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Electron microprobe analysis of elemental distribution in excavated human femurs.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 62:409-423 (1983)
Electron Microprobe Analysis of Elemental Distribution in
Excavated Human Femurs
JOSEPH B. LAMBERT, SHARON VLASAK SIMPSON,
JANE E. BUIKSTRA, AND DOUGLAS HANSON
Departments of Chemistry and A nthropobgy, Northwestern University,
Euanston, Illinois 60201
KEY WORDS
Gibson site, Ledders site, Diagenesis, Ancient diet
ABSTRACT
Elemental distributions have been determined for femur cross
sections of eight individuals from the Gibson and Ledders Woodland sites. The
analyses were obtained by x-ray fluorescence with a scanning electron microscope. Movement of a n element from soil to bone should give rise to inhomogeneous distributions within the bone. We found that the distributions of zinc,
strontium, and lead are homogeneous throughout the femur. In contrast, iron,
aluminum, potassium, and manganese show clear buildup along the outer
surface of the femur and sometimes along the inner (endosteal) surface, as the
result of postmortem enrichment. The buildup penetrates 10-400 pm into the
femur. The major elements calcium and sodium show homogeneous distributions, but considerable material could be lost by leaching (10-15%) without
causing a palpable effect on the electron maps. Magnesium shows buildup on
the outer edge of some samples. These results suggest that diagenetic contamination may exclude Fe, Al, K, Mn, and probably Mg from use as indicators of
ancient data. The homogeneous distributions of Zn, Sr, and Pb suggest that
these elements are not altered appreciably and may serve as useful dietary
indicators.
Chemical analysis of the mineral portion
of excavated human bone has come into increased usage as a method for the assessment of the ancient diet (Brown, 1973;
Gilbert, 1975; Lambert et al., 1979; Schoeninger, 1979; Sillen, 1981; Price and Kavanagh, 1982). Successful employment of a
given chemical element requires that analyzed elemental proportions must accurately
reflect those present in the skeleton a t the
time of death; i.e., analyzed levels must be
equal to or proportional to the original levels.
Alteration of elemental levels in buried bone
can occur by several mechanisms (Parker and
Toots, 1980).Infiltration of elements from the
environment can occur either into voids
formed by loss of organic components such as
collagen or into the inorganic matrix by substitution. Leaching of elements can occur
frcm the buried bone into the surrounding
soil. Some elements can move in either
direction.
Because understanding postmortem effects
is central to the use of any element for the
0 1983 ALAN R. LISS, INC
assessment of ancient diet, we have explored
diagenesis by four different approaches. (1)
Comparison of observed elemental levels in
excavated bones with those in normal, modern samples can suggest diagenetic alteration when differences are substantial
(Lambert et al., 1979). (2) Comparison of human ribs and femurs shows differences in
elemental levels that may be attributed to
diagenetic causes (Lambert et al., 1982). (3)
Analysis of soil directly around human burials reveals changes caused both by leaching
of elements from bone to soil and by infiltration of elements from soil to bone (Lambert
et al., 1983). (4) Finally, we report herein on
the distribution of elements in femoral cross
sections by electron microprobe analysis. Detailed analysis of the location of buildup or
loss of elements can provide information
about the processes of infiltration or leaching. Parker and Toots (Parker, 1967; Parker
Received June 20, 1983; revision accepted August 16, 1983
410
J.B. LAMBERT, S.V. SIMPSON, J.E. BUIKSTRA, AND D. HANSON
and Toots, 1970, 1974) carried out such studies on numerous nonhuman samples by scanning electron microscopy. More recently
Badone and Farquhar (1982) analyzed concentration gradients by neutron activation
analysis, also on nonhuman samples. In the
present study we have examined human
samples. We report results on several elements that may be useful dietary indicators.
