EPA/600/A-94/030
Heavy Metals and Toxic Organic Pollutants in
MSW-Composts:
Research Results on Phytoavailablity,
Bioavailability, Fate, Etc.
Rufus L. Chancy
Environmental Chemistry Lab
USDA-Agricultural Research Service
Beltsville, MD 20705
James A. Ryan
: Risk Reduction Engineering Lab
U.S.-Environmental Protection Agency
Cincinnati, Ohio
Abstract
This paper is a review and interpretation of research which has been
conducted to determine the faie, transport, and potential effects of heavy
metals and toxic organic compounds in MS W-composts and sewage sludges.
Evaluation of research findings identified a number of Pathways by which
these contaminants can be transferred from MSW-compost or compost-
amended soils to humans, livestock, or wildlife. The Pathways consider direct
ingestion of compost or compost-amended soil by livestock and children,
plant uptake by food or feed crops, and exposure to dust, vapor, and water to
which metals and organics have migrated.
. InresearchonthesequesuonSpthechemicalpropertiesofsludgesand
composts were found to be very important in binding the metals and toxic
organics. Amorphous oxides of Fe, Al,.and Mn provide persistent specific
metal adsorption capacity for the heavy metals of concern in MSW-compost
and sludges. When properly cured modern MSW-composts containing low
levels of metals and organics were land applied, there was no evidence of
adverse effects to humans, livestock, or wildlife except temporary B phyto-
toxicity. Adverse effects have only been found when highly metal contami-
nated sludges or MSW+sludge-composts with highly metal contaminated
sludges were used at high cumulative application rates, at very strongly acidic
soil pH. Based on the quantitative estimates of sludge constituent cumulative
loadingsor concentrations which cause NoObserved Adverse Effect (NOAEL
sludges) according to the Pathway Approach for risk analysis, and strong
evidence that this quality sludge and MSW-compost may be regularly used as
part of sustainable agriculture, EPA has proposed using sludge composition
limits (APL = Alternative Pollutant Limits) to regulate low contaminant
sludges. High contaminant concentration sludges would continue to be
regulated by cumulative contaminant application limits.
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452 Science and Engineering of Composing
The "bioavailability" of contaminants in MSW-composts describes
the potential for accumulation in animals of metals or organics from ingested
sludges or composts, or from food/feed materials grown on sludge or compost
amended soils. Risk assessment for direct ingestion is very important since
ihis allows ihe greatest potential for transfer for many constituents. Limited
feeding studies have been reported for sludges, while research on ingestJon of
properly composted MSW has.only recently begun. The presence of high
levels of humic materials and hydrous Fe oxides in sludges, and the presence
of other elements with the element being evaluated, cause the bioavailability
of Pb, Cd, and other elements and organics in sludges to be quite low. Because
Cd is 'ordinarily about 0.5% of Zn in MSW-composts, it is not possible for
compost Cd to cause injury to the most exposed home gardeners who grow a
large fraction of their garden foods on compost amended soils for a lifetime.
Presently, it appears that the most limiting heavy metal in MSW-
composts may be Pb. A large body of data from feeding studies, and risk
evaluation using the EP A Pb Uptake Biokinetic Model, indicate that composts
with up to 300 mg Pb/fcg will not comprise a significant risk to children who
inadvertently ingest compost products. Thus, MSW-compbst may provide
fend izerand soil conditioner benefit in agriculture and horticulture if compost
manufacturers carefully reject Pb rich wastes.
INTRODUCTION
During the preparation, review.and revision of the Clean Water Act-
503 Proposed Regulation (US-EPA, I989b), a Pathway Approach lorisk
assessment was developed (US-EPA, 1989a), This Pathway Approach is a
comprehensive evaluation of potential worst-case risk to humans, livestock,
soil fertility, and wildlife. It considers all receptors and pathways identified
by researchers. As a result of the 503 process, important lessons have been
learned about risk assessment for land application of sewage sludge, a residual
.with properues somewhat similar to those of MSW-Compost. This paper
reviews the limited research on the potential environmental problems which
might result from land application of MSW-compost, and relevant research
on sludges and sludge composts which we believe should provide the basis for
development of limitations for utilization of MSW-composis.
Table 1 shows the Pathways which may allow transfer of compost-
applied contaminants to most exposed individuals (humans, livestock, plants,
microbes, or wildlife) (see Ryan and Chancy (1992) for detailed review of the
risk analysis protocols). As summarized in Chancy (1990a, 1990b, 1992),
Chancy, Ryan, and O'Connor (1991), and other papers, several pathways
predominate in risk for metals or organics because of the chemical properues
of the contaminants, soils, etc. The importance of these pathways was
identified during the last 20 years of sludge risk analysis research (Logan and
Chancy, 1983; Chancy et al., 1987; Chancy afld Giordano, 1977)! Phytotox-
icity from compost-applied Zn, Cu, Ni, and B is the principle limitation for
these elements. Direct ingestion of composts or sludges by children, livestock
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Table 1. Pathways for risk assessment of |x>tential transfer of sludge-applied trace contaminants to humans, livestock, or the
environment, and the Most Imposed Individual 10 be protected by regulation to be based on the Pathway Analysis (US F,PA. 1989a).
Pathway
Most exposed Individual
1 Sludge Soil Plant Human
I-Future Sludge Soil Plant Human
l-D&M Sludge Soil Plant Human
2 Future Sludge Soil Human child
2 D&M Sludge Human child
3 Sludge Soil Plant Animal Human
4-Surface Sludge Animal Human
4 Mixed Sludge Soil Animal Human
5 Sludge Soil Plant Animal
6-Surfacc Sludge Animal
6-Mixed Sludge Soil Animal
7 Sludge Soil Plant
8 Sludge Soil Soil biota
9 Sludge Soil Soil bioLa Predator
9 Direct Sludge Soil (Soil biota) Predator
10 Sludge Soil Airborne dust Human
11 Sludge Soil Surface water Human
12 Sludge Soil Air Human
12-Waler Sludge Soil Ground water Human
General food chain; 2.5% of all plant derived fds for lifetime.
Home garden 5 yr after last sludge application, 50% of garden foods for lifetime.
ll
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454 Science and Engineering of Composing,
or wildlife is the principle limitation on potentially toxic organics such as
PCBs, DDT, etc, and from Pb, Fe, and F. Plant uptake and transfer to ihe
human food chain is the principal limitation on Cd application, while transfer
to the feed chain for ruminant livestock is ihe principle limitation for Mo and
Se. , ; • • '
Although these summaries are based on a large body of sludge
research in the Held, it is necessary to consider the data from studies of MSW-
compost application to see if results are sufficiently similar 10 allow develop-
ment of limitations for MSW-compost 10 be based on the more complete
sludge database. Unfortunately, potential risks from utilization of MSW-
Compost research has not had the intensity of research using modem scientific
technology that sludge application has received. When sludge research began
in the early 1970's, some research on MSW+sludge composts was included,
but little new or detailed work was conducted on MSW-compost in the U.S.
until the 1990s.
