close

Вход

Забыли?

вход по аккаунту

?

Bone microstructure in juvenile chimpanzees.

код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:368–375 (2009)
Bone Microstructure in Juvenile Chimpanzees
Dawn M. Mulhern1* and Douglas H. Ubelaker2
1
2
Department of Anthropology, Fort Lewis College, Durango, CO 81301
National Museum of Natural History, Smithsonian Institution, Washington, DC 20013
KEY WORDS
osteon; Hominoidea; histomorphometry; primate
ABSTRACT
The growth, development, and maintenance of bone are influenced by genetic and environmental variables. Understanding variability in bone
microstructure among primates may help illuminate
the factors influencing the number and size of secondary osteons. The purpose of this study is to assess the
bone microstructure in 8 humeral and 12 femoral sections of 12 juvenile chimpanzees, aged 2–15.3 years,
and one adult chimp. Secondary osteons were counted
and measured for 16 fields per section. Results indicate
that the femur exhibits a mean osteon population density (OPD) of 4.46 6 2.34/mm2, mean Haversian canal
area of 0.0016 6 0.0007 mm2, and mean osteon area of
0.033 6 0.006 mm2. The humerus has a mean OPD of
4.72 6 1.57/mm2, mean Haversian canal area of 0.0013
6 0.0003 mm2, and mean osteon area of 0.033 6 0.005
mm2. Differences are not significant between the humerus and femur, possibly indicating similar mechanical demands during locomotion. Osteon population density exhibits a moderate correlation with age (r 5
0.498) in the femur of the juvenile chimps, but the
adult chimp has an OPD of 10.28/mm2, suggesting that
osteons likely accumulate with age. Females exhibit
higher osteon densities in the periosteal envelope compared to males in the humerus, indicating more remodeling during periosteal expansion. Overall similarities
between chimpanzees and humans as well as previously
published data on Late Pleistocene hominids (Abbott
et al.: Am J Phys Anthropol 99 [1996] 585–601) suggest
that bone microstructure has been stable throughout
human evolution. Am J Phys Anthropol 140:368–375,
2009. V 2009 Wiley-Liss, Inc.
Studies in bone histomorphometry have the potential to
shed light on the variety of factors contributing to growth,
development, and maintenance of bone tissue. Identifying
similarities and differences among species in bone microstructure provides a basis for assessing the relative importance of biological and environmental factors. In addition,
identification of species-specific differences is important in
a forensic context in cases of extreme fragmentation.
Since nonhuman primates share the greatest genetic similarities with humans compared to other mammals, studies
of primate histomorphometry supply information about
the range of variability within Order Primates, serve as
models for diseases affecting bone, illustrate microscopic
differences due to biomechanical strain (such as strain
due to locomotor pattern), and provide models for early
hominid skeletal development.
Early studies in bone histomorphometry focused on
describing variability among mammalian species. Muller
and Demarez (1934) reported Haversian canal diameters
for five apes (gorillas and chimpanzees) and one macaque. Jowsey (1966) measured Haversian canal and
osteon dimensions for two rhesus monkeys in a comparative mammalian study. Singh et al. (1974) quantified the
number and size of primary canals and lacunae in a
sample of 12 nonhuman primates, including two galagos,
four old world monkeys, five new world monkeys, and
one gibbon. Schaffler and Burr (1984) studied percent
osteonal bone and osteon density in 20 primates, including three prosimians, fifteen monkeys, and two chimpanzees, to assess microscopic differences due to locomotor
pattern. More recent studies focus on using primates as
models for human pathology, such as osteoporosis. Przybeck (1985) studied age changes in bone mass and bone
remodeling dynamics in rib samples from 15 macaques.
Burr (1992) studied femoral intracortical bone turnover
for a sample of 54 immature and mature macaques to
assess their utility as models for skeletal pathology in
humans. Havill (2004) utilized 42 of Burr’s bone samples, in addition to samples from another 33 older macaques to provide additional data on bone remodeling dynamics and the applicability of macaque models to studies of human aging and bone pathology. Lees and
Ramsay (1999) studied changes in trabeculae, bone formation rates, mineral apposition rate, and activation frequency with age in 28 cynomolgus monkeys to determine
whether they are appropriate models for perimenopausal
skeletal changes. Mulhern and Ubelaker (2003) compared histological data for 12 juvenile humans and 12
chimpanzees using Kerley’s (1965) method for age estimation to identify similarities and differences during
growth and development.
The purpose of the present study is to expand on the
study by Mulhern and Ubelaker (2003) and provide additional information regarding juvenile chimpanzee microstructural variables, including osteon population density,
Haversian canal area, and osteon area in the femur and
humerus. The results of this study will also be compared
with published results for humans and nonhuman primates. As outlined in Mulhern and Ubelaker (2003), in
addition to providing needed data on chimpanzee microstructural variables, this study has the potential to contribute to a better understanding of the evolution of
C 2009
V
WILEY-LISS, INC.
C
*Correspondence to: Dawn M. Mulhern, Department of Anthropology, Fort Lewis College, 1000 Rim Drive, Durango, CO 81301, USA.
E-mail: mulhern_d@fortlewis.edu
Received 21 May 2008; accepted 3 September 2008
DOI 10.1002/ajpa.20959
Published online 11 May 2009 in Wiley InterScience
(www.interscience.wiley.com).
