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Cortical bone loss with age in three native American populations.

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Cortical Bone Loss with Age in Three Native
American Populations
MARY FRANCES ERICKSEN
Department of Anatomy, George Washington University Medical Center,
Washington, D.C. 20037
KEY WORDS Aging . Cortical bone . Eskimo . Pueblo . Arikara ,
Osteoporosis.
ABSTRACT
Age-related thinning of cortical bone was investigated in archaeological populations of Eskimos, Pueblos, and Arikaras. Medial-lateral cortical
thickness was measured on radiographs of humerus and femur, and thickness of the
anterior femoral cortex was measured directly on samples taken for histologic
study. Maximum length of the bones was used to calculate indices of relative cortical thickness, in order to minimize differences due to body size and build.
Bone loss in the humerus begins before middle age in all three populations and,
except for Eskimo males, the same is true of the anterior femoral cortex. In general,
overall female loss of cortical bone amounts to two or three times that of the males,
and in the case of the humerus and the anterior cortex of the femur, this difference
is evident by middle age. The weight-bearingfemoral medial-lateral cortex shows
less sexual difference but has the greatest number of statistically significant differences between populations and the greatest contrast between populations in pattern of loss with age. It appears that of the cortical regions studied this is the area
upon which environmental factors have the greatest effect, whereas areas more
subject to tensile stress, the humerus and anterior femoral cortex. are less affected
by these factors.
Among the major findings of the recent maturity and cortical thickness at any
upsurge of interest in bone biology are: given age level (Garn et al., '69; Garn, '70).
bone involution is a normal concomitant of On the other hand, workers comparing two
aging in all human populations; females or more ancient populations or comparing
lose bone at a greater rate than males; ancient and modern populations found difand bone loss -thinning of cortex and ferences in the total amount of bone loss
cancellous trabeculae -begins soon after over time and/or in the pattern (or timing)
maturity is reached (Nordin, '66; Garn et of loss (Dewey, Bartley, and Armelagos,
al., '67; Garn et al., '69; Garn, '70; De- '69; Perzigian, '73).
queker, '72). Several recent studies have
It is possible, of course, that these disinvestigated bone loss with age in archae- crepancies resulted from differences in
ological populations (Dewey, Armelagos, technique, from differences between the
and Bartley, '69; Dewey, Bartley, and Ar- areas of the skeleton studied, or from the
melagos, '69; VanGerven et al., '69; Mazess limitations inherent to archaeological popand Jones, '72; Perzigian, '73). Garn and his ulations, especially the difficulty of detercolleagues, studying thousands of in- mining age at death. However, recently
dividuals in several countries, at first found Garn ('72) reported differences between
no differences in bone loss between popu- American white and black females in
lations of diverse diet, environment, and amount of bone loss in the second metacargenetic background, although these factors pal. Similarly, Dequeker ('72) found that
were found to affect overall skeletal size at once he had rigorously controlled for body
-4~
J. .PHYS. ANTHROP., 45: 443-452.
443
444
MARY FRANCES ERICKSEN
size, Nigerians differed from Europeans in
rate of bone loss with age, although the differences were not statistically significant.
Thus, it is possible that genetic and environmental factors do affect aging bone
loss. The purpose of the present study is to
add to the data on bone loss with age in archaeological populations and also to determine whether environmental and/or genetic factors may have affected rates or patterns of bone involution in these groups.
MATERIAL AND METHODS
Three native American groups differing
greatly in lifestyle, diet, and physical environment were selected for study: Pueblo
of the Southwest, Arikara of South Dakota,
and coastal Alaskan Eskimo. Descriptions
of the physical types and environmental
and cultural settings of these groups are
given elsewhere (Ericksen, '73; also
Spencer et al., '65). Briefly, the Pueblo
were sedentary town-dwelling farmers of
the Colorado Plateau, whose diet consisted
almost entirely of vegetable foods. The
Arikara were village-dwelling horticulturists, but they also spent a large part of
each year roaming the Plains hunting bison.
Their diet was well balanced b y modern
standards, between animal and vegetable
food. The Eskimo lifestyle was dominated
by the seasonal movements of the birds,
fish, and sea mammals they hunted, and
their diet consisted almost entirely of animal products. Although all three groups
lived in harsh environments, that of the
Eskimo was especially rigorous. Genetically, the Arikara and Pueblo are considered to be more closely related to each
other than to the Eskimo.
