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Anatomical physiological and epidemiological correlates of the aging process A confirmation of multifactorial age determination in the Libben skeletal population.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 68:87-106 (1985)
Anatomical, Physiological, and Epidemiological Correlates of the
Aging Process: A Confirmation of Multifactorial Age
Determination in the Libben Skeletal Population
C. OWEN LOVEJOY
Departments of Anthropology and Biology, Kent State University, Kent,
Ohio 44242 (C. 0.L., R.P. M.) and Department of Orthopaedic Surgery, Case
Western Reserve University, Cleveland, Ohio 44106, Cleveland Museum of
Natural History, Cleveland, Ohio 44106, Department of Human Anatomy,
Northeast Ohio Universities College of Medicine, Rootstown, Ohio 44272,
and Cuyahoga County Coroner’s Office, Cleveland, Ohio 44106 (C. 0.L.1
ROBERT P. MENSFORTH AND
KEY WORDS
Paleodemography, Cortical bone dynamics, Fracture
epidemiology, Skeletal age at death
ABSTRACT
Paleodemographic analyses based on estimates of skeletal age
at death consistently report high levels of young adult mortality with few
individuals living in excess of 50 years. Critics assert these data indicate
systematic underaging of adults and justifiably remark that 1) criteria for
estimating skeletal age a t death may be unreliable, 2) age determinations are
too frequently based on one or two criteria alone, and 3) adult paleodemographic age profiles often mimic the age distributior, of the modern population
from which a n age indicator’s standards were originally derived. This study
reports a series of tests based on well-documented biological aging phenomena
that can be used to investigate potential effects of systematic underaging in
adults, assuming the skeletal population is of sufficient size to permit such
tests. These include patterns of third decade sternal clavicular epiphyseal
fusion, multiple age and sex criteria associated with cortical bone dynamics,
and fractures known to occur throughout the entire adult ages range. These
phenomena are examined here for the Libben site skeletal population where
adult age at death was determined by the multifactorial summary age technique. None of the biological criteria reported here were used in the Libben
summary age analysis and thus serve as a n independent test of accuracy in
age determination. In addition, the summary age method has recently been
applied to a series of modern skeletons of known age (Todd samples 1 and 21.
Age standards for criteria employed with Libben and Todd 1 were identical.
Since Todd 1displayed underaging in older adults, a second Libben age distribution adjusted for Todd 1bias was generated for comparison. A third Libben
adult survivorship profile based on a Coale and Demeny West level 3 mortality
experience, considered by some to be a more realistic model for skeletal populations, was produced for comparison. For all criteria examined, original Libben summary ages provided superior concordance with known patterns of
biological aging in human populations. While Libben ages adjusted for Todd 1
bias were slightly better in the third decade, both Todd 1 adjusted and Coale
and Demeny West level 3 age distributions produced unrealistic patterns of
biological aging for individuals greater than 35 years. Implications of these
results are discussed.
Received January 19, 1984; revised January 2, 1985; accepted
January 3, 1985.
G 1985 ALAN R. LISS, INC
88
R.P. MENSFORTH AND C.O. LOVEJOY
INTRODUCTION
One of the most significant features to
emerge from recent comparisons of archaeological (“extinct”) and ethnographic (“extant”) populations is their marked divergence
with respect to survivorship or mortality (Lovejoy et al., 1977; Bocquet-Appel and Masset,
1982).Recently Howell (1982),using the Libben population as a n example, presented an
important paper detailing the social and economic effects of the higher adult mortality
seen in archaeological groups. Many of these
effects are dramatic and almost surely require revision of our biological and social
reconstruction of preurban human populations. As Howell points out: “we now have
empirical evidence . . . that life was far more
difficult for prehistoric people in North
America than we have observed it to be anywhere in the world during the 19th and 20th
centuries” (1982:268; emphasis added).
She also points out, however, that a second
interpretation of skeletal data must be considered: that they are the result of “interaction of the usual mortality pattern with
selective biases in the preservation of skeletal materials, errors introduced by the necessarily indirect methods of aging and sexing
skeletons, perhaps complicated by cultural
practices of the living population that produced the cemetery concerning burial of persons of various ages” (1982264).
Howell is addressing two issues. First is
the degree to which a cemetery adequately
censuses the living population that created
it. Second is the accuracy of age determination. We will deal with the first of these two
questions in a separate communication. The
present paper is an attempt to investigate
the second.
The reader might immediately question
how such a check of the accuracy of age assignments can be carried out, since age at
death can never be “known” for a n extinct
group. The Libben life table and survivorship
curve were obtained by means of the multifactorial (“summary”) age method (Lovejoy
et al., 1977). This technique employs multiple anatomical age indicators. In the discussions that follow, the population age
distribution, derived from these individual
age assignments, will be compared to a series
of populational phenomena of physiological,
pathological, andor developmental character that bear a strong ineasureable relationship with age. That is, the time sequence of
a series of individual anatomical events
(changes in age indicators) will be compared
to the time sequence of biological events that
are well documented from the study of living
populations of known age.
Although the methods by which the Libben
population was aged have already been presented (Lovejoy et al., 1977, 19851, some comment is appropriate here concerning the age
estimates used for the oldest segment of the
population. Because so few individuals at
Libben were found to have ages at death
exceeding 50 years, the oldest category used
for life table calculations was 50 + (which for
calculation was assumed to be of 10 years
duration). In fact, individuals clearly older
than 60 years were present at Libben, but
were so few in number as not to be formally
set into higher age categories. During the
assignment of values for each age criterion
(to be entered into multifactorial age calculation by principal components analysis), a
maximum age was set a t 55+ years. This
value simply indicated a very old individual.
Several individuals had all age indicators set
independently a t 55 years. This meant that
the specimen was clearly very old, but that
there was no need to estimate age more exactly for the purposes of life table calculations.
