Childhood lead exposure and uptake in teeth in the Cleveland area during the era of leaded gasoline
Introduction
Beginning in the 1970s, the blood lead levels (PbB) of American children declined along with the usage of leaded gasoline and atmospheric lead concentration (Billick et al., 1979, Annest et al., 1983, Rabinowitz et al., 1984, US EPA, 1986, Schwartz and Pitcher, 1989; review, Thomas et al., 1999). Analogous data were obtained from a comparison of deciduous tooth lead in the 1970s vs. the 1990s (Tvinnereim et al., 1997). However, the level of lead uptake in earlier years, during the introduction of leaded gasoline, is unknown because analyses of PbB prior to the peak of leaded gasoline usage were considered unreliable because of contamination (Patterson and Settle, 1976, Everson and Patterson, 1980, Thomas, 1995). Given the known exposure of children, prior to the 1970s, to other major lead sources, such as leaded paint (Weaver, 1989, Nriagu, 1990, President's Task Force, 2000, Jacobs et al., 2002) and soldered food cans (Jelinek, 1982, Bolger et al., 1992, National Research Council, 1993), at least two scenarios could describe the lead burden of American children through the period when leaded gasoline was introduced and later phased out (from about 1930 to 1990).
In the first scenario, exposures to other major pre-existing lead sources (paint, solder in food cans) would themselves have produced high PbB levels prior to the 1930s so that the additional exposure to newly introduced leaded gasoline might have modestly increased PbB. Indeed, Facchetti (1989) reported that airborne lead contributed only 24% to PbB (bone and non-atmospheric sources contributing the remainder). Leaded paint was used in most housing until the 1940s (Weaver, 1989) and in a substantial number of houses until about 1960 (President's Task Force, 2000, Jacobs et al., 2002). Indeed, in much of the Cleveland population of this study, such housing was not substantially replaced over the next 30 years. Solder in food cans, said to account for 20–30% of dietary lead intake (US EPA, 1977, US EPA, 1986), could also have been a major source of lead uptake. For instance, in New Zealand, PbB fell nearly two-fold from 1978 to 1985, presumably due to decreased use of leaded food cans, because lead in gasoline and in drinking water was constant (Hinton et al., 1986). In the US, canned infant milk had high levels of lead until the 1970s (Jelinek, 1982) and 90% of food cans were lead-soldered as late as 1979, declining to 6% by 1988 (Bolger et al., 1992). As explained in Methods, drinking water and atmospheric industrial sources were probably not major lead sources in the Cleveland area. Thus, if lead in paint or food was already causing substantially high PbB before the advent of leaded gas, population lead levels would already have been high before the advent of leaded gasoline. Therefore, the decline of PbB after the 1970s could have resulted from the combined phase-out of leaded gasoline, lead in food cans, and lead in paint.
In the second scenario, pre-existing lead exposure sources would have been small compared to lead exposure due to newly introduced gasoline, so that PbB plotted over time would be predicted to be a unimodal curve, increasing to a maximum and then decreasing, and closely corresponding to the rise and fall of leaded gasoline and atmospheric lead.
The choice between these two scenarios is of public health significance because the severity of clinical and behavioral effects of lead increases with uptake (ATSDR, 2007). Thus, the first and second scenarios would predict different expected impacts of lead exposure on populations now living who were children from about 1930 to 1985), depending on whether (scenario one) uptake was already high and steadily declined or whether (scenario two) it showed a wave of increase and decrease corresponding to usage of leaded gasoline (e.g. compare Nevin, 2000 vs. McCall and Land, 2004).
In order to retrospectively distinguish between these scenarios, and in the absence of reliable PbB data before the 1970s, lead concentrations were determined in permanent tooth enamel as a measure of exposure and uptake. Teeth were obtained from mostly African-American adults who grew up in the Cleveland area and whose molars were formed from about 1936 to 1993. Core enamel in adult teeth preserves virtually unchanged the record of both childhood lead exposure and childhood ratio of lead isotopes throughout an individual's life (Gulson et al., 1997, Gulson and Gillings, 1997). Next, since continuous national measurements of atmospheric lead were unavailable until the mid-1970s (US EPA, 1986), the temporal changes in teeth enamel lead were compared to two different proxies of historic atmospheric exposure: lead in two dated Lake Erie core sediments, and national data on lead consumption in gasoline (US Bureau of Mine, 1941–1990, Nriagu, 1990), which is closely correlated with atmospheric lead (Figs. 5–7 in US EPA, 1986). In addition, since PbB is the most widely used metric to relate lead burden to toxic effects, a correlation was sought between lead in teeth and reported values of PbB during the phase-out of leaded gasoline, in order to estimate the peak PbB at the time of peak lead in teeth.
Finally, it was determined whether values and changes of 207Pb/206Pb isotope ratios of molar tooth enamel formed in the years 1936–1993 were consistent with those of atmospheric lead found in the dated Lake Erie sediment cores. Ratios of lead isotopes from different sources (e.g. paint, industrial, leaded gasoline) may have source-characteristic values depending on both the predominant mining or recycling sources at the time, and the relative abundance of such sources in the samples analyzed (Gulson et al., 1997, Gulson and Gillings, 1997).
In a similar vein, Farmer et al. (2006) correlated lead isotopic ratios in teeth sections and in sphagnum moss (as an indicator of atmospheric lead) in materials collected in Scotland over 100 years. However, as the authors pointed out, the temporal resolution was constrained by the limitations of teeth samples containing dentine, which integrates life-long rather than just childhood exposure to lead. They recommended use of core tooth enamel, as employed here. In addition, Scotland apparently experienced relatively much more pre-gasoline industrial lead atmospheric exposure than reported in the US (Farmer et al., 1996).
Section snippets
Tooth and donor characteristics
Mandibular and maxillary first and second molars, extracted strictly for reasons of dental necessity, were obtained with the cooperation of the Northeast Ohio Neighborhood Clinics and The Free Clinic of Greater Cleveland. Donor consent and information preserving anonymity were obtained according to a protocol reviewed and approved by the Case Western Reserve University Institutional Review Board. Tooth donors were 10 years of age or older, and grew up at least from ages 2 to 5 years (when the
Lead in tooth enamel and surrogates of atmospheric lead
Using date of birth and estimated age at half-maximal enamel formation in first and second molars, as well as smoothing techniques (see Methods), trends in tooth enamel lead concentration were plotted from 1936 to 1993 (Fig. 1). These data show a unimodal increase and later decrease in lead uptake over these years, as predicted in Scenario two (see Introduction). The peak smoothed value of tooth lead (4.94 μg/g) was about five-fold (and significantly) greater than the average value in the
Sources of variation in tooth data
Many factors probably increased the variation in the tooth data. As noted in Methods, the age at 50% first or second molar enamel formation varies between individuals by 2 years, and varies in different reports (Simpson and Kunos, 1998). However, a shift analysis showed that a deviation of 2–3 years in the assigned single “age” of 50% enamel formation would not have substantially changed the observed correlation between trends in lead concentration of teeth and that of Graney et al. (1995) lake
Acknowledgments
Funded by The Mary Ann Swetland Endowment, Case Western Reserve University. We thank G. Matisoff and C. Wilson for the 2002 Lake Erie sediment core. M. Ketterer acknowledges the support for the ICPMS instrumentation from the NSF MRI Program (CHE-0118604). J. Sun and Z. Zhang were supported in part by NSF grants from the Division of Mathematical Sciences. We are obliged to the dental clinics at the Free Clinic and Northeast Ohio Neighborhood Health Clinics for providing the opportunity to
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