The skeletons studied are in the Anthropology Department of the Smithsonian Institution. The 142 Pueblo skeletons are
from three archeological sites in New Mexico: Pueblo Bonito, Puye, and Hawikuh.
Pueblo Bonito was abandoned around 1130
A.D., and Hewett ('09) found no sign of
European influence at Puye. Smith et al.,
('66)consider the Hawikuh skeletons in the
Smithsonian collection to date mainly from
the late pre-Spanish and early Spanish pe-
riods, that is, the sixteenth and seventeenth
centuries. The 134 Arikara skeletons were
excavated from 11 archaeological sites in
northern South Dakota along the upper
Missouri River and its tributaries. Principal
sources for site identification and dating
were: Wedel, '55; Lehmer, '54; Lehmer
and Jones, '68; Jantz, '70; Bass et al., '71. A
few of the skeletons are from sites dated
t o t h e Extended Coalescent Horizon,
1550-1675 A.D., but most are from the
Post-Contact Coalescent Horizon, 16751845 A.D. (Lehmer and Jones, '68). The
Alaskan Eskimo sample consists of 123
skeletons found from 14 mainland coastal
settlements between Point Hope on the
Arctic Ocean and Pastolik on the south
shore of Norton Sound. According to the
Anthropology Department catalog, the
material from Point Hope dates from the
late eighteenth and early nineteenth centuries, and the other skeletons are from the
late nineteenth and early twentieth centuries.
These samples obviously are not true
populations, especially the Eskimo and
Arikara. However, when juvenile, fragmentary, and pathological skeletons, and
those whose age or sex is doubtful are
eliminated, no collection from a single site
is large enough to provide a reasonable
sample for statistical analysis. The three
groups are sufficiently separated geographically so that there is no question of
intermixture, and within -group differences
are likely to be less than between-group
differences. Corruccini ('72) demonstrates
this for the Pueblo groups used in the present study.
Skeletons showing pathological change
other than simple osteoarthritis or trauma
were excluded from the study. Age determination was based on assessment of the
whole skeleton, mainly using the method of
McKern and Stewart ('57).Although their
method may be unreliable for groups like
those of the present study, especially for
females over the age of 40 (Gilbert, '73;
Gilbert and McKern, '731, they should provide reasonably accurate estimates for
dividing the samples into three gross age
44s
CORTICAL BONE LOSS WITH AGE
groups: young (18-251, middle-aged (30under 501, and old (50 and above). Individuals between the ages of 25 and 30
were excluded, in the hope that any earlydeveloping age changes might thereby become more evident. Except among the
Pueblo and the Arikara males, the collections include very few individuals over 40.
The humerus and femur were chosen for
study because they are two of the bones
which Trotter et al. ('59) report to be
unlike in the amount of sexual differences
in density loss with age. These authors consider that differences in functional stress
-weight bearing and tension -are related to their finding less difference between the sexes in density of the femur
than in the humerus. For each skeleton, the
maximum lengths of one humerus and one
femur were measured on an osteometric
board, whenever possible, the bones used
were those of the left side. In 23 cases maximum Length of one of the bones was estimated by the regression formulae of Steele
and McKern ('691. The midpoint of the
shaft was marked by a lead shot, so that it
could be located on a radiograph of the
bone. Radiographs were taken at a
tube-film distance of 60 inches, with the
bones laid directly on the film holder. An
exposurt. of 70 milliampere-seconds at 70
kilovolts was found to be best for distinguishing trabecular from cortical bone on
the endosteal surfaces. The humerus was
oriented with its posterior surface on the
film holder, but the femur was positioned
with its anterior surface on the film holder,
to avoid distortion of the image due to
bowing of the shaft.
Medial-lateral diameter and medullary
cavity diameter were measured on the
radiographs, to the nearest 0.5 mm, using a
Helios dial caliper and excluding trabecularized endosteal bone. The femur
was measured at midshaft, but preliminary
examination of the radiographs indicated
that it would be impractical to measure the
humerus at midshaft. The lateral cortex in
the area of the deltoid tuberosity tends to
become divided into distinct inner and
outer "tables" with increasing age and
does not give a realistic picture of simple
cortical involution. Therefore, the measurements were taken at a level immediately below the tuberosity, where the
shaft becomes relatively parallel-sided.