MEDIAL CLAVICULAR FUSION
The human sternal clavicular epiphysis is
a secondary center of ossification for which
the age a t onset and process of closure are
TABLE 1. Medlal clavicular fusion with age
Nonfusion
Sample
-
( 0)
Active Completed
fusion
fusion
(1-2)
(3)
Libben
(males and females)
r\r
X
SD
Modern white’
(males)
N
xSD
Modern black’
(males)
N
~
X
SD
19
22.3
2.1
15
25.4
2.2
9
26.7
1.9
11
21.8
2.5
24
24.8
2.1
11
27.8
1.2
17
21.4
1.6
42
24.1
2.4
11
26.6
2.2
‘Data from Todd and D’Errlco (1928)
SKELETAL CORRELATESOF THE AGING PROCESS
delayed (Stevenson, 1924; Todd and D’Errico,
1928). Fusion usually begins by the twentyfirst year and proceeds slowly, often taking
up to 4 years for completion. Though unfused
epiphyses were occasionally noted in individuals as old as 27 years, anomalous acceleration and retardation rarely varied beyond 2
years.
Owing to the restricted age range for sternal clavicular fusion, it was not incorporated
into multifactorial age determination for the
Libben population. Therefore, population
patterns of clavicular fusion with age can be
used to test for any systematic bias in Libben
third decade age assignments. All Libben
clavicles recovered from burials ranging in
age between 20 and 30 years were assessed
for nonfusion (O), active fusion (1-21, and completed fusion (3). Table 1 and Figure 1 summarize the mean age and standard deviation
for stages of clavicular fusion in Libben males
and females compared to modern American
blacks and whites studied by Todd and D’Errico (1928). Because their female sample was
unusually small, only their male data are
given here. They point out however, that no
significant sex differences were observed for
patterns of clavicular fusion with age.
Results show that clavicular fusion patterns for Libben and the modern samples are
‘9
35
,Ot
A Whlto mslo
0 BIsck mslo
0 Llbbon msle h lomalo
0
1-2
3
STAGE OF CLAVICULAR FUSION
Fig. 1. Mean age for stages of sternal clavicular fusion comparing modern American black and white males
to Libben males and females. 0, nonfusion; 1-2, active
fusion; 3, completed fusion.
89
remarkably concordant. In fact, the age a t
onset for Libben clavicular fusion is 5 months
later than modern whites and only 10 months
later than modern blacks. Similarly, Libben
clavicular fusion is completed 14 months earlier than modern whites and l month later
than modern blacks. Hence, the Libben data
indicate that fusion of the sternal clavicular
epiphysis would both commence and terminate within the same years as the modern
sample. Moreover, variation in mean age for
Libben stages of fusion fall well within the
range of the modern groups. We interpret
these findings as confirmation that Libben
third decade age assignments are reasonably
accurate and we regard the analysis as constituting a n independent check €or systematic bias in young adult age determination.
AGE-RELATED CORTICAL BONE DYNAMICS
Cortical Area and Bone Mineral Density
We recently completed a study of cortical
bone dynamics for a sample of 156 Libben
adults. Two variables used in this study were
cortical area and intracortical porosity of the
femoral midshaft. Since radiographic involution of the proximal femur was a criterion
originally used in Libben age determinations, a new summary age was generated for
each specimen included in the sample. This
assured complete separation of dependent
and independent variables. To obtain cortical
area, 78 male and 78 female femurs were
sectioned at midshaft, cleaned, and photographed. A radial grid was superimposed
over enlarged photographs of each section,
periosteal and endosteal intersects were recorded (77 of each), and a scaling factor for
each photographic enlargement was computed. Actual cortical area was obtained using the GEOBONE program (Lovejoy and
Burstein, 1977; Lovejoy and Barton, 1980).
Each midshaft area was then divided by femoral length to normalize for size (Dewey et
al., 1969b). In addition, each cross section
was examined and scored for presencelabsence and degree of involvement (slight,
moderate, heavy) of intracortical porosity of
the haversian envelope.
Van Gerven et al. (1969) demonstrated that
radiographic insensitivity to intracortical porosity may introduce substantial error in
measurements of cortical thickness and crosssectional area. Similar errors are possible
with GEOBONE measurement (in this program only endosteal and periosteal intersects are recorded and area calculated from
90
R.P. MENSFORTH AND C.O. LOVEJOY
TABLE 2. Libben midshaft femur cortical area (mm2)/femurlength (mm)
Age
(years)
18-19
20-24
25-29
30-34
35-39
40-44
45-49
50
+
Total
Female
X
Male
~
N
4
8
7
7
16
21
10
5
78
0.8156
0.7630
0.7202
0.8379
0.7528
0.6981
0.6598
0.5882
SD
N
0.065
0.089
0.060
0.079
0.087
0.112
0.116
0.141
2
9
7
16
34
10
their spatial distribution). A Dietzen compensating polar planimeter was therefore
used to calculate area evacuated by porosity
and this total area was then subtracted from
the cortical area of each specimen. Thus, all
cortical area measurements reported here
have been adjusted for intracortical porosity.
From a modern clinical perspective, bone
mineral density (BMD) and cross-sectional
area are among the most useful measurements of age- and sex-related skeletal homeostasis in adults. Such studies demonstrate a
slow rate of bone loss in males and females
beginning between 35 and 40 years of age
(Garn, 1970; Goldsmith et al., 1973; Arnold
et al., 1966; Atkinson et al., 1962).The onset
of bone loss in otherwise healthy subjects
may be related to a decrease in calcium absorption that begins in middle life, affects
both sexes, and becomes more pronounced
with advancing age (Gallagher and Riggs,
1978). Superimposed on this slow decrease in
skeletal mass is a 10 to 15-year period of
accelerated bone loss in females following
the onset of menopause (45 to 50 years) and
consequent ovarian insufficiency (Davis et
al., 1966; Meema and Meema, 1976; Cohn et
al., 1976, Horsman et a]., 1977).
Two persistent limitations restrict the utility of modern clinical studies of bone loss for
comparisons with skeletal data. First, clinical surveys often sample attenuated age
ranges (many include few or no individuals
under 40 years). Second, even fewer studies
provide data normalized for size effects, a
methodological consideration shown to be
important (Dewey et al., 1969b; Cohn et al.,
1976).
