (c.v.) for repeat
measurements of the microscopically determined bone
and void areas ranged from 1% to 7%, averaging
5%. To determine the eect of a frame shift on the
measurements one section was tiled ve times keeping
all conditions constant but moving the section to a
new starting position each time. This resulted in a c.v.
for the bone area of 1.4% and for the void area of
4.5%. The dierence between the 2 c.v.s could be
explained as follows. The measurement of total bone
area was simply a count of the pixels in the tile image
that were above the threshold (i.e. nonblack) and thus
fairly consistent, while the measured void area varied
slightly with the location of tile boundaries. Voids
that intersected tile boundaries were not counted (it
was not possible to ascertain for certain that they were
not part of the MA) and thus a shift in tile position
changed the population of voids that was measured.
Data analysis and size normalisation
Ru (1984) and his coworkers (Ru et al. 1993) have
demonstrated that femoral cross-sectional size varies
with bone length. The dierences in height between
individuals may thus have an eect, unconnected with
ageing, on the measured parameters. For this reason
the results for TSPA and CA but not MA, which is
discussed below, are presented as height normalised.
A simple allometric model (Albrecht et al. 1993) was
used for the size adjustment. A power law equation
was tted to the measurements for all variables as a
function of height, data from both sexes being
combined for this purpose. The variables TSPA and
CA were found to be correlated with height and were
proportional to height to the power of 1.72 (r# l0.41)
and 2.36 (r# l0.43) respectively. However, MA
showed a much poorer correlation (r# l0.16) and so
height normalisation was not carried out for this
parameter.
Using SPSS software (SPSS Inc., Chicago, Illinois)
LOWESS regression lines were used to show age
trends in MA, ICP and TSPP. The denition of Laval-
Jeantet et al. (1983) was adopted for ICP, i.e. the
percentage of cortical bone occupied by vascular and
resorption cavities. TSPP was dened as MA plus
intracortical void area (ICVA) as a proportion of total
subperiosteal area (TSPA), i.e. (MAjICVA)\TSPA.
Age trends were explored further by grouping the
subjects into decades and plotting mean values. The
TukeyHSD test with a signicance level of 0.05 was
used to determine dierences between decade means
and t tests used for the determination of sex
dierences. To highlight sex dierences in age-related
changes in TSPP, the MA and ICVA were expressed
as fractions of TSPA. This approach removed the
eects on these parameters of bone size dierences
between the sexes. LOWESS curve tting was again
used for a qualitative assessment of age trends in the
variables. Linear least squares regression was then
applied to grouped values (55 and l55 y) of
MA and ICVA (taken as a percentage of TSPA) in
order to study dierences between young and old. The
age of 55 y was chosen as the majority of women
beyond this age could be considered to have passed
menopause; the grouping is also consistent with a
previous study using the same specimen collection
(Feik et al. 1996).
rrsii1s
Total subperiosteal area and cortical area (Table 1)
Height normalised TSPA was consistently greater in
males than females over the age range studied and
showed a tendency to increase from the 20s on, being
signicantly greater in the 7th decade than in the 3rd.
Dierences between the nal 4 decades were not
signicant, suggesting that no real change occurred
beyond the 70s. In females, TSPA remained relatively
constant till around the age of menopause when it
tended to decrease. It then increased to around the 7th
decade and, as in males, showed no signicant increase
beyond this time (the nal decade was excluded
because the number of specimens was small). The
pattern of change with age in height normalised CA
was very similar to that of TSPA up to the 70s, then
Age changes in femoral cortical porosity 409
Table 1. Measured values of parameters (meansp1 S.D.)