In addition to t h e data from the
radiographs, it was possible to measure
thickness of the anterior femoral cortex directly in a few individuals of each age and
sex group. For purposes of future histologic
study, I used a 5/8-inch core drill to take
samples of the anterior cortex just below
the midshaft (to preserve this anthropometric landmark). The midline cortical
thickness of these samples was measured to
the nearest 0.5 mm with the same caliper
used for the radiographs.
Three indices of relative cortical thickness were calculated from the measurements, to minimize differences due to size
and body build. Kerley ('61) notes, for example, that gross cortical thickness is not
consistently associated with age, and
Dewey, Bartley, and Armelagos 1'69) found
correction for body size extremely important in comparing populations. Dequeker
('72) also strongly emphasizes the importance of correcting for body size. The
three indices are:
(1) Femur medial-lateral index (FM-
LI):
shaft diameter - medullary diameter
2
maximum length
(21 Femur anterior index (FAI):
midline anterior cortical thickness
maximum length
(3) Humerus medial-lateral index (HMLI): same as (11,above.
RESULTS
The data were processed by the Computer Center of the Smithsonian Institution; differences between sample means
were tested by Student's t and the variances b y the Fratio. Differences significant
according to the t test but whose F ratios
were also significant were discarded from
the analysis. Test results were analyzed according to differences between age levels
446
MARY FRANCES ERICKSEN
(sex and population held constant), sex (age
and population constant), and population
(age and sex constant). Table 1 gives sample sizes, means, and standard errors of the
three indices and also indicates statistically
significant sex differences within each agepopulation group. Figures 1-3present the
indices graphically.
Cortical loss (or gain) between age levels
is presented in table 2, and the statistical
ly significant differences are indicated.
Change from one age level to the next is
expressed as a percentage of the mean of
the younger age group:
younger mean - older mean
younger mean
All but three values in table 2 represent
cortical loss, but the most striking features
of the table are the differences between
the sexes in amount of loss and the contrast
between femur and humerus in regularity
of pattern.
Medial-lateral femoral cortex
Ten of the 12 statistically significant
population differences occur in the index
measuring relative thickness of the mediallateral femoral cortex, FM-LI. T h e
greatest contrast in cortical thickness is between Eskimos and Pueblos, with the
Arikara tending to be intermediate, except
in old age, when Eskimo females and both
sexes of Arikara show pronounced loss of
cortex. Eskimo males have a statistically
significant advantage over other males in
relative amount of cortex at each age level.
Female Eskimos have greater cortical
T4RLE 1
Indices: cortical thickness as a percentage of hone length. Sample size, means, standard errors,
and statistically significant male-femule differences
Young
Mean
Mean
Mean
(W)
S.E.
No.
(%I
S.E.
28
10
27
1.67 0.04
1.11 0.05
1.43 0.05
26
10
24
1.71
1.17
1.37
0.03
0.05
0.05
7
7
7
1.64
1.07
1.20
0.08
0.08
0.12
27
8
26
1.65 0.05
1.24 0.05
1.39 0.04
27
12
25
1.63 0.05
1.12 0.05
1.16' 0.06
6
6
6
1.29
0.70
0.80 2
0.06
0.07
0.09
17
10
16
1.48 0.06
1.18 0.05
1.38 0.06
26
12
26
1.41
1.14
1.34
0.04
0.06
0.04
20
11
22
1.37
1.08
1.16
0.04
0.05
22
13
24
1.41 0.04
1.10 0.03
1.30 0.05
27
10
27
1.36 0.05
0.91 8 0.08
1.09 0.06
23
13
24
1.26
0.82 1
0.80
0.05
0.05
0.05
20
10
18
1.50 0.04
1.24 0.04
1.46 0.05
49
24
49
1.59
1.17
1.36
0.03
0.03
0.03
10
10
10
1.39
1.02
1.16
0.06
0.07
0.05
25
12
26
1.53 0.03
1.14 0.04
1.37 0.03
25
1.52 0.04
1.022 0.04
1.15' 0.05
2
2
2
1.18
0.73 9
0.60 1
0.42
0.10
0.06
No.