One comprehensive study that overcomes
these limitations is available, however, and
will be used here for evaluation of Libben
-
X
SD
0.8080
0.8546
0.8673
0.8962
0.8969
0.8291
0.095
0.089
0.059
0.075
0.086
0.061
78
age-related cortical bone dynamics. Goldsmith et al. (1973) report bone mineral density (BMD) in a sample of 3,515 American
blacks, whites, and orientals. BMD was determined by photon absorptiometry of the
distal radius, and all measurements were
normalized for size effects. Age ranged from
18 to 80+ years. It is instructive that patterns of BMD reported in the modern study
of Goldsmith et al. (1973) strongly parallel
Libben age- and sex-related cortical bone dynamics. These data are summarized for Libben in Table 2 and Figures 2 and 3. The
Goldsmith et al. (1973) data are illustrated
in Figure 4. Specifically:
1.Among 18-to 20-year-old individuals, the
Libben sample shows no sex differential in
cortical area just as the modern sample lacks
a sex differential in BMD.
2. Both the Libben and modern samples
display parabolic relationships of cortical
area and BMD with age, respectively. However, the Libben male curve (Fig. 2, 3a) is
clearly truncated only 5 years after peak cortical area is achieved. Thus, both Libben
males and those observed in the modern
study reach peak density a t age 35. In the
modern sample, bone loss progresses after
that age a t a slow and fairly uniform rate
until age 65 at which time it accelerates. The
only inconsistency between the Goldsmith et
al. (1973) and Libben graphs is the more dramatic slope of bone loss in Libben males between ages 37.5 and 42.5. Since the Libben
male midshaft femoral sample is truncated
a t this point, these are the oldest males in
the Libben population represented here. If
this particular group were systematically underaged by about 5 to 10 years, then the rate
of bone loss in Libben and modern groups
would be similar. However, it should also be
91
SKELETAL CORRELATES OF THE AGING PROCESS
1.0,
I
I-
P
W
A
a
a
5
W
Y
n
W
U
a
3
5:
v)
a
W
LI
3
1
-
e---.-.3
Female
Male
18 2 0
25
30
35
40
45
50
55
AGE IN YEARS
Fig. 2. Age- and sex-specific means and standard deviations for Libben midshaft femur
cortical area (millimeters squared) normalized by femur length (millimeters).
pointed out that Libben males between the
ages of 35-40 show no evidence of loss (in
fact, this group has the greatest amount of
femoral cortical area), whereas bone loss in
this group is seen in the modern study. This
would suggest slight overaging of these Libben males. We will return to these points
later.
3. The Libben and modern female samples
also reach peak area and density a t age 35
and the onset of bone loss is apparent in both
samples by age 40.Furthermore, there is a n
acceleration of bone loss following menopause in both samples (which is superimposed on the normal rate of loss). In the
Libben females, however, bone loss appears
slightly earlier (about 2.5 years). A more rigorous method of determining the age at
which bone loss accelerates in Libben females is discussed below.
smith et al. (1973) in their modern survey,
several studies have documented a 2 to 6%
bone mineral loss from the cortex of normal
healthy lactating females (Sorenson and
Cameron, 1967; Atkinson and West, 1970;
Goldsmith and Johnston, 1975). In Figure 5
Libben female cortical area has been graphed
with the modal fertility curve of Weiss (1973).
It is of interest that these two curves are the
inverse of one another.
We suggest, as have others (Dewey et al.,
1969a; Armelagos, 1969; Martin and Armelagos, 1979; Stout and Simmons, 1979), that
this age-specific bone loss may represent calcium stress imposed by the increased nutritional demands of pregnancy and lactation.
Further support of a sex-specific pregnancy
stress at Libben is provided by observations
on the frequency of unremodeled porotic hyperostosis among third decade Libben females. Porotic hyperostosis is a descriptive
Lactation and Pregnancy Stress: The Modal term that refers to macroscopically discerniFertility Curve
ble cranial lesions appearing most frequently
We have observed a 6 to 12% reduction of on the anterior portion of the supraorbital
midshaft femoral cortex in Libben females plate (cribra orbitalia) and on the external
during the third decade (Fig. 2). While no table of the frontal, parietal, and occipital
similar phenomenon is reported by Gold- bones (cribra cranii, spongy hyperostosis,
92
R.P MENSFOKTH AND C.O. LOVEJOY
...
.
.44
18 20
30
25
a
1.0-
35
40
50
45
55
AGE IN YEARS
..
O
.6.
.
...
.
*
.
m
m
.
.*
:.. :
.
..
.
0
. .
\
.4.
18 2 0
b
25
30
35
40
45
50
55
AGE IN YEARS
Fig. 3. a) Relationship between Libben male midshaft femur cortical area (millimeters
squared) normalized by femur length (millimeters) and age. b) Relationship between Libben
female midshaft femur cortical area (millimeters squared) normalized by femur length (millimeters) and age.
93
SKELETAL CORRELATES OF THE AGING PROCESS
females
melee
4
20
50
40
30
i
70
00
80
AGE IN YEARS
Fig. 4. Patterns of age- and sex-related bone mineral density (grams per square centimeter)
normalized by bone width (centimeters) as measured by photon absorptiometry of the distal
radius in a sample of 3,515 modern American black, white, and oriental adults. Adapted from
Goldsmith et al. (1973)
2 .o
1.o
I
l-
0
z
y
.9
1.5
a
3
B
t
B
a
.8
1.0
a
K(x)
3
s:
.7
v)
a
w
.5
t;
-
.6
A
o---o
I
cortical area
fertility
i0
i5
30
35
40
45
50
55
AGE IN YEARS
Fig. 5. Adult Libben female midshaft femur cortical area (millimeters squared) in relation
to the human archetypal fertility curve K(x) and age. Fertility data adapted from Weiss (1973).
94
R.P. MENSFORTH AND ‘2.0.
LOVEJOY
modern studies showing iron deficiency anemia to be more common in adult females of
all ages compared to adult males, but particularly during the child-bearing period (Witts,
1966; Finch, 1968; Yusufji et al., 1973).
The bone loss observed for third decade
Libben females occurs at a time when nutritional demands for iron and calcium would
be markedly elevated, as would the incidence
of iron deficiency anemia. Indeed, the latter
disorder has been shown to contribute to
malabsorption of dietary calcium and iron
(leading to bone loss) (Aksoy et al., 19661,
impaired immune response (Prasad, 19791,
and a more pronounced anemic response (Yusufji et al., 1973).