.Perhaps ihe most important perspective on the potential for persistent
risks from utilization of composts from separated MSW (ignoring the shon
term problems from N-i'mmobilizaiion, inadequately curing, salts, etc.) is the
simple statement that no adverse effects from contaminants in MSW-compost
have been reported other than B toxicity to plants (a temporary problem).
'Neither Zn, Cu, or Ni phytotoxicity has been observed, nor have Cd, Pb, or
xenobiouc organic compounds been observed to cause injury to humans,
livestock or wildlife.
One ad verse effect of com post has been lime:induced Mn-deficiency
'in low Mn light textured soils (Haan, 1981). Where other problems from
metals or organics have been identified, they have resulted from composting
MSW with highly contaminated sewage sludge. Although increases in metaJs
or organics in compost-amended soils have been found as expected, demon-
strations of-potemia! risk from the increases in soil metals have not been
reported. Some have expressed concern that soJ metals or organics have
exceeded background levels for agricultural soils. We conclude thai the basis
for regulating land application of MSW-compostsand sewage sludge should
be the potential for compost utilization to cause ad verse effects on agriculture
or on the environment due to the metals or organics in these resources, not the
simple soil enrichment with known potentially toxic metals and organics.
In general, we believe that soil enrichment without demonstrable risk
is a different perspective that agronomists and ecologists must learn how to
deal with. We conclude that utilization of MSW-compostsand sewage sludge
can provide significant benefit to sustainable agriculture; compost utilization
can safely continue for an indefinite period without risk to agriculture or the
environment. Thus, this paper is a review of the limited data on the potential
adverse effects of land-applied MSW-compost, and perspectives on risk
ana lysis from our work on municipal sewage sludge and sludge composts. We
believe that an appropriate risk analysis methodology for potentially toxic
contaminants in land-applied organic residuals has been developed, and that
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Chancy and Ryan . 455
ihere is little evidence that compost prepared from MSW will be found to
comprise risk to highly exposed individuals even at very high cumulative
applications, .
Others have re vie wed.these subjects, and readers should consider this
paperan extension of the information summarized by these previous workers.
The MS W -compost research in the 1960s and 1970s is important in increasing
the efficiency of our research in the 1990s. We need not "rein vent the wheel"
about many of ihe questions about MSW-compost, considering that new plans
to pre-separaie the compostable fraction of MSW before il becomes contami-
nated by other materials will substantially decrease the concentration of many
potentially toxic constituents. Some important re views include those of Haan,
1981; Andersson, 1983; Herms and Sauerbeck, 1983; Sauerbeck, 1991;
Peu-uzzelli, 1989; Terman and Mays, 1973; Gallardo-Laia and Nogales,
1987).
COMPOSITION OF MSW-COMPOST:
MSW-compost contains higher levels of many trace elements than
do US background soils, but lower levels than do sewage sludges (Table 2).
Modern sludges coniajn far lower mean concentrations of metals than found
in earlier large surveys, but many sludges still exceed levels attainable by
ind usuialpreueatment and treating the drinking water to reduce corrosiveness
of the tap water (a significant source of Pb now that gasoline is Pb-fre«). The
so called "green-wastes" composts prepared by separate collection of only the
compostable fraction of MSW a I lowproduction of composts with lower metal
residues than can be attained by general pre-sepaiation, or by centraJ-
sepaxanon of MSW into different fractions. However, just because lower
concentrations can be reached in MSW-composts doesn't mean thai they have
to be aitajned to make utilization of MSW-compost on cropland a valuable
practice of sustainable agriculture, Comparison of US soil metal levels with
sludge and MSW metal levels indicates that modem MSW-composts are only
somewhat enriched in metals compared to soils (although Pb is now higher in
MSW-compost than in sewage sludges). The "non-volatile" fraction of
MSW-compost (30-60% depending on the nature of the wastes and methods
of separation utilized [Lisk ei ai. 1992a]) indicates the maximal concentra-
tion which would be in soils if the soil were comprised of biodegraded MSW-
compost. As noied in Ryan and Chaney (1992), if a compost contains 50%
inorganic matter, the maximum concentration of contaminants in undiluted
oxidized compost would be double the original compost. Analytical results
of Lisk ei at. (I992a) are in agreement with the above discussion; further, they
showed that PCBs were quiie low in yard waste-, sludge-, and MSW-
composts, Lisk el al. (I992b) noted small variance in metals, etc., in yard
waste compost and sludge compost.
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456 Science and Engineering of Composing
TABLE 2. Geometric mean heavy meial conieni of composts from mixed
MS W from the L'niicd States and separated organic wastes from Europe (dry
mailer basis) (MSW-composis from on Epstein ei a!., 1992) (US sludge data
[lognormal means wiih multi-censoring] from US-EPA, 1990); "Green"
MSW-composis from Fricke, Peril, and Vogtmann (1989); NOAEL sludge
limits from Chaney (1992)- US soil metals data from Holmgren ei al. (1992)
(Cd, Cu, Pb, Ni, Zn) or Shackleue and Boemgen (1984) (Cr).
Element MSW-composis
No.' Geometric
Simples
As', pg/g
Cd, pg/g
Cr, Mg/g.
Cu, pg./g
Pb, pg/g
Hg, Pgy'g
N'.Mg-'g
Zn, pg/g
Cd.Tri, ug/pg
8
'72
66
73
73
31
66-
72
-> \
'Mean
2.6
• 2.0 .
32,6
107 .,
169
1.09
22.7
418
u.005'5.
"Green"
MSW
NOAEL
Sludge
Gomposi Limili
.100 •
0,5
.>3000
40.
86.
0.17
17. .
255.
0.0020
9.9
25
118.
1200
300
20
500
2700
0.015
US Sludges
Ceo. Mean
NSSS
6.9
53.
741.
134.
5.2
42.7
1200.