BONE MICROSTRUCTURE IN JUVENILE CHIMPANZEES
TABLE 1. Sample age and sex distribution
Specimen
Age (years)
Sex
86
113
114
66
82
57
8
45
11
30
1
18
B
2.0
2.0
2.0
5.0
5.0
7.0
9.6
10.0
12.0
13.0
13.4
15.3
35.0
M
F
M
M
M
M
F
F
F
M
F
M
M
human skeletal development as well as developmental
differences between apes and humans related to locomotor pattern. Chimpanzees experience more rapid skeletal
and dental maturation compared to humans (Michejda,
1980; Kuykendall, 1996) and also lack the adolescent
growth spurt found in humans (Hamada and Udono,
2002). Understanding how bone develops in chimpanzees
on a microstructural level allows a more holistic perspective regarding growth and development in hominoids.
MATERIALS AND METHODS
In 1966, Kerley conducted a histological analysis of 30
juvenile and adult chimpanzees of known age (Kerley,
1966). He reported age-related changes in osteon number
and amount of circumferential lamellar bone, but he did
not provide specific quantitative data. In this study,
twelve femoral and eight humeral midshaft cross sections from Kerley’s sample were evaluated, including 12
chimpanzees ranging in known age at death from 2 to
15.3 years (Table 1). The femur from one adult chimpanzee, 35 years of age, was also evaluated and results are
provided, since almost no data on adult chimpanzees
have been published. The samples, prepared by Kerley,
include undecalcified, ground thin sections from the middle third of the diaphysis of each bone. It is unknown
whether the bones came from the right or left side.
According to Kerley’s assessment of epiphyseal closure,
the humerus and femur were completely fused by about
15 years; so, the chimpanzees in this study are considered to be skeletally immature. Unfortunately, the sections from Kerley’s adult sample were not housed with
the immature sections and their whereabouts were
unknown when this study was conducted. Histomorphometric data collected include the number of secondary
osteons and osteon fragments as well as Haversian canal
and osteon areas.
For each section, 16 fields were observed, including
fields adjacent to the periosteal and endosteal borders in
the following locations: anterior–posterior axis, mediolateral axis, anteriomedial–posteriolateral axis, and anteriolateral–posteriomedial axis. Since the slides are not
labeled and therefore side is unknown, ‘‘medial’’ and ‘‘lateral’’ were used for recording purposes only. For this reason, comparisons within each bone section are limited to
the periosteal versus endosteal envelopes. Field sizes
ranged from 1.30 to 4.15 mm2 depending on the overall
size of the bone, but each field size was measured using
image analysis software. The border of each field was
outlined and the area calculated automatically. Haver-
369
sian canal areas and osteon areas were measured in the
same way. Osteon counts were conducted on the monitor,
although they were sometimes viewed through the
microscope also for clarification. For future reference,
individual osteons were numbered and areas were
recorded directly on the images captured. Morphometric
analysis was conducted at 1003 using a Leica DM LB
standard light microscope and Spot Insight color camera
and image capture software.
The symbols for variables used follow Parfitt et al.
(1987) or Stout and Paine (1992, 1994). The following
variables relating to secondary osteons were assessed:
1. Intact osteon density in number/mm2 (N.On): number
of secondary osteons per mm2 with at least 90% of the
perimeter of the Haversian canal intact. At least half
of the osteon’s area had to be within the defined field
to be counted.
2. Fragmentary osteon density in number/mm2
(N.On.Fg): number of osteon fragments or osteons
with 10% or more of the Haversian canal compromised by resorption. At least half of the fragment’s
area had to fall within the defined field to be counted.
3. Osteon population density (OPD): total number of
intact (N.On) and fragmentary (N.On.Fg) osteons.
4. Haversian canal area (H.Ar): average area of Haversian canals.
5. Osteon area (On.Ar): average area of osteons
(including their Haversian canals). Osteons with
round Haversian canals were measured to avoid
measuring oblique osteons.
The total number of osteons measured varied among individuals, but an average of 29 osteons (including both H.Ar
and On.Ar) were measured for each humeral section and
an average of 47 were measured for each femoral section.
Statistical analysis was conducted using SPSS 15.0.
Tests for normality and homogeneity of variances were
conducted and indicated that parametric tests are appropriate, despite the small sample size. Independent Student’s t tests were used to compare count and area variables between the periosteal and endosteal envelopes.
Paired t tests were used to compare counts and areas
between the humerus and femur for the eight individuals represented by both bones. Pearson’s correlation coefficients were calculated to assess possible relationships
between variables, and regression analyses were applied
to identify relationships between chronological age and
histomorphometric variables.
RESULTS
Morphometric data, including numbers of intact
osteons (N.On), osteon fragments (N.On.Fg), osteon population density (OPD), Haversian canal area (H.Ar), and
osteon area (On.Ar), for each specimen are presented in
Tables 2 and 3 for the femur and humerus, respectively.
Osteon population density ranges from 0.35/mm2 to 8.47/
mm2 in the femur, with the lowest value occurring in a
2-year-old chimp and the highest in a 7-year-old chimp.
Haversian canal area ranges from 0.0011 to 0.0021 mm2
and osteon area ranges from 0.025 to 0.046 mm2 in the
femur. In the humerus, OPD ranges from 2.19 to 7.31
mm2, Haversian canal area ranges from 0.0009 to 0.0017
mm2, and osteon area ranges from 0.026 to 0.041 mm2.