100
Female
Male
80
so
%
40
20
-
18-29
30-39
40-55
AGE IN YEARS
Fig. 6. Frequency of occurrence of unremodeled porotic hyperostosis for male and female Libben adults.
symmetrical osteoporosis)(Angel, 1966; Carlson et al., 1974; Henschen, 1961; Hengen,
1971; El-Najjar et al., 1976). The lesions are
a response to erythroid marrow hyperplasia
and exhibit a coral, cribriform, or sieve-like
porosity associated with marginal hypervascularity and variable osseous tissue hypertrophy. These skeletal changes are common
in iron deficiency anemia and a number of
other relatively infrequent disease states
(Moseley, 1974; Mensforth et al., 1978).
The age and sex distribution of unremodeled porotic hyperostosis (the acute phase)
in Libben adults is presented in Figure 6.
Libben females are more frequently affected
than males throughout the adult years. The
only significant difference occurs in the third
decade where Libben females show a much
higher frequency than males of the same age
(x2 = 8.55; p < 0.01). This is in accord with
The Age of Menopause
As previously noted, rapid bone loss is
clearly evident in Libben females above the
age of 35. To isolate as closely as possible the
actual age a t which bone loss begins in the
Libben sample, we used the method of serial
splines. This method of analysis is most appropriate because it more accurately approximates the age at which bone loss in older
Libben females becomes greater than third
decade lactationallpregnancy variation and
fourth decade normal bone loss. The female
sample was progressively divided into only
two age classes at 5-year increments (for example, those above and below 30;those above
and below 35; and so forth). For each bisected
sample a linear regression was generated for
bone loss and age for each of the two age
groups (above and below the bisection point).
The intersection of the two linear regression
slopes was then determined graphically. In
all cases, the intersection occurred between
44 and 52 years (Fig. 7), with the best fit to
the actual population data at 46 years. In a
previous investigation by Frommer (19641,
45 years was found to be the modal age of
menopause prior to recent secular trends toward later ages (i.e., up to 50 years).
Intracortical Porosity
Intracortical porosity specifically affecting
the endosteal and haversion envelopes of
femoral cortical bone is another useful criterion for estimating the age at onset of normal
bone loss in males and females and menopausal loss in females. While some degree of
porosity is normal in cortical bone at any
age, a definite increase in the number and
size of resorption spaces in femoral cortex
becomes evident in both sexes by the end of
95
SKELETAL CORRELATES OF THE AGING PROCESS
1.o
I
I-
pw
.9
4
a
a
3
.a
a
a
J
t
Ba
$
v)
a
-6
w
c
w
p
-I
4
5
.5
*- - -* 20-39/40-55
C-. 20-44/43-55
*-,-*20-49/50-53
25
30
s
yr. spilnes
i
Yr. 8PhO8
Yr. 8Pfh08
3s
40
45
50
4
55
AGE IN YEARS
Fig. 7. Serial spline analyses of adult Libben female midshaft femur cortical area with age.
The splines intersect in the age range of 44 to 52 years, indicating a n approximate age at onset
of menopausal bone loss at Libben.
the fourth decade (Jowsey, 1960; Atkinson,
1965; Arnold et al., 1966; Van Gerven et al.,
1969). Furthermore, females experience a
more rapid and extensive femoral intracortical trabecularization, resulting in a sex differential apparent by the end of the fifth
decade (Arnold et al., 1966; Atkinson et al.,
1962). Figure 8 illustrates a continuum of
midshaft femur intracortical porosity a t Libben classified from slight to marked. Resorption spaces follow a n endosteal to periosteal
gradient, with greater concentrations of POrosity occurring along the endosteal envelope
(Atkinson, 1965). More specifically, intracortical porosity affecting the haversian envelope at midshaft femur first aligns along the
anteroposterior axis of the bone and progressively spreads to the mediolateral cortex (Van
Gerven et al., 1969; Mensforth and Lovejoy,
1978). The ultimate result of continued endosteal and intracortical bone resorption is a
cortical shell (Fig. 8, specimen h). It is worthy
of comment here that only two Libben females aged 55 + exhibit cortical shells. Thus,
only 1.3% of the Libben femoral sample show
dramatic bone loss.
Libben intracortical porosity data are summarized in Table 3. The mean age a t onset
for slight macroscopically observable concentrations of porosity is 39 years in Libben
males and females. This finding is concordant with modern observations reporting a n
increase in the number and size of resorption
spaces in both sexes by the end of the fourth
decade of life (Atkinson, 1965; Arnold et al.,
1966). In addition, both Libben and modern
data demonstrate a sex differential in femoral intracortical porosity that becomes evident by the end of the fifth decade. Only
20.5%of Libben males over 35 display intracortical porosity compared to 46% of Libben
females (x2 = 11.54; significant at the 0.001
level of probability). Furthermore, females
show a significantly greater degree of moderate and heavy involvement compared to
males (x2 = 7.28; p < 0.05).
The results presented above are consistent
with termination of the Libben male sample
at 45 years. Libben females would thus have
greater opportunity to be affected by intracortical porosity. Therefore, the analysis was
adjusted to compare males and females lim-
96
R.P. MENSFORTH AND C.O. LOVEJOY
Fig. 8. Series of Libben midshaft femur cross sections displaying 1) slight (a, h), moderate (c,
d, el, and heavy (f, g) concentrations of intracortical porosity; 2) age progressive endosteal bone
resorption; and 3) a cortical shell 01)exhibiting substantial endosteal and intracortical bone
resorption.
ited to the 35-45 age interval. The results
are similar. Here 65% of females and 34% of
males displayed intracortical porosity (x2 =
7.62; p < 0.01). Again, females show a significantly greater degree of moderate and heavy
involvement compared to males (x2 = 4.19; p
< 0.01). Thus, Libben patterns of age- and
sex-related intracortical porosity are in full
agreement with modern clinical observations
that fifth decade females show more rapid
and extensive cortical trabecularization at
midshaft femur compared to males (Arnold
et al., 1966).
