Chaney, R.L., H.W. Mielke and S.B. Sterrett. 1989. Speciation, mobility, and bioavailability of Soil Lead. [Proc.
Intern. Conf. Lead in Soils: Issues and Guidelines. B.E. Davies & B.G. Wixson (eds.)]. Environ. Geochem. Health
11(Supplement):105-129.
Speciation, Mobility, and Bioavailability of Soil Lead
Rufus L. Chaney
USDA-Agricultural Research Service, Soil-Microbial Systems Laboratory, Building 318, BARC-West, Beltsville,
Maryland, 20705, USA.
Howard W. Mielke,
College of Pharmacy, Xavier University of Louisiana, New Orleans, Louisiana, 70125, USA.
and
Susan B. Sterrett
Eastern Shore Agricultural Experiment Station, Virginia Polytechnic Institute and State University, Painter, Virginia,
23420, USA
ABSTRACT
The contamination of urban soils by Pb is a persistent source of risk to children. Pb concentration increases as soil
particle size decreases, and smaller particles are more easily moved into homes to become Pb-rich housedust, and
onto hands where mouthing behaviour allows children to ingest soil particles. We have evaluated the roles that
chemical speciation of soil Pb and bioavailability of Pb in ingested soils play in risk of soil Pb to children. Nearly all
forms of Pb pollution [automotive PbClBr and PbSO4; mining PbS and PbCO3; paint PbCO3Pb(OH)2 and PbCrO4]
are transformed by soil chemical and microbiological processes into adsorbed soil Pb. Soils have a high capacity to
adsorb Pb on to surfaces of hydrous Fe oxide and organic matter. Typical soils can hold over 10,000 mg Pb/kg in
short term adsorption experiments, and larger amounts of Pb in longer studies. Crystalline PbSO 4 added to a moist
soil was quickly transformed to non-crystalline materials. A fundamental property of Pb adsorption by soils is the
increase in concentration of Pb in the equilibrium solution phase as soil Pb concentration increases. The adsorption
fits the common Langmiur adsorption isotherm.
Ingested soil enters the stomach and the adsorbed Pb is solubilized by the pH 1 environment. As the digesta enters
the small intestine, pH rises to 5-7 within a few cm. Here, soil can play an important role by adsorbing Pb and
reducing the solubility of Pb. Thus, because of the adsorption equilibrium process, higher soil Pb concentration
should strongly increase the bioavailability of soil Pb. Feeding studies with rats have confirmed this model.
Besides soil Pb concentration, another process may be important in Pb bioavailability. Feeding studies with human
volunteers have shown that Pb ingested by fasting humans has 50-80% absorption. When the Pb is ingested with
meals, only 2-10% of the Pb is retained. This "meal effect" reduces Pb absorption when food in consumed from
about 2 hours before the Pb dose to 3 hours after the dose; this time corresponds to gastric emptying time.
Increasing dietary Ca and P reduced retention of Pb by humans, possibly due to Pb coprecipitation with Ca
phosphates formed in the duodenum as the digesta pH rises. Although Fe status strongly affects Pb absorption by
many animal species, human studies indicated Fe had little affect. However, recent examination of longitudinal
childhood blood Pb studies show that blood Pb rises if serum Fe-binding capacity increases (indicative of low body
Fe supply in children). Taken together, these findings indicate that nutritional status of Fe, and the Ca and P levels
in meals affect absorption of Pb in that meal. Pb ingested in water or paint chips between meals is much more
bioavailable than when ingested with meals. However, soil Pb ingested between meals should not have the such
greatly increased bioavailability because, in contrast to water or paint chips, soil can adsorb Pb.
Larger particles of metallic Pb and paint Pb have been shown to have lower bioavailability, partly because larger
particles are not solubilized as readily as small particles during the short incubation in the stomach. Although
powdered PbS is essentially as available as Pb acetate to humans, some forms of mine wastes may be less
bioavailable because of the larger particle size. Research is needed to clarify the role of individual soil properties
1
(CaCO3, organic matter, and hydrous Fe oxide concentration) on the bioavailability of soil Pb, and to determine if
long term equilibration of Pb in soil allows formation of more stable chemical species of lower bioavailability. It is
possible that soils containing CaCO3 could reduce Pb bioavailability because of the higher Ca level, but most soils
have substantial adsorbed Ca.
Thus the effect of soil adsorbing Pb in the intestine must be considered in setting limits for maximum soil Pb in
areas where children live or play in order to protect children. Because the worst case child may have pica for soil,
the ultimate soil Pb limit will depend more on the bioavailability of soil Pb than on the amount of soil ingested.
INTRODUCTION
Over the last decade, we have conducted, reported, and reviewed research on potential risks of excessive soil Pb.
Our interest began with the increase in urban gardening and questions about the safety of consuming vegetables
grown in urban gardens (Chaney et al., 1984). In that work we examined the overall pattern of soil Pb concentration
in vegetable gardens in the metropolitan Baltimore, Maryland area (Mielke et al., 1983). Soils in urban areas have
become extensively polluted by Pb from automotive emissions, flaking paint and industrial emissions.
In 1986, Chaney and Mielke reviewed the sources of Pb and extent of Pb contamination of urban soils, and
analyzed the available data upon which maximum soil Pb limits for habitation by children could be based. These
previous papers are detailed reviews of complicated environmental contamination and risk analysis regarding soil
Pb.
The present paper considers several aspects of soil Pb risk in further detail. "What is the evidence for chemical
species of Pb in Pb-enriched soils and dusts, and do Pb species affect risk?" "What is the mobility of Pb in soil?"
And, most important, "How bioavailable is soil Pb to children who ingest soil inadvertently or by pica?"
Chemical speciation usually controls food chain transport and risk from heavy metals in the environment (Chaney,
1988). In simple water Pb toxicity to aquatic organisms, the chemical activity of Pb2+ ions appear to control toxicity
(e.g. Freedman et al., 1980). In the case of Pb-rich urban soils and dusts, chemical speciation, particle size, and
human nutritional factors appear to each be very important in Pb risk to children. Further, the ultimate question of
speciation is the chemical form of Pb in the duodenum when soil is included in the diet with meals or between
meals.
Pb Contamination Remains Near the Soil Surface
The major source of Pb in the environment is from its use as an antiknock additive to petrol (Nriagu and
Pacyna, 1988). Research has repeatedly shown that small Pb-rich particles reaching the surface of a soil
profile largely remain on or near the surface for a prolonged period (Chaney and Mielke, 1986). Good
evidence of this is shown in Jordan and Hogan (1975), Preer et al. (1984), Getz et al. (1977), and many
other publications. Humans often mix soils to aid growth of plants or lawns, and the Pb is mixed to tillage
depth. Individuals often cover old contaminated soil with new soil, or dilute it with soil amendments, sod,
or potting soil. Eventually, soil movement by earthworms, or through macropores, etc., allow mixing of
surface soil and Pb to deeper strata in the horizon. Human activities are the most important factor
affecting the Pb concentration at different soil depths.
Table 1. Effect of depth in soil and distance from a painted
wall on Pb concentration in "houseside" soil in Bowie, Maryland.
Three sides of the house (over 100 years old) were sampled.
Each sample represents a composite of 10 subsamples; samples
dried, sieved < 2 mm, and extracted with 1.0 N HNO3 according
to Chaney et al., (1984).
Distance
m
Depth
cm
A
Side of House
B
C
------mg Pb/kg dry soil-------2
0-1
0 - 5
5 - 10
10 - 15
1050
1060
940
44700
20600
7270
7330
4680
3300
5
0 - 5
5 - 10
10 - 15
431
404
400
110
2020
2110
298
366
286
10
0 - 5
5 - 10
10 - 15
194
162
248
1940
374
2175
730
686
452
A student (Ms. J. Gillespie) working with us characterized the effect of distance from a house, and depth
in the profile, on soil Pb concentration. Table 1 shows the results. This location had extreme surface soil
Pb enrichment, up to 4.5% Pb, mostly due to paint Pb released from the painted wooden structure.
Perhaps the most important aspect of mobility of soil Pb is its ability to be transported into homes and
become part of housedust. Chaney and Mielke (1986) reviewed the available data. It is clear from the
strong correlation of soil Pb concentration and housedust Pb concentration in several large surveys that
soil Pb contributes to housedust Pb (Thornton et al., 1985;
Jordan and Hogan, 1975). While higher concentrations of Pb are often found for housedust than in soil,
the exterior reservoir of Pb is much larger. Interior dust Pb covers surfaces while exterior soil Pb
accumulates to considerable depth as noted in Table 1.
After many years research on transport of automotive emission Pb to children, it became clear that much
of the transport occurred through ingestion of contaminated housedust rather than inhalation of
contaminated air. Respirable size particles quickly agglomerate into particles too large to reach
absorption sites in the lung. As with soil Pb, hand to mouth transfer of housedust allows ingestion of
persistent environmental Pb contamination.
Pb Concentration in Particle Size Fractions of Soil.
Soil usually has a larger average particle size than housedust or hand dust. The concentration of Pb in
soil and dust increases as particle size decreases (Duggan and Inskip, 1985; Duggan et al., 1985;
Fergusson and Ryan, 1984; Que Hee et al., 1985; Spittler and Feder, 1979). This is especially important
because research has shown that smaller dust particles are more easily transferred to the hands and tend
to remain on hands longer. Generally, particles remaining on hands are <50-100 microns in diameter.
Thus the higher concentration of Pb in smaller soil/dust particles increases the potential risk of soil Pb
(Duggan et al., 1985). As will be noted below, both smaller particle size and greater Pb concentration in
the smaller particles both increase the bioavailability of Pb in dust and soil, increasing the risk in yet
another way.
Chemical Species of Pb in Pb-Rich Soils.