Summary data are presented by bone and by sex in
Table 4. Results for the femur include separate data for
American Journal of Physical Anthropology
370
D.M. MULHERN AND D.H. UBELAKER
TABLE 2. Histomorphometric variables by individual for the femur
Specimen
Age
(years)
Sex
N.On
(number/mm2)
SD
N.On.Fg
(number/mm2)
SD
OPD
(number/mm2)
SD
H.Ar
(mm2)
SD
On.Ar
(mm2)
SD
86
113
114
66
82
57
8
45
11
30
1
18
B
2.0
2.0
2.0
5.0
5.0
7.0
9.6
10.0
12.0
13.0
13.4
15.3
35.0
M
F
M
M
M
M
F
F
F
M
F
M
M
0.35
4.35
3.22
2.82
2.00
8.08
4.94
3.92
8.22
3.89
5.01
4.91
10.28
0.83
2.20
3.54
2.29
2.40
4.76
3.67
2.41
3.80
3.29
3.57
3.85
4.45
0.00
0.25
0.00
0.09
0.00
0.39
0.17
0.03
0.22
0.28
0.23
0.11
0.48
0.00
0.52
0.00
0.23
0.00
0.50
0.25
0.12
0.39
0.46
0.31
0.26
0.36
0.35
4.60
3.22
2.91
2.00
8.47
5.11
3.95
8.44
4.17
5.24
5.02
10.77
0.83
2.28
3.54
2.41
2.40
5.09
3.85
2.45
3.49
3.65
3.78
4.02
4.56
0.0011
0.0018
0.0019
0.0012
0.0015
0.0012
0.0016
0.0013
0.0016
0.0021
0.0016
0.0014
0.0012
NA
0.0010
0.0010
0.0005
0.0007
0.0009
0.0006
0.0006
0.0013
0.0010
0.0006
0.0008
0.0006
0.025
0.036
0.034
0.033
0.030
0.032
0.046
0.025
0.032
0.032
0.031
0.037
0.031
NA
0.017
0.015
0.014
0.021
0.012
0.019
0.008
0.017
0.013
0.013
0.019
0.013
TABLE 3. Morphometric variables by individual for the humerus
Specimen
Age
(years)
Sex
N.On
(number/mm2)
SD
N.On.Fg
(number/mm2)
SD
OPD
(number/mm2)
SD
H.Ar
(mm2)
SD
On.Ar
(mm2)
SD
86
113
114
82
57
45
11
1
2.0
2.0
2.0
5.0
7.0
10.0
12.0
13.4
M
F
M
M
M
F
F
F
3.78
6.88
3.22
2.19
4.78
5.24
5.54
4.73
2.79
5.16
3.49
2.42
3.98
2.47
3.25
2.80
0.03
0.44
0.14
0.00
0.39
0.05
0.04
0.31
0.10
0.82
0.40
0.00
0.75
0.12
0.15
0.45
3.81
7.31
3.36
2.19
5.17
5.29
5.58
5.04
2.79
5.58
3.56
2.42
4.29
2.52
3.30
3.07
0.0011
0.0011
0.0013
0.0015
0.0016
0.0013
0.0009
0.0017
0.0003
0.0004
0.0005
0.0008
0.0007
0.0006
0.0004
0.0010
0.030
0.033
0.032
0.041
0.035
0.033
0.026
0.039
0.010
0.015
0.020
0.017
0.021
0.013
0.012
0.023
TABLE 4. Summary data by bone and sex
Bone
Femur
Sex
n
F
5
M
7
Both 12
Botha 8
Humerus F
4
M
4
Both
8
Mean
age
N.On.
(years) (number/mm2)
9.4
7.0
8.0
6.7
9.4
4.0
8.0
5.29
3.61
4.31
4.39
5.60
3.50
4.55
SD
N.On.Fg
(number/mm2)
SD
OPD
(number/mm2)
SD
H.Ar
(mm2)
SD
On.Ar
(mm2)
SD
1.70
2.44
2.25
2.73
0.92*
1.08*
1.46
0.18
0.12
0.15
0.14
0.21
0.14
0.17
0.09
0.15
0.13
0.15
0.20
0.18
0.18
5.47
3.73
4.46
4.53
5.81
3.64
4.72
1.73
1.97
2.34
2.86
1.03*
1.23*
1.57
0.0016
0.0015
0.0016
0.0015
0.0013
0.0014
0.0013
0.0002
0.0004
0.0005
0.0003
0.0004
0.0002
0.0003
0.034
0.032
0.033
0.031
0.033
0.034
0.033
0.008
0.004
0.006
0.004
0.005
0.005
0.005
* Denotes P \ 0.05 between males and females.
a
Individuals also represented by humerus.
the eight individuals also represented by the humerus.
Overall, the femur and humerus exhibit similar OPDs of
4.46 6 2.34/mm2 and 4.72 6 1.57/mm2, respectively. The
eight individuals represented by the humerus and femur
have a femoral OPD of 4.53 6 2.86/mm2. A paired t test
between the eight individuals represented by both bones
shows no significant differences in osteon number.