Additional Evidence From Bone Dynamics
There are, in addition, a variety of qualitative indications that the Libben cemetery
population contained minimal numbers of individuals over the age of 50 years. The first
concerns the phenomenon of periosteal expansion with age, an effect observed primarily in tubular bones of the appendicular
skeleton. Periosteal expansion has variously
been interpreted to reflect secular trends,
continuing bone growth, or increase in sec-
tion modulus related to biomechanical demands of aging bone tissue (Smith and
Walker, 1964; Smith and Frame, 1965; Garn
et al., 1972; Epker et al., 1965; Trotter et al.,
1968).Nonetheless, data show that periosteal
expansion is common in both sexes over 50
years of age and is usually more pronounced
in osteoporotic females (Smith and Walker,
1964). Libben males and females show no
discernible trend for midshaft femur periosteal expansion with age and this indicates
that few individuals survived beyond 50
years.
Second, the typical deceleration of postmenopausal bone loss, which normally occurs following 10 to 15 years of accelerated
bone loss (Goldsmith et al., 1973), is not evident in the Libben female sample. Third, our
female sample terminates with an average
bone loss of 29.8% at the femoral midshaft.
From a modern clinical perspective radiographic diagnosis of osteoporosis requires a
loss of 30 to 60% bone mineral density. This
does not usually become apparent until the
age of 60 years when 10 t o 15 years of cumu-
97
SKELETAL CORRELATES OF THE AGING PROCESS
TABLE 3. Qualitative assessment of Libben adult midshaft femur intracortical porosity
Males
Intracortical
porosity
N
Mean
age
(years)
Slight
Moderate
Heavy
Total
14
1
1
16
38.9
46.0
36.0
37.3
% Of
% Of
total
sample
(N = 78)
porosity
sample
(N = 16)
N
17.92
1.28
1.28
20.51
87.50
6.25
6.25
100.00
15
9
12
36
Females
% Of
Mean
total
age
sample
(years)
(N = 78)
39.0
43.9
44.4
42.0
19.23
11.54
15.38
46.15
% Of
porosity
sample
(N = 36)
41.67
25.00
33.33
100.00
TABLE 4. Libben population fracture data'
Age
(years)
dx
Person
years
at risk
5-10
11-15
16-20
21-25
26-30
31-35
36-40
41-45
46-50
f50
117
94
92
63
78
115
154
97
50
33
2.5
7.5
12.5
17.5
22.5
27.5
32.5
37.5
42.5
47.5
Observed
fractures
0
1
3
4
(N)
4
14
20
11
8
6
Total
person
years
at risk
Fractures
per person
years
at risk x lo5
293
705
1,150
1,103
1.755
31163
5,005
3,638
2,125
1.568
0
142
260
363
230
443
400
302
376
382
'From Lovejoy and Heiple (1981)
lative postmenopausal bone loss has become
a significant factor in fracture risk (Arnold,
1960; Meema and Meema, 1963; Baylink
et al., 1964; Saville, 1965; Chalmers and
Weaver, 1966).
FRACTURE PATTERNS
Test of Sequence Accuracy
Previous discussions have dealt with the
question of age bias in the Libben life table.
There remains the question of an outside test
for proper age sequence. That is, while previous examples showed a clear correspondence between Libben age-related biological
events and those in modern populations of
known age, we have yet to apply a test to
determine the accuracy of the rank ordering
of Libben individuals.
Such a test is made possible by the collection of data on long bone fractures. Recently,
Lovejoy and Heiple (1981) have reported a
review of all skeletons and the incidence of
long bone fractures with age for the Libben
population. All intact bones were observed,
normalized to a population size of 1,000, and
adjusted for missing (unrecovered) bones (for
methods see Lovejoy and Heiple, 1981).Table
4 presents the results of this survey. It was
found that virtually no fractures at Libben
were the result of interpersonal aggression
and that most were clearly the result of accident. If this is the case, then the longer a
person lives, the more likely the individual
will bear a fracture. We tested this hypothesis by comparing the number of fractures in
an age class with the total years of risk for
that age class, which yielded a product moment correlation of +0.97. Thus, years at
risk accounts for 94% of the variance in the
frequency of occurrence of fractures in individual members of the population. We regard
this as a useful demonstration that the Libben lustral age sequence is almost free of
error.
Fractures of Old Age
In addition to information regarding proper
age sequence, the study of fracture incidence
in modern populations provides several criteria from which the probable lifespan of a
98
R.P. MENSFORTH AND C.O. LOVEJOY
&-.-A
..-.-A
M
50
I
Female dlital forearm
Male distal forearm
Female proximal femur
Male proximal femur
500
400
40
Y
8
v)
v,
4
8
4
300 0
30
8
P
P
200
20
I
d
10
/-.-
x.
- -A-.-
100
__
-. ‘AT”
X
I
30
40
50
60
70
80
+
I
AGE IN YEARS
Fig. 9. Distal forearm and proximal femur fracture
incidence in a contemporary population from England
and Wales. Annual fracture rates are represented as the
number of cases per million. The left vertical margin
shows the distal forearm fracture rates, and the right
vertical margin shows the proximal femur fracture rates.
Adapted from Buhr and Cooke (1959).
skeletal population may be inferred. These
include the age progressive shift in sex ratio
for fractures of the distal radius (Colle’s fractures) (Bauer, 1960) and the age progressive
shift in the total fracture sex ratio (Knowelden et al., 1964).The biological phenomenon
of old age or “J” type fracture patterns (illustrated in Fig. 9) are of interest to us here for
two reasons. First, old age fractures (primarily distal radius and proximal femur) result
almost exclusively from accidental falls precipitated or exacerbated by the degenerative
effects of aging (Buhr and Cooke, 1959).Cultural and technological factors therefore play
only a minor role in their etiology (Knowelden et al., 1964). Second, though different
populations vary in overall fracture rates,
they nonetheless tend t o display similar age
and sex patterns in old age fractures (Alffram and Bauer, 1962).
Figure 10 illustrates the age and sex distribution for distal radius fractures in Libben
adults. In general, very few old age fractures
have been recovered from Libben. Those observed are given as a percentage of all individuals displaying fractures of the same type.
These data show that Libben fracture patterns strongly mimic those reported for modern populations (Buhr and Cooke, 1959).
Under 40 years of age, Libben males and
females have a comparably low incidence of
distal radius fractures. By 45 years, Libben
females have experienced a substantial increase, while males retain a low profile
throughout adulthood. Figure 9 demonstrates that in modern populations there is a
20-year period between the marked acceleration in distal radius fractures and those of
the proximal femur. The precipitous rise in
fractures of the distal radius is present a t
99
SKELETAL CORRELATES OF THE AGING PROCESS
100-
-
&.-A
Female distal radius
Male distal radius
.-.-
80-
60-
%
P
40-
;
I’
I’
20-
20
I‘
I‘
I
‘
30
40
50
i
60
AGE IN YEARS
20
-0
AGE IN YEARS
Fig. 10. Age- and sex-specific frequency of Occurrence
for Libben fractures of the distal radius.
