Retention of lead and cadmium in prehistoric and modern human teeth

ENVIRONMENTAL RESEARCH53, 6--15 (1990)

REVIEW Retention of Lead and Cadmium in Prehistoric and Modern Human Teeth PHILIPPE GRANDJEAN* AND POUL J. JORGENSEN'~

*Institute of Community Health and ?Institute of Clinical Research, Odense University, 5000 Odense, Denmark Received October 10, 1989 In 5000-year-old premolars from Nubia and in 500-year-old teeth from Greenland, the lead concentrations were very low; modern teeth contained 10-100 times more lead. In contrast, cadmium concentrations varied by 30-fold in the two prehistorical populations; modern-day cadmium levels were in the lower range of this interval. These data suggest that, when compared to preindustrial exposures, the impact of current environmental lead pollution is considerable, while that of cadmium pollution is much less. © 1990AcademicPress,Inc.

INTRODUCTION

Many toxic substances, such as lead and cadmium, have always occurred in the biosphere, and a certain level of exposure must be considered inevitable as part of natural conditions for life on this planet. Although H o m o sapiens has adapted to the environment and its chemical substances (Eaton and Konner, 1985), the magnitude of current-day exposures may differ considerably from those in which our genetic material developed by means of natural selection. Thus, anthropogenic releases of cadmium to the atmosphere are about 20-fold above estimated emissions from natural sources, and lead pollution is much more extensive (Lantzy and MacKenzie, 1979). Also, increasing environmental deposition of lead has been implicated by analyses of environmental samples that reflect both past and present conditions, such as ice cores, marine water, sediments, peat, tree rings, and various types of museum specimens (MARC, 1985). Also, pioneering studies by Patterson and his colleagues (Patterson, 1965; Ericson et al., 1979) have suggested that only a small fraction of modern lead exposure is of natural origin. Lead is efficiently retained in the calcified tissues, and over 90% of the body burden of lead is located in the skeleton (McDonald et al., 1951; U.S. EPA, 1986). Similarly, a certain, although in this case much smaller, part of the body content of cadmium is stored in calcified tissues (Friberg et al., 1986; Christoffersen et al., 1988). Thus, chemical information contained within preserved human calcified tissues may be used to provide insight into the activities and environmental conditions of prepollution populations, provided that postmortem alterations have not changed the content of the pollutant (Grandjean, 1988). Special consideration must be given to the question of selecting the most appropriate samples for analysis. The samples must represent human populations with true background exposures, and avoidance of postmortem changes in metal

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7

Pb AND Cd IN ANCIENT AND MODERN TEETH

concentrations is a major problem in the selection, as well as in the analysis, of archeological samples. Obviously, the best specimens are those that originate from premetallurgical populations and have been well preserved in extremely dry environments or in frozen condition. Meticulous care is needed, because contamination may occur at any stage of the process, and such exogenous traces may be difficult, if not impossible, to identify or remove (Grandjean, 1988). Circumpulpal (or secondary) dentin from teeth would seem to be an ideal tissue for analysis (Grandjean et al., 1986; Grandjean, 1988). The formation of circumpulpal dentin starts soon after tooth eruption and continues throughout the active life of the tooth; this tissue is known to accumulate the highest lead concentrations in the body. With the root canal almost sealed off from the environment, the dentin is well protected against postmortem contamination. METHODS

Selection of Samples On the basis of strict criteria for selection (Grandjean, 1988), specimens for analysis were chosen to represent prehistoric and modern populations (Table 1). Teeth from premetallurgical humans were procured from the Scandinavian Expedition to Sudanese Nubia (Nielsen, 1979). Of nine well-preserved premolars, four belonged to the A group, i.e., 5300-4900 before the present time (b.p.), four were from the C group (4000-3600 b.p.), and one was from the Pharaonic period (3650-3350 b.p.) as determined by archeological criteria. Four individuals were males, four were females, and in one case the sex could not be determined with confidence. Five were considered adults (18-35 years), one was mature (35-55 years), and one was senile (above 55 years), while the age was undetermined in two cases. Lead was probably known in Egypt and Mesopotamia from about 5000 b.p., but it was not used until about 1500 years later, and only as an ingredient in TABLE 1 ORIGIN OF TOOTH SPECIMENS SELECTED FOR ANALYSIS

Place of origin Nubia, Sudan Greenland Qilakitsoq Ummannaq-Nuuk Denmark Svendborg Funen

Number

Time period (b.p.)