Figure 1 shows a comparison of values for OPD in the
humerus and femur for the eight individuals represented
by both humerus and femur. The correlation coefficient
for OPD in the femur and humerus is r 5 0.547, indicating that 29.9% of the variation in humeral OPD is
explained by the variation in femoral OPD. Overall,
Haversian canal area is slightly larger in the femur
(0.0016 6 0.0007 mm2) compared to the humerus
(0.0013 6 0.0003 mm2), even when the subgroup of eight
individuals is isolated (0.0015 6 0.0003 mm2). Finally,
mean osteon area is the same in the femur (0.033 6
0.006 mm2) and humerus (0.033 6 0.005 mm2) for the
American Journal of Physical Anthropology
Fig. 1. Scatterplot of OPD in the femur and humerus.
371
BONE MICROSTRUCTURE IN JUVENILE CHIMPANZEES
TABLE 5. Osteon counts by envelope in the humerus
N.On (number/mm2)
Specimen
OPD (number/mm2)
Age (years)
Sex
Periosteal envelope
Endosteal envelope
Periosteal envelope
Endosteal envelope
2.0
10.0
12.0
13.4
9.4
5.1
2.0
2.0
5.0
7.0
4.0
2.5
F
F
F
F
5.06
5.50
6.36
3.45
5.09*
1.22
1.58
0.46
0.78
1.31
1.03*
0.51
9.00
5.03
4.73
5.97
6.18
1.95
5.43
5.97
3.59
7.37
5.59
1.56
5.44
5.50
6.36
3.61
5.23*
1.16
1.94
0.64
0.78
1.31
1.17*
0.59
9.50
5.12
4.81
6.29
6.43
2.14
6.03
6.08
3.59
8.06
5.94
1.83
113
45
11
1
Mean
SD
86
114
82
57
Mean
SD
M
M
M
M
* P \ 0.01 between males and females.
TABLE 6. Mean histomorphometric variables by envelope for the humerus and femur
Periosteal
envelope
(number/
mm2)
Endosteal
envelope
(number/
mm2)
Periosteal
envelope (mm2)
Endosteal
envelope (mm2)
Periosteal
envelope
(mm2)
Endosteal
envelope
(mm2)
Bone
n
OPD
SD
OPD
SD
H.Ar
SD
H.Ar
SD
On.Ar
SD
On.Ar
SD
Femur
Humerus
12
8
3.19
3.2
2.03*
2.33*
5.85
6.19
3.08*
1.86*
0.0015
0.0012
0.0002
0.0002
0.0015
0.0014
0.0004
0.0003
0.032
0.03
0.007
0.008
0.034
0.035
0.006
0.006
* P \ 0.05 for a Student’s t test between periosteal and endosteal envelopes within the same bone.
entire sample and slightly lower in the femur (0.031 6
0.004 mm2) when the subgroup of eight individuals is
isolated. Paired t tests indicate that Haversian canal
area and osteon area are not significantly different
between bones within the same individual.
In the humerus, N.On and OPD are significantly different between males and females (P \ 0.05; Table 4).
Osteon population density is 5.81 6 1.03/mm2 in females
and 3.64 6 1.23/mm2 in males. Upon further inspection
of the data, these differences are due to differences in
the periosteal envelope (Table 5). Osteon population density in the periosteal envelope is 5.23 6 1.16/mm2 in
females compared to 1.17 6 0.59/mm2 in males. Females
also exhibit a higher osteon density in the femur compared to males, but differences are not significant.
Haversian canal area and osteon area do not differ
between the sexes.
Table 6 shows the breakdown for each variable by envelope for the femur and humerus. Osteon population
density is significantly different between the periosteal
and endosteal envelopes in both the femur and humerus
(P \ 0.05). In the femur, OPD is 3.19 6 2.03/mm2 in the
periosteal envelope and 5.85 6 3.08/mm2 in the endosteal envelope. In the humerus, OPD is 3.20 6 2.33/mm2
in the periosteal envelope and 6.19 6 1.86/mm2 in the
endosteal envelope. Haversian canal and osteon areas do
not differ significantly between the periosteal and endosteal envelopes in the femur or the humerus.
Pearson’s correlation coefficients between age and histomorphometric variables as well as between histomorphometric variables for the femur and humerus are presented in Table 7. None of the histomorphometric variables exhibit significant correlations with age in the
femur or humerus. A scatterplot of age and osteon population density in the femur shows a somewhat linear
pattern, with a correlation coefficient of 0.498 (see Fig.
2). In the femur, age predicts 25% of the variation in
TABLE 7. Correlation coefficients for age and
histomorphometric variables for the femur and humerus
Femur
Age
OPD
HcA
OA
Humerus
Age
OPD
HcA
OA
H.Ar
(mm2)
On.Ar
(mm2)
0.498
1.000
0.146
0.110
1.000
0.164
0.314
0.348
1.000
0.222
1.000
0.244
20.308
1.000
Age
(years)
OPD
(number/mm2)
1.000
1.000
0.058
20.370
0.863*
1.000
* P \ 0.01.
number of osteons and OPD and 12% of the variation in
osteon fragments when using a linear model. OPD, H.Ar,
and On.Ar do not show any significant correlations with
each other in the femur. Correlation coefficients for
known age and histomorphometric variables in the humerus are very low, and a scatterplot of OPD and age
shows that there is no clear pattern (see Fig. 3). In the
humerus, one pair of histomorphometric variables does
exhibit a significant relationship. Specifically, osteon
area and Haversian canal area show a significant positive correlation (r 5 0.83; P \ 0.01), suggesting that
larger osteons have larger canals in the humerus. Quadratic and cubic regression models do not provide appreciably better fits with the data, indicating that these variables are generally poor predictors of age in juvenile
chimpanzees. The small sample size may also be a factor
in a lack of any discernible relationship.