Fig. 11. Age-progressive shift in female/male ratio for
distal forearm fracture rates in a contemporary population from Malmo, Sweden. Adapted from Bauer (1960).
Libben and its age a t onset is identical to
that of the modern population. On the other
hand, only one Libben female (aged 5 5 + )
(and no males) displayed a transcervical femoral fracture. This strongly suggests that no
significant portion of the population survived
beyond the age of 60 years.
of Libben individuals displaying fractures of
the distal radius is 50.5 years. This figure
compares well with the age of 52.5 years that
this ratio would predict in the population
reported by Bauer (1960). A substantially
higher or lower ratio would imply that older
Libben individuals had been significantly
over- or underaged.
Fracture Sex Ratio of the Distal Radius
Figure 11 presents the age-progressive sex
ratio for distal radius fractures reported by
Bauer (1960)for a modern European population. The sigmoid curve demonstrates the acceleration and age-specific sensitivity of the
sex ratio between 40 and 60 years. Age- and
sex-related characteristics of this pattern
have repeatedly been observed in modern
groups (Buhr and Cooke, 1959; Bauer, 1960;
Alffram and Bauer, 1962; Knowelden et al.,
1964).
The Libben female/male distal radius fracture ratio for individuals aged 40 to 55+ is
4:l. This is represented by the horizontal and
vertical intersect in Figure 11. The mean age
Total Fracture Sex Ratio
Age-related changes in the total fracture
sex ratio (TFSR) of a population are another
criterion that can be used to assess the accuracy of adult skeletal age assignments.
Knowelden et al. (1964) reported fracture incidences for both men and women aged 35 to
85 years in a large contemporary population
of the Oxford and Dundee areas of Great
Britain. Fracture patterns in these two areas
were similar and the TFSR data from both
areas have been combined for the present
study. They are summarized in Table 5 . The
change in TFSR shows a strong relationship
with age; Pearson’s r is +0.98. While frac-
100
R.P. MENSFORTH A N D C.O. LOVEJOY
tures are more common in males under the
age of 50 years, female fractures become progressively more prevalent in successive age
categories.
The absolute values of the TFSR for any
age are obviously determined not only by
biological factors (bone loss, body weight) but
also by sex-specificrisk factors related to cultural practices and habits. Though most of
the fractures seen in the Libben population
are clearly of the accidental type, they occurred at very high frequencies (Lovejoy and
Heiple, 1982), and female fracture rates must
clearly be expected to be greater than those
of a modern British group because of the
more active role Libben females must have
played in the group's economic activities.
Nonetheless, the rate of change in the TFSR
TABLE 5. Change in total fracture sex ratio (TFSR)
with age'
Age
(years)
Femalehale
TFSR
0.37
0.68
1.18
1.71
2.02
1.89
40
50
60
70
80
85
'Adapted from Knowelden et al. (1964)
is a more direct consequence of the physiological effects of aging. We therefore obtained a
linear regression for the TFSR and age from
data in Table 5 (TFSR = -1.132 +
0.038(age)),and used this equation to predict
the TFSRs for Libben. Because so few burials
were available for observation over the age
of 45 years, the Libben data were compressed
into two groups as presented in Table 6. The
observed modern and Libben fracture ratios
are listed in Table 7. The critical observation
here is that rate of change in TFSR between
the two age groups is virtually identical for
Libben and the modern group. These data
suggest that Libben fourth, fifth, and sixth
decade age assignments are reasonably accurate given expected standard error associated with skeletal age criteria and their
performance in this time range.
Vertebral Compression Fractures
Subsequent to age determinations made on
the Libben material, a complete survey of
spinal pathology was conducted Wacoska,
n.d.). Included in this study was a compilation of various forms of vertebral fracture,
including senile compression fractures (Lonergan, 1961). These are prevalent in older
females suffering postmenopausal osteoporosis. Four vertebral compression fractures
(1.7%)were found in Macoska's survey (n.d.1
of all adult Libben vertebral columns. One
TABLE 6. Libben adult total fracture sex ratio (TFSR) data
Age
group
(years)
30-44
45-60
Mean age of
Libben
sample
N
F(x)
%
N
F(x)
%
Female/
male
TFSR
37.3
49.3
122
13
23
3
18.9
23.1
95
32
14
9
14.7
28.1
0.78
1.22
Male
Female
TABLE 7. Total fracture sex ratio (TFSR) change with age
Age
(years)
37.3
49.3
ATFSR
Modern'
Libben
summary age
Libben
bias revised
Coale-Demeny
Libben expected
0.29
0.74
+0.45
0.78
1.22
+0.44
0.38
1.17
+0.79
0.91
1.68
+0.77
'Modern rate of change in TFSR was derived from the investigation of Knowelden et al. (1964) of contemporary
fracture epidemiology. A linear regression was obtained from their data to generate comparable ratios for
the Libhen mean ages sampled. The equation is given here as y = -1.132 t O.O38(x), x = age in years, y =
TFSR. Comparable ages for the Libben bias-revised survivorship profile are 39.8 and 60.7, respectively.
Comparable ages for the Coale-Derneny Libhen expected survivorship profile are 53.8 and 73.9, respectively.
101
SKELETAL CORRELATES OF THE AGING PROCESS
. .
...........
Libben Actual
Libben Bias-Revised
.-._.-.- C-D
Age in
West 3
Years
Fig. 12. Comparison of the original Libben population survivorship curve t o 1) Libben
survivorship with adult ages revised for Todd sample 1 bias, and 2) the Coale and Demeny
(1966)West level 3 model life table age distribution.
occurred in a 31-year-old male who otherwise
showed no evidence of osteoporosis and in
whom the defect may possibly have been the
consequence of trauma or a congenital defect.