Gender ~

Age, median (range) a

9

5300-3300

4 m, 4 f

(18, >55)

3 14

500 0

3f 7 m, 7 f

(20-50) 19 (10-43)

19 33

750-350 0

9 m, 6 f 28 m, 5 f

(20--40) 26 (10-62)

Note. All teeth were caries-free and in good condition. The Nubian teeth were well preserved by the dry conditions in the desert, the Qilakitsoq samples by low humidity and low temperatures; the Svendborg samples were excavated from alkaline soil. With the root canal almost sealed off from the environment, the circumpulpal dentin was well protected against postmortem contamination. a m, male; f, female; definite gender and age group (years) were determined in 8 individuals from Nubia and 15 from Svendborg.

GRANDJEAN AND JORGENSEN

glasses and bronzes (Montet, 1958). Thus, in the premetallurgical A group, any exposures to lead and cadmium would almost exclusively originate from the diet; possible anthropogenic exposures cannot be excluded for the later populations (the C group and, in particular, the Pharaonic). Although little is known about the prehistoric Nubian diet, one can safely assume that it was almost entirely terrestrial and based on cereals. In Ancient Egypt, the staple diet was wheat and barley; most peasants may have existed on a purely vegetarian diet, and fowl and freshwater fish would provide the major sources of animal protein (Montet, 1958; Wilson, 1988). No current-day control population could be identified, as many migrations have taken place, and because Lake Nasser now covers the Nubian Nile banks where past civilizations thrived. The second group of prepollution samples originates from Qilakitsoq near Ummannaq, Greenland (Hansen et al., 1985). The mummified bodies of six adults and two children had been discovered in a north-facing cave, where low temperature and humidity had resulted in an almost perfect preservation. 14C-dating showed that the individuals died about 1485 AD, i.e., 500 b.p. Because of the interest in preserving these unique mummies in a complete state, only three teeth could be removed for analysis: from two women in grave II, one aged 18-22 years (II/7) and the other about 50 years (II/8), while the third tooth was found separately in the grave and might have originated from one of the same mummies or from an additional woman of about 50 years. Although the southernmost part of Greenland was occasionally reached by ships from Europe at the time, Inuits at Qilakitsoq and all of Disko Bay had probably never had any contact at all with Western culture and its sources of metal contamination (Hansen et al., 1985). Animal bones found in ancient settlements in this part of Greenland indicate that seals constituted the main part of the diet (MChl, 1979). For contemporary reference, 14 caries-free and uninfected premolars were obtained from extractions at the dental clinics in Ummannaq and Nuuk, Greenland. Seven teeth were obtained from each clinic; seven patients were male and seven were female. The median age was 19 years, with a range of 10-43 years. The dietary habits in contemporary Greenland tend to approach those of industrialized countries but the diet includes more fish and occasional meals of seal, in particular in settlements away from the capital, Nuuk. Seal liver and kidney from Greenland contain high cadmium concentrations, but only low levels of lead (Johansen, 1981). Blood analyses have confirmed that the cadmium intake is higher than in Denmark, if seal is a significant part of the diet, although smoking is a major source of exposure (Hansen, 1981). As historical material from Denmark, 19 premolars were selected from the excavations of the medieval Franciscan cemetery for laymen in Svendborg, Denmark (Tkocz and BrCndum, 1985). Nine individuals were male, six were female, and sex was undetermined in four cases; dental wear and bone morphology suggested that all individuals were between 20 and 40 years of age, mostly in the third decade. The excellent preservation of the material is illustrated by the fact that cerebral remains with recognizable histology were present in most of the cases where a complete skull was found, perhaps preserved by the alkaline claycontaining soil. The monastery was founded in 1236, and the cemetery was probably used for some 400 years. One tooth belonged to a skeleton which was dated