In addition to the present study, Table 8 shows comparative data for chimpanzees (Schaffler and Burr,
1984), macaques (Havill, 2004), humans (Ericksen, 1991;
American Journal of Physical Anthropology
372
D.M. MULHERN AND D.H. UBELAKER
Fig. 2. Scatterplot of chronological age and OPD in the
femur.
Fig. 3. Scatterplot of chronological age and OPD in the
humerus.
Jowsey, 1966; Burr et al., 1990; Pfeiffer et al., 2006; Mulhern and Van Gerven, 1997), and Late Pleistocene hominids (Abbott et al., 1996) in femoral osteon number
(N.On), OPD, Haversian canal area, and osteon area.
The adult chimpanzee from the present study exhibited
an osteon population density of 10.77/mm2 compared to
4.46/mm2 in the juvenile sample. Mean Haversian canal
and osteon areas are slightly smaller in the adult than
those observed for juvenile chimpanzees including an
H.Ar of 0.0012 mm2 compared to 0.0015 mm2 and On.Ar
of 0.031 mm2 compared to 0.033 mm2.
Using a t distribution comparison of two samples, juvenile chimpanzees have significantly larger osteon
areas (0.033 6 0.006 mm2) compared to macaques (0.024
6 0.006 mm2; P \ 0.001) although Haversian canal sizes
are about the same (0.0014 6 0.0005 mm2 in macaques
and 0.0015 6 0.0003 mm2 in chimps), indicating that
chimpanzees have more bone per osteon.
Compared to adult humans, the juvenile chimpanzees
in the present study exhibit fewer intact osteons, but the
adult chimp is well within the range observed in adults.
Compared to most of the human samples, the juvenile
chimps exhibit significantly smaller Haversian canals (P
\ 0.01). Only the difference in Haversian canal size
between the chimpanzees and the Holocene forager population is not significant. Osteon area in the juvenile
chimpanzees is more clearly in the range of human populations. The juvenile chimpanzees also exhibit significantly smaller Haversian canals (P \ 0.01) compared to
a Late Pleistocene hominid sample, although osteon area
and osteon density are not significantly different.
Percent osteonal refilling, which represents the proportion of space within an osteon’s cement line that has
been filled in with bone, is similar in chimpanzees and
humans, with the chimp value of 95.4% falling just
above the upper end of the range observed for the
human samples.
ity. This means that the effective age of the adult compacta is less than the chronological age of an individual
(Frost, 1987). The weak association between chronological age and osteon density in immature chimpanzees
may be due to modeling drifts and the fact that many of
these individuals have not achieved the ‘‘birth’’ of their
adult compacta.
Schaffler and Burr (1984) reported 7.4 secondary
osteons/mm2 in an adult chimpanzee and the present
study found 10.28 secondary osteons/mm2. Although
these data only represent two individuals, it is interesting to note that the mean number of secondary osteons
in immature chimps is 4.66/mm2, suggesting an overall
pattern of accumulating osteons with age, as seen in
humans. This pattern of increased osteon density with
age in chimpanzees is reported by Kerley (1965), but not
quantified. Additional studies on adult chimpanzees are
necessary to further assess this relationship.
The presence of more secondary osteons in the endosteal compared to periosteal bone in juvenile chimpanzees is likely due to the older mean tissue age in that
portion of the cortex. Osteon density and size do not differ between the humerus and femur in the present
study, revealing histologically similar bone in the forelimbs and hindlimbs. These results suggest that mechanical demands may be similar for both bones during locomotion in juvenile chimpanzees.
Females exhibit more osteons than males in the femur
and humerus (with significant differences in the humerus only). The femur did demonstrate a moderate
relationship between OPD and age; so, the lower mean
age in the male femoral sample could explain this discrepancy. In the humerus, no relationship between age
and OPD was found, arguing against the lower male
mean age as an explanation for the observed difference.
However, given the small sample size, this must be considered. The significant differences in the humerus are
restricted to the periosteal envelope, possibly suggesting
more pronounced mechanical stress and loading during
periosteal expansion in this group of females compared
to the males.
DISCUSSION
Chimpanzees
The accumulation of femoral osteons exhibits only a
moderate linear relationship with age in immature chimpanzees (r 5 0.498 for OPD). This is likely affected by
cortical drift, which erases previous bone turnover activAmerican Journal of Physical Anthropology
Chimpanzee and macaque
Juvenile chimpanzees exhibit fewer, but larger osteons
in the femur compared to juvenile macaques. In the
Abbott et al., 1996
92.5
0.008
6.80–7.45b
5.53–7.06b
0.0021
0.0023
0.0024
9.28–13.42b
Chimpanzee and human
0.0006
0.028
93.2
94.1
0.010
0.009
0.034
0.041
0.0024c
0.0019
0.0037
0.0032
0.0021
0.0009
0.0008
0.016
0.022
0.017
0.007
0.0014
0.0039
0.0019
0.0007
0.039c
0.036
0.045
0.035
0.038
0.006
1.01
% Osteonal refilling 5 OA-HcA/OA.