0.0058
US Soils
0.18
18.0
10,6
16.5
42.9
000-41
IDENTIFIED PERSISTENT PROBLEMS FROM
LAND-APPLIED MSW-COMPOSTS
A number of short-duration problems have occurred when high rates
of MSW-composis were applied lo cropland (phytoioxiciiy from biodegrada-
uon by-products in inadequately cured composi; excess soluble salts; N-
immobilization). Fortunately, good managemeni of MSW composting or
utilization can avoid these serious limitations to beneficial use of MSW-
composi. •' '
Hov-ever, two significant persisient agricultural problems have
occasionally been observed in fields amended wiih MSW-compost; Boron
phyioioxicuy and Mn-deficiency. Each has occurred under unusual condi-
tions, and ihe potential for yield reduciions were very site specific. Further,
high raies of composi application used in research were required 10 cause ihe
B phytoioxicny or Mn-deficiency, and these rates are much higher irian
commonly applied in normal agricultural practices.
Boron Phytotoxicity: In conuasi wiih municipal sewage sludge,
MSW-compost contains substantial levels of soluble boron (B). B loxicity
from sewage sludge application was reported only for an unusual case of a
sensitive uee species growing in soils amended wiih a sludge coniaming lots
of glass fibers (Vimmersiedi and Glover, 1984;.see also Neary ei a/., 1975,
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Chaney and Ryan 457
regarding high B levels in phosphate-free'detergents). The glass fibers
contained borosilicaie and release of B caused phytotoxicity. Research has
shown that much of the soluble B in MSW-composi comes from glues (Volk,
1976). It has long been known thai plant samples placed in paper bags can
become contaminated from B from glue used to hold the bag together. El
Bassam and Thorman (1979) and Gray and Biddlestone (1980) noted that the
B level in MS W-composts was quite variable as might be expected if composis
are not well mixed.
In general, B phytotoxicity has occurred when high application rates
were used, and B-sensiu ve crops were grown. However, when MS W-compost
is used at fertilizer rates in normal fields, the B might be important as a
fertilizer rather than as a potentiaJ phytotoxicity problem.
Boric acid and most borates aie quite water soluble, although B can
be adsorbed on clays and by organic matter. Low soil pH facilitates B uptake
by plants because ihe H^BO, molecule (predominant form at lower soil pH)
is absorbed by roots rather than anionicborates(Oenli and Grgurevic, 1975).
AJthough most B toxicity has been reported on aJkaline soils, ihisisduetothe
lack of leaching for most of these soils. Excess applications of soluble B are
much morephytotoxic in acidic soils, and liming can correct B phytotoxicity.
The usual liming action of compost should help prevent this problem.
There are large differences among crop species in tolerance of
excessive SOL! B. Some crops are very sensitive, and these are the species
which have suffered phytotoxicity from compost-applied B (bean, wheat, and
mum). Francois has summarized the significant differences among severaJ
groups of crops (Francois and Clark, 1979; Gupta, 1979; Francois, 1986).
Ornamental horticultural species have been examined to some extent (infor-
mation on individual species can be found by literature searching), but many
horticultural crops have not been studied. This is one research need related
to practical microelement phytotoxicity from compost.
Perhaps the first repon on B toxicity from MSW-compost is that of
Purves (1972) who noted B; phytotoxicity to beans on field plots which
received high rates of MSW-compost. The full description of the compost
experiment is reported, in Purves and Mackenzie (1973), and a careful
examination to prove B phytotoxicity was reported by Purves and Mackenzie
(1974). Bean (but not potato or other species examined) suffered severe yield
reduction at high compost rates; this yield reduction was proponional to rate
of compost application. Bean is known to be especially sensitive to B
phytotoxicity. Gray and Biddlestone (1980) also found B phytotoxicity in
sensitive species grown in field plots with high rates of MSW-compost.
Cogue and Sanderson (1975) reported B phyioioxicity tochrysanthe-
mums in potting media containing MSW-compost. Foliar analysis clearly
supported the conclusion that B was toxic and that Mn, Cu, Zn, and other
elements were not at toxic levels. They conducted a calibration experiment
to determine the sensiuvity of chrysanthemums^Gogue and Sanderson,
1973), and the levels found in the mums grown on .the test media were in the
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458 , Science and Engineering of Composting
phytotoxic range. In iheir research, they adjusted ihe pH of ihe media to 6
using sulfur, rather than allowing the MSW-compost 10 raise ihe pH of ihe
media, This probably contributed 10 ihe severity of Bphytotoxicity observed,
Some oiher horticultural species.also suffered B phytoioxicity in compost-
containing media (Gilliam and Watson, 1981). Sanderson (1980) reviewed
B toxicity in compost amended potting.media, In contrast to MSW-compost,
sewage sludge composis wilh wood chips have not been found to'cause B
phytotoxichy (Chancy, Munns, and Cathey, 1980). Only a few acid-loving
species require acidification of media lo do well on neutral compost-amended
media.
Interestingly, because ihe B which causes phytotoxicity is water
soluble, the B phytotoxicity problem from MSW-compost is short-lived,
Purves and Mackenzie (1973) noted that pre-leaching MSW-compost pre-'1
vented B phytoiox icily. Oiher studies noted that ihe B-phytotoxicity occurred
only during the year of application, and that soluble B was laached out of ihe
root zone over winter (Volk, 1976) or by I&aching potting media with normal
horticultural watering practices. Sanderson (1980) noted that perlite also adds
B to potting media, and that use of both may cause B toxiciiy when either
perlite or MSW-compost alone might not have done so. Lumis and Johnson
(198-2) studied leaching of B in relation totoxicity of salts and B loForsyihia
and Thuja. They reported that a simple leaching treatment removed excess
soluble salts, but was unable to remove enoughB to prevent phytotoxicity (the
compost they studied contained 225 mg B/fcg, higher than most reports).
Nogalese/a/. (1987) also found compost-applied B leached quickJy such that
crop B was reduced in each successive ryegrass crop,
B phytotoxicity is significantly more severe when plants a/e N-
deficient (Cogue and Sanderson, 1973; Nogales ei a/,, 1987; .Gupta ei a!.,
1973). This makes the B in MSW-compost which is not properly cured (to
avoid N immobilization) potentially more phytotoxic than in well cured
composis. Further, B flows with the transpiration stream and accumulates in
older leaves. In environments with low humidity, more transpirauon occurs
(e.g., greenhouses), and B toxiciiy is more severe. B and salt toxiciry are easily
confused; both are first observed in leaf tips or ma/gins of older leaves.
Diagnosis of B phytotoxicity requires a knowledge of relative plani tolerance
of B, or analysis of the leaves bearing symptoms.