Researchers have used several approaches to identify the chemical species of Pb in soils. This goal was
attempted because from many research areas indicated that availability depended on the chemical activity
of Pb2+ which in turn depended on the chemical species of Pb present in an environmental sample. The
form of Pb emitted by automobiles is the water soluble PbBrCl. Researchers found that this form of Pb is
rapidly transformed to PbSO4 in the atmosphere (Biggins and Harrison, 1979).
Four general approaches were taken to characterize the chemical species of Pb in soils, dusts, and street
dusts: 1) identify crystalline Pb compounds using X-ray diffraction; 2) determine which compound controls
the solubility of Pb in soil solution; 3) extract soils with different reagents and compare results with known
compounds added to soils; and 4) add compounds to soil and see if they persist or are transformed to
3
other chemical species.
Because Pb is held near the surface of soil, researchers looked for crystalline Pb compounds in the soil.
Olsen and Skogerboe (1975) used density and magnetic separation methods to concentrate the Pb
bearing particles of roadside soils. They found crystalline PbSO4 and PbCO3 in a calcareous soil, but
these accounted for < 5% of the soil Pb. This approach was used to characterize Pb in street dusts by
Harrison et al. (1981). They found PbSO4, Pb, Pb3O4, PbOPbSO4, and 2PbCO3Pb(OH)2 in nonmagnetic, high density, fine fraction of several street dusts. However, only 0.5 to 2.0% of the Pb existed
as a crystalline form susceptible to X-ray diffraction analysis.
Harrison et al. (1981) added 3000-4000 mg Pb/kg of PbSO4 to an uncontaminated soil and incubated the
mixture for a short period. They used sequential extractions with several reagents to characterize species
of Pb present, and found the extracts were very similar to normal Pb-rich soils rather than to PbSO4 mixed
with dry soil. These findings suggest that PbSO4 is quickly converted by soil chemical processes to other,
noncrystalline, species of Pb.
The equilibrium solubility approach has been used by several research groups. Santillan-Medrano and
Jurinak (1975) first tried this approach and concluded that Pb(OH)2, Pb3(PO4)2, Pb4O(PO4)2,
Pb5(PO4)3OH, and PbCO3 should control solubility depending on soil pH and phosphate status. Lindsay
(1979) summarized the solubility of Pb in soils compared to theoretical equilibrium solubility of many Pb
compounds as a function of soil pH, sulfide, chloride, phosphate, redox etc. Pb4+ cannot persist in soils
because it is reduced to Pb2+. Pb cannot persist (e.g. from Pb shot mixed in soil). PbSO4 is too soluble
to persist in soils, while PbCO3 was more soluble than Pb5(PO4)3Cl. Nriagu (1974) initially studied the
solubility of Pb phosphates, and found evidence to indicate that Pb5(PO4)3Cl should form in soils if
adequate phosphate is present, and is the least soluble compound identified. However, when GarciaMiragaya (1984) examined the solubility of Pb in "old" Pb-rich road-side soils, Pb was generally less
soluble than could be accounted for by these known crystalline compounds at equilibrium, but more
soluble than Pb5(PO4)3Cl. We believe there are two possible explanations for the inability to demonstrate
that Pb solubility is controlled by crystalline compounds: 1) Pb is present in the form of amorphous
compounds after only a few years to reach equilibrium; or 2) Pb is adsorbed to strong adsorption sites in
the soil and not present in inorganic compounds.
Adsorption of Pb by Soils.
Numerous studies have shown that large amounts of Pb can be adsorbed by soils. This adsorption fits
the Langmuir adsorption isotherm, in that as the amount of soil-adsorbed Pb increased, the Pb
concentration in the equilibrium solution phase increased. Two groups studies many soils and used
multiple linear regression to relate soil properties to the ability of soils to adsorb Pb (Hassett, 1974;
Zimdahl and Skogerboe, 1977). The latter authors simplified their multiple regression equation to pH and
CEC (which replaced clay and organic matter identified by stepwise regression). Table 2 shows the
results of these regressions, with a model calculation for a "typical" pH 7 soil containing 20 milliequivalents of cation exchange capacity (CEC). CEC is usually correlated with soil clay and organic
matter levels, and soil clays are usually covered with a layer of hydrous Fe oxide with strong Pb adsorption
ability.
Other researchers have examined adsorption or specific binding of Pb by soil components such as
organic matter, hydrous iron oxides, and even manganese oxides (Wolf et al., 1977; McKenzie, 1978;
Kinniburgh et al., 1976). In general, humic acids in soil can bind large amounts of Pb very strongly, and
the bound Pb is less susceptible to release by acidification than is Pb bound to mineral portions of the soil.
However, at the pH of the duodenum, pH 6-7, soil organic matter and Fe oxides can bind large quantities
of Pb.
Table 2. Adsorption of Pb by soils fits the Langmuir
adsorption isotherm. Best fit multiple linear regression
models calculated for "typical" soil of cation exchange
4
capacity (CEC) = 20 milli-equivalents/100 g and pH = 7.
Zimdahl and Skogerboe, 1977 (Pb(NO3)2:
Soil Pb Adsorption Maximum (μmol/g) =
= 2.81CEC (meq/100g) + 10.7pH - 49.3
=20
=7
= 56.2
+ 74.9
- 49.3
= 81.8 μmoles/g = 16900 mg Pb/kg
Hassett, (1974) (PbCl2):
Soil Pb Adsorption Maximum (μmol/g)
= 5.34CEC (meq/100g) + 5.36pH + 0.0774Pi - 34.3
=20
=7
=30
= 106.8
+ 37.5
+ 2.32
- 34.3
= 112.3 μmol/g = 23200 mg Pb/kg
Further, Pb absorption maxima from leaching were 1.6 times
greater than from batch studies.
Recent work by Harter (1979; 1982) has provided further data on soil properties related to adsorption of
Pb. Unfortunately, nearly all these studies suffered from an inherent error in the method used to measure
adsorption. Most researchers fail to correct soil pH of the soil + metal solution slurry for acidification which
results from the metal ion displacing protons bound by the soil. When soils bind 100 μmoles of Pb/g soil,
about 100 μmoles of protons are displaced, driving the soil pH down several units. Because significantly
more Pb is bound at higher pH than lower pH, the inherent lowering of soil pH during the adsorption
capacity test causes a false low estimate of adsorption capacity. One can correct the pH by titrating the
mixture with KOH, and then one finds many fold higher Pb adsorption at pH 6-7 than found when a soil
initially pH 6-7 is measured for adsorption capacity without pH correction (Harter, 1982). Thus, the very
high values noted in Table 2 significantly underestimate potential Pb adsorption capacity. Worse, the role
of soil properties (organic matter versus Fe-oxides) may be falsely evaluated because the equilibration
took place at pH 4 rather than at pH 6-7. In general, the evidence is very strong that adsorption of Pb by
soil accounts for the solubility of Pb in soil, the rapid solubilization of soil Pb upon acidification, and the
lack of crystalline Pb compounds in soils.
Adsorption is important in soil in the field in terms of leaching of Pb down the soil profile. However, this
process is also important in the small intestines of children who ingest Pb-rich soil. Although soil-bound
Pb is solubilized in the pH 1 monogastric stomach (Day et al., 1979), in need not remain soluble during
transit of the digesta through the intestines. As the pH rises in the duodenum, soil materials should readsorb Pb released by acidification in the stomach. This process should still follow the Langmiur
adsorption isotherm, and the relative bioavailability of soil Pb should increase with increasing soil Pb
concentration according to the adsorption model.
What Factors Should Influence Risk of Soil Pb?
Pb concentration in soil, size of soil particles rich in Pb, chemical species of Pb in soil, and nutritional
factors together interact with human behavioural factors in controlling risk from soil Pb. We have
reviewed the behavioural factors (Chaney and Mielke, 1986), and must note that children vary remarkably
in blood Pb (Pb-B) when exposed to similar Pb sources. Parental supervision, personal habits (mouthing
of fingers, hands, toys; chewing fingernails; washing hands), pica behaviour, and quality of nutrition vary
among children so greatly that some children can have little risk when they live or play in areas with high
soil Pb. However, we must consider the child described by Duggan and Inskip (1985), the average child
playing in a normal dirty way. Further, we support the view of the EPA that a proper regulatory evaluation
must consider the "most-exposed, most-susceptible individual." In the case of soil Pb risk analysis, this
individual is a poorly-supervised child who regularly plays in Pb-rich soil, has pica for soil, and has poor
nutrition. This child would ingest much soil Pb, and absorb a higher percentage of this Pb than the well
cared for child. Society must protect this child from excessive soil Pb in the urban environment.
5
Bioavailability of ingested Pb
When Pb in soil or dust is ingested by humans, the potential for adverse effects depends on absorption of
the ingested soil/dust borne Pb. Research on laboratory animals over many years has characterized the
effect of nutritional factors on Pb absorption (Mahaffey, 1982, 1985; Mahaffey and Michaelson, 1980).
More recently, adult human Pb isotope absorption studies and Pb balance studies in infants have clarified
understanding of human Pb absorption. In addition, several feeding studies using livestock and laboratory
animals have directly tested Pb absorption from dietary soil/dust.
Effect of Pb compound and particle size on Pb absorption
Research was conducted to evaluate the bioavailability of Pb in different compounds. Allcroft (1950)
reported feeding several compounds to cattle, and found effects of both Pb compound and particle size.