MATERIALS AND METHODS
Femurs were chosen from the Gibson (Middle Woodland) population (samples 1-17,2-40,
3-1, and 5-28) and from the Ledders (Late
Woodland) population (1-16, 1-28, 1-41,and 1146) (Lambert et al., 1979). Cross-sectional
slices were made through the midshaft, and
thin sections were prepared for analysis by
x-ray fluorescence with a scanning electron
microscope (SEM) equipped with a microprobe. Initial cross sections of 1-inch width
were embedded in a methyl methacrylate
polymer resin. From these, thin sections were
cut transversely with a high-speed diamond
blade bandsaw at the Argonne National Laboratory. Thin sections were soaked in ethanol
to remove surface debris. In order to identify
the outer and inner edges of the femur, the
sections were cut with an Exacto knife into
triangular wedges, the longer edge of which
corresponded to the outer surface (the exterior) of the bone. The wedges were mounted
with tweezers onto a 0.5-inch-diameter carbon stub by means of liquid graphite. The
dried carbon stub was mounted with epoxy
onto a 0.5-inch-diameter aluminum stub,
which was used as a mount in the holder of
the SEM vacuum chamber. Graphite was applied to all edges of the carbon stub to ensure
good conductive contact through the samples. Since bone is nonconductive, the entire
mount was carbopcoated to a depth of approximately 300 A in a JEOL Model JEE 4C
evaporator.
Analysis of Na, Mg, and A1 was carried out
at Northern Illinois University on a JEOL
JSM-50A scanning electron microscope with
a wavelength dispersive crystal x-ray spectrometer attachment. The SEM was equipped
with a preamplified pulse-height analyzer,
pX system 7000 Naisel control computer, and
Canberra gas flow proportional counter. The
gas flow detector contained a mixture of 10%
methane and 90% argon. Polypropylene windows on the detector were used to allow penetration of light x-rays from Na, Mg, and A1
to the counter. The analyzing crystal was
rubidium acid phthalate (RAP, ortho-RbOOCC6H4-COOH).
The electron microprobe analysis of all other
elements was carried out in the Northwestern
University Materials Research Center SEM
Facility, with a n identical instrument that
used a xenon-filled proportional counter. The
windows of the detector were covered with a
thin layer of beryllium to allow penetration of
heavy metal x-rays to the counter. The linear
focusing x-ray spectrometer contained pentaerythritol (PET, C(CHzOH),) or lithium
fluoride (LiF) crystal.
The RAP, PET, or LiF crystals were used
to calibrate the spectrometer wavelength,
which was optimized with appropriate standards: KaKanoi Horneblende (A1and Mg), AN
30%NdCa Anarthite (Na), KN03, Sr(NO3)2,
ZnO, CaC03, Pb(N03)2, Mn metal (99.0%),
and Fe metal (99.9%). During analysis, the
samples were irradiated by a finely focused
electron beam. The samples were placed in
the vacuum chamber of the instrument (5 x
lop5 torr), and the distribution of elements
within the section was determined by x-ray
mapping. Each element was analyzed separately. Experimental conditions are given in
Table 1. Each section was analyzed from the
outer edge through to the inner edge. X-ray
maps were photographed with Polaroid positivehegative Type 55 film (ASA 50). Specific
regions of interest were analyzed three times
for the number of x-ray counts per 20-second
period. The volume of these regions was approximately 1 pm3. The sample holder was
normally level. The stage occasionally was
tilted k6.0" to test for aberrations.
RESULTS AND DISCUSSION
As a visual representation of elemental distributions we have used a dot map in which
the density of dots signifies relative concentration. The density of dots depends on the
actual level of a given element, on background noise, and on the sensitivity of the
particular wavelength. Samples were analyzed throughout the entire cross section, but
we illustrate here only the elemental densities on the outer or inner surfaces of the
femur.
Zron
Figure 1shows the distribution of iron from
Gibson 3-1. All figures are 400 pm wide. A
buildup of approximately 20-fold occurs along
the outer surface, and a buildup of twofold
along the inner surface. The surfaces of the
Fig. 1. Iron distribution in femur from Gibson 3-1.
The width of the scan is 400 pm. The figures on the right
are the average number of x-ray counts in 20 seconds for
a volume of approximately 1 pm’ located at the left end
of the white line.