Thus, in general use, compost application at a reasonable fertilizer
rate would simply add enough B to serve as a fertilizer for B-deficiency
susceptible crops such as alfalfa or cole crops. However, use of MSW-
compost at high rates in soils or potting media could cause phyioioxici'ty if
high soluble B were present. The B phytotoxicity would not be persistent
because soluble B would leach from the root zone with normal rainfall or
irrigation. Compost-applied B would be morephytotoxic in N-deficient soils,
which might result from application of improperly cured compost Water
soluble B should be'one chemical which is regularly monitored in MSW-
composis so that the need for warning about rates of application and use with
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Chancy and.Ryan 459
sensitive crops can be identified. Deliberate use of MSW-compost as a B
fertilizer for high B-requiring crops such as the cole crops (cabbage family)
might become a regular agronomic practice. Sources of soluble B in modern
MSW-compost should be evaluated, and alternative to B use identified.
Compost-induced Mn deficiency. In contrast with most sewage
sludges, application of MSW-compost usually raises the pH of the soil-
compost mixture, Sludges usually contain more reduced N and S, and
oxidation of these after mixing sludge wiih soil generates acidity. Some
sludges from areas with hard water do contain enough lime equivalent 10
correct ihe acidity they add' to the soil, but all MSW-composts have been
reported 10 contain lime equivalent. This could come from useofCaCO,and
other materials as fillers in paper, or from stabilization of crop residues.
When MSW-compost was added to naturally lowMn acidic soils, the
resultant high pH was been found to cause Mn-deficiency in some cases, Haan
(1981) noted ihaiMn deficiency occurred in several cases in the Netherlands,
and Andcrsson (1983) noted this effect in some Swedish soils,
One w ay to assure that MSW-compost does not cause Mn deficiency
is 10 add Mn to the MS W during composting (inclusion of identified industrial
Mn w 3stes or Mn ore), Composts usually contain fairly low Mn levels. Most
a Saline soils do noica use Mn deficiency if they contain high enough to taJMn,
and composts with added Mn should prevent this problem. Crops differ
substantially in susceptibility to lime-induced Mn deficiency. Soybean and
wheat are well known to suffer severe Mn deficiency when oiher crops (e.g.
com) grown on the same soil have no Mn deficiency.
Besides the pH of ihe soil and the susceptibility of the crop, the native
Mn level of soils are important in whether Mn deficiency will be induced by
lime rich sludges or composts, In general, Mn concentration in soils increases
with increasing clay content. Besides coarse texture, a very important factor
in affecting loss of Mn from soils is height of the water table. Soils which were
submerged dunng soil formation have had Mn02reduced to Mn1' and leached
from the soil. Thus, coarse-textured, CoastaJ plain soils are often very
susceptible to Mn deficiency. In a long term field experiment with a single
1976 application of high rates of lime-treated anaerobically digested sewage
sludge applied to Galestown loamy sand at Beltsville, severe Mn deficiency
was noted in wheat and soybean grown in 1991 and 1992 (R.L. Chaney and
B.R. James, unpublished). .In previous years, corn had been grown and no
apparent deficiency occurred,
Lime induced Mn-deficiency has also become a problem in some .
cases when high metal sludges were used at such high cumulative rates that
the soils had to be limed to prevent metal phytoioxicity. Spotswood and
Raymer (1973) noted that crops on a sewage farm which also received a high
metal concentration sludge suffered Mn deficiency when lime wasapplied to
prevem Zn toxicity. In that case, the repeated heavy irrigation with sewage
caused depletion of soil Mn, increasing the potential for liming to induce
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460 Science and Engineering of Composting
deficiency (as was observed at sewage irrigated light textured soils on sewage
farms at Pahs, France, and Berlin, Germany; Doring, 1960; Rinno, 1964;
Rohde, 1962; Trocme et a!, 1950).
It seems clear that MSW-compost manufacturers need to consider
the potential of MSW-compost 10 induce Mn deficiency if the soils in their
marketing region are susceptible to Mn deficiency, and the crops commonly
grown include suscepuble species. The manufacturer could warn users of this
potential problem, or could choose to add Mri during corn posting to assure that
Mn defic iency would not occur. Research has not yet clarified the amount of
compdsi-Mn required to avoid Mn deficiency on suscepuble soils.
HEAVY METAL CONCERNS IN USING MSW-COMPOST
ON CROPLAND '
Because metals in MSW-compost are conserved in the soil-compost
mixture, application of-MSW-compost to cropland causes an increase in ihe
concentration of potentially phytotoxic heavy metals (Zn, Cu, Ni) in soils.
Many scientists have expressed concern about this simple increase in soil
metals, and have implied that this is a problem. As noted above, we believe
the potential for adverse effects of heavy metals should be the basis for
concern, not the simple presence of metals in soils. It is important that we
understand that metals in sludges and composts with low concentrations of
metals have not been shown to cause adverse effects, and that an improved
understanding of the chemistry of sludges and composts appears to explain the
low poteniial for phytotoxicity and phytoavailability of metaJs in low metal
concentration sludge and compost materials.
Proper approach to evaluate potential compost heavy metal
questions: Over 25 years of research have been conducted to better
understand the potential, for risk from heavy metals in sewage sludge applied
to agricultural land. During this period, a number of principals of "heavy
metal agronomy" have been identified. Foremost among these is the
recommendation from the W-170 Peer Review Committee Report (Page et
a!., 1989); In development of regulations, use results from "field studies with
municipal sludge instead of non-field studies with metal salts or pure organic
compounds:" This recommendation was made because research showed that
pot studies in greenhouses, metal sources other than sludge, or even studies.
on high contaminant concentration sludges were not valid for evaluation of
risks from sludges with low concentrations of these contaminants.
Many studies were conducted to determine the relationship between
plant uptake and tolerance of metals in pots vs. the field, and from metal salts,
metal salt amended sludges, and sludges of different quality (see Logan and
Chaney, 1983;Pagce;a/., 1987). Somesiudiesincludedcomparisonofplants
grown in pots inside and pots outside the greenhouse compared to plants
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; Chaney and Ryan 461
grown with equal sludge applications in the field (deVries and Tiller, 1978;
Davis, 1981). When sludge was applied in the field, much lowe; [(plant meial
concenLraiion):(soil metal concentration)] slopes were obtained than when
outdoor pots were used w ith the same soil; indoor pois had even higher slope,
about 3-10 fold higher than in the field. This is now understood in terms of
the differences between salts and sludge, and between pots vs. the field (see
also deVries, 1980), Pot studies overestimate metal phytoavailabiliiy be-
cau,se: 1) The indoor and outside environments differ in soil temperature and
water use patiems (the humidity microenvironment in a greenhouse is quite
unlike the field; in the greenhouse, transpiration is increased which increases
metal flow to the root by convection and transfer to leaves in the transpiration
stream); 2) In pots, the whole amount of fertilizer nutrients required to support
the growth of the test plants must be applied to a limited soil volume; this soil
volume has much higher soluble salt concentration which increases the
concentration of metals and diffusion of metals from the soil panicles to the
roots; 3) When ferulizers contain NH4-N, rhizosphere acidification in ihe
small volume of soil in a pot can increase metal uptake; and 4) In pots, the soil-
sludge mixture comprises the whole rooting medium, while in the field the
sludge is only mixed into the tillage depth (usually < 20 cm deep) and much
of the plant root system is below this'depih.