Height normalised
Total subperiosteal Cortical area Medullary area Total subperiosteal Intracortical
Age (y) Number area (mm#) (mm#) (mm#) porosity porosity
Females
2130 14 142.6 p17.7 220.9p19.3 101.3 p48.2 0.2371 p0.06 0.0456 p0.01
3140 8 143.9 p17.3 223.2p26.1 103.5 p29.7 0.2532 p0.04 0.0591 p0.02
4150 11 141.2 p21.9 224.4p31.6 93.3 p35.1 0.2348 p0.04 0.0520 p0.02
5160 11 149.4 p15.2 200.6p38.2 158.8 p63.2 0.3668
a
p0.11 0.0707 p0.02
6170 11 165.3
a
p12.9 235.3p34.0 148.4 p38.9 0.3398 p0.08 0.0794
a
p0.03
7180 14 159.5 p13.7 201.9p33.3 190.5
a
p63.6 0.4085
a
p0.10 0.0757
a
p0.03
8190 15 171.0
a
p15.2 193.5p41.4 232.5
a
p73.0 0.4887
a
p0.10 0.0948
a
p0.03
91100 3 188.7
a
p33.9 179.1p23.9 308.4
a
p122.8 0.5596
a
p0.09 0.0960
a
p0.02
Males
2130 12 154.7 p21.3 222.2p43.3 141.2 p60.5 0.2708 p0.09 0.0577 p0.02
3140 12 158.1 p14.3 231.8p27.9 132.9 p32.3 0.2572 p0.04 0.0521 p0.02
4150 15 169.5 p15.3 241.1p27.7 159.7 p63.2 0.2881 p0.08 0.0612 p0.02
5160 13 175.4 p17.4 242.4p33.0 171.8 p69.4 0.3066 p0.08 0.0665 p0.02
6170 13 181.0
a
p26.4 254.3p45.7 175.2 p38.1 0.3083 p0.06 0.0688 p0.03
7180 12 177.2 p15.3 240.8p38.9 190.7 p78.0 0.3428 p0.10 0.0824 p0.03
8190 12 179.4
a
p16.9 236.7p45.0 204.4 p83.2 0.3743 p0.11 0.0924
a
p0.04
91100 4 188.5
a
p18.8 212.1p40.4 290.2
a
p142.8 0.4398
a
p0.12 0.0754 p0.02
a
, Dierences between the marked values and that for the 2130 decade are signicant at the 0.05 level.
Fig. 1. Change with age of medullary area. The means for subjects
were classied by decades. Statistically signicant dierences (P
0.05) between the mean results for the 3rd decade (*) and all other
decades are indicated by the letter a.
CA showed a tendency to decline in both sexes, but
more so in females.
Medullary area
From early adulthood to middle age there was a
tendency towards a decrease in MA, particularly in
females, although this trend was not statistically
signicant (Fig. 1, Table 1). From the 3rd to the 7th
decades MA increased on average at 6% per decade
in males and 11% per decade in females. However,
between the 5th and 7th decades, MA in males
increased by about 10% whereas in females the
increase was close to 60%. Females had signicantly
Fig. 2. Change with age of intracortical porosity. The means for
subjects were classied by decade; n denotes the number of subjects
in each decade. Statistically signicant dierences (P0.05)
between the mean results for the 3rd decade (*) and all other
decades are indicated by the letter a.
smaller medullary cavities than males in the 5th
decade (P0.05) but, because of the marked changes
in the immediate postmenopausal decades, females
beyond 70 y tended to have larger mean marrow
cavities than males, despite their smaller bone size.
Intracortical porosity
In both sexes ICP increased from 46% in the 3rd
decade to over 9% in the 9th decade (Fig. 2, Table 1).
However, gender patterns diered in that ICP in-
creased rapidly in postmenopausal females, becoming
signicantly dierent from the young adult in the 60s
410 S. A. Feik, C. D. L. Thomas and J. G. Clement
Table 2. Values from regression analyses with age as the independent variable
95% condence interval 95% condence interval
Measured parameter Slope P value Lower Upper Intercept P value Lower Upper R#
MA as % of TSPA
Females 2055 y 0.077 0.50 k0.150 0.304 19.76 0.00 11.20 28.31 k0.02
Females 55 y and
older
0.697 0.00 0.379 1.015 k9.58 0.43 k33.81 14.64 0.28
Males 2055 y k0.056 0.65 k0.302 0.189 26.41 0.00 16.93 35.88 0.01
Males 55 y and older 0.423 0.00 0.157 0.689 1.59 0.87 k18.08 21.26 0.16
Intracortical voids as 0.014 0.02 0.003 0.025 3.77 0.00 3.07 4.46 0.35
% of TSPA
while in males the increase was more gradual and
signicance was not attained till the 80s. LOWESS
regression lines showed a trend towards the main-
tenance of slightly higher ICP levels in females after
the rise in the postmenopausal period. However, the
only signicant dierence between the sexes was in the
3rd decade when males showed greater ICP.
Total subperiosteal porosity
Changes in whole bone porosity were determined
by examining the fraction of TSPA occupied by MA
and ICVAconsidered individually and together. Total
bone loss was therefore taken to be the sum of the
increase in MAplus the increase in ICVA. When these
areas were summed and expressed as a fraction of
TSPA the result was equivalent to TSPP. The
fractional changes in MA and ICVA were considered
indicators of the extent of endosteal and intracortical
bone loss respectively, although it is acknowledged
that this is an oversimplication of the situation as it
exists in life.