Eskimo males
Femur medial-lateral index
Femur anterior index
Humerus medial-lateral index
Eskimo females
Femur medial-lateral index
Femur anterior index
Humerus medial-lateral index
Puehlo males
Femur medial-lateral index
Femur anterior index
Humerus medial-lateral index
Pueblofemales
Femur medial-lateral index
Femur anterior index
Humerus medial-lateral index
Arikara males
Femur medial-lateral index
Femur anterior index
Humerus medial-lateral index
Arikarafemales
Femur medial-lateral index
Femur anterior index
Humerus medial-lateral index
(%I
Old
Middle-aged
10
25
Female mean significantly below male mean of the same age-population group, P
Female mean significantly below male mean of the same age-population group, P
<
<
0.01.
0.05.
?Go.
S.E.
0.05
447
CORTICAL BONE LOSS WITH ACE
I .5
f
\
\
‘1
\\
I .3-
Y
M
O
&3
\
\
I
Y
ESK I MO
M
O
PUEBLO
\
Y
M
O
AR IKARA
Fig. 1 Femur medial-lateral index means (Y axis) plotted against age (X axis) for three native
American populations. Index expresses average medial-lateral cortical thickness as a percentage of
maximum femur length. Y, young (18-25);M, middle-aged (30-under 50);0, old (50 and above).
1.2
1
t
\
I .o
/
\
\
\
\
L
0.8
0.6
Y
M
ESKIMO
O
Y
M
O
PUEBLO
Y
M
O
AR I K A R A
Fig. 2 Femur anterior index means (Y axis) plotted against age (X axis) for three native American
populations. Index expresses anterior cortical thickness as a percentage of maximum femur length. Y,
young (18-25);M,middle-aged (30-under 50); 0, old (50 and above).
thickness than other females in youth and
middle age, and the differences from
Pueblo females are significant. Pueblo
female bone loss between youth and middle age is enough so that they also have a
significantly lower FM-LI than Arikara
females in middle age.
Although all groups show a drop in FMLI between youth and old age, the curves
or “patterns” of loss are different (fig. 1).
448
MARY FRANCES EHICKSEN
$
\
\
\
\
\
\
L
0.5
Y
M
ESKIMO
O
Y
M
O
PUEBLO
Y
M
O
AR I KARA
Fig. 3 Humerus media1-lateral index means (Y axis) plotted against age (Xaxis) for three native
American populations. Index expresses average medial-lateral cortical thickness as a percentage of
maximum humerus length. Y,young (18-25), M, middle-aged (30-under 501, 0, old (50 and above).
The decline is not statistically significant in
either Eskimo or Pueblo males, but the
Pueblo males show a steady loss, amounting to 7.43%between youth and old age.
Eskimo males gain in this index into middle
age, and their total loss is a mere 1.80%.
Arikara males also gain between youth and
middle age, so that in middle age they
have a significantly higher FM-LI than
Pueblo males, but they lose much more
than the other males between middle and
old age. Pueblo females show the same sort
of steady reduction in FM-LI as Pueblo
males, but Eskimo and Arikara females
show little loss until after middle age. Loss
in FM-LI is greater between youth and
middle age in Pueblos than in the other
groups. On the other hand, Pueblo cortical
loss between middle and old age is considerably less than in the other groups of
the same sex.
Table 2 indicates that the female rate of
cortical loss is appreciably greater than
that of the males. However, it is uncertain
how much of the difference among old
Eskimos and Arikaras is due to small sample size in these groups. The sexual difference between old Pueblos is considerably
less.
Anterior femoral cortex
In contrast to the medial-lateral cortex,
sex differences in loss of anterior femoral
cortex are evident by middle age. In all
three female groups loss in FA1 between
youth and old age is statistically significant,
but among males only the Arikara show a
significant difference between young and
old. By middle age Arikara and Pueblo
female means are significantly below male
means, and in all three groups FA1 is significantly lower in old females than in old
males.