Pb A N D Cd IN A N C I E N T A N D M O D E R N T E E T H

9

at 1465 by ~4C analysis. Thus, the samples represent a time span which includes the time of the Qilakitsoq people. Both poor and wealthy citizens were buried in the cemetery, mostly without coffins. Coffins were not lead-lined, nor were lead artifacts found in the immediate vicinity of the human remains analyzed. Apart from cases of degenerative joint disease, few pathological changes were found, and only a minority of the individuals showed caries (and not in the teeth analyzed). ~3C measurements indicated that the food was mostly of terrestrial origin. Historical records and analytical data indicate that several sources of lead exposure were prevalent at the time in Denmark (Grandjean, 1975). However, cadmium was not known and anthropogenic sources of this metal would be unlikely. A total of 33 modern-day premolars without caries were obtained from consecutive medicolegal autopsies at Odense, Denmark. Twenty-eight individuals were male and 5 were female; the median age was 26 years with a range of 10--62 years.

Analytical Techniques Circumpulpal dentin was isolated by a preparation technique designed to minimize contamination risks (Grandjean et al., 1984). To expose the pulp chamber, each tooth was cleaved by applying pressure (with a mandrel or a special vise) on a groove cut vertically in the midline of the anterior surface of the tooth by a diamond grinder. Soft tissue residues in cleaved contemporary teeth were cautiously loosened with an acid-rinsed dental explorer and removed by a 1 min immersion in 10% hydrogen peroxide. All cleaved teeth were rinsed in an ultrasonic bath with 96% ethanol for 20 sec followed by drying for 30 min at 50°C. Circumpulpal dentin from the thin layer bordering the pulp chamber was separated with an acid-washed wolfram carbide rosette burr (Borer rund 008, Hager & Meisinger, D~sseldorf, FRG). The resulting dentin powder was weighed into a sampling cup, and 100 Ixl ultrapure nitric acid was added for overnight dissolution. The following day, the sample was diluted by adding 400 txl purified water. Detection of lead and cadmium took place in a designated trace elements laboratory that has been installed in a former operating theatre with sterile-filtered air under excess pressure and an air lock for change of shoes and laboratory coats. Floor and walls are covered with tiles for easy cleaning, horizontal surfaces have been avoided whenever possible, and extensive efforts have otherwise been made in the laboratory design to avoid sources of sample contamination with trace elements. Likewise, only purified chemicals and acid-washed laboratory ware are used, and tests for trace element contamination are carried out before use. For measurement of lead and cadmium, we used a Perkin-Elmer Model 5100 atomic absorption spectrometer with Zeeman background correction, HGA-600 graphite furnace, and an AS-60 autosampler (Perkin-Elmer, Norwalk, CT). All samples were analyzed in duplicate, and each group of samples were analyzed on different days to avoid potential cross-contamination. The average detection limits (average plus two times the standard deviation) were 0.03 i~g/liter for cadmium and 1.7 ~g/liter for lead. With about 1 mg of dentin dissolved in 500 i~1 of dilute acid, these limits correspond to about 0.015 and 0.85 Ixg/g for tissue concentrations of cadmium and lead, respectively. The average coefficient of variation in duplicate determinations was about 5% for lead concentrations in modern and medieval samples, and 24% in the samples from Nubia and Qilakitsoq. With