412
J.B. LAMBERT, S.V. SIMPSON, J.E. BUIKSTRA, AND D. HANSON
TABLE 1. Experimental conditons of the electron microprobe analysis
Element
Crystal'
Fe
A1
K
Mn
Zn
Sr
Pb
Na
Mg
Ca
LiF
RAP
PET
LiF
LiF
PET
LiF
RAP
RAP
PET
x-ray'
K,,
K,,
K,"
K<,
K,
L,
L',
K"
K,"
K,.
Wavelength
(nm)
Absorbed3
current
(PA x lo8)
Voltage
(KeV)
134.60
89.39
119.84
146.12
99.78
219.80
83.94
127.68
106.01
107.56
1.0- 3.0
6.0-10.0
2.5- 6.0
1.4- 4.7
1.6- 2.1
1.6- 8.6
2.4- 3.0
6.0-10.0
6.0-10.0
1.0- 2.4
30
15
30
30
30
30
30
15
15
25
Magnification
x 300
x 300
x 300
x300
x 300
x 300
x 300
x 300
x 300
x 300
'LiF indicates lithium fluoride: RAP indicates rubidium acid phthalate; PET indicates pentaerythritol.
'X-ray line in which K, is from the n = 1 shell and L, is from the n = 2 shell.
?rhe absorbed current on the bone from the beam.
femur are easily detected by the abrupt dropoff in iron concentration. The numerals to
the right of the dot pictures are the average
x-ray counts over a 20-second period a t the
indicated spot. The distribution of Fe is homogeneous throughout the interior of the femur. The large buildup along the outer
surface penetrates only 10-20 pm, is not present continuously along the surface, and has
a variable depth of penetration.
Samples from Ledders 1-16, 1-41, and 1-146
and Gibson 5-28 also were examined in this
fashion. In all cases a strong buildup (fivefold
or more) is observed along the outer surface
and a lesser buildup along the inner surface.
The buildup penetrates 5-20 pm from the
surfaces. The interior contains a homogeneous distribution of Fe. In Ledders 1-41,
however, isolated areas of excess Fe (up to
fivefold) were observed further from the surface, but never more than 150 pm in.
The pattern of Fe distribution corroborates
our earlier conclusion that Fe is contaminative, based on overall concentration (Lambert et al., 1979),on higher concentrations in
rib than in femur (Lambert et al., 1982), and
on Fe distribution in the soil (Lambert et al.,
1983).These x-ray pictures, however, provide
the first direct evidence in human samples.
After deterioration of organic matter, the
outer surface of the bone is in direct contact
with the soil and experiences a n influx of Fe.
The medullary cavity normaliy is more protected, so that there is less buildup of Fe on
the inner surface.
Because these SEM observations are not
quantitative, it is not possible to calculate
the absolute level of contamination. Moreover, it is not possible to generalize from
these results, because other conditions of soil
pH, duration of burial, temperature, flooding, and so on might lead to different results.
In the present case, the soil was neutral to
slightly alkaline, and the bones had been
buried since c. A.D. 175 (Gibson) or c. A.D.
1000 (Ledders) (Lambert et al., 1979).
Aluminum
Distribution of A1 was studied in Ledders
1-16, 1-41, and 1-146 and Gibson 3-1. Figure
2 shows the dot map for A1 in Ledders 1-16.
In this sample and the others, there is a
buildup of twofold to 26-fold along the outer
surface, with a penetration of 10-20 pm. The
distribution of A1 is homogeneous throughout the interior and along the inner surface
of the femurs. The only exception to this pattern is Ledders 1-41, in which there is no
buildup of A1 in any portion of the femur.
The present observation of penetration of
A1 into the surface of the femur gives direct
evidence for contamination and corroborates
our earlier conclusions (Lambert et al., 1979,
1982, 1983). Although relative levels of
buildup are similar for Fe and Al, the absence of buildup along the inner surface of
all femurs and along all surfaces of one femur suggests that A1 is slightly less prone
than Fe to infiltration into buried bone.