LOWESS curve tting to a scatter diagram of MA
as a fraction of TSPA indicated that rates of change
diered between the sexes and varied over age for
females. In males there was little evidence for a change
in the rate of endosteal bone loss with age. Further
analysis, where both sexes were divided into two age
groups ( 55 and 55 y), yielded the following
results. Details are presented in Table 2. There was a
highly signicant dierence ( P0.001) in the rate of
change of MA as a fraction of TSPA between the
younger and older groups of females but this
dierence was not signicant for males ( Pl0.08)
(Fig. 3). In the younger group there was no signicant
dierence between the sexes. Between the sexes in the
older group the dierence was greater but still not
signicant (Pl0.11).
The same analysis was done for ICVA as a fraction
of TSPA but in this case no signicant dierences
Fig. 3. Change with age in medullary area as a fraction of total
subperiosteal area.
Fig. 4. Change with age in intracortical void area as a fraction of
total subperiosteal area.
were found between younger and older groups or
between the sexes. In light of this uniformity the sexes
and age groups were combined and a regression line
tted over the age range studied. For the combined
sample, the regression results were highly signicant
Age changes in femoral cortical porosity 411
Fig. 5. Change with age in the area occupied by intracortical voids, cortical bone and medullary cavity within the total subperiosteal area.
(Pl0.01) and indicated that the increase from"4%
to "5% with age, although small, was real (Fig. 4;
Table 2).
TSPP was similar in both sexes in early adulthood
showing values of 2426% i.e. approximately three-
quarters of the total area beneath the perimeter
consisted of bone, the remainder voids (Table 1).
Females in their 50s showed a signicant rise in TSPP
which continued to increase so that in the 80s it was
approximately 50%; only half TSPA was then
occupied by bone. This was signicantly dierent
from males ("37% TSPP in the 80s) in whom the
increase was more gradual and of lesser magnitude;
the change in bone area was "11% (vs "25% in
females) between the 3rd and 9th decades (Fig. 5).
In summary, by far the largest contribution to the
change in the amount of bone present was from the
increase in MA, i.e. from endosteal resorption. The
change in the intracortical component, although
statistically signicant, was very small and appeared
to play little part in the increasing TSPP of the femur
that occurred with age. However, great variability in
the development of TSPP in elderly individuals of
similar chronological age was seen (Fig. 6). Some had
bones that diered little from those in younger
subjects having small medullary cavities and little
ICP, others displayed greatly increased ICP and little
change in cortical width, while others still showed
reduced cortical widths with low ICP.
bi scissi oN
In this study we compared ageing trends between the
sexes in the development of porosity within the total
subperiosteal area of femoral midshaft cross-sections.
Both sexes showed a signicantly greater height
normalised TSPA in the 70s as compared with the 20s,
with males having consistently larger bones and a
greater cortical area. The latter parameter showed a
tendency to decline beyond the 7th decade particularly
in females. Endosteal resorption (as reected in
changes in MA) showed diering patterns in the 2
sexes, being relatively stable in females till the
menopausal decade, then rising steeply, so that MA
trebled over the age range studied and the marrow
cavities of females were, on average, larger than males
in the nal decades despite their smaller bone size. In
males the increase in endosteal resorption commenced
a decade earlier than in females and was more
uniform and not as great, MA doubling over the age
range studied. ICP showed less change with age and
sex, increasing less than 5% over 6 decades in both
sexes. As in the case of endosteal resorption, females
displayed a greater change in ICP in the postmeno-
pausal decades. Therefore, ICP diered signicantly
from that in the young adult approximately 2 decades
earlier in females than in males. Whole bone porosity
reects bone lost both intracortically and through an
increase in MA. Females showed a much greater
decrease between the 3rd and 9th decades in the
fraction of TSPA occupied by bone, a change from 76
to 50% in females contrasting with 74 to 63% in
males, i.e. "25% loss in females as against "11% in
males. In both sexes the intracortical loss was only
"1% over this time period.
We believe this study to be unique in that entire
cross-sections of the femoral midshaft were measured
directly to ascertain concurrently both the intracor-
tical and medullary components of bone loss within
the total perimeter taking bone size into account. In
no previous study, as far as we know, has such a task
been undertaken using a relatively precise and
objective method with good reproducibility on such a
large number of well-documented specimens. The
412 S. A. Feik, C. D. L. Thomas and J. G. Clement
Female Male
Fig. 6. Microradiographs of transverse sections of the femoral midshaft from(left) females and (right) males in their 80s showing the variation
found in intracortical porosity and medullary area in individuals of similar chronological age.i1.8
sample represented a modern urban population and
covered the age range from 21 y onwards. Details
such as the age, height, weight, and in most cases the
cause of death of each subject were known. The
ndings should be widely applicable to other urban-
ised Western countries, as the prevalence of osteo-
porosis in Melbourne, Australia resembles that in
similar communities in USA and Europe (Seeman et
Age changes in femoral cortical porosity 413
al. 1993). The study, however, was of necessity cross-
sectional and, therefore, the age changes reported may
be subject to cohort bias. In Australia the secular
increase in height of young adults early this century
and approximately 70 y later was on average 3.3 cmin
females and 4.6 cm in males (Meredith, 1976). Height
normalisation compensated to some extent for this
secular increase but not all the measured parameters
could be height normalised and, inevitably, other
unknown secular changes may have aected the
dierent-aged cohorts.