Range of mean values reported by decade.
Calculated from perimeter.
c
10
18–501 years
b
28
23
21–60 years
21–60 years
3.37
5.76–10.68b
Human (prehistoric males)
Human
(prehistoric females)
Hominid
(Late Pleistocene)
a
4.46
10.77
2.25
7.70
7.40
4.31
10.28
4.96–15.69b
34
41
1
1
12
1
319
26
15
20
20
43
\6 years
[6 years
Immature
Adult
2–15.3 years
35 years
20–97 years
Adult
Adult
25–50 years
17–81 years
20–501 years
Macaque
Macaque
Chimpanzee
Chimpanzee
Chimpanzee
Chimpanzee
Human
Human
Human (Holocene foragers)
Human (18th century)
Human (19th century)
Human (medieval)
373
present study, chimpanzees exhibited an average OPD of
4.46/mm2, H.Ar of 0.0016 mm2, and On.Ar of 0.033 mm2
compared to an OPD of 6.89/mm2, H.Ar of 0.0014 mm2,
and On.Ar of 0.024 mm2 in a sample of 34 immature
macaques (Havill, 2004). Haversian canal size is similar
in these two taxa; so, this may reflect an adaptation to
greater strain in the chimpanzee femur due to mechanical loading during locomotion, with fewer osteons, but
more bone volume per osteon. Schaffler and Burr (1984)
found that suspensory and bipedal primates exhibit a
higher percent osteonal bone compared to arboreal and
terrestrial quadrupeds, probably due to mechanical
strain on the hindlimbs when walking or braking.
Although the juvenile chimpanzees exhibited lower
osteon densities compared to macaques (Havill, 2004),
they also exhibit more bones per osteon; so, this could
result in more secondary bone throughout the cortex.
2.34
0.0015
0.0012
0.0003
0.033
0.031
95.4
93.8
94.7
91.8
90.9
94.5
Havill, 2004
Havill, 2004
Schaffler and Burr, 1984
Schaffler and Burr, 1984
Present study
Present study
Ericksen, 1991
Jowsey, 1966
Pfeiffer et al., 2006
Pfeiffer et al., 2006
Pfeiffer et al., 2006
Mulhern and Van
Gerven, 1997
Burr et al., 1990
Burr et al., 1990
94.2
93.8
0.006
0.005
0.024
0.024
6.89
9.00
3.05
3.36
0.0014
0.0015
0.0005
0.0005
SD
On.Ar
(mm2)
SD
HcA (mm2)
SD
OPD
(number/mm2)
SD
N.On
(number/mm2)
N
Age
Taxon
TABLE 8. Comparative histomorphometric data for the femur
% O Ref a
Study
BONE MICROSTRUCTURE IN JUVENILE CHIMPANZEES
Osteon density does not exhibit a strong relationship
with age in juvenile chimpanzees. A lack of age-related
change in osteon density is also found in subadult
humans. A recent study by Rauch et al. (2007) found no
change in osteon density or dimensions with age in a
sample of 56 iliac crest samples from individuals between
1.5 and 22.9 years. Streeter (2005) found no correlation
between osteon density and age in a sample of human
subadult ribs. In adult humans, osteon density has been
correlated with age in modern and archaeological populations (Currey, 1964; Kerley, 1965; Stout and Lueck, 1995;
Mulhern and Van Gerven, 1997, Mulhern, 2000). The
lack of a demonstrable relationship between osteon density and age in juvenile chimpanzees could be related to
active drift that erases previous remodeling activity. As
mentioned previously, the cessation of active drift determines the age of the effective birth of the adult compacta.
In humans, a gradual decline in the rate of bone drift
occurs between about 14 and 19 years with the onset of
skeletal maturity (Frost, 1987). In chimpanzees, this
likely occurs earlier, since skeletal maturity is reached
sooner. This means that in a given bone, a chimpanzee
likely exhibits older compacta than an age-matched
human. In a previous comparison of this juvenile chimpanzee sample with Kerley’s (1965) sample of 12 human
subadults, results showed that osteon density was 27%
higher in the chimps compared to humans, although the
difference was not statistically significant (Mulhern and
Ubelaker, 2003). The lack of a strong age association
between osteon density and chronological age in juvenile
chimpanzees suggests an overall pattern of development
similar to that reported for juvenile humans.
The overall similarities between chimpanzees and
humans suggest that the femur does not exhibit significant differences due to locomotor pattern. Without comparable data on the humerus, it is impossible to discuss differences that may be present in the upper limb. Certainly,
both species experience mechanical strain in the femur
during growth and development as well as throughout
adulthood during locomotion, although strains in the
upper limb would differ significantly after human infants
begin walking. If humans do differ significantly in bone
microstructure between the humerus and femur, then the
similarity between the humerus and femur observed in juvenile chimpanzees may be related to locomotor pattern.
If not, then bone microstructure in the limbs may be more
heavily influenced by other factors.
American Journal of Physical Anthropology
374
D.M. MULHERN AND D.H. UBELAKER
Osteon density for the adult chimpanzee from the
present study and the chimpanzee studied by Schaffler
and Burr (1984) falls within the range for human adults
(Burr et al., 1990; Ericksen, 1991; Mulhern and Van
Gerven, 1997). Although these data should be considered
with caution at present, the higher osteon densities in the
adult chimps compared to juvenile chimps suggest that
the overall pattern of an accumulation of osteons with age
seen in humans may be found in chimpanzees as well.