Perhaps the biggest source of difference among ihese incorrect
methods to evaluate sludge metals is the difference in uptake and toxiciiy from
metal salts vs. sludge-metals. In many studies, sludge or metals equivalent to
the sludge were added 10 the same soil, and crops grown. In many studies the
salts caused severe phytotoxiciiy, while the sludge caused yield increase.
Although many of these studies suffered from errors due to difference in pH
between the sails and sludge (added metal salts displace protons from the soil
and low. erpH), some had equal pH. For example, in the greenhouse pot study
of Korcak and Fanning (1986), equivalent metal salts or 224 Mg/ha of sludge
v,ere added to a number of soils with widely different properties; saltscaused
ph>ioioxicity 10 com on all soils, but sludge caused no phytotoxicity. Soil;
propcrues strongly affected metal uptake on the metal-salt-amended soils, but
had little effect on ihe sludge-amended soils, Some comparisons of metal-
salts and sludge were conducted in the field. For instance, Ham and Dowdy
(197 8) compared metal uptake by soybean when equivalent metals and sludge
were applied in the field, and found much higher metal uptake from the salts.
Although metals added as salts may approach the phytoavailabiliiy of sludge-
applied metals over time, the lack of other sludge constituents makes results
from study of additions of single metals of little value (Bell/James and
Chaney, 1991). . . •
Another pattern related to the effect of sludge metal binding proper-.
ties became apparent in the early 1980s. R.B.Corey (University of Wisconsin,
Madison) had predicted (at the 1980 annual meeting of the W-170 Regional
Research Committee) that sludge adsorption chemistry should control the
activity of free metal ions in the soil solution of sludge-amended soils after
-------
.462 Science and Engineering of Composting
reaching the sludge application rate which saturated the soil metal binding
sites (see also Corey et al,, 1981), Based on this model, Chaney « a/. (1982)
used orthogonal contrast analysis of variance to.analyze data from a long-term
study of leuuce uptake of Cd from sludge-amended field plots and found thai
the rate-squared term was highly significant. This indicated that useof simple
linear regression to evaluate data from sludge studies was in error. Subse-
quently, Logan and Chaney (1987) used plateau regression to evaluate these
data. Figure 1 shows several approaches to evaluate the effect of application
rate of a low Cd sludge on the uptake of Cd by lettuce (averaged over 1976
to 1983). The plateau regression predictions, and their 95 percent confidence
intervals are shown for each soil pH, as are the simple linear regressions.
These data c leajly demonstrate the over-estimation of Cd uptake when simple
linear regression is used to evaluate plateau response data. With time, other
. studies were eval uated and found to fit this curvilinear response pattern (Corey
et al., 1987; Change/ al., 1987),
Based on these understandings, researchers attempted to character-
ize the chemical aspects of sludge which made metals so much less available
to plants (phy unavailable) than were metal -salts. A review and interpretation
of this information was published by the Corey ei al. (1987) workgroup. In
short, the specific metal adsorption capacity (ability to selectively adsorb
heavy metaJs in the presence of 3-10 mMCa2+ present in the soil solution of
most ferule soils) of sludge persistently increases the ability of the soil-sludge
mixture to adsorb metals, thereby reducing the phyioavailability of sludge-
borne metals.- As noted below, because the sludge chemistry controls the
phytoavajlability of sludge-applied metals, plant uptake approaches a plateau
with increasing sludge .application rate rather than showing the usual linear
increase with increasing applications of metal-salts,
Another aspect of these data showing that sludge chemical factors.
reduce the phytoavailability of sludge metals is that it takes time for the
reacuons of metaJs'io reach their lowest "free energy" condition; by this we
mean thai by the time sludge metals are applied to soils, the metals have
reached strong adsorption sites in the sludge, greatly reducing their
phytoavailability compared to fresh additions of metal salts to soils. Soils and
sludges contain metal binding with a wide range of specificity for metal
adsorption; freshly added metals are bound to the population of all binding
sites, then slowly equilibrate to the strongest specific adsorption sites. Several
scientists evaluated the extractabihty and phytoavailability of sludge metals
when the metaJs were added to the sludge before anaerobic digestion, or after
digestion (Bloomfield and McGrath, 1982;Cunninghame/a/., 1975a, 1975b,
1975c; Davis and Carlton-Smith, 1981,1984). In each case, adding the metals
after digestion (immediately before application to soil) caused the metals to
be much'more phytoavailability than metals added during sewage treatment
or before sludge stabilization. However, metals added to sludge were less
phytoavailable than metaJ salts added to'the soil without the sludge. This
could result from the presence of high levels of many metals competing for
-------
Chaney and Ryan 463
CM
— O
MQ 6/6r/ '
Figure 1. Linear vs. plaieau regression analysis of leiiuce uptake of Cd from,
C Tins1,1, a.-, a fine sandy loam amended with 0, 56, 112, or 224 Mg dry heai-urated
sludge/ha, and pH adjusied to 6i2-6.5 with limesione (Hi pH) or uncontrolled (^5,5
in 1983) (Lo pH). Predicted responses extrapolated to 1000 Mg/ha to show
Lmp lie a i ions of the data. Results are average for 197 6 to 1983. Data points shown are
aiithmeiic means tone send, error; plateau regressions show predicted (dashed lines)
wrtn±95% confidence interval (dotted lines). Equations for linear regressions (solid
lines) are: Leiiuce Cd= 1.22+(1291 Rate (low pH); Lettuce Cd = 0.774+0.0900 Rate
(HighpH). Sludge applied in 1976 contained !3.4pgCd, 1330 pg Zn, and 83 mg Fe/
g dry weight (data originally reported in Chaney el at. [1982]). Small dashed line
shows the geometric mean simple linear regression slope for increased lettuce Cd on
all strongly acidic (pH<6) Held soils used in the CWA-503 final rule/over-estimating
effect of low Cd sludges.