The method lends itself to a detailed study of the
regional distribution of porosity and how this alters
with age. Unfortunately further studies, which are
dependent on a precise knowledge of specimen
orientation, are limited with this sample as, at removal
from the body, the specimens were not oriented with
respect to the rest of the femur. Similarly, because
only midshaft specimens were available, studies of the
development of porosity in regions more prone to
fracture and hence of greater interest, are precluded.
The large spread of values around the decade means
may reect the heterogeneity of the population of
Melbourne. The variability was greater in males in
our sample as Garn (1970) also found and more
pronounced in the older age groups, akin to the
ndings of Mazess et al. (1990) on bone density.
Radiomicrographs of the specimens clearly illustrated
this, for specimens of similar chronological age varied
widely in appearance and it was impossible to estimate
an individuals age on the basis of the degree of TSPP
present. Some individuals in their 80s showed very
little ICP or cortical thinning, in others ICP was very
marked and the cortex honeycombed by large re-
sorption cavities with little reduction in cortical width.
Still others displayed cortices a few millimetres wide
with very little ICP.
The method of measurement consistently, but
arbitrarily, classies any void as either intracortical or
as part of the medullary cavity. The situation in life is
much more complex and constantly changing. As
cortical bone becomes increasingly porous and trabe-
culised discontinuities appear in the endosteal surface
and precise delineation into 2 separate and distinct
compartments is not possible. The study was cross-
sectional and it was not possible to determine the
sequence and timing of events in this resorptive
process. Did all the femoral midshafts go through a
stage of high ICP preceding the reduction in cortical
width and was this stage largely undetected because
such porous structures are transient and of short
duration? Partt (1996) has pointed out that, although
structures intermediate between cortical bone with its
low porosity and surface-to-volume ratio, and cancel-
lous bone, where these values are high, do occur they
are infrequent and tend to be temporary (Fyhrie et al.
1994). Our study supports this for ICP increased
minimally with age, "1% as a fraction of TSPA,
whereas total bone loss was substantial, implying that
shafts with reduced cortical widths were the norm in
old age. Atkinson (1965) and others (Martin et al.
1980) have reported that ICP is greater near the
medullary cavity than near the periosteal surface. Our
observations concur with this. As these resorption
cavities enlarge, not only is the surface-to-volume
ratio of cortical bone raised but bone surface contact
with the marrow cavity is also increased as the
intervening bone is resorbed.
Since fractional bone loss is proportional to surface-
to-volume ratio (Partt, 1995), and absolute rates of
loss are much greater from the endosteal surface
(Partt, 1989), the turnover rate in appendicular
cortical bone (Partt, 1983) can be greatly enhanced.
Similar mechanisms can be invoked to explain the rise
in ICP and MA seen in this study in females in the
postmenopausal period. With oestrogen deciency
bone loss increases (Riggs & Melton, 1986) with
increasing turnover rate: the greater resorption depth
(Partt, 1989) and consequent negative balance in
remodelling produce irreversible bone loss (Eriksen,
1986). This loss is exacerbated by the concurrent rise
in activation frequency (Eriksen & Mosekilde, 1990)
thus increasing the remodelling space. Our results
showed that beyond the immediate postmenopausal
decades the rate of increase in % ICP and MA slowed
somewhat, presumably as the oestrogen eect waned
and the rise in activation frequency declined (Stepan
et al. 1987). However, since residual surface-to-
volume ratios would be greater because of the previous
irreversible loss, bone removal continued into old age
at a faster rate than premenopausally. In males the
rates were more uniform (Stepan et al. 1985),
consistent with the well-documented age-related de-
cline in their bone mass (Garn, 1970).
Age changes in MA from a comparable sample
representing the whole lifespan were discussed in an
earlier publication (Feik et al. 1996) and will be
discussed only briey here. The greater endosteal
resorption seen in females in this study concurs with
that in an archaeological population (Ru & Hayes,
1982) where sex dierences were marked. In a modern
US population sex dierences in MA were not
statistically signicant and the percentage increase in
MA ranged from 8 to 11% per decade in both sexes
(Ru & Hayes, 1988). Comparable gures from our
study were 6 to 11% per decade, not greatly dierent.