In particular, large particle PbS had lower toxicity and caused lower tissue levels of Pb than small particle
PbS or other compounds. Although these were long term feeding studies, cattle were studied. Ruminant
animals use the anaerobic rumen to process forages, and this anaerobic environment is usually rich in
sulfide. Further, the pH of the rumen is near neutral. PbS would not be expected to be dissolved under
these conditions. The pH of the stomach fluid in cattle is much higher than that of monogastric organisms
such as humans. Gastric fluid is normally pH 3.5-4.5 in cattle, while gastric fluid of humans is usually pH
1. Barltrop and Meek (1975, 1979) studied bioavailability of different Pb compounds and paint pigments
(of varied particle size) to rats. Their design used a 48 hour feeding period with very high Pb
concentrations. Although their results should provide a good indication of the bioavailability of these
compounds in an "acute" protocol, their method should not allow proper evaluation of the effect of dietary
constituents on the "chronic" bioavailability of the different Pb compounds. In their work, larger particles
had lower bioavailability than smaller particles of several materials. This would appear to result from
poorer dissolution of larger particles during the short period of acidic treatment in the stomach, and would
be relevant to materials with lower solubility. Compounds which are readily dissolved in weak acid were
highly bioavailable. Interestingly, human feeding studies of Rabinowitz et al. (1980) tested the absorption
of finely divided PbS to fasting human volunteers. In this test, PbS was highly bioavailable. More recently,
Healy et al. (1982) tested the solubility of different particle size preparations of PbS in gastric fluid. They
found the expected more rapid solubility of smaller particles. Their work was focused on bioavailability of
PbS from cosmetics (e.g. surma) which appear to be transferred to the mouth after hand contact (Healy et
al., 1982; Healy, 1984). The implication of these findings for soil Pb are that larger particle size PbS (e.g.
galena ore particles dispersed by mining, transport, or smelting) would be expected to have lower
bioavailability than other soil Pb. However, grinding of these particles by shoes in the home could produce
a fine particle PbS in housedust which would have high bioavailability.
Effect of nutritional factors on Pb absorption
Nutritional studies, mostly with rats, showed that deficiency of calcium (Ca) and iron (Fe) had very strong
effects on Pb absorption. When dietary Ca fell below about 50% of the dietary levels recommended by
the National Research Council (NRC) for growing rats, Pb absorption increased strongly (Mahaffey et al.,
1977). Not only was Pb absorption increased due to low dietary Ca, but the deposition of Pb in bone
decreased, allowing Pb to reach higher levels in soft tissues than is usually observed for similar bone Pb
levels. Many factors interact with Ca nutrition. A complex vitamin D interaction with Ca and Pb (Smith et
al., 1978) did not explain seasonal variation in Pb-B in children (Mahaffey and Michaelson, 1980).
Mahaffey (1982) has summarized these nutritional interactions in relation to known dietary limitations in
urban poor children and pregnant women, the largest groups who comprise the "most-susceptible"
individuals for excessive soil Pb.
Iron deficiency was also found to strongly affect Pb absorption in rats. Pb absorption declined with further
increase in dietary Fe above the minimum dietary requirement (Mahaffey et al., 1978). Not all
experiments came to this conclusion, although rat and chick feeding studies generally found low Fe status
6
increased Pb retention.
Independent research programs evaluated Pb absorption by adult humans. One of the most important
findings of this research was that Pb absorption is greatly reduced by simultaneous ingestion of food
(Blake et al., 1983; Flanagan et al., 1982; Heard et al., 1983; James et al., 1985; Chamberlain, 1987;
Rabinowitz et al., 1980) compared to Pb ingested during fasting. The effect of a meal on Pb absorption
lasted about 2-3 hours after eating because of slow gastric emptying after a meal (James et al., 1985).
This result has important implications for absorption of soil/dust Pb compared to water Pb or paint Pb
ingested between meals. Studies of which dietary components reduce Pb absorption identified minerals,
then Ca, phosphate (P), phytate (inositol hexaphosphate), and fibre (Blake et al., 1983; Blake and Mann,
1983; James et al., 1985). Combinations of Ca and P had more effect on Pb absorption than did Ca alone
(Blake and Mann, 1983; Heard et al., 1983). Pb isotopes were incorporated into lamb liver and kidney,
and into spinach to allow comparison of Pb intrinsic to a food with Pb isotope extrinsically added to a meal
with that food. This research showed that "food" Pb was absorbed equal to Pb salts added to an
equivalent meal (Heard et al., 1983). Pb in oysters was about 70% as bioavailable to Japanese quail as
Pb acetate added to the purified diet (Stone et al., 1981). James et al. (1985) evaluated a number of
meals and dietary components. Test meals components such as phytate or EDTA
(ethylenediaminetetraacetate) reduced Pb absorption compared to the effect of an equal amount of Ca
and P in a low phytate refined diet basal meal (James et al., 1985; Flanagan et al., 1982). On the other
hand, milk in a meal increased Pb absorption compared to the expected effect of an equivalent amount of
Ca and P in the milk (as was seen in animal studies by Zmudzki et al., 1984; Kello and Kostial, 1979).
Thus, phytate, fibre, and Ca in whole grain foods would tend to appreciably reduce Pb absorption
compared to more highly refined grain products.
Although Ca reduction of Pb absorption by humans has been independently corroborated, and generally
mimics results found in laboratory animals (Barltrop and Khoo, 1975; 1976), results from studies of the
effect of Fe deficiency on Pb absorption have been contradictory. The Watson et al. (1980) study reported
that individuals with low serum ferritin (indicating low body Fe reserves), who absorb an increased fraction
of dietary Fe, also absorbed increased amounts of carrier free Pb. However, a study by Flanagan et al.
(1982), using 203Pb with 200 μg carrier Pb, found no effect of Fe status (serum ferritin) or added dietary Fe
on Pb absorption by humans. This was a direct test of the previous report, but used an improved
experimental design. Under fasting conditions, one subject who regularly consumed Fe supplements
absorbed only 6% of dietary Fe, but absorbed 75% of dietary Pb. Interestingly, the researchers found no
effect of dose on absorption of Pb within the range 4 - 400 μg Pb/meal (Flanagan et al., 1982). The
contradictory results of these two studies are hard to explain, and the authors exchanged comments
(Watson and Hume, 1983; Flanagan et al., 1983). It must be considered that the detailed experimental
design, the proven methodologies, and numbers of subjects in the Flanagan et al. (1982) study strongly
support their interpretation of the data.
Another aspect of diet effect on Pb absorption was corroborated independently: Addition of EDTA to a
test diet reduced absorption (Flanagan et al., 1982; James et al., 1985) Chelation of an element can
reduce both its chemical activity and its absorption. The role of phytate (James et al., 1985; Wise, 1981),
and some tannin and fibre components (Peaslee and Einhellig, 1977; Paskins-Hurlburt et al., 1977) should
be similar to EDTA, so that by chelating or adsorbing Pb in the small intestine (pH > 6), intestinal Pb
absorption is reduced. Soil and dust should act like fibre in this regard, by adsorbing Pb, and reducing
soil Pb bioavailability.
Nutritional interactions usually depend on molar ratios of ions in the lumen of the intestine. Because
typical dietary Pb may be only 20 μg/day for children now, and < 100 μg/d for adults, testing 200 μg Pb in a
single test meal now seems somewhat high for food Pb research. Nevertheless, higher levels may be
required to test for interactions relevant to pica levels of ingestion of Pb-rich soils.
Pb balance studies were conducted in babies fed experimental formula diets which differed in Pb
concentration because of soldered cans used for some formulas and juice products at that time (Ryu et
al., 1983; 1985; Ziegler et al., 1978). The very young infants received milk as the bulk of their diets, and
41% of dietary Pb was absorbed when intake exceeded 5 μg Pb/kg body weight/day. Increased dietary
Ca significantly reduced Pb retention in these babies (Ziegler et al., 1978). In a second study (Ryu et al.,
7
1983; 1985), infants ingesting milk from paper cartons got 16 μg Pb/day, while infants ingesting canned
milk or formula products ingested 61 μg/day. Blood Pb levels were significantly different, 7.2 versus 14.4
μg/dL. These infants absorbed a much higher portion of milk Pb than do adults, confirming the effect of
age on Pb absorption that was found in laboratory animal studies (Mahaffey and Michaelson, 1980).
As with Ca, P also reduces Pb absorption by animals (Quarterman and Morrison, 1975; Barton et al.,
1978), but P is seldom deficient in human diets. As noted by Mahaffey (1982), "... Western-type diets are
usually quite high in phosphorus so that no special attention is required to maintain an adequate intake of
this nutrient."
Coprecipitation of Pb with Ca-phosphates
The above discussion of the importance of Ca and P concentration in test human diets on Pb absorption
raises the question "How do Ca and P interfere with Pb absorption?" There are several possible
mechanisms. One is simple interaction of Ca and Pb at the intestinal Pb absorption site. This mechanism
would not explain why P is shown to be significant in humans. Another possible mechanism is the role of
deficient levels of Ca on Ca-binding protein in the intestine (the level of this protein also depends on the
1,25-dihydroxy-cholecalciferol, the active form of vitamin D in serum). Although increased dietary vitamin
D does increase Ca and Pb absorption by the intestine (Smith et al., 1978), the diet must be low in Ca for
some period before the body increases synthesis of active Vitamin D. Thus, a high Ca level in a single
meal should not be able to affect Pb absorption through the Ca-binding-protein.
The most likely mechanism for the effect of Ca and P on Pb absorption appears to be co-precipitation with
Ca-phosphates formed during the digestion process. Evidence for the importance of this mechanism
comes from research to explain the difference in bioavailability of Zn from human milk compared to bovine
milk. That question arose because human milk, but not bovine milk, could correct a Zn deficiency disease
of humans. Until Zn deficiency was shown to be the cause of "acrodermatitis enteropathica" (Moynahan,
1974; Neldner and Hambridge, 1975), human milk was used to correct the disease (see reviews by
Chaney, 1988; Hurley and Lonnerdal, 1982; Lonnerdal et al., 1984). Several theories were examined,
including 1) a role for citrate forming a highly bioavailable low molecular weight chelate with Zn in human
milk but not cow's milk (Lonnerdal, et al., 1980; Martin et al., 1981), and 2) binding of Zn by casein in
cow's milk but not in human milk (Cousins and Smith, 1980; Blakeborough et al., 1983). In the end, these
carefully examined possibilities could not explain the difference in Zn bioavailability.