Comparing Haversian canal and osteon areas between
chimpanzees and humans is problematic, since the present study is focused on juvenile chimpanzees and data
for osteon dimensions in humans comes from adults.
Although several studies have documented age-related
changes in Haversian canal area in humans (Singh and
Gunberg, 1970; Thompson, 1980), a number of studies
have found no significant relationship between osteon
dimensions and age, including samples with both subadults and adults (Frost, 1963; Mulhern and Van Gerven,
1997; Mulhern, 2000; Pfeiffer, 1998; Rauch et al., 2007).
It is unknown at present whether chimpanzees exhibit
any age-related changes in osteon dimensions, but it is
not unlikely that they follow a similar pattern to
humans. Even so, the following discussion should be considered within this context.
The juvenile chimpanzees in the present study exhibit
significantly smaller Haversian canals compared to most
of the comparative human groups. Osteon areas, however,
are within the range of modern adult humans, although
at the smaller end of the range. In addition, percent
osteonal refilling is similar in the chimpanzee and human
samples, indicating that, despite any differences in overall
dimensions, chimpanzees and humans exhibit a similar
balance of bone formation and resorption.
Abbott et al. (1996) found smaller and fewer osteons
and therefore slower bone turnover in a sample of Late
Pleistocene humans compared to recent humans. Small
osteon sizes were attributed to less vigorous osteoclastic
activity at the cellular level, indicating a lower metabolic
rate for skeletal remodeling. The possibility of nutritional and disease stress as contributing factors was also
suggested. According to the Abbott et al. (1996) study,
low osteon densities in the Late Pleistocene groups could
be attributed to high bone strains during adulthood that
depressed remodeling rates or to a biologically determined lower setpoint for bone response. While osteon
density in the juvenile chimps is comparable to that
observed for the Late Pleistocene hominids, osteon densities for the adult chimps suggest that this may be an
age-related phenomenon, with chimpanzees attaining
higher densities as adults. Since Haversian canal area
and osteon area do not appear to be significantly affected
by age-related changes, it is interesting to note that
while Haversian canal sizes are significantly different,
with chimpanzees exhibiting smaller canals, osteon sizes
are smaller in the Late Pleistocene sample, but differences are not significant, resulting in slightly greater bone
volume per osteon in the chimpanzees. Specifically,
osteonal refilling in the Late Pleistocene sample was
92.5% compared to 95.4% in the chimpanzees.
The overall similarities between chimpanzee and Late
Pleistocene and human histomorphometrics observed in
the present study indicate that underlying genetic factors influencing the general patterns of osteon density
and size during growth and development may not have
changed much during the course of human evolution and
support the idea that populational differences are priAmerican Journal of Physical Anthropology
marily responses to mechanical factors related to activity
and differences in patterns of growth. The effect of activity pattern on bone microstructure in humans is not well
understood. Burr et al. (1990) attributed greater osteon
densities in males and smaller Haversian canals in
females to an active lifestyle in a Native American population from Pecos, New Mexico. Mulhern and Van
Gerven (1997) observed greater osteon densities in males
and larger osteons in females in the femur in a sample
from Kulubnarti, Nubia, but Mulhern (2000) did not
observe any differences between males and females in
the rib for the same population, potentially indicating
different responses in males and females to mechanical
demands or to different types of loading on the femur in
males and females. However, in a recent study comparing rib and femur histomorphometry, Pfeiffer et al.
(2006) found no clear relationship between osteon dimensions and physical activity in three human populations,
suggesting that the relationship between bone microstructure and aspects of lifestyle are complex.
CONCLUSIONS
1. In general, histomorphometric variables do not demonstrate a strong relationship with age in juvenile chimpanzees. This pattern has been reported in juvenile
humans, indicating that chimpanzees and humans follow a similar pattern of histological development.
2. Juvenile chimpanzees do not exhibit differences in
histomorphometric variables between the humerus
and femur, suggesting similar mechanical demands
during locomotion.
3. Juvenile female chimpanzees exhibit higher N.On and
OPD in the periosteal envelope of the humerus compared to males, possibly suggesting greater remodeling during periosteal expansion in this group of
females compared to males.
4. Chimpanzees exhibit larger, but fewer osteons compared to juvenile macaques. These differences may
reflect differences in mechanical demands, with greater
loading on the chimpanzee femur during locomotion.
5. Haversian canal areas are significantly smaller in juvenile chimpanzee femoral bone compared to most
adult human samples, but the amount of bone
replaced per osteon is comparable.
6. Overall, histomorphometric variables are similar
between chimpanzees, Late Pleistocene hominids, and
modern humans, suggesting continuity in skeletal development and microstructure during human evolution, despite differences in locomotor pattern.
ACKNOWLEDGMENTS
The authors thank the Armed Forces Institute of Pathology of the National Museum of Health and Medicine
in Washington, DC, for the loan of Ellis Kerley’s chimpanzee bone thin sections.
LITERATURE CITED
Abbott S, Trinkaus E, Burr DB. 1996. Dynamic bone remodeling
in later Pleistocene fossil hominids. Am J Phys Anthropol
99:585–601.