-------
464 Science and Engineering of Composting
the suong adsorption sites. The weaker sites are filled and equilibration is
more rapid during sludge stabilization when, concenirations are higher
(compared to dilution with soil). Reaching the strongest binding sites should
take a long lime when meials saJts are added directly to soils.
The importance of metal adsorption by sludges was also seen when
researchers examined the relationship of pH to solubility of metals in sludges
or soil-sludge mixtures. In all heavy metal cation (Zn, Cd, Cu, Ni, Pb, Hg)
siudies, solubility increases with decreasing pH. Sanders and co-workers
found for each sludge and metaJ,'that as pH was decreased, some threshold pH
was reached below which metal solubility was sharply increased. They then
studied the effect of metal concentration in the sludge on this threshold-pH.
Adams and Sanders (1984) found that the higher the sludge metal concentra-
tion, ihe higher the threshold pH pointof increasing metal solubility (see also
Sanders'and Adams, 1987; Sanders et al., 1986). This can, readily be
interpreted in terms of filling the specific metal adsorpuon sites vs. sludge
meiaJ concentration.
These bodies of data on specific metal adsorption by sludge constitu-
ents is very important in understanding, sludge metal research. In studies of
ph> totoxinty of sludge-applied metaJs, it is now clear that phytotoxiciry to
sensitive crop species has only resulted when high metal concentration
sludges were used, or extremely low pH was reached: 1) When high
cumulative applications of low me taJ sludges (NO AEL quality) were applied,
and soil pH allov-ed to drop to near 4.5, phytotoxicity to soybean (Lutrick et
al., 1982) and rye (King and Moms, 1972) were observed; simple correclion
of so'il pH to near 6 completely corrected yield reduction; normally, good
agricultural practice requires thai soil pH be 5,5 for nearly all crops to avoid
natural Al and Mn phytotoxiciiy, of more strongly acidic soils; Mn and Al
contributed to or caused the yield reductions noted by Lutrick ei al. and King
and Moms; and 2) High metal sludges at lower cumulative applications
caused metal phytotoxicity which was not simply corrected by liming the soil
vMarkse/a/., 1980; Webber era/., 1981; Minnich era/. 1987). When sludge
Zn, sludge+MSW compost Zn, and ZnS04 were applied at equal Zn rates,
only ihe Zn salt caused phytotoxicity even when soil pH levels were made
equal by addiuon of sulfur to acidify the sludge and MSW+sludge compost
plots (Giordano et al,, 1975).
- Specific metal adsorption is involved in the effect of sludge metal
concentration on the phytoavailabi lity and bioavailability of sludge metals. It
had been apparent from many studies that sludges with higher metaJ concen-
trations could cause higher metal uptake by plants when equal amounts of
metals were applied (i.e., different amounts of sludge dry matter and hence
adsorption capacity v,cre applied), This was part of ihe plateau response data
set. Recently, Jing and Logan (1992) reported on the phytoavailability of
sludge applied Cd from many different sludges, where equal amounts of Cd
were applied in each pot,,- Crop uptake of Cd increased with increasing sludge
Cd concentration. This is explained in terms of the filling of specific Cd
-------
Chancy and Ryan 465
binding sites in the sludge; the population of Cd binding sites vary widely in
strength of specific Cd adsorption; as sludge Cd concentration increases, the
least strongly bound Cd is more phyioavailable. Similarly, when amounts of
metals required 10 reduce yields of barley or vegetables were determined with
salts in greenhouse pots, with mixtures of high metal sludges in pois in the
greenhouse, or with normal quality sludges in the-field, the salts and high
metals sludges caused phytotoxicity (Davis and Car lion-Smith, 1984), but the
normal quality sludges caused only yield increase (Johnson, Beckett, and
Waters, 1983).
One question of importance for use of sludge and MSW-compost in
sustainable agriculture is: "How long does the reduced metal phytoavailability
of sludge-applied metals due 10 sludge specific metal adsorption capacity
lasi7".. Some field plots have been studied up to 20 years after the last sludge
application. Other soils from long-term sludge or sewage farms have been
examined by basic studies in the greenhouse. The demonstration of persis-
tence of the "sludge effect" on metal sorption was well illustrated by the daia
of Mahler e\ at, (1987,1988a,1988b) in which Cd rich sludge orCdsalls'were
added to soils from long-term sludge plots, and a high Cd accumulating crop
grown. The slope of the crop response to the added sali-Cd or fresh sludge-
Cd was lov-er for soils with historic sludge application due to ihe increase in
metal adsorpuon capacity, of the sludge-amended soils (pH was not different
between treatments). All evidence available indicates that the specific metal
adsorpuon capacity added with'sludge will persist as long as the heavy metals
of concern persist in the soiK Although this effect strongly confounds
estimating the phytoavailabilily of Cd in different soils which received
different amounts of different sludges, it is clear that the specific metal
adsorption capacity added by sludge plays a very significant role in controlling
the phytoavailability of metals of concern regarding phytotoxicity or food-
chain contamination.
The inorganic pan of the sludge contributes much of the sludge-
applied specific metal adsorption capacity. As summarized by Corey el at
(1987), Fe, Al, and Mn oxides in soil and sludge exhibit specific metal
adsorption properties. As noted above, even though sludge organic matter is
oxidized o\er time, if soil pH does not fall, the ability of crops to accumulate
soil'metals is only decreased over lime. This indicates that the non-organic
matter adsorption sites are adequate to protect agajnst metals added in sludges.
Part of ihe sludge-applied specific metal adsorption capacity is due to humic
acids formed from sludge organic matter; interestingly, metals stabilize soil
humic acids against biodegradation. Further, in the long term, pan of the
added metals become occluded in Fe oxides (Bruemmer ei ai, 1986).
All these data from research on sludge vs. metal salts, and the effect
of sludge metal concentration on phytoavailability of sludge-apphed metals
(including the plateau response finding of Chancy el ai, 1982) led the Corey
et al. (1987) workgroup to conclude that specific adsorption of metals by
sludge surfaces would normally be the controlling factor in metal
-------
466 Science and Engineering of Composting
phytoavailabiliiy in soil-sludge mixtures. They concluded that a plateau
response would be the expected pattern of response, and that some sludges
could be so low in metals, and so high in meial specific adsorption capacity
that addition of sludge could actually reduce metal uptake by plants. This
response has been observed for Cd with several studies in pots and field. This
model integrates data from many studies which initially appeared to offer
conflicting results, Sludge-applied Cd is additive, but aJong a'plateau
response curve rather than a linear response curve.