Other researchers examined what happened to Zn during the digestion process. When the digesta enter
the stomach of monogastrics, the solution pH is lowered to near pH 1. At this pH, many proteins are
denatured (casein forms curds at pH < 4.5), and Zn is displaced from the protein by protons in a simple
competition for binding by the ligand sites on the protein. During the next step in digestion, the digesta
enter the small intestine where bicarbonate is pumped into the lumen to raise the pH. While the digesta
move a few cm into the duodenum, the pH is raised to eventually reach near 7. If Ca and PO4 are high
enough in the solution phase of the digesta, a precipitate forms as the pH rises. Nelson et al. (1985) first
studied model systems and found that Ca-phosphate quickly (within minutes) formed when Ca and PO4
were present at levels common in whey, the solution remaining after curds form in acidified cow's milk.
Further study showed that Zn coprecipitated with the Ca-phosphates above pH 5.0 as the pH increased
and coprecipitation was complete by pH 6.0 (Nelson et al., 1986; 1987). In total, their data are very
convincing as an explanation of the difference in Zn availability from human versus bovine milk (Nelson et
al., 1987).
We believe this is very likely the model for the effect of dietary Ca and P on Pb absorption. The clear
interaction of dietary Ca and P concentrations in animal and human studies of Pb absorption fit a solubility
product model. Pb coprecipitation with Ca-phosphate should be complete at even lower pH than found for
Zn. This hypothesis can be readily tested by a combination of in vitro and animal studies. The bulk of
animal research findings clearly support this model (Mahaffey, 1985).
Bioavailability of Pb in ingested soil and dust
8
Wildlife are unable to avoid exposure to and absorption of soil/dust Pb in their habitat (Elfving et al., 1978;
Hutton and Goodman, 1980; Ireland, 1977; Scanlon et al., 1983; Young et al., 1986). These studies
indicated appreciable bioavailability of soil/dust Pb, but did not make specific comparison with Pb added to
control diets. Similarly, livestock grazing pastures on soils rich in Pb (mine wastes, naturally Pb-rich soils)
had increased Pb levels in body tissues showing soil Pb had at least some bioavailability (Allcroft, 1950;
Egan and O'Cuill, 1970; Harbourne et al., 1968; Wardrope and Graham, 1982).
Several studies were conducted to test the bioavailability of soil/dust Pb. Stara et al. (1973) reported
studies of rats fed tunnel, highway, or smelter dusts. Accumulation of Pb in bone or kidney was non-linear
with dose (Table 3), with lower %-absorption as dose increased. Bone lead tended to approach a plateau
as the amount of soil Pb in the diet increased. Another way to view these results is that the highest %absorption of soil Pb occurred at the lowest soil ingestion level. Table 4 shows results from their
comparison of the absorption of Pb by rats fed different dust sources. El Paso smelter dust (0.67% Pb)
had appreciably lower effect on blood Pb than Queens tunnel dust (2.22% Pb) or Los Angeles freeway
dust (1.04% Pb) when the rats were fed 1 mg Pb/d as dust in gelatin capsules, equivalent to about 100 mg
Pb/kg diet. Bone and kidney Pb were also lower for the lower Pb concentration smelter dust than for the
tunnel or freeway dusts. These tests did not compare absorption from dusts with Pb acetate. They did
use a purified diet rather than a lab chow diet which favored Pb absorption.
Table 3. Effect of the daily dose of ingested dust Pb on
Pb in tissues of rats fed Queens, NY tunnel dust (sieved)
mixed in purified diet for 42 days before analysis of
tissues. Dust contained 22 g Pb/kg (Stara et al., 1973).
Daily
Dose
Blood
Peak Pb
mg Pb/d
μg/dL
0.0
0.5
1.0
5.5
11
33
39
51
Femur
Tissue Pb
Kidney
Liver
Brain
------- μg Pb/g tissue -------0.75
25.7
33.6
66.1
2.5
3.2
9.4
0.13
0.56
0.52
1.3
0.032
0.030
0.055
0.28
Table 4. Effect of dust source and Pb concentration on Pb in
tissues of rats fed dust supplying 1 mg Pb/day for 36 days.
(Stara et al., 1973).
Dust Source
Dust-Pb
mg/g
Control
NY Tunnel
22.2
LA Freeway
19.4
El Paso Smelter 6.7
Blood
Peak-Pb
μg/dL
12
45
39
32
Tissue Pb
Kidney
Liver
Femur
Brain
------- μg Pb/g tissue ------0.75
33.6
32.5
23.6
3.2
2.7
2.5
0.13
0.52
0.32
0.36
0.032
0.055
0.094
0.035
Dacre and TerHaar (1977) conducted an evaluation of the bioavailability of Pb in houseside soil (990 mg
Pb/kg) and roadside soil (2300 mg Pb/kg) compared to Pb acetate. Equal Pb concentrations were added
to diet from the three sources, 50 mg Pb/kg diet. A high fibre, high nutrient rat chow was used as the
basal diet. Much lower blood-Pb and bone-Pb levels were reached in their experiment than seen by Stara
et al. (1973) (Table 5). Bone and kidney concentrations after 90 days feeding showed that soil Pb had
significantly lower effect than Pb acetate. Bone results indicated that soil
9
Pb was about 70% as bioavailable as Pb acetate.
10
Table 5. Bioavailability of soil Pb compared to Pb acetate fed to
rats at 50 mg Pb/kg diet for 30 or 90 days mixed in a laboratory
chow diet (Dacre and TerHaar, 1977). Roadside soil fed at 2.15%
of diet; houseside soil fed at 5.0% of diet.
Diet
Soil Pb
Concn.
mg/kg
Control
Roadside
Houseside
Pb acetate
2300
990
-
Measured
Diet Pb
mg/kg
0.6
56.0
51.8
49.1
Bone Pb, mg/kg
Kidney Pb
@ 30 days @ 90 days @ 90 days
------------mg Pb/kg---------1.71
5.93
5.20
5.21
a
b
b
b
1.27
4.48
4.98
6.28
a
b
b
c
0.25
0.77
0.76
0.96
a
b
b
c
Means in a column followed by the same letter are not significantly
different.
Chaney et al. (1984) reported data from a more detailed evaluation of the effect of soil on dietary Pb
absorption (Table 6). This research was conducted in collaboration with Drs. S. Welsh and O.A. Levander
at Beltsville, Maryland. Rats were fed purified complete casein-sucrose diets with and without 5%
uncontaminated soil, and with and without 50 mg Pb (as Pb acetate)/kg diet to test the effect of dietary soil
on Pb absorption (50 mg Pb/kg diet and 50 g soil/kg diet = 1000 mg Pb/kg "soil" during test). Rats were
also fed five Baltimore urban garden soils to compare bioavailability of real Pb-rich urban soils with that of
Pb acetate. All Pb was added at 50 mg Pb/kg dry diet (unequal soil amounts). The results are shown in
Table 6. Bone Pb concentrations were used to evaluate diet Pb bioavailability (kidney-Pb, liver-Pb, and
blood-Pb were also determined and showed the expected close relationship to bone-Pb among
treatments. The addition of 5% uncontaminated soil to the diet reduced Pb acetate control to 53% of Pb
acetate alone. Four soils with about 1000 mg Pb/kg yielded bone Pb about 24% (15-44) of Pb acetate,
while a garden soil with 10240 mg Pb/kg yielded bone Pb 70% of the Pb acetate control. Pb in real soils
was appreciably less bioavailable than was Pb freshly mixed with soil. The general trend showed
increased soil Pb bioavailability at higher soil Pb concentration (when soil Pb concentrations were higher,
percent soil in the diet was correspondingly lower). We believe this would be expected because soil acts
like a fibre and a Ca and P source in the diet. These properties should allow soil to adsorb Pb in the
lumen of the intestine and reduce net Pb absorption.
Our use of purified diets (Chaney et al., 1984) yielded much greater Pb absorption from dietary soil than
that found by Dacre and TerHaar (1977). The experimental protocols were similar, and dietary Pb was fed
at the same level. Pb in tibia ash reached 247 mg Pb/kg in rats fed 50 mg Pb (Pb acetate)/kg purified
diet, but femur Pb reached only 5-7 mg Pb/kg in rats fed the same level of Pb in a lab chow diet (Dacre
and TerHaar, 1977). Mahaffey and Michaelson (1980) discussed this phenomenon, and stated it resulted
from the much higher levels of Ca, Fe, and fibre in chow diets compared to "NRC" purified complete diets.
A similar effect of diet was observed by Mylroie et al. (1978) in a direct comparison of diet type on the
absorption of paint Pb. (Table 7) Much higher bone and kidney Pb were reached using the purified
complete rat diet normally recommended for toxicology studies. In many ways, these purified diets are
similar to US diets because of low fibre and mineral levels (Mahaffey, 1985).