The three remaining cases were found in females aged 55 +. No senile compression fractures were found in any females aged
younger than 55 years, and because traumatic injuries (including fractures) were
found to occur at a very high rate a t Libben
(Lovejoy and Heiple, 1982),this serves as further evidence that a major portion of the
population had died before high rates of bone
loss were manifested in the form of spontaneous fractures.
DOES THE LIBBEN SURVIVORSHIP CURVE
REQUIRE REVISION?
We have seen thus far that a variety of
developmental, pathological, and physiological phenomena, which have a strong relationship with age, prove strikingly concordant to the Libben survivorship curve. However, two important issues must now be addressed. First, the Libben population was
aged by means of the multifactorial (“summary”) method, which has been subjected to
a comprehensive blind test for accuracy and
bias (Lovejoy et al., 1985).The first test (Todd
sample 1) showed a tendency to underage
individuals over 40 years. Since the age standards used in this test were the same as
those used to age the Libben population, one
might expect that the Libben life table was
affected by this bias. To test this possibility
we carried out a systematic revision of all
adult Libben age estimates. A third order
polynomial’ was fit to the observed bias by
decade found in Todd test 1 (Lovejoy et al.,
1985). This polynomial was then used to revise the age of each adult Libben burial, and
a new life table and survivorship curve were
constructed. The latter is shown in Figure 12
(along with the original curve).
Second, to generate conclusions about the
social and economic effects of the Libben
mortality profile, Howell (1982) compared
Libben survivorship data to a series of Coale
and Demeny’s model life tables (1966), which,
as she points out, are extrapolated “from populations with better mortality conditions”
(1982:264).Therefore, for the discussions that
follow, we have constructed a third survivorship curve (also illustrated in Fig. 12) based
on a Coale and Demeny West level 3 popula‘Polynomial regression adjustment for Todd sample 1 underaging bias. x = Todd sample 1 age; y = Libben bias-revisedage;
and y = 5.24859 + 0.5922054(x) + 0.0033306(x2) +
0.00015182(x3).
102
R.P. MENSFORTH AND C.O. LOVEJOY
tion with the same total adult percent survivorship as the Libben population; that is, in
both the Libben and the Coale and Demeny
curves, individuals over 20 years comprise
45% of the total population. A third order
polynomial' was then fit to the Libben mortality data such that age-specific survivorship would yield the Coale and Demeny
model population. Both the Coale and Demeny and the revised Libben curves were
extremely close fits to their respective data.
Table 8 presents the results of these two formulas in 5-year age intervals for comparison
to the original Libben age estimates.
We may now examine whether the Libben
bias-revised curve or the Coale and Demeny
curve provide a more parsimonious fit to observed biological trends in the Libben population. For comparison with modern
biological age standards, age reassignments
for each Libben burial have been carried out,
and the data have been summarized in
Tables 7, 8, and 9, which show that in virtually every category of biological phenomena discussed earlier, the original Libben age
assignments are preferable to either the biasrevised or Coale and Demeny adjustments.
Therefore, several points require discussion. It may be noted that the bias-revised
ages are only minimally different from the
original Libben age assignments. For example, there is only a + 1.6 year difference after
revision for burials in the 30-40 age category
and a +3.4 year difference for those in the
35-45 year age range. No significant change
occurs until ages 45 and above are revised.
As previously noted, however, in the original
Libben age assignments older individuals
were simply assigned a n age of 55 years.
Because such assignments were rarely required, revision would have virtually no effect on vital statistics of the population
(fertility rate, population growth, and soforth). There were, without question, individuals at Libben who survived into relatively
old age, but such individuals were few in
number. A comparison of the original and
revised Libben survivorship curves clearly
demonstrates this fact.
However, one significant change is possibly
required as a consequence of the bias tests
carried out by Lovejoy et al. (1985). In that
study (Todd sample l),the greatest error occurred in the age determination of late middle-aged males (35-50 years), who tend to
demonstrate a quiescence of age-related anatomical change during this period. Thus, it
TABLE 8. Comparison of Libben adult age
distributions
Original Libben
summary age
20
25
30
~~
35
40
45
50
55
Libben
Bias revised
Coale-Demeny
expected
19.6
24.5
30.1
36.6
44.0
52.5
62.2
73.2
20.0
28.9
38.9
49.2
59.1
67.8
74.7
79.1
In the first column, Libben adult age distribution is simply
represented as reported for 5-year age intervals. In column two
is the Libben adult survivorsbip adjusted for Todd sample 1
underaging bias in age indicator performance. Column three
lists Libben adult age distribution fit to the Coale and Demeny
(1966)West level 3 model life table. Age revisions reported here
were derived from polynomial regression equations (see text
footnotes 1 and 2).
is possible that the oldest males a t Libben
are underaged slightly (approximately 5
years). However, comparisons between Libben and modern males in the 35-45-year age
category show remarkable consistency in all
the variables discussed above, and the Libben population contained virtually no males
beyond the age of 55 years. In fact, most were
dead by age 40, and revision of older males
therefore has little effect on the vital statistics of the population. In addition, the comparisons listed in Table 9 show a slight
overaging of Libben males under 40 years,
although this is quite possibly attributable
to sampling error.
Since the bias observed by Lovejoy et al.
(1985) was substantial in older age categories, it is important to consider why revision of the Libben age distribution did not
have a more substantial effect. Two reasons
appear paramount. First, most of the bias
detected in the study was observed in both
sexes over 40 years, and especially over 45
years. Most Libben individuals were dead by
these ages, and their original age assignments therefore reflect the general accuracy
of the earlier years. Second, and equally important, was the central role played by dental attrition in the original aging of the
Libben population. Lovejoy et al. (1985)found
2Polynomial regression distributing adult Libbeu burials according to the Coale and Demeny West level 3 mortality experience. x = Libben original summary age; y = Libben expected
age according to Coale and Demeny model; and y = 9.9984 1.00768(x) + 0.095053(x2)- 0.00098(X3).
'Coale and Demeny (1966).
menopause in females
V. Fracture epidemiology
a. Age at onset for dramatic
rise in female distal
radius fractures
b. Mean age at which the
F N distal radius fracture
ratio is 4:l
IV. Age range for onset of
Garn (1970);Goldsmith
et al. (1973)
111. Age at onset of bone loss
a. Total cross-sectional area
and bone mineral density
b. Age at onset for increase
in intracortical porosity
27.2
35.0
35.0
35.0
35-40
35-40
35-40
35-40
35-40
35-40
45-52
Stage 3
Female
Male
Total
Female
Male
Total
Female
Male
Total
40-50
52.5
Bauer (1960)
1-2
21.6
24.5
Stage 0
Stages
Buhr and Cooke (1959);
Bauer (1960)
Frommer (1964)
(1966)
Jowsey, (1960);Atkinson
(1965);Arnold et al.