414 S. A. Feik, C. D. L. Thomas and J. G. Clement
Even though in the elderly the absolute magnitude of
MA in males and females was not signicantly
dierent, the proportional medullary cavity expansion
was much greater in females. They had signicantly
smaller marrow cavities than males in the 5th decade
yet ended up with the same or larger ones despite their
smaller bone size. The greater endosteal resorption in
females was particularly striking in the immediate
postmenopausal decades (5th to 7th) where the
average increase per decade was "5% in males and
"30% in females. Such variations with time are not
usually reported (Ru & Hayes, 1988) for they are
obscured if simple age regressions are used. The sex
dierence during this period can be explained in terms
of hormonal changes aecting bone turnover, as
discussed above.
It is dicult to compare our ndings on ICP
directly with other studies for none has examined
entire cross-sections. Yet it is known that regional
variations in ICP in the femoral midshaft do occur
(Arnold, 1970) and, with age, porosity is much greater
endosteally and in the anterior and posterior regions
(Martin & Burr, 1984). However most studies, like
ours, have either shown that there is little dierence in
ICP in elderly males and females (Thompson, 1980;
Martin &Burr, 1984) or the authors make no mention
of sex dierences (Atkinson, 1965; Jowsey, 1960).
Again there seems to be general agreement that ICP
increases with age (Jowsey, 1960; Atkinson, 1965),
although the reported levels may vary somewhat.
Partt (1994) stated that ICP averages 25% in
dierent bones in adults. Laval-Jeantet et al. (1983) in
their study of the humerus gave gures of "4% at
age 40 increasing to 10% or more at age 80. These
values accord closely with ours at 46% in adults
50 y, rising to over 9%in the elderly. Slightly higher
ICP values at 918% from 40 to 90 y were presented
by Martin et al. (1980) in their study of men only.
However, they stated that because of sample variation,
conrmation of their results was needed. The signi-
cantly greater ICP shown in our study in males in the
3rd decade may be a consequence of their later
maturation relative to females. Statural growth in
males may not cease till 21 y or beyond, depending on
the generation and the population studied, although
the average for modern Western man is approximately
18 y. During rapid growth bone turnover increases,
accompanied by a proportional increase in ICP
(Partt, 1981). This porosity declines as growth ceases
and bone density is increased during the subsequent
process of consolidation (Partt, 1994). Peak bone
mineral content (BMC) was shown to be achieved by
"26 y in females (Teegarden et al. 1995) and
presumably occurs somewhat later in males. The
mechanism proposed above could explain the greater
ICP seen in males in their 20s in this study.
Alterations in the fraction of TSPA occupied by
MA, CA and ICVA provide a measure of the amount
and location of bone loss with age. In young adults of
both sexes MA as a fraction of TSPA was 2224%,
the corresponding values for CA were 7074% and
ICVA "4%. By the 80s the fraction occupied by CA
had declined by "29% in females and "12% in
males, whereas ICVA had only increased 12% in
both sexes. Thus bone loss was largely due to marrow
cavity expansion leading to cortical thinning, rather
than to an increase in ICP. These results are
remarkably similar to those of Laval-Jeantet et al.
(1983) on the humerus, the only study that is
comparable to ours. They found a 28% decrease in
CA due to thinning and 2% by an increase of ICP in
females between 40 and 80 y. In men an almost
identical increase of porosity without provable loss of
CA was observed. However, other studies on the
femur have shown declines in CA in males (Ru &
Hayes, 1988), particularly beyond age 80 (Martin et
al. 1980).
This study, examining entire cross-sections, clearly
shows age-related sex dierences in the pattern of
bone loss in appendicular cortical bone. The loss from
changes in MA, which is much greater in females, far
outweighs the small amount lost from increasing ICP
which, by contrast, shows little sex dierence with age.
Such changes may explain why exponential increases
in fracture rates are not seen in diaphyseal bone in
either sex, for as shown here and previously (Feik et
al. 1996), continued periosteal apposition, at least into
the 70s, largely compensates for this medullary loss.
:ciNovirbcrxrN1s
The authors wish to thank the sta at the Victorian
Institute of Forensic Medicine for collection of the
specimens, Dr P. Bertelsen for advice and considerable
specimen preparation, Dr M. Stein for critical analysis
and Sherie Blackwell for technical assistance. They
are also grateful to the National Institute of Forensic
Science for providing much of the computer equip-
ment and software used for this study.
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