Research on risk from Pb in ingested sewage sludge provides other data relevant to the question of
bioavailability of urban soil Pb. Sewage sludge has been added to usual, or practical, diets of livestock
(comprised of normal fibrous feed ingredients fed in commercial production practices) to evaluate food
chain transfer (bioavailability) of Pb and other potentially toxic materials in the sludges. Substantial
percentages of sludge in diets were used to simulate poor livestock management (worst case) situations
in which cattle ingest up to 14% soil (Fries et al., 1982). Sludges used in these studies contained varied
levels of Pb and other elements such as Fe and Ca known to interact with Pb. Studies reported by
Kienholz et al. (1979) and Johnson et al. (1981) in which cattle ingested sludge with 780 (Table 8) or 466
mg Pb/kg, respectively, found increased bone, liver, and kidney Pb. Response was curvilinear, with the
slope of increase in tissue Pb decreasing at higher sludge dose. In other studies, cattle grazing pastures
amended with sludges or sludge compost containing lower amounts of Pb (380 mg/kg) had no significant
11
change in bone or liver Pb concentration (Decker et al., 1980). Cattle fed sludge compost containing 215
mg Pb/kg had little change in bone Pb (Table 9).
Table 6. Effect of soil on bioavailability of Pb to rats, and
bioavailability of Pb in urban garden soils.
Treatment1
PbOAc Soil
-
113
+
+
113
-
7061
995
1080
1260
10240
Pb in Tibia
mg/kg tibia ash
mean + std. err.
0.3
0.0
Pb absorption
compared to that
of Pb acetate, %
±
±
0.3
e2
e
-
247.
130.
±
±
10.1
29.5
a
bc
100
53
40.0
108.
37.1
53.6
173.
±
±
±
±
±
6.1
26.3
7.3
7.4
21.8
de
c
de
d
b
16
44
15
22
70
1A
purified casein-based complete diet was fed to Fisher rats for 30 days. Pb acetate
and garden soils were added to supply 50 mg Pb/kg dry diet. The experimental
garden soils comprised 7.08, 5.02, 4.64, 3.95, and 0.488 % of the dry diet, respectively;
control soil was fed at 5% of diet.
2Means followed by the same letter are not significantly different (P < 0.05) according to
Duncan's Multiple Range Test.
3Unpolluted farm soil near Beltsville, MD, (Chillum silt loam, 11 mg Pb/kg), similar
to original soil in the urban gardens used in this experiment.
Table 7. Effect of lab chow versus purified diet on absorption of
Pb from paint chips fed at 1% of diet for 35 days. Paint
contained 10% Pb as Pb-octoate; diet contained 1000 mg Pb/kg
(Mylroire et al., 1978).
Diet Type
Pb-Blood
μg/dL
Lab Chow
Casein-sucrose
Significance
Pb-Femur
Pb-Liver
Pb-Kidney
-------- μg/g wet weight --------
<10
140
97
400
**
**
0.24
2.7
**
12
5.6
300.
**
Table 8. Effect of percentage of sewage sludge in diet on Pb
residues in tissues of cattle which consumed the test diets for
180 days (Kienholz et al., 1979). The digested sludge was from
Denver, Colorado, and contained 780 mg Pb/kg.
Sludge
in Diet
%
Diet
Pb
Kidney
Pb in tissues
Liver
Bone
---------------mg Pb/kg dry wt.----------------
0
4
12
0.5
29.0
80.0
0.9 a
12.2 b
15.8 c
0.2 a
3.3 b
4.6 c
0.8 a
3.7 b
11.0 c
Within a column, means followed by the same letter are not significantly
different at the 5% level.
Table 9. Effect of percentage of sewage sludge compost in diet
on Pb residues in tissues of cattle which consumed the test diet
for 180 days (Decker et al., 1980). The compost contained 215
mg Pb/kg, and high levels of Fe and Ca.
Dietary
Compost
%
0.
3.3
10.0
Diet
Feces
Pb concentration
Duodenum
Liver
Kidney
Femur
------------------mg Pb/kg dry weight----------------6.0
11.2
19.9
14.7
23.8
46.7
2.81 a
3.18 a
4.21 a
2.36 b
2.48 b
8.44 a
3.96ab
5.26 a
2.92 b
3.70 a
4.74 a
3.37 a
Within a column, means followed by the same letter are not significantly
different at the 5% level.
13
Many scientists have considered the bioavailability of Pb in ingested soil and dust (Chaney et al., 1984;
Day et al., 1979; Duggan and Inskip, 1985; Fergusson, 1986; Gibson and Farmer, 1984; Harrison et al.,
1981; Thornton, 1986). Some have conducted chemical extractions to simulate conditions of the
stomach, and found soil Pb was very soluble (Chaney et al., 1984; Day et al., 1979; Duggan and Inskip,
1985; Fergusson, 1986; Harrison et al., 1981). Although some argue that solubility means availability, the
above research shows that soil components may adsorb Pb at the pH of the intestine and thereby reduce
Pb absorption. This effect would cause increased Pb absorption at higher soil/dust Pb concentration at
any particular Pb dose. Further, the above research showed that a decreasing response slope results
when increasing amounts of a soil are fed. These responses are different characteristics of the
bioavailability of soil Pb in the diet. In contrast one human isotope feeding study evaluated doseresponse; they compared absorption of 4, 40, and 400 µg Pb fed to a fasting individual, and found no
effect of dose (i.e. a linear dose effect on absorption) (Flanagan et al., 1982). Other studies of children
ingesting Pb-rich water contaminated by soft water and Pb water pipes, found that blood Pb increased
with the logarithm or the cube root of daily Pb intake. This is also a decreasing slope of response with
increasing dose (Sherlock et al., 1984; 1985). Whether this effect can be explained by the food versus
fasting effect on Pb absorption is unclear. More research is needed to characterize soil/dust Pb
bioavailability. The infants of animal species close to humans should be studied using Pb isotopes.
Deliberate soil Pb absorption studies with human infants are unethical whether radioactive or stable Pb
isotopes are used.
Bioavailability of Soil Pb should be considered in setting limits for Pb levels in soils for areas
where children live and play.
In 1984, Chaney, Sterrett, and Mielke considered the relationship of soil ingestion rate and soil Pb
concentration on daily Pb ingestion. Figure 1 shows a model of this relationship with logarithmic axes to
aid interpretation. At that time the daily Pb ingestion of children was thought to be 100 μg, and inadvertent
ingestion of 100 mg (due to mouthing behaviour) of a typical urban soil with 1000 mg Pb/kg caused one to
ingest as much soil Pb as food Pb. In the inner city, and beside old painted houses, most soils exceed
1000 mg Pb/kg, and daily ingested soil Pb could reach mg/d. Although this model displays the importance
of behaviour (mouthing activity or pica) and parental care in limiting soil/dust ingestion, we cannot easily
show the effect of soil Pb concentration on soil Pb bioavailability on this figure.
Figure 2 compares a linear response model for bioavailability of soil Pb versus soil Pb concentration with
the non-linear (increasing slope) model presented above. In the critical range below 1000 mg Pb/kg,
adsorption on soil could have a very large effect of risk of soil Pb.
Chaney and Mielke (1986) discussed in detail the sources of information on the relationship of soil Pb
concentration to blood Pb of children exposed to several environmental sources of Pb. In the end, they
supported the statement of CDC that "In general, lead in soil and dust appears to be responsible for blood
(lead) levels in children increasing above background levels when the concentration in the soil or dust
exceeds 500-1000 ppm." This refers to the surface 1 cm of soil (V. Houk, Center for Disease Control,
Atlanta, Georgia: personal communication). The Center for Disease Control (1985) advice specifically
notes "In severely contaminated residential areas, unless an effective barrier can be established between
the children and soil, surface soil must be removed and replaced with soil having a low lead content."
CDC advises that remediation of excessive soil Pb should follow source control for air or paint Pb
pollution. The best action is removal of Pb-rich soil and replacement, or relocation of populations.
However, this consensus was reached at a time when the acceptable Pb-B was still 30 μg/dL, two or more
times higher than current acceptable safe levels. Presently, lower limits will be needed on soil Pb if
children are to attain the current desired blood Pb levels. Perhaps the most conservative view has been
that of Patterson (1980) who concluded that urban areas are so Pb polluted that they will need to be
abandoned to protect the health of US children. The CDC concurs with this idea when they state that
"...where concentration of Pb in soil and dust are high, large-scale excavation of soil or relocation of
populations is the ideal means of reducing the exposure of children to lead."
After considering the blood Pb:soil Pb relationship for many studies, Chaney and Mielke (1986) concluded
that "Soils with 500 mg Pb/kg contribute to increased Pb-B in children, but seldom cause Pb-B to exceed
14
25 µg/dL in the absence of pica. Soil/dust Pb especially contributes to the Pb exposure of the urban
disadvantaged child who is the most susceptible, most exposed individual for Pb. If a < 15 μg Pb/dL Pb-B
standard is to be attained for all children, special care would be required to reduce inadvertent soil/dust
ingestion even at 500 mg Pb/kg. Such special care is not available in the homes of many urban children.
Further, children with pica are not protected by a 500 mg Pb/kg soil limit." We note that 5-10% of children
exhibit pica at some time during childhood, and that recent efforts to measure soil ingestion by children
has found individuals who consume 10 g soil/day (Binder et al., 1986; Clausing et al., 1987).
Because Pb in soil and dust contributes to a health hazard for children, it is essential that a soil Pb
standard be established for child-accessible areas in order to begin dealing with this problem (Chaney et
al., 1984; Duggan and Inskip, 1985). Citizens need a soil Pb standard to make it possible to limit Pb
sources and to reduce soil Pb levels in the urban environment. A standard sets in motion societal
mechanisms which should make it possible to prevent Pb disease and protect children from this obvious
Figure 1. Model for the interaction of daily soil ingestion rate and soil Pb concentration on daily soil Pb
ingestion rate.
environmental hazard both now and in the future. The fundamental question is "What limit on soil Pb will
prevent excessive Pb absorption in exposed children?"