Potassium
X-ray data were obtained for K in Ledders
1-16, 1-41, and 1-146 and Gibson 1-17, 2-40,
and 3-1. Figure 3 shows the dot map for Ledders 1-146.For this sample, there is a buildup
of fivefold to 13-fold along the outer surface,
extending 10-20 pm into the femur. The concentration of K is uniform throughout the
MICROPROBE ANALYSIS OF FEMURS
Fig. 2. Aluminum distribution in femur from Ledders 1-16.See Figure 1 for details.
413
414
J.B. LAMBERT, S.V. SIMPSON, J.E. BUIKSTRA, AND D. HANSON
Fig. 3. Potassium distribution in femur from Ledders 1-146.See Figure 1 for details
MICROPROBE ANALYSIS OF FEMURS
rest of the femur, including along the inner
surface. Similar patterns are observed for
Gibson 1-17 and 3-1. For Ledders 1-16, a twoto threefold buildup is also observed along
the inner surface. In contrast, Ledders 1-41
and Gibson 2-40 exhibit a homogeneous distribution of K through all portions of the
femur.
Like A1 and Fe, K was previously classified
as a contaminative element (Lambert et al.,
1979, 1982, 19831, and these x-ray results
confirm this conclusion. The variable degree
of influx of K into the bone, however, s u g
gests a sensitivity of the process to specific
environmental characteristics of the burial.
Manganese
This element shows the highest levels of
contamination of any we examined. Buildup
along the outer surfaces of Ledders 1-16 and
1-41 is 30- to 60-fold greater than in areas of
Mn homogeneity and extends 200-400 pm
into the interior (Fig. 4). Furthermore, Mn
concentrates within the femur as patterns
that correspond to osteonal and other canals
within the framework of the bone matrix.
These structures were filled with collagen
and other proteins during the lifetime of the
individual (Goffer, 1980).Deterioration of the
organics after death permits minerals to fill
the voids. We see that Mn is particularly well
suited to fill this role. These results with Mn
are similar to those of Parker and Toots
(1970). Beyond about 400 pm, the distribution of Mn is homogeneous. There is no apparent buildup along the inner surface.
Similar results were obtained with Ledders
1-146 and Gibson 1-17 and 3-1. We observe
stronger buildup of Mn than of Fe, Al, or K,
particularly within structures in the interior
of the bone. The observation of severe contamination is in agreement with our earlier
conclusions CLambert et al., 1979,1982,1983).
Zinc
The distribution of Zn in Ledders 1-16(Fig.
5) is seen to be entirely homogeneous. There
is no evidence for buildup of Zn a t any point
in the bone. Analyses of Ledders 1-28, 1-41,
and 1-146 and Gibson 1-17 show similar homogeneous distributions. Unlike Fe, Al, K,
and Mn, there is no apparent influx of Zn
into the femur. This conclusion agrees with
what we previously observed (Lambert et al.,
1979,1982,1983). All indications are that Zn
concentrations in excavated bone are the
same as those at the time of death and should
415
be a valid indicator of the ancient bone condition and, by inference, diet.
Strontium
Analysis for Sr was carried out on Ledders
1-16and 1-41and Gibson 2-40 and 3-1. Figure
6 shows the results for Ledders 1-16. The xray counts are low because of the inherently
low sensitivity of Sr even a t the best wavelength. Background counts were two to five
times lower than the signal from the bone.
In all samples, the Sr concentration is homogeneous throughout the femur, in agreement
with conclusions from other methods (Lambert et al., 1979, 1982, 1983). This result confirms the validity of using Sr as an indicator
of ancient diet.
Lead
The distribution of Pb in Ledders 1-16 and
1-41 and Gibson 2-40 was found to be entirely
homogeneous along both surfaces and
throughout the femurs (Fig. 7). In our comparison of Pb levels in ribs and femurs (Lambert et al., 1982), we found a lower
concentration in the rib. In most cases, such
a n observation was associated with leaching
of the element from bone to soil. Mackie et
al. (19751, however, suggested that Pb is not
distributed evenly throughout the skeleton
during lifetime, so that the lower levels in
rib may be physiologically inherent rather
than caused by diagenesis. Thus Pb becomes
useful in the analysis of dietary levels and
health (Aufderheide et al., 1981). Our observation of a homogeneous distribution of Pb
in femurs is in agreement with these
conclusions.