Very similar conclusions about sludge constituents binding metaJs
could have been drawn from the animal literature with sludge or compost.
amended diets. ,In numerous studies to assess the risk from sludge contami-
nation of diets of grazing livestock, different livestock species were fed
sludges or composts for prolonged periods. Sheep and cattle aie.notoriously
sensitive to excess dietary Cu, and the sludges added as much as 5-10 times.,
higher Cu than required to kill cattle or sheep if Cu salts axe mixed into
practical diets. Surface application of high Cu swine manure to pastures for
sheep did not cause Cu toxicity (e.g. Poole ei ai, 1983; Bremner, 1981,).
Moreover, depletion of liver Cu reserves or even frank Cu deficiency was the
common result unless sludge Cu concentration was above 1000 mg/kg (Baxter
eial., 1982, 1983; Beruand el at,, 1981; Decker el at., I980a; Sanson ei at.,-
1984). Thus, the bioavailability of sludge meials was very low compared to
metal salts (based on both toxicity and on liver metal concentrations). Similar
results were seen for bioavailability of Pb and Cd in ruminants fed sludge, and
for Cu and Cd in non-ruminants fed sludge (Logan and Chancy, 1983).
Another source of over-estimation of sludge metal phyioavailability
has resulted from high rates of application of sludge in field research studies
Often, high rates are applied at one time to apply high cumulative rates of
sludge in a short time rather than applying N-fenilizer rate sludge application
raies for 20-50 years, In numerous studies, crop uptake of Cd and other metals
has been followed for a number of years after application ceased. Crop uptake
fell by as much as 80-90% compared to the last year sludge was applied (e.g.,
Bidwell, and Dowdy, 1987; Chang.ei at., 1982; Hinesly etal,,, 1979). One
significant cause of this pattern is the biodegradation of sludge organic matter
When high rates of sludge application are used, the biodegradation rate can
be so high that anaerobic biodegradation by-products are formed in the soil.
and these increase metal diffusion from soil panicles to plant roots. This is
well illustrated by the study of Sheaffer et at. (1981) reported in Logan and
Chaney (1983).- On plots treated with 112 Mg/ha of a higher metal concen-
tration sludge, soil temperatures were varied. Immediately after mixing
sludge and soil and imposing soil temperature, radishes were sown. At high
soil temperature (which hastens biodegradation) severe phytoioxicity re-
sulted in stunted radishes, no edible globes, and high enough Zn and Cu in
leaves to indicate phytotoxicity (>1000 rrigZn/kg.and>60 mgCu/Vcg); in the
second year and 6th year after the sludge application, radishes were again
grown but no phytotoxiciiy resulted. In year 2, soil pH on the sludge treated
-------
Chaney and Ryan 467
plots had dropped, and pH was corrected to the pH of the control soil before
cropping in the 4th year. Not only was no phytotoxicily seen in either year
2 or year 6, but also foliar Zn and Cu were appropriate for healthy radish; and
normal radish globes resulted. Thus, rapid biodegradation of higher ratesof
sludge can cause temporary increase in sludge metal phytoavailability and
over-estimate the risk of sludge: metal phytotoxicity. This error would be
expected to be greater for higher metal concentration sludges.
These conclusions should have been apparent to the scientific
community earlier than 1980, but concern about metal enrichment of soils
caused great caution by researchers. Not only are NOAEL sludges and
composts able 10 be used as fertilizer and soil conditioner with very low risk
of phytotox icity or excessive food-chain transfer of metals, but these sludges
has e also been found to be able to correct (remediate) soils which were already
metal toxic (Gadgil, 1969; Bergholm and Steen, 1989), although sludges are,
clearly more effective than MSW-composts in correcting severe phytotoxic-
iiy from soil metals. Metal phytotoxicity from mine or smeller wastes or
corrosion residues were corrected in a number of siudies (increase in soil pH
was not the basis for coneciion of loxiciiy). This 100 shows the specific metal
adsorption capacity of sludges can control phytoavailability in the soil-sludge
mixture. ,
Thus, only data from field siudies of low conLaminaniconcentraiion
sludges or composts are appropriate for development of regulations for these
maienals. The lack of adverse effects from use of NOAEL sludges, and even
lo^er concentrations of metals in MSW-composis, should be considered a
valid basis for development of risk-based quality standards forMSW-compost
•products which could be marketed for general use.
?•
Can Cd in MSW-compost cause risk to the human food-chain:
Since 1969 when the itai-itai disease of Japanese farm families was
attributed to consumption of rice containing high levels of Cd, scientists have
expressed high concern about food Cd and about Cd contamination of soils,
However, we now knov, thai this concern was based on ignorance of the factors
v.hich control risk to humans from soil contajning increased levels of total Cd
(Ryan ei at., 1982). McKenna and Chaney (1991) McKennae; al. (1992), and
Chaney (I990b; 1992) recently summarized new concepts of the food-chain
risk from Cd in land-applied MSW-composi and sewage sludges. Excessive
dietary Cd can accumulate over one's lifetime in the kidney cortex and cause.
renal tubular dysfunction (Fanconi syndrome), a disease in which low
molecular weight proteins are excreted in urine. Although farm families in
Japan experienced this disease after prolonged consumption of rice grown on
highly Zn+-Cd contaminated paddies, the properties of rice and flooded soils,
and malnutrition in Japan before, during, and after World War II,played very
importam roles in allowing high transfer of soil Cd 10 kidneys. The rice grain
v. as greaily increased in Cd but its Zn concentration was not increased because
ZnS was formed in flooded soils; crops grown in aerobic soils usually, have a
-------
468 Science and Engineering of Composting
greater increase in Zn ihan Cd in edible crop tissues,
In another case, New Zealand oyster fishers and their families
consumed high amounts of Cd-rich oysters, ingesting nearly as much Cd as
the Japanese who suffered Cd disease. However, because oysters or the New
Zealand diet are not deficient in Ca, Zn, or Fe, these persons did not suffer
tubular proieinuria (Sharma el a!., 1983), and did not accumulate high
amounts of Cd in iheir kidneys (McKenzie-Pamell and Eynon, 1987; McKenzie
eial,, 1988). Thus,ihebioavailabilityofCd in different foods or diets can be
quite different. In two locations (Shipham, UK [Strehlow and Barluop, 1988]
and Stolberg, FRG [KOnig el al, 1991]) vegetable garden soils were highly
contaminated with Zn and Cd from mining wastes, which caused garden crops
to be Cd enriched; yet no tubular proieinuria resulted in long-term residents
who consumed high amounts of garden crops.