If we were preparing a new regulation for addition of Pb to unpolluted soils as a pesticide or as a
component of sewage sludge or fertilizer, the evaluation would be straight forward. The "worst case"
would be identified, and the regulation would have to protect the most-exposed, most-susceptible
population. As noted above, children's behaviour and socioeconomic status are very important factors in
estimating the effects of soil/dust Pb ingestion. Thus, in the soil/dust Pb case, the "most-exposed, most
susceptible" population would be disadvantaged urban children with pica for soil/dust. The regulation
would require soil/dust Pb concentration to be limited to such a level that the most susceptible child with
pica for soil could not exceed acceptable blood Pb levels. Any regulation would have to take into
consideration the background level of Pb consumption and background blood Pb levels for the mostexposed most-susceptible children, and the bioavailability of Pb in soil/dust.
As described in the introduction, the mean Pb-B of children 0.5 to 5-years-old in 1976-1980 was greater
than 15 μg Pb/dL, the level currently believed to be at or above the threshold for adverse effects of
ingested Pb on neurologic development of children. Hence, there is room for no more environmental Pb,
and present urban Pb pollution must be abated to correct existing adverse effects.
15
Figure 2. Model
for response of
bioavailable soil
Pb to total soil Pb
concentration. In each A and B, upper line is for 100% bioavailability of soil Pb compared to Pb acetate. Open
circles are garden soils shown in Table 6; filled circle is for control soil plus Pb acetate. Lower line is fit to soil
feeding trial data including the control soil. 2A shows log bioavailable soil Pb versus log total soil Pb; 2B shows %bioavailable soil Pb (linear) versus log total soil Pb. These data indicate that Pb adsorption by soil reduces soil Pb
bioavailability more at lower soil Pb concentration. Many more soils must be tested before data may be used reliably
for prediction.
The study of excessive Pb-B in children in Port Pirie, Australia offers new and important data on what soil Pb
level may be too high. A study was undertaken because possible Pb health effects on fetal development were
noted in a city with long term and extensive Pb pollution from a primary Pb smelter. This was a prospective,
longitudinal study, in which children were sampled repeatedly from birth to age 7. Thus, peak levels of Pb-B
were observed for each child, taking into account age and season dependent processes and behaviours. This
avoids limitations of the cross-sectional one-time sample where peak Pb-B levels are seldom observed for
individual children. In this study, Pb-B was significantly raised (Baghurst et al., 1985; McMichael et al., 1985,
1988; Vimpani et al., 1985) when soil Pb was in the range of 150 - 500 mg Pb/kg, for a 0 - 10 cm soil depth
sample (Cartwright et al., 1976; Merry et al., 1981; Tiller et al., 1976). Further, the EDTA extraction method
used by Tiller and co-workers to analyze soil Pb extracted about 85% of the total Pb. As noted by Farrell (1988)
at this conference, the pattern of slag utilization as fill confounded the pattern of soil Pb concentration with
distance from the smelter within Port Pirie. Thus, the maps of soil Pb used by Vimpani, McMichael, et al. to
estimate soil Pb zone for the children in the longitudinal blood Pb study were not appropriate for this use
(Vimpani et al., 1986). A separate cross-sectional survey of children's Pb-B was made after the severity of the
problem was demonstrated. Soil from the child's home was confirmed as a highly significant factor in Pb-B
variation, as were bare soil percentage of lot, fingernail biting, dirty clothes and hands at school, mouthing
behaviour, and housedust Pb concentration (Wilson et al., 1986). Further planned examination of the test
children at age 4 was found to show a highly significant impairment in cognitive development (reduction in I.Q.)
related to blood Pb concentration, further supporting the need to reduce soil and dust Pb exposure of children
(McMichael et al., 1988).
Other research offers strong evidence that soil/dust Pb contributes to Pb-B well below average levels of 500 mg
Pb/kg. These include studies by Angle et al. (1979), Bornschein et al. (1986), Brunekreef et al. (1981), Cohen et
al. (1973), and Vimpani et al. (1986). Further, research results from the "middle class" prospective blood Pb
study in Boston show a strong relationship of hand Pb and soil/dust Pb with Pb-B in infants with relatively low
Pb-B levels (Rabinowitz et al., 1985). We interpret these data that soil must be  150 mg Pb/kg in order to
prevent excessive Pb absorption in children.
16
ACKNOWLEDGEMENT
We gratefully acknowledge support from the Saint Paul Foundation, the Center for Urban and Regional Affairs of
the University of Minnesota, and the City of Saint Paul for the Studies of Pb levels in Saint Paul neighborhoods.
Pat Reagen and others of The Lead Coalition encouraged us, provided references and advice. We were able to
conduct our studies because we had the assistance of M.M. Leech, C.H. Gifford, P.T. Hundemann, and
Baltimore Urban Gardening staff. We acknowledge discussions with J.R. Preer, R. Bornschein, B.E. Davies, R.
Elias, I. Thornton, B. Beck, and many others who shared their understandings of the data and issues related to
soil Pb risk.
LITERATURE CITED
Allcroft, R. 1950. Lead as a nutritional hazard to farm livestock. IV. Distribution of lead in the tissues of bovines after ingestion of various lead compounds. J.
Comp. Path. 60:190-208.
Angle, C.R., and McIntire, M.S. 1982. Children, the barometer of environmental lead. Adv. Pediatr. 29:2-31.
Baghurst, P., Oldfield, R., Wigg, N., McMichael, A., Robertson, E. and Vimpani, G. 1985. Some characteristics and correlates of blood lead in early childhood:
Preliminary results from the Port Pirie study. Environ. Res. 38:24-30.
Barltrop, D. and Khoo, H.E. 1975. The influence of nutritional factors on lead absorption. Postgrad. Med. J. 51:795-800.
Barltrop, D. and Khoo, H.E. 1976. The influence of dietary minerals and fat on the absorption of lead. Sci. Total Environ. 6:265-273.
Barltrop, D. and Meek, F. 1975. Absorption of different lead compounds. Postgrad. Med. J. 51:805-809.
Barltrop, D. and Meek, F. 1979. Effect of particle size on lead absorption from the gut. Arch. Environ. Health 34:280-285.
Barton, J.C., Conrad, M.E., Harrison, L. and Nuby, S. 1978. Effects of calcium on the absorption and retention of lead. J. Lab. Clin Med. 91:367-376.
Biggins, P.D.E., and Harrison, R.M. 1979. Atmospheric chemistry of automotive lead. Environ. Sci. Technol. 13:558-565.
Biggins, P.D.E., and Harrison, R.M. 1980. Chemical speciation of lead compounds in street dusts. Environ. Sci. Technol. 14:336-339.
Binder, S., Sokal, D. and Maughan, D. 1986. Estimating soil ingestion: The use of tracer elements in estimating the amount of soil ingested by young children.
Arch. Environ. Health 41:341-345.
Blake, K.C.H., Barbezat, G.O. and Mann, M. 1983. Effect of dietary constituents on the gastrointestinal absorption of 203Pb in man. Environ. Res. 30:182-187.
Blake, K.C.H., and Mann, M. 1983. Effect of calcium and phosphorus on the gastrointestinal absorption of 203Pb in man. Environ. Res. 30:188-194.
Blakeborough, P., Salter, D.N. and Gurr, M.I. 1983. Zinc binding in cow's milk and human milk. Biochem J. 209:505-512.
Bornschein, R.L., Succop, P.A., Krafft, K.M., Clark, C.S., Peace, B. and Hammond, P.B. 1986. Exterior surface dust lead, interior house dust lead, and
childhood lead exposure in an urban environment. Trace Subst. Environ. Health 20:322-332.
Brunekreef, B., Veenstra, S.J., Biersteker, W. and Boley, J.S.M. 1981. The Arnhem lead study. I. Lead uptake by 1 to 3-year-old children living in the vicinity of
a secondary lead smelter at Arnhem, The Netherlands. Environ. Res. 25:441-448.
Cartwright, B., Merry, R.H. and Tiller, K.G. 1976. Heavy metal contamination of soils around a lead smelter at Port Pirie, South Australia. Aust. J. Soil Res.
15:69-81.
Centers for Disease Control. 1985. Preventing lead poisoning in young children: A statement by the Centers for Disease Control -- January 1985. US-DHHS
No. 99-2230. 35 pp.
Chamberlain, A.C. 1987. Tracer experiments with lead isotopes. pp. 179-188. In Thornton, I. and Culbard, E. (eds.) Lead in the Home Environment: Sources,
Transfer and Exposure Assessment. Science Reviews Ltd., Northwood, England.
Chaney, R.L. 1988. Metal speciation and interaction among elements affect trace element transfer in agricultural and environmental food-chains. pp. 219-260.
In Kramer, J.R. and Allen, H.E. (eds.) Metal Speciation: Theory, Analysis, and Application. Lewis Publishers, Chelsea, MI.
Chaney, R.L. and Mielke, H.W. 1986. Standards for soil lead limitations in the United States. Trace Subst. Environ. Health 20:355-377.
Chaney, R.L., Sterrett, S.B. and Mielke, H.W. 1984. The potential for heavy metal exposure from urban gardens and soils. pp. 37-84. In J.R. Preer
(ed.). Proc. Symp. Heavy Metals in Urban Gardens. Agric. Exp. Sta., Univ. Dist. Columbia., Washington.
Clausing, P., Brunekreef, B. and van Wijnen, J.H. 1987. A method for estimating soil ingestion by children. Int. Arch. Occup. Environ. Health 59:73-82.
Cohen, C.J., Bowers, G.N. and Lepow, M.L. 1973. Epidemiology of lead poisoning. A comparison between urban and rural children. J. Amer. Med. Assoc.
226:1430-1433.
Cousins, R.J., and Smith, K.T. 1980. Zinc-binding properties of bovine and human milk in vitro: Influence of changes in zinc content. Am. J. Clin. Nutr. 33:1083-
17
1087.