Goldsmith e t al. (1973)
11. Peak bone mineral density
and peak cortical area
Reference
Todd and D'Errico (1928)
(mean ages for black
and white males)
I. Stage of clavicular fusion
Biological age criteria
Age
(years)
50.5
45.0
26.7
32.5
37.5
35.0
37.5
42.5
40.0
38.9
39.0
39.0
44-52
22.3
25.4
Libben
summary
age
63.2
52.5
26.3
33.2
40.1
36.6
40.1
49.7
44.0
42.3
42.4
42.4
51-64
21.8
24.9
Libben
bias
revised
74.7
67.8
32.2
44.0
54.2
49.2
54.2
64.1
59.1
56.9
57.i
57.0
66-76
23.9
29.7
C-D'
Libben
expected
TABLE 9. Age and sex relationships for biological phenomena as they occur in modern populations and as reported for the Libben skeletal
population
104
R.P. MENSFORTH AND C . O . LOVEJOY
almost no bias in this age indicator, despite
having been applied to a population with
minimal and irregular attrition. At Libben
there was consistent, progressive dental wear
(Lovejoy, 1985).This clearly provided reasonably accurate and unbiased age determinations for the majority of the older members
of the population. That such is the case is
demonstrated by the very high loading dental wear achieved in the original intercorrelation matrix used to generate the principal
components weightings for summary age
(Lovejoy et al., 1977).
One additional point is worthy of mention.
The tests carried out on Todd sample 1 (Lovejoy et al., 1985) also indicated a slight oueraging of individuals in the beginning of the
third decade. It may be noted here that the
bias-revised Libben ages, as seen in relation
to the onset and progress of clavicular fusion,
provide a slightly better fit than the original
age assignments. The error involved is only
minimal, but results of the correction due
indicate the sensitivity of tests for bias in
this age range.
Turning to the revised age distribution
which results from Coale and Demeny modeling, we find the results far more dramatic.
New age assignments made after revision by
this model are completely inconsistent with
known biological phenomena. Even in the
earliest years, as reflected in clavicular fusion, the Coale and Demeny ages are greatly
in excess of those associated with biological
events in a modern population, and this de.
monstrable discordance becomes magnified
in older age groups (Table 9).
DISCUSSION
that bone loss and porotic hyperostosis associated with pregnancy and lactation occur at
the peak of the modal fertility curve; that
menopause occurs a t a n almost identical age
in the archaeological sample; and that a variety of advanced degenerative changes of
osteopenia, old age fractures, and age-progressive fracture ratios are absent from the
Libben population, which was originally reported to contain few individuals over 55
years of age.
Last, we must address the basic question of
rate of change in anatomical indicators of
skeletal age a t death. If these indicators supposedly age at different rates in earlier populations, what are the supposed differences?
On what a priori grounds would, for example, metamorphosis of the pubic syphysis occur a t higher or lower rates in an archaeological sample? It is difficult to generate
a hypothesis to explain why metamorphosis
of the pubic symphysis should be delayed. It
is possible to presume that higher levels of
musculoskeletal stress would accelerate
changes in the pubis, but this assumes that
pubic changes are dependent on and sensitive to stress. No such demonstration has
ever been presented, save for distortions produced by successive pregnancies, which are
known to occur in modern specimens, thus
allowing appropriate age correction (Gilbert
and McKern, 1973; Suchey, 1979; Meindl et
al., 1985). Sex differences in changes of the
auricular surface are especially important in
this regard. Both Lovejoy et al. (1985) and
Sashin (1930) found that female auricular
surfaces change less rapidly than those of
males, despite the traumatic effects of pregnancy wherein the sacroiliac joint possibly is
subjected to the same estrogen-induced
changes as the pubis. In this case stress does
not accelerate alteration of the age indicator
whatsoever. The paramount feature of the
pubis for the third and early part of the fourth
decades is the “delayed epiphysis” in the
form of the ventral rampart. For what reason
would we expect musculoskeletal stress to
alter the metamorphosis of this feature? It
is, in fact, quite likely that differences in rate
between modern and skeletal populations are
only minor and that classic anatomical indicators of age are equally applicable to prehistoric and modern populations.
Two primary criticisms are frequently leveled at mortality profiles derived from essentially complete archaeological sites. The first
is that skeletal age indicators are not accurate. That question is considered separately
(see Lovejoy et al., 1985). The second criticism is that even given the accuracy of age
indicators for modern populations, we have
no assurance that the rates of change in these
various indicators are the same in archaeological and modern test populations from
which they were derived.
This paper has proposed several tests of
internal consistency that can be applied to a
population for comparison with similar
CONCLUSION
events in modern (“known age”) populations.
We regard the paper presented by Howell
The results appear definitive. We have found
that clavicular fusion patterns show the same (1982) as a major contribution to the study of
age distribution as in modern populations; paleodemography. For far too long paleode-
SKELETAL CORRELATES OF THE AGING PROCESS
mographers have failed to consider the social
and economic consequences of the survivorship and mortality data generated by the
study of skeletal populations. The present
review of the Libben mortality data, furthermore, confirms the dramatic nature of Howell’s social and economic projections. The
accuracy and bias tests presented here (as
well as additional ones yet to be devised)
should be applied to other major skeletal
samples in a n effort to determine whether
the pronounced differences in mortality between those seen a t Libben and those seen in
extant primitive groups are localized or truly
represent a major demographic shift that occurred following development of large urban
population centers whose contact effects became worldwide. Not until this problem is
resolved will we have a complete understanding of the demographic history of human populations and the nature of those
forces of natural selection that operated on
human populations of the late Pleistocene.
105
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ACKNOWLEDGMENTS
Dewey, JR, Bartley, MH, and Armelagos, G J (1969b)
Rates of femoral cortical bone loss in two Nubian popThe research reported in this paper was
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funded by the National Science Foundation,
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