10

GRANDJEAN AND JORGENSEN

cadmium, the average coefficient of variation in duplicate determinations was about 4% in the samples with high concentrations and otherwise 12%. A reference material (animal bone H-5) from the International Atomic Energy Agency (Vienna, Austria) was included in each analytical series. The cadmium concentrations found were close to the detection limit, and 18 determinations averaged 0.008 txg/g (average of results accepted by IAEA was 0.023 ~g/g, range 0.0040.055 Ixg/g); the lead concentrations averaged 2.87 ~g/g (provisional certified value, 3.1 Ixg/g; acceptable interval, 2.6-3.7 txg/g). The total analytical imprecision of the lead analysis of the IAEA material was 8.0% in 21 separate determinations; the cadmium concentration in the material was too low to provide a useful assessment of the analytical imprecision in this study. Following analysis of lead and cadmium, the samples were diluted fivefold in purified water, and the calcium concentration was then detected by flame emission spectrometry (Filcek, 1958) using an Eppendorf FCM 6341 spectrometer (Eppendorf Ger~tebau, Hamburg, FRG). The analytical quality was ensured by analyzing a laboratory serum control sample with a calcium concentration within the range of those found in the dissolved dentin specimens. The precision averaged 1.3%. RESULTS

Detectable amounts of the two metals were present in all samples, except for lead in one tooth from Qilakitsoq (the young woman). One Nubian tooth originating from the A group had a lead concentration of 1.4 txg/g; circumpulpal dentin from the root canal from another tooth from the same individual contained 1.2 txg/g when examined previously in another laboratory by a different analytical method (Grandjean et al., 1979). The very low lead concentrations in the mummies from Nubia and Greenland (Table 2) do not differ statistically. However, present-day lead levels are one to TABLE 2 LEAD CONCENTRATIONS (~g/g DRY WEIGHT) AND MOLAR RATIOS FOR LEAD VS CALCIUM (X 10 -6) IN CIRCUMPULPALDENTIN FROM HUMAN TEETH Pb concentration

Nubia Ancient Greenland Ancient Present Denmark Medieval Present

Pb/Ca molar ratio

Number

Median

Range

9

2.0

1.4-3.4

1.46

0.86-2.62

3a 14

0.71 16.8

0.39-0.95 5.0-172

0.72 14.6

0.39-1.05 4.4-112

36-381 3.5-163

88 21.8

24.8-239 4.2-183

19 33

100 23.7

Median

Range

Note. Analysis was by electrothermal atomic absorption spectrometry under strict contamination control. The coefficient of variation in duplicate determinations was about 5% for lead in modern and medieval samples, but 24% in samples from Nubia and Qilakitsoq. a The lead concentration in one tooth was below the detection limit.

Pb AND Cd IN ANCIENT AND MODERN TEETH

11

tWO orders of magnitude higher than prehistoric levels. Present-day lead exposure appears to be increased by one to two orders of magnitude in Denmark and Greenland when compared to the prehistoric situation. Even higher lead concentrations were seen in the medieval samples. Within the latter three groups, lead concentrations varied widely. The Nubian mummies contained the lowest cadmium concentrations; significantly higher levels (P < 0.01, Mann-Whitney U test) were found in each of the other groups (Table 3). The three highest cadmium concentrations were from Qilakitsoq, the average being 30-fold higher than in Nubia. In the modern samples from Greenland, somewhat higher cadmium concentrations were found in Ummannaq (median, 0.24 ixmole/mole Ca) than in Nuuk (median, 0.10 txmole/mole Ca) (P < 0.01, Mann-Whitney U test). 14C analysis had shown (Tkocz and BrCndum, 1985) that the adult male with the highest cadmium concentration in the Svendborg group had died about 525 years ago. Within the groups examined, the cadmium concentrations otherwise showed little variation. In the modern-day samples, the lead concentration increased with age (Fig. 1). A relation similar to age could not be determined in the archeological materials. However, among the Nubian samples, the two highest lead levels were seen in an adult male from the (most recent) Pharaonic period and the oldest individual (a female above 55 years) from the A group, the latter perhaps related to an accumulation with age. With regard to cadmium, no age relation could be found. DISCUSSION Analytical results obtained from archeological samples must be evaluated with caution. Considerable evidence suggests that interred skeletal materials are likely to undergo postmortem contamination from soil moisture (Grandjean, 1988). Although no method is currently available to distinguish lead accumulated in vivo from that resulting from exogenous contamination, the samples analyzed in the present study have been carefully selected, handled with utmost care, and anaTABLE 3 CADMIUM CONCENTRATIONS (ng/g DRY WEIGHT) AND MOLAR RATIOS FOR CADMIUM VS CALCIUM (X 50 -6) IN CIRCUMPULPALDENTIN FROM HUMAN TEETH Cd concentration