Dacre, J.C., and TerHaar, G.L. 1977. Lead levels in tissues from rats fed soils containing lead. Arch. Environ. Contam. Toxicol. 6:111-119.
Day, J.P., Fergusson, J.E. and Chee, T.M. 1979. Solubility and potential toxicity of lead in urban street dust. Bull. Environ. Contam. Toxicol. 23:497-502.
Decker, A.M., Chaney, R.L., Davidson, J.P., Rumsey, T.S., Mohanty, S.B. and Hammond, R.C. l980. Animal performance on pastures topdressed with liquid
sewage sludge and sludge compost. pp 37-4l. In Proc. Nat. Conf. Municipal and Industrial Sludge Utilization and Disposal. Information Transfer, Inc., Silver
Spring, MD.
Duggan, M.J., and Inskip, M.J. 1985. Childhood exposure to lead in surface dust and soil: A community health problem. Public Health Rev. 13:1-54.
Duggan, M.J., Inskip, M.J., Rundle, S.A. and Moorcroft, J.S. 1985. Pb in playground dust and on the hands of schoolchildren. Sci. total. Environ. 44:65-79.
Egan, D.A., and O'Cuill, T. l970. Cumulative lead poisoning in horses in a mining area contaminated with Galena. Vet. Rec. 86:736-738.
Elfving, D.C., Haschek, W.M., Stehn, R.A., Bache, C.A. and Lisk, D.J. 1978. Heavy metal residues in plants cultivated on and in small mammals indigenous to
old orchard soils. Arch. Environ. Health 33:95-99.
Farrell, T. 1988. Management of soil lead contamination in Port Pirie, Australia. Environ. Geochem. Health. In press.
Fergusson, J.E. 1986. Lead: Petrol lead in the environment and its contribution to human blood lead levels. Sci. Total Environ. 50:1-54.
Fergusson, J.E., Forbes, E.A., Schroeder, R.J. and Ryan, D.E. 1986. The elemental composition and sources of house dust and street dust. Sci. Total
Environ. 50:217-221.
Fergusson, J.E. and Ryan, D.E. 1984. The elemental composition of street dust from large and small urban areas related to city type, source, and particle size.
Sci. Total Environ. 34:101-116.
Flanagan, P.R., Chamberlain, M.J. and Valberg, L.S. 1982. The relationship between iron and lead absorption in humans. Am. J. Clin. Nutr. 36:823-829.
Flanagan, P.R., Chamberlain, M.J. and Valberg, L.S. 1983. Iron and lead absorption in humans -- Reply to a letter by Watson and Hume. Am. J. Clin. Nutr.
38:334-335.
Freedman, M.L., Cunningham, P.M., Schindler, J.E. and Zimmerman, M.J. 1980. Effect of lead speciation on toxicity. Bull Environ. Contam. Toxicol. 25:389393.
Fries, G.F., Marrow, G.S. and Snow, P.A. 1982. Soil ingestion by dairy cattle. J. Dairy Sci. 65:611-618.
Garcia-Miragaya, J. 1984. Levels, chemical fractionation, and solubility of lead in roadside soils of Caracas, Venezuila. Soil Sci. 138:147-152.
Getz, L.L., Haney, A.W., Larimore, R.W., McNurney, J.W., Leland, H.V., Price, P.W., Rolfe, G.L., Wortman, R.L., Hudson, J.L., Soloman, R.L. and Reinbold,
K.A. 1977. Chapter 6. Transport and distribution in a watershed ecosystem. pp. 105-134. In W.R. Boggess and Wixson, B.G. (eds.). Lead in the Environment. Report to Nat. Sci. Found., NSF/RA-770214. NTIS Report PB-278278.
Gibson, M.J., and Farmer, J.G. 1984. Chemical partitioning of trace element contaminants in urban street dirt. Sci. Total Environ. 33:49-57.
Harbourne, J.F., McCrea, C.T. and Watkinson, J. l968. An unusual outbreak of lead poisoning in calves. Vet. Rec. 83:5l5-5l7.
Harrison, R.M., Laxen, D.P.H. and Wilson, S.J. 1981. Chemical associations of lead, cadmium, copper, and zinc in street dusts and roadside soils. Environ.
Sci. Technol. 15:1378-1383.
Harter, R.D. 1979. Adsorption of copper and lead by the Ap and B2 horizons of several Northeastern United States soils. Soil Sci. Soc. Am. J. 43:679-683.
Harter, R.D. 1983. Effect of soil pH on adsorption of lead, copper, zinc, and nickel. Soil Sci. Soc. Am. J. 47:47-51.
Hassett, J.J. 1974. Capacity of selected Illinois soils to remove lead from aqueous solutions. Commun. Soil Sci. Plant Anal. 5:499-505.
Healy, M.A. 1984. Theoretical model of gastrointestinal absorption of lead. J. Clin. Hosp. Pharm. 9:257-262.
Healy, M.A., P.G. Harrison, M. Aslam, S.S. Davis, and C.G. Wilson. 1982. Lead sulphide and traditional preparations: Routes for ingestion, and solubility and
reactions in gastric fluid. J. Clin. Hosp. Pharm. 7:169-173.
Heard, M.J., Chamberlain, A.C. and Sherlock, J.C. 1983. Uptake of lead by humans and effect of minerals and food. Sci. Total Environ. 30:245-253.
Hurley, L.W. and Lonnerdal, B. 1982. Zinc binding in human milk: Citrate versus picolinate. Nutr. Rev. 40:65-71.
Hutton, M., and Goodman, G.T. 1980. Metal contamination of feral pigeons Columbia livia from the London area: l. Tissue accumulation of lead, cadmium, and
zinc. Environ. Pollut. A22:207-217.
Ireland, M.P. 1977. Lead retention in toads (Xenopus laevis) fed increasing levels of lead-contaminated earthworms. Environ. Pollut. 12:85-92.
James, H.M., Hilburn, M.E. and Blair, J.A. 1985. Effects of meals and meal times on uptake of lead from the gastrointestinal tract in humans. Human Toxicol.
4:401-407.
Johnson, D.E., Kienholz, E.W., Baxter, J.C., Spanger, E. and Ward, G.M. 1981. Heavy metal retention in tissues of cattle fed high cadmium sewage sludge. J.
Anim. Sci. 52:108-114.
Jordan, L.D., and Hogan, D.J. 1975. Survey of lead in Christchurch soils. N.Z. J. Sci. 18:253-260.
18
Kienholz, E., Ward, G.M., Johnson, D.E., Baxter, J.C., Braude, G.L. and Stern, G. 1979. Metropolitan Denver sewage sludge fed to feedlot steers. J. Anim.
Sci. 48:735-741.
Kinniburgh, D.G., Jackson, M.L. and Syers, J.K. 1976. Adsorption of alkaline earths, transition, and heavy metal cations by hydrous oxide gels of iron and
aluminum. Soil Sci. Soc. Am. J. 40:796-799.
Kostial, K., and Kello, D. 1979. Bioavailability of lead in rats fed "human" diets. Bull. Environ. Contam. Toxicol. 21:312-314.
Lau, W.M., and Wong, M.H. 1983. The effect of particle size and different extractants on the contents of heavy metals in roadside dusts. Environ. Res. 31:229242.
Lindsay, W.L. 1979. Lead. pp. 328-342. In Chemical Equilibrium in Soils. John Wiley and Sons, NY.
Lonnerdal, B., Keen, C.L. and Hurley, L.S. 1984. Zinc binding ligands and complexes in zinc metabolism. Adv. Nutr. Res. 6:139-167.
Lonnerdal, B., Stanislowski, A.G. and Hurley, L.S. 1980. Isolation of a low molecular weight zinc binding ligand from human milk. J. Inorg. Biochem. 12:71-78.
Mahaffey, K.R. 1982. Role of nutrition in prevention of pediatric lead toxicity. pp 63-78. In J.J. Chisolm, Jr., and O'Hara, D.M. (eds.) Lead Absorption in
Children: Management, Clinical, and Environmental Aspects. Urban and Schwarzenberg, Baltimore.
Mahaffey, K.R. 1985. Factors modifying susceptibility to lead toxicity. pp. 373-419. In K.R. Mahaffey (ed.) Dietary and Environmental Lead: Human Health
Effects. Elsevier Biomedical Press, Amsterdam.
Mahaffey, K.R., Banks, T.A., Stone, C.L., Capar, S.G., Compton, J.F. and Gubkin, M.H. 1977. Effect of varying levels of dietary calcium on susceptibility to lead
toxicity. Proc. Intern. Conf. Heavy Metals in the Environ. 3:155-164.
Mahaffey, K.R. and Michaelson, I.S. 1980. The interaction between lead and nutrition. pp. 159-200. In H.L. Needleman (ed.) Low Level Lead Exposure: The
Clinical Implications of Current Research. Raven Press, Boston.
Mahaffey, K.R., Stone, S.L., Banks, T.A. and Reed, G. 1978. Reduction in tissue storage of lead in the rat by feeding diets with elevated iron concentrations.
Proc. Int. Symp. Trace Elements Metabolism in Man and Animals 3:584-588.
Martin, M.T., Licklider, K.F., Brushmiller, J.G. and Jacobs, F.A. 1981. Detection of low molecular weight copper(II) and zinc(II) binding ligands in ultrafiltered
milks -- The citrate connection. J. Inorg. Biochem. 15:55-65.
McKenzie, R.M. 1978. The effect of two manganese dioxides on the uptake of lead, cobalt, nickel, copper, and zinc by subterranean clover. Aust. J. Soil Res.
16:209-214.
McMichael, A.J., Baghurst, P.A., Robertson, E.F., Vimpani, G.V. and Wigg, N.R. 1985. The Port Pirie cohort study: Blood lead concentrations in early
childhood. Med. J. Aust. 143:499-503.