In all groups, except the Eskimo males,
loss begins between youth and middle age
and is steady thereafter (fig. 2). Pueblo
449
CORTICAL BONE LOSS WITH AGE
TABLE 2
Cortical hone loss with age: dijferences between means of successive age
levels, expressed as a percentage of the younger group mean
Population group
Eskimo males
Young vs. middle-aged
Middle-aged vs. old
Young vs. old
Puehlo males
Young vs. middle-aged
Middle-aged vs. old
Young vs. old
Arikara males
Young vs. middle-aged
Middle-aged vs. old
Young vs. old
Eskimofemales
Young vs. middle-aged
Middle-agrd vs. old
Young vs. old
Pueblofemales
Young vs. middle-aged
Middle-aged vs. old
Young vs. old
Arikara females
Young vs. middle-aged
Middle-aged vs. old
Young vs. old
I
Fernur
medial-lateral
index
Femur
anterior
index
Humerus
medial-lateral
index
%
%
%
difference
difference
difference
+
+
- 4.73
- 2.84
- 7.43
-
2.40
- 4.09
- 1.80
3.40
- 8.55
- 3.60
- 4.19
- 12.41
- 16.08
3.39
- 5.26
- 8.47
-
5.64
- 12.82
- 17.74 2
-
2.90
13.43 '
- 15.94 1
-
+
6.002
- 12.58 1
- 7.33
-
1.21
- 20.86 I
- 21.82
- 9.68
- 37.50
- 43.55 '
- 31.03
- 3.55
- 7.35
- 10.64
-
17.27
- 9.89
- 25.45 1
- 16.15 2
- 26.60 1
- 38.46
-
J
'
- 0.65
- 22.37
- 22.88
Difference between age levels statistically significant, P
Difference between age levels statistically significant, P
-
10.53
- 28.43
- 35.96
<
<
'
6.85
- 14.70 1
- 20.55 1
-
16.55 1
- 42.45
16.06
- 47.83
- 56.20
'
'
-
J
0.01.
0.05.
females, but not the males, differ from the
other groups in that the greatest percentage of loss occurs between youth and middle age, but as in FM-LI, they appear to
lose appreciably less anterior cortex than
the other females over a total lifespan (table 2 ) .
ences in HM-LI are evident by middle age.
From the beginning females show higher
percentages of loss, and their total loss is at
least twice that of the males. The sexual
difference in HM-LI is statistically significant in middle-aged Eskimos and
Arikaras and in all groups in old age.
Medial -lateral humeral cortex
The pattern of involution of the mediallateral humeral cortex is similar to that of
the anterior femoral cortex and cven more
regular (fig. 3 ) . All groups show a steady
decline in HM-LI from youth onward,
statistically significant between all age
levels in Eskimo and Pueblo females and
from middle age onward in all but Eskimo
males (table 2). As in FAI, sexual differ-
DISCUSSION
The present investigation agrees with
many previous studies in finding that sex is
consistently related to rates of cortical
bone involution. However, it is evident that
another factor must be taken into account
when interpreting the findings of a given
study -the effect of function upon the
patterns of aging in different bones and in
different areas within the same bone. What
450
MARY FRANCES ERICKSEN
we perceive depends upon where we look.
As mentioned above, Trotter and her coworkers ('59) noted that sex differences in
density were less in weight -bearing bones
than in bones more subject to tensile stress.
Similarly, Garn et al. ('69) found that the
tibia and second metacarpal differed in
both onset (earlier in the tibia) and rate
(less in the tibia) of cortical involution.
VanGerven et al. ('69) presented evidence
that different areas around the circumference of the mid-femoral cortex change
differently with aging, just as they do during growth (Johnson, '66). The present
study confirms these findings.
The humerus shows the most consistent
and steady change in all three groups, but
by middle age females have lost at least
twice as much cortex as males (table 2). No
differences appear which could be attributed to race, and such environmental
factors as physical activity and nutrition,
which differed a great deal in these
groups, apparently had little or no effect,
as the curves of loss are parallel and even.
These findings for the humerus are similar
to those reported by Garn et al. ('70) for
cortical loss in the second metacarpal in
several thousand subjects in North and
Central America. They found that bone
loss began in both sexes by age 40 and
averaged 30%in females between ages 30
and 80, whereas males lost only 12%in the
same time span. The sexual difference was
evident by age 40, and the average percentage of overall loss was no greater in Central American women, who tended to nurse
babies from one to three years (Frisancho
et al., '71) than in Ohio white females,
among whom breast feeding is rare and
tends to be of short duration. For this
reason and because Garn and his colleagues (Garn et al., '70) have presented
evidence that high parity is associated with
decreased cortical thinning, I am reluctant
to ascribe the sex differences found in the
present study to the effects of pregnancy
and lactation. It appears that a greater rate
of aging bone loss in females is a universal
fact of life and not dependent upon such
factors .