Nubia Ancient Greenland Ancient Present Denmark Medieval Present

Cd/Ca mo5ar ratio

Number

Median

Range

Median

Range

9

32

14-72

0.05

0.02-0.51

3 54

893 86

707-972 42-363

5.79 0.55

5.44-2.00 0.07-0.43

59 33

537 97

37-768 35-314

0.58 0.56

0.04-5.39 0.05-0.33

Note. As with lead, analysis was by electrothermal atomic absorption spectrometry under strict contamination control The coefficient of variation in duplicate determinations was about 4% in the samples with high concentrations and otherwise 12%.

12

GRANDJEAN AND JORGENSEN 200. A

150-

[] []

100-

50-

"" z% Zk

,x A

~ I I0

Z~O ~,~ rnzx z~ i 20

I 30

I 40

i 50

i

I

60

70

Age (years) FI6. 1. Age-related increase in lead (atomic ratio × 10 6 in relation to calcium) in contemporary circumpulpal dentin from Danes (triangles) and Greenlanders (squares). In the archeological samples, no difference in lead was seen between age groups. Also, the cadmium concentrations showed no relationship to age.

lyzed under conditions to minimize laboratory contamination. The Nubian and Qilakitsoq samples were preserved under almost ideal conditions, but the medieval remains from Svendborg were exposed to alkaline soil moisture. The rate of dissolution and transfer of metal ions by soil water into or from calcified tissues is hard to judge. However, circumpulpal dentin is well protected and would presumably be less influenced by such changes than would more superficial mineralized tissue. Extensive data (U.S. EPA, 1986) have indicated that lead is continuously being accumulated in calcified tissues, as also found in the present study (Fig. 1). With cadmium, no age relation could be found in the modern samples, perhaps due to the overriding importance of cadmium exposure from tobacco smoking or a less stable binding of cadmium in mineralized tissues. As the age distribution was similar in the groups studied (Table 1), comparison of metal levels would seem admissible. An important question is to identify an appropriate prepollution reference group. The geochemical conditions, dietary habits, and other factors may have been unique in Nubia and may not be necessarily characteristic of an unpolluted environment. The 500-year-old frozen mummies from Greenland therefore provide an interesting comparison. They contained lead levels even lower than those seen in the much older samples from Nubia, i.e., resulting in an average ratio of 1/30 when compared to present-day Danish samples. That the Qilakitsoq people had a very low lead exposure is also documented by the low lead retention in bone from six of the adult mummies (Grandjean, 1990), i.e., a factor of about 25 below the levels found in bone 10 years ago (Grandjean et al., 1979). Further, for premetallurgical Peruvians, Ericson et al. (1979) calculated from a small number of analyses that the lead concentration could be as low as 0.2 nmole/g and the