McMichael, A.J., Baghurst, P.A., Wigg, N.R., Vimpani, G.V., Robertson, E.F. and Roberts, R.J. 1985. The Port Pirie cohort study: Environmental exposure to
lead and children's abilities at the age of four years. New Engl. J. Med. 319:468-475.
Merry, R.H., Tiller, K.G., deVries, M.P.C. and Cartwright, B. 1981. Contamination of wheat crops around a lead-zinc smelter. Environ. Pollut. B2:37-48.
Mielke, H.W., Anderson, J.C., Berry, K.J., Mielke, P.W., Chaney, R.L. and Leech, M.M. 1983. Lead concentrations in inner-city soils as a factor in the child lead
problem. Am. J. Public Health 73:1366-1369.
Moynahan, E.J. 1974. Acrodermatitis enteropathica: A lethal inherited human zinc-deficiency disorder. Lancet II(7877):399-400.
Mylroie, A.A., Moore, L., Olyai, B. and Anderson, M. 1978. Increased susceptibility to lead toxicity in rats fed semipurified diets. Environ. Res. 15:57-64.
Neldner, K.H. and Hambridge, K.M. 1975. Zinc therapy of acrodermatitis enteropathica. N. Engl. J. Med. 292:879-882.
Nelson, L.S., Jr., Jacobs, F.A. and Brushmiller, J.G. 1985. Solubility of calcium and zinc in model solutions based on bovine and human milks. J. Inorg.
Biochem. 24:255-265.
Nelson, L.S., Jr., Jacobs, F.A., Brushmiller, J.G. and Ames, R.W. 1986. Effect of pH on the speciation and solubility of divalent metals in human and bovine
milks. J. Inorg. Biochem. 26:153-168.
Nelson, L.S., Jr., Jacobs, F.A. and Brushmiller, J.G. 1987. Coprecipitation modulates the solubility of minerals in bovine milk. J. Inorg. Biochem. 29:173-179.
Nriagu, J.O. 1974. Lead orthophosphates. IV. Formation and stability in the environment. Geochim. Cosmochim. Acta 38:887-898.
Nriagu, J.O. and J. Pacyna. 1988. Quantitative assessment of worldwide contamination of air, water, and soil by trace metals. Nature 333:134-139.
Olsen, K.W. and Skogerboe, R.K. 1975. Identification of lead compounds from automotive sources. Environ. Sci. Technol. 9:227-230.
Paskins-Hurlburt, A.J., Tanaka, Y., Skoryna, S.C.,Moore, W., Jr. and Stara, J.F. 1977. The binding of lead by a pectic polyelectrolyte. Environ. Res. 14:128-140.
Patterson, C.C. 1980. An alternative perspective -- Lead pollution in the human environment: Origin, extent, and significance. pp. 265-349. In Lead in the
Human Environment. 1980. National Academy of Sciences, Washington, D.C. 525 pp.
Peaslee, M.H. and Einhellig, F.A. 1977. Protective effect of tannic acid in mice receiving dietary lead. Experientia 33:1206.
Preer, J.R., Akintoye, J.O. and Martin, M.L. 1984. Metals in downtown Washington, D.C. gardens. Biol. Trace Element Res. 6:79-91.
Quarterman, J. and Morrison, J.N. 1975. The effects of dietary calcium and phosphorus on the retention and excretion of lead in rats. Brit. J. Nutr. 34:351-362.
Quarterman, J., Morrison, J.N. and Humphries, W.R. 1978. The influence of high dietary calcium and phosphate on lead uptake and release. Environ. Res.
19
17:60-67.
Que Hee, S.S., Peace, B., Clark, C.S., Boyle, J.R., Bornschein, R.L. and Hammond, P.B. 1985. Evolution of efficient methods to sample lead sources, such as
house dust and hand dust, in the homes of children. Environ. Res. 38:77-95.
Rabinowitz, M.B., Kopple, J.D. and Wetherill, G.W. 1980. Effect of food intake and fasting on gastrointestinal lead absorption in humans.
Am. J. Clin. Nutr. 33:1784-1788.
Rabinowitz, M., Leviton, A., Needleman, H., Bellinger, D. and Waternaux, C. 1985. Environmental correlates of infant blood lead levels in Boston.
Environ. Res. 38:96-107.
Ryu, J.E., Ziegler, E.E., Nelson, S.E. and Fomon, S.J. 1983. Dietary intake of lead and blood lead concentration in early infancy. Am. J. Dis. Child. 137:886-891.
Ryu, J.E., Ziegler, E.E., Nelson, S.E. and Fomon, S.J. 1985. Dietary and environmental exposure to lead and blood lead during early infancy. pp. 187-209. In
K.R. Mahaffey (ed.) Dietary and Environmental Lead: Human Health Effects. Elsevier Press, Amsterdam.
Santillan-Medrano, J., and Jurinak, J.J. 1975. The chemistry of lead and cadmium in soil: Solid phase formation. Soil Sci. Soc. Am. Proc. 39:851-856.
Scanlon, P.F., Kendall, R.J., Lochmiller, R.L. and Kirkpatrick, R.L. 1983. Lead concentrations in pine voles from two Virginia orchards.
Environ. Pollut. B6:157-160.
Sherlock, J.C., Ashby, D., Delves, H.T., Forbes, G.I., Moore, M.R., Patterson, W.J., Pocock, S.J., Quinn, M.J., Richards, W.N. and Wilson, T.S. 1984. Reduction
in exposure to lead from drinking water and its effect on blood lead concentrations. Human Toxicol. 3:383-392.
Sherlock, J.C., Barltrop, D., Evans, W.H., Quinn, M.J., Smart, G.A. and Strelow, C. 1985. Blood lead concentrations and lead intake in children of different
ethnic origin. Human Toxicol. 4:513-519.
Sherlock, J., Smart, G., Forbes, G.I., Moore, M.R., Patterson, W.J., Richards, W.N. and Wilson, T.S. 1982. Assessment of lead intakes and dose-response for a
population in Ayr exposed to a plumbosolvent water supply. Human Toxicol. 1:115-122.
Smith, C.M., Deluca, H.F., Tanaka, Y. and Mahaffey, K.R. 1978. Stimulation of lead absorption by vitamin D administration. J. Nutr. 108:843-847.
Spittler, T.M., and Feder, W.A. 1979. A study of soil contamination and plant lead uptake in Boston urban gardens. Commun. Soil Sci. Plant Anal.
10:1195-1210.
Stara, J., Moore, W., Richards, M., Barkely, N., Neiheisel, S. and Bridbord, K. 1973. Environmentally bound lead. III. Effects of source on blood and tissue
levels in rats. pp. 28-29 In EPA Environmental Health Effects Research Series A-670/1-73-036.
Stone, C.L., Fox, M.R.S. and Hogye, K.S. 1981. Bioavailability of lead in oysters fed to young Japanese quail. Environ. Res. 26:409-421.
Thornton, I. 1986. Lead in United Kingdom soils and dusts in relation to environmental standards and guidelines. Trace Subst. Environ. Health 20:298-307.
Thornton, I., Culbard, E., Moorcroft, S., Watt, J., Wheatley, M. and Thompson, M. 1985. Metals in urban dusts and soils. Environ. Technol. Lett. 6:137-144.
Tiller, K.G., deVries, M.P.C., Spouncer, L.R., Smith, L. and Zarcinas, B. 1976. Environmental pollution of the Port Pirie region. 3. Metal contamination of home
gardens in the city, and their vegetable produce. CSIRO Div. Soils Report No. 15. 18 pp.
Vimpani, G., McMichael, A., Robertson, E. and Wigg, N. 1985. The Port Pirie cohort study. A prospective study of pregnancy outcome and early childhood
growth and development in a lead-exposed community -- Protocol and status report. Environ. Res. 38:19-23.
Wardrope, D.D., and Graham, J. 1982. Lead mine waste: Hazards to livestock. Vet. Rec. 111:457-459.
Watson, W.S., and Hume, R. 1983. Iron and lead absorption in humans (letter to Editor). Am. J. Clin. Nutr. 38:334-335.
Watson, W.S., Hume, R. and Moore, M.R. 1980. Oral absorption of lead and iron. Lancet 2:236-237.
Wilson, D., Esterman, A., Lewis, M., Roder, D. and Calder, I. 1986. Children's blood lead levels in the lead smelting town of Port Pirie, South Australia.
Arch. Environ. Health 41:245-250.
Wise, A. 1981. Protective action of calcium phytate against acute lead toxicity in mice. Bull. Environ. Contam. Toxicol. 27:630-633.
Wolf, A., Bunzl, K., Dietl, F. and Schmidt, W.F. 1977. Effect of Ca2+ ions on the adsorption of Pb2+, Cu2+, Cd2+, and Zn2+ by humic substances. Chemosphere
6(5):207-213.
Young, R.W., Ridgely, S.L., Blue, J.T., Bache, C.A. and Lisk, D.J. 1986. Lead in tissues of woodchucks fed crown vetch growing adjacent to a highway.
J. Toxicol. Environ. Health 19:91-96.
Ziegler, E.E., Edwards, B.B., Jensen, R.L., Mahaffey, K.R. and Foman, S.J. 1978. Absorption and retention of lead by infants. Pediatr. Res. 12:29-34.
Zimdahl, R.L. and Skogerboe, R.K. 1977. Behavior of lead in soil. Environ. Sci. Technol. 11:1202-1207.
Zmudzki, J., Bratton, G.R., Womac, C., and Rowe, L.D. 1984. The influence of milk diet, grain diet, and method of dosing on lead toxicity in young calves.
Toxicol. Appl. Pharmacol. 76:490-497.
20
21