Burr DB. 1992. Estimated intraortical bone turnover in the femur of growing macaques: implications for their use as models in skeletal pathology. Anat Rec 232:180–189.
BONE MICROSTRUCTURE IN JUVENILE CHIMPANZEES
Burr DB, Ruff CB, Thompson DD. 1990. Patterns of skeletal
histologic change through time: comparison of an Archaic
Native American population with modern populations. Anat
Rec 226:307–313.
Currey JD. 1964. Some effects of ageing in human Haversian
systems. J Anat 98:69–75.
Ericksen MF. 1991. Histologic estimation of age at death using the
anterior cortex of the femur. Am J Phys Anthropol 84:171–179.
Frost HM. 1963. Mean formation time of human osteons. Can J
Biochem Physiol 41:1307–1310.
Frost HM. 1987. Secondary osteon populations: an algorithm for
determining mean bone tissue age. Am J Phys Anthropol
30:221–238.
Hamada Y, Udono T. 2002. Longitudinal analysis of length
growth in the chimpanzee (Pan troglodytes). Am J Phys
Anthropol 118:268–284.
Havill LM. 2004. Osteon remodeling dynamics in Macaca
mulatta: normal variation with regard to age, sex and skeletal
maturity. Calcif Tissue Int 74:95–102.
Jowsey J. 1966. Studies of Haversian systems in man and some
animals. J Anat 100:857–864.
Kerley ER. 1965. The microscopic determination of age in
human bone. Am J Phys Anthropol 23:149–164.
Kerley ER. 1966. Skeletal age changes in the chimpanzee.
Tulane Stud Zool 13:71–82.
Kuykendall KL. 1996. Dental development in chimpanzees (Pan
troglodytes): the timing of tooth calcification stages. Am J
Phys Anthropol 99:135–157.
Lees CJ, Ramsay H. 1999. Histomorphometry and bone biomarkers in cynomolgus females: a study in young, mature,
and old monkeys. Bone 24:25–28.
Michejda M. 1980. Growth standards in the skeletal age of rhesus monkey (M. mulatta) chimpanzee (Pan troglodytes) and
man. Dev Biol Stand 45:45–50.
Mulhern DM. 2000. Rib remodeling dynamics in a skeletal population from Kulubnarti, Nubia. Am J Phys Anthropol 111:519–530.
Mulhern DM, Ubelaker DH. 2003. Histologic examination of
bone development in juvenile chimpanzees. Am J Phys
Anthropol 122:127–133.
Mulhern DM, Van Gerven DP. 1997. Patterns of femoral bone
remodeling dynamics in a Medieval Nubian population. Am J
Phys Anthropol 104:133–146.
375
Muller M, Demarez R. 1934. Le diagnostic différentiel de l’os de
singe et de l’os humain. Ann Med Legale Criminol Police Sci
Toxicol 14:598–607.
Parfitt AM, Drezner MK, Glorieux FH, Kanis JH, Malluche H,
Meunier PJ, Ott SM, Recker RR. 1987. Bone histomorphometry: standardization of nomenclature, symbols, and units. J
Bone Miner Res 2:595–610.
Pfeiffer S. 1998. Variability in osteon size in recent human populations. Am J Phys Anthropol 106:219–227.
Pfeiffer S, Crowder C, Harrington L, Brown M. 2006. Secondary
osteon and Haversian canal dimensions as behavioral indicators. Am J Phys Anthropol 131:460–468.
Przybeck TR. 1985. Histomorphology of the rib: bone mass and
cortical remodeling. In: Davis RT, Leathers CW, editors.
Behavior and pathology of aging in rhesus monkeys. New
York: Alan R. Liss. p 303–326.
Rauch F, Travers R, Glorieux FH. 2007. Intracortical remodeling during human bone development—a histomorphometric
study. Bone 40:274–280.
Schaffler MB, Burr DB. 1984. Primate cortical bone microstructure: relationship to locomotion. Am J Phys Anthropol
65:191–197.
Singh IJ, Gunberg DL. 1970. Estimation of age at death in
human males from quantitative histology of bone fragments.
Am J Phys Anthropol 33:373–381.
Singh IJ, Tonna EA, Gandel CP. 1974. A comparative histological study of mammalian bone. J Morphol 144:421–438.
Stout SD, Lueck R. 1995. Bone remodeling rates and skeletal
maturation in three archaeological skeletal populations. Am J
Phys Anthropol 98:600–604.
Stout SD, Paine RR. 1992. Histological age estimation using rib
and clavicle. Am J Phys Anthropol 87:111–115.
Stout SD, Paine RR. 1994. Bone remodeling rates: a test of an
algorithm for estimating missing osteons. Am J Phys Anthropol 93:123–129.
Streeter M. 2005. Histomorphometric characteristics of the subadult rib cortex: normal patterns of dynamic bone modeling
and remodeling during growth and development. Unpublished
dissertation. University of Missouri, Columbia.
Thompson DD. 1980. Age changes in bone mineralization,
cortical thickness and Haversian canal area. Calcif Tiss Int
31:5–11.
American Journal of Physical Anthropology
Документ
Категория
Без категории
Просмотров
0
Размер файла
129 Кб
Теги
chimpanzee, juvenile, microstructure, bones
1/--страниц
Пожаловаться на содержимое документа