Magnesium
We have obtained contradictory indicators
concerning Mg from the other techniques we
have used (Lambert et al., 1979,1982, 1983).
Comparison of ribs and femurs showed no
difference in amounts, but examination of
soil around burials suggested that Mg had
leached from the bone to the soil. We examined Ledders 1-16, 1-41,and 1-146and Gibson
3-1 by electron microprobe and found the distribution of Mg to be inhomogeneous (Fig. 8).
For Ledders 1-16, there is a buildup of twoto 20-fold along the outer surface. Excess Mg
penetrates into the bone 10-30 pm. The distribution of Mg is homogeneous in the interior and along the inner edge of the femurs.
Thus in contradiction to the riblfemur and
soil studies, we observe Mg distributions that
416
J.B. LAMBERT, S.V. SIMPSON, J.E. BUIKSTRA, AND D. HANSON
Fig. 4. Manganese distribution in femur from Ledders 1-16(upper) and 1-41 (lower). See Figure 1for details.
MICROPROBE ANALYSIS OF FEMURS
Fig. 5. Zinc distribution in femur from Ledders 1-16. See Figure 1for details.
417
Fig. 6 . Strontium distribution in femur from Ledders 1-16,See Figure 1 for details.
Fig. 7. Lead distribution in femur from Ledders 1-16. See Figure 1 for details
420
J.B. LAMBERT, S.V. SIMPSON, J.R. BUIKSTRA, AND D. HANSON
Fig. 8. Magnesium distribution in femur from Ledders 1-16.See Figure 1 for details.
421
MICROPROBE ANALYSIS OF FEMURS
appear to result from infiltration of Mg from
the soil into the bone. It is also possible that
surface buildup could result from outward
migration from within the bone as well as
from external contamination. Since we cannot distinguish the two processes, magnesium may in fact be different from, e.g., iron.
A possible explanation of these results has
been provided by Parker et al. (1974) and by
Parker and Toots (1976,19801, who suggested
that Mg moves in both directions; i.e., it
leaches from the bone after death but is reintroduced into the pore spaces of the bone.
Thus any use of Mg levels to assess ancient
diet should prove to be very difficult.
Sodium
We now come to elements that are major
constituents of bone and are found in percentage rather than ppm levels. Thus extremely large amounts of mineral would have
to move in either direction to be detected by
the x-ray technique. Visual examination of
dot maps for Ledders 1-16, 1-28, and 1-41and
Gibson 3-1 shows completely homogeneous
distributions of Na, with the possible exception of small pockets of buildup along the
outer edge. These areas are just barely significant and do not extend along the entire
edge. We observed Na depletion from the
bone into the surrounding soil (Lambert et
al., 1983), so it is possible that Na, like Mg,
moves in both directions.
Calcium
Analysis for Ca in Ledders 1-16 and 1-41
and Gibson 3-1 shows a homogeneous distribution throughout the bone, with two qualifications. First, the high level of Ca skews
the x-ray counts toward the center of the
map. This distortion is a n experimental arti-
fact rather than a reflection of the Ca distribution. Second, certain regions appear to be
almost devoid of Ca. By comparison with the
electron micrograph of the same portion of
the femur, these empty regions were found
to correspond to osteonal canals or other features (Fig. 9). These regions of the bone structure are not part of the inorganic matrix but
were filled with other materials during the
lifetime of the individual. Thus the absence
of Ca in these regions reflects the actual levels before death. Results from the rib/femur
and soil studies (Lambert et al., 1982, 1983)
suggested that Ca is leached from the bone
into the soil. Because of high levels of Ca in
the bone, leaching can occur to a significant
extent without influencing the dot drawing
representation.
SUMMARY AND CONCLUSIONS
Influx of elements from soil to human bone
during burial is successfully and graphically
demonstrated by x-ray analysis with the
electron microprobe. Results for the analysis
of ten elements in eight human femurs from
Woodland sites are summarized in Table 2.