Pb A N D Cd IN A N C I E N T A N D M O D E R N T E E T H

13

lead/calcium molar ratio about 0.06 × 10 - 6 in mineralized tissues. Although the validity of this conclusion is unclear, lead concentrations in bone tissue would probably be much lower than in secondary dentin. However, these observations would support the notion that "natural" lead exposure is not of constant magnitude but may vary from region to region and with dietary habits. Ten years ago, by the use of less advanced techniques, samples of circumpulpal dentin from premetallurgical Nubia were found to contain about 1/30 of the lead concentrations seen in Denmark at that time (Grandjean et al., 1979). The present study used improved analytical methods and contamination control, but suggested a ratio of about 1/15. This decreased ratio could well be due to the decline in environmental lead exposures during the most recent decade. When comparing analytical data from contemporary populations, it should also be noted that lead concentrations in secondary dentin from teeth sampled in a U.S. metropolitan area averaged about 7-fold higher than in Danish samples (Shapiro et al., 1975). Thus, the evidence tends to support the conclusion (National Academy of Sciences, 1980) that present-day exposures are 10- to 1,000-fold above those in which Homo sapiens originally adapted. The Svendborg samples are in sharp contrast to the other archeological specimens with regard to lead. Although definite conclusions cannot be made about the exact magnitude of the in vivo concentrations, the relative increases are supported by other evidence. Other medieval bone material contained very high lead levels, including samples from Denmark (Grandjean, 1975) and from the remote Faroe Islands in the North Atlantic (Nielsen et al., 1982). A range of possibilities existed at the time for massive lead exposure. For example, considerable amounts of lead could leach from poorly burned ceramic glaze and from pewterware; lead was used for many purposes, such as water pipes; and lead compounds were used as therapeutic agents and for preservation of certain beverages (Grandjean, 1975). However, the fact that past ignorance produced heavy lead exposures does not change the fact that current environmental lead pollution results in human lead retention levels that are much above "natural" levels. Considerable variations in unpolluted cadmium exposures are suggested by the 30-fold difference between the concentrations found in the samples from Nubia and Qilakitsoq (Table 3). A traditional Inuit diet that also at that time may have contained much cadmium is the likely reason for the very high cadmium levels in the Greenland mummies. Although cadmium exposure from smoking has been widely documented in modern populations (Vahter, 1982), an increased cadmium concentration in the contemporary teeth from Ummannaq, as compared to Nuuk, may well be due to a difference in consumption of marine mammals. This finding would be in agreement with a similar tendency reflected in blood-cadmium concentrations in Greenland (Hansen, 1981). Few studies have dealt with past cadmium exposures. Deciduous teeth from the 13th-18th centuries and excavated underneath the floor of a Norwegian church contained an average cadmium concentration of about 1 txg/g (9 nmole/g), and similar levels were found in present-day controls from Norway (Fosse and Wesenberg, 1981). In the present study, the highest cadmium concentration in secondary dentin from modern-day Danes was only 0.31 Ixg/g (2.8 nmole/g), and the

14

GRANDJEAN AND JORGENSEN

average of the modern Danish teeth was similar to that seen in the archeological samples from Svendborg (Table 3). Thus, although whole deciduous teeth and secondary dentin of permanent teeth may not contain comparable concentrations, both studies suggest that environmental pollution has not resulted in current cadmium exposures that are in significant excess of variations seen in past centuries. However, museum specimens of human kidney from the 19th century showed cadmium concentrations about one-fourth of those found in present-day samples from Sweden; the authors noted that interpretation of these data must take into account that cadmium could be released from the tissue to the preservative medium during the long storage (Elinder and Kjellstr6m, 1977). A suggested fourfold increase in cadmium exposure would agree with the threefold difference between the cadmium concentrations in ancient Nubians, when compared to modern-day Danes and Greenlanders (Table 3). However, this small difference is within the range explained by variations in dietary habits and may not necessarily be due to environmental pollution. CONCLUSIONS Although both lead and cadmium are considered priority pollutants, lead would appear to be a much more widespread hazard with current exposures being 10-100 times above prepollution levels. On the assumption that the human body has limited tolerance toward increments in exposures to toxic metals, a goal for preventive efforts would be that anthropogenic releases should not add significantly to the original background levels. Although variations seem to occur from region to region and with dietary habits, "natural" exposure levels may provide a useful reference, in particular with regard to lead. ACKNOWLEDGMENTS For supplying teeth we thank Drs. O. V. Nielsen, J. P. H. Hansen, N. BrCndum, and J. Simonsen, and the dental clinics in Nuuk and Ummannaq, Greenland. For technical assistance we thank H. Albaek and R. Bjerring. This study was supported by the Danish Medical Research Council.

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Pb AND Cd IN ANCIENT AND MODERN TEETH

15

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