The anterior femoral cortex, which is
away from the main axis of weight bearing
(Evans, '571, follows a pattern of involution
much like that of the humerus, but the
medial-lateral cortex presents a more complex picture of bone loss with age. Most
notable is the late appearance of appreciable male-female differences in amount of
cortical loss. For instance, Eskimo females
show a 1.21%loss in FM-LI between youth
and middle age, and the males show a
2.40%gain in this period, but this difference is much less than that seen in HM-LI,
in which Eskimo females lose almost four
times as much cortical thickness as the
males between youth and middle age. Similarly, in the anterior femoral cortex
Eskimo males gain between youth and
middle age, while the females lose almost
10%.The midshaft medial-lateral cortex of
the femur is closer to the main axis of
weight bearing than is the anterior cortex
(Johnson, '661, and it is possible that this
has a "maintenance" effect, somewhat suppressing cortical loss in the female during
the early decades of maturity.
Pueblos show earlier and more regular
loss of femoral medial-lateral cortex than
the other groups. Eskimo and Arikara
males have a rise in FM-LI between youth
and middle age and a drop thereafter,
minimal in Eskimos. Eskimo and Arikara
females show a slight decline into middle
age and a steep one thereafter, with the result that their lifetime loss of cortex is
greater than that of the Pueblo females.
Apparently in this area environmental or
genetic factors are superimposed upon the
"normal" pattern of aging, so that population differences appear in both onset and
rate of involution. Although, as described
above, Garn ('72) and Dequeker ('72)
found racial differences in aging bone loss
in the second metacarpal, especially among
females, it is difficult to ascribe a major
role in the differences between the present groups to genetic factors for two
reasons. Principally, if this were the main
cause of the differences, the Arikara and
Pueblo should most closely resemble each
other and the Eskimo stand apart. Instead,
CORTICAL BONE LOSS WITH AGE
45 1
it is the Pueblo who differ from the other Frisancho, A. R., S. M. Garn and W. Ascoli 1971
Unaltered cortical area of pregnant and lactating
two groups. Second, genetically deterwomen: studies of the second metacarpal bone in
mined differences, if they are important in
North and Central American populations.
Invest.
. .
this case, should appear in the humerus as
Radlol., 6: 119-121.
well as the femur. Therefore, I feel that Garn. S. M. 1970 The Earlier Gain and the Later
h s s o f Cortical Bone. Chas. C Thomas, Springfield,
some environmental factor or factors -at
Illinois.
a guess, both nutrition and level of physical
1972 The course of bone gain and the
activity -must play a part in determining
phases of bone loss. Orthop. Clin. N. America, 3:
the pattern and amount of age-related loss
503-520.
in the medial-lateral cortex of the femur. Garn, S. M., C. G. Rohmann and B. Wagner 1967
ACKNOWLEDGMENTS
I am grateful to Dr. J. Lawrence Angel,
Curator of Physical Anthropology, and to
the other members of the Department of
Anthropology of the Smithsonian Institution for their hospitality and assistance
during the gathering of the data for this
study. I am especially indebted to Dr.
Donald J. Ortner for arranging the computer processing of the data and to Dr. T.
Dale Stewart for his guidance and support
throughout the project. The material presented here is taken from a dissertation
presented to the George Washington University in partial fulfillment of the requirements for the Doctor of Philosophy
degree.
LITERATURE CITED
Bass, W. M., D. R. Evans and R. L. Jantz 1971 The
Leavenworth Site Cemetery: Archaeology and
Physical Anthropology. Univ. Kansas Publ. in
Anthrop., 2. University of Kansas, Lawrence.
Corruccini, R. S. 1972 The biologic relationships of
some prehistoric and historic Pueblo populations.
Am. J. Phys. Anthrop., 37: 373-388.
Dequeker, J. 1972 Bone Loss in Normal and Pathological Conditions. Leuven Univ. Press, Leuven,
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