The concentrations of Sr and Zn are homogeneous throughout the cross sections observed. By this technique, these elements
appear to be free from diagenetic effects and
should be useful in the assessment of ancient
diet. Postmortem enrichment by Fe, K, Al,
and Mn is documented by observation of
buildup along the outer surface and sometimes along the inner surface of the femur.
The areas of buildup usually penetrate 1030 pm into the surface for Fe, Al, and K, and
up to 400 pm for Mn. These elements previously were classified as contaminative on the
basis of comparison of ribs and femurs and
on analysis of the adjacent soil (Lambert et
al., 1982, 1983).
TABLE 2. Elemental distribution in femurs'
Sample
Fe
A1
K
Mn
Zn
Sr
Pb
Mg
Na
Ca
Ledders 1-16
Ledders 1-28
Ledders 1-41
Ledders 1-146
Gibson 1-17
Gibson 2-40
Gibson 3-1
Gibson 5-28
C
C
C
C
N
N
N
C
N
2
N
N
-
-
-
-
C
C
N
C
N
-
-
C
C
C
C
C
N
N
N
N
N
-
-
C
-
C
-
-
-
C
C
C
-
-
N
N
N
N
N
-
-
N
N
C
-
N
-
-
-
N
C
-
N
-
-
-
N
-
2
N
-
'C denotes contamination on the inner or outer surface; N denotes homogeneous distribution throughout the femur.
'Low level of contamination on the outer surface.
-
Fig, 9. (Upper) Calcium distribution in femur from Gibson 3-1.See Figure 1 for details. (Lower) Photomicrograph of bone structure for same region ( ~ 3 0 0 ) .
MICROPROBE ANALYSIS OF FEMURS
The concentrations of Pb, Na, and Ca generally are homogeneous within the femurs.
In the case of Pb, lower levels in ribs compared with femurs were attributed to antemortem physiological differences between the
bones rather than to leaching of Pb out of the
bone (Lambert et al., 1982). For Na and Ca,
other results suggested that these elements
leach into the soil (Lambert et al., 1982,
1983). Leaching of significant amounts of
these major elements would not show up in
the x-ray maps but could still cause the rib/
femur differences and observable buildup in
the soil. For example, a decrease in Ca from
37% to 33% would not be visible in the maps
but would still represent a large mass if
moved to the soil and a significant difference
between rib and femur. The greater resistance of femurs to diagenesis also may make
the effects of leaching from the bone more
difficult to observe in the present study. It
would be of interest to examine cross sections
of ribs for this group of elements, since more
extensive effects of diagenesis should be observable. The role of Mg remains ambiguous.
Although proportions of Mg were identical in
ribs and femurs, we have observed leaching
of Mg into the soil and buildup on the outer
edge of femurs. The best explanation for these
results is that Mg undergoes flux in both
directions, leaching out of the bone and redepositing on the surface.
As the first study of elemental distributions in excavated human bone, these results
cannot be considered to be general. Differences in soil and climate conditions, duration
of burial, and choice of bone might lead to
different results. More acid soil, older burials, or analysis of more porous bone could
result in greater contamination.
Since most of the contamination of femurs
reaches only a few tens of microns into the
surface, it would be of interest in the assessment of ancient diet to analyze bones whose
surface has been removed down to several
hundred microns. Such a study would have
to be done in conjunction with the x-ray analysis of cross sections. Some workers have removed surface material, but without using
SEM a s a monitor. The procedure would offer
the opportunity to augment the list of dietarily important elements from Sr, Zn, and Pb
possibly to include Fe, Al, K, Na, Mg, and
Ca, but probably not Mn. The inclusion of Fe,
Mg, and Na would be particularly useful because of their physiological importance.
'
ACKNOWLEDGMENTS
This work was supported by the Research
423
Committee of Northwestern University and
by funds from the local and national organizations of Sigma Xi, the Scientific Research
Society. We are grateful to Dr. Robert Bailey
of Northern Illinois University for the use of
the SEM.
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Parker, RB, and Toots, H (1974) Minor elements in fossil
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Parker, RB, and Toots, H (1980)Trace elements in bones
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