This difference between effect of Cd in rice and Cd in other foods is
evidence that Cd has different bioavailability depending on the presence of
differeni nutrients in the same food, and perhaps depending on.the chemicaJ
speciation'of Cd in thefoods. In studies of the bioavailability ofCd in sludge-
grown food, Chaney eial, (1978a; 1978b) fed lettuce and Swiss chard (grown
on both control and sludge amended soils) to mice or guinea pigs, respectively.
Chaid had up to 5-fold higher Cd when grown on strongly acidic sludge
amended soils, but caused no change in kidney or liver Cd concentration.
When grown on digested sludge-compost amended soil, leUuce had 2-umes
the Cd of the control crop, yet caused significant reduction in kidney Cd
compared to the control. Thus, Cd concentration in crops is not related to the
risk of Cd from-those crops because the bioavailability of the crop Cd can be
affected by other elements in the sludge or compost.
In order to estimate the maximum allowable, increase in Cd in garden
crops, Chancy eial. (1987) extended the dietary models of Ryan ei al (1982)
relaung Cd in lettuce vs, Cd in the garden foods part of the diet grown on a
Cd ennched soil (Table 3), In strongly acidic soils which cause increased Cd
levels in foods, the'relative uptake of Cd was fairly consistent (Chancy e'r a/.,
1987). By multiplying the dry weight of each food group by its relative'
increased Cd uptake on acidic sludge amended soils,one can estimate that diet ,
Cd will be increased 1.67 ug/day when lettuce is increased by 1 ug/g dry'
weight (100% of garden foods grown on the amended soil). [As discussed in
Ryan and Chancy (1992), it is extremely unlikely that individuals will grow
a substantial fraction of their garden vegetables for a lifetime, always using
strongly acidic soils, and always having a poor quality diet which favors Cd
absorption.]
Cd in MSW-composts appears to be even less likely to cause food-
chain Cd problems than can the Cd in sewage sludges because theCd:Zn ratio
of MSW-composts is about 0.005 compared to the 0.010 of domestic sludges
(Table 2) (Chaney, 1992). For many years, Chancy has noted that the Zn
which accompanies Cd in sludge and compost provides further protection
against excessive dietary Cd (see Logan and Chancy, 1983; Chaney, 1990b;
-------
Chancy and Ryan 469
MeKenna and Chancy, 1991). The worst-case scenario for food-chain Cd risk
(Pathway IF) has always'involved acidification of the amended soil to very
acidic pH which promotes Cd and Zn uptake by plants. Besides interactions
of Zn and Cd which reduce plant Cd bioavailability, another basis for the
protection from Cd risk due to Zn in sludge and compost is that Zn
phyiotox icily occurs in crops if leaf Zn exceeds about 500 mg/kg. thus limiting
yield of Cd-rich foods, Poor yields and visual symptoms of problems such as
chlorosis1 (in more sensitive crops such as bet and lettuce) alert the gardener
16 the need 10 identify the reason for the toxicily, Thus, in sludge- or compost-
amended soil, Zn becomes a "natural" factor which limits Cd risk to gardeners
who consume a substantial portion of iheir diei grown on amended soils.
Either they maintain reasonable soil pH for vegetable crop production (which
protects them from increased crop and diet Cd), or eventually, when ihe soil
pH drops enough to allow high Cd uptake and potential Cd risk, Zn
phyiotoxicity reduces yield and hence reduces potential for consumption of
Cd-enriched garden crops.
Table 3, 1991 Home garden dietary Cd risk assessment, using lifetime die^
model, and relative Cd uptake among garden crops (Chancy, 1990b; Chancy
•eta! , 1987), . .' '
FOOD GROUP Food
Intake ;
g DW/d
Leafs Vegetables '1.97
Potato 15.60
Root Vegetables 1.60
Legume Vegetables 8,75
Garden Fruits 4, 15
All Garden Foods
Relative
" Cd Uptake
Lettuce=l
0.536
0.020
0.096
0.010
0,014
Increased Diet Cd (ug/d)
if lettuce Cd increased
by 1 ug/g DW
1.056
0.312
0.154
0.088
0.058
1.67
Clear evidence of this protection is found in Chaney's (1992)
analysis of daia published by Baker and Bowers (1988). They grew lettuce
in gardens contaminated by Zn-smelier emissions over the last century,
Garden soil Cd reached as high as 100 mgAg, and Zn, 10,000 mg/kg-
Gardeners added limestone and livestock manure to their soils to reduce the
effect of soil'Zn and many grow a wide variety of garden crops. As pan of an
effort to assess need for remediation under a Superfund "Remedial Investiga-
tion", Baker and Bowers grew Romaine,lettuce in many gardens. Chancy
(1992) calculated the Cd:Zn ratio for each garden, and designated each point
on Figure 2 as belonging to one of three classes of Cd:Zn, < 0.010, 0.010-
0,020, and > 0.020, It is clear ihai all gardens with Cd:Zn < 0.010 produced
-------
470. Science and Engineering of Composting
leuuce which would increase diet Cd no more than about 10 pg Cd/day. This
was for 100% of garden crops grown on the acidic garden rich in Cd-t-Zn for
50years,anextremely unlikelyevent. MSW-composthasCd:Znabout0.005,
which indicates that the likely worst case for gardens with high rates of MS W-
compost would beabout 5 pg Cd/day. Present U.S. daily intake of Cd is about
12 pg/day (lifetime diet model) (based on Adams, 1991). The Risk Reference
Dose (RfD) for Cd is 70 pg/day, with a difference between RfD and normal
intake of 58 pgyday (if lettuce were increased about 35 pg Cd/g DW [(58 pg/
day) -i- (1.67 ug/day if lettuce increase by 1 pg/g) = 34.7 pg/g allowable
increase in lettuce Cd], 100% of garden vegetables would be increased by 58
pg/day). The RfD is designed to protect the highly exposed persons with
sensitive kidneys from lifetime consumption of excessive Cd. Of course, the
protections -from :Zn reducing Cd bioavailability in sludge-grown crops
discussed above would also occur, making this small increase in crop Cd of
even low'er significance to humans.
Researchers have worried about Cd in sludges and composts since
the 1970's, and conducted much research on this subject. Although we still
conduct research on crop Cd bioavailability to settle other specific questions
about risk from Cd in foods, we now conclude that uncontaminated sludges
and MSW-composts comprise no Cd risk even in extremely worst-case risk
analysis scenarios. The improvement in our understanding of soil Cd risk
during the last few years, ending with the more valid soil Cd:diet Cd model
summarized here, strongly supports this conclusion. The low bioavailability
of crop Cd noted above supports this conclusion. And the new evidence on
natural'limitation of increased diet Cd due 10 Zn which accompanies Cd shown
in Figure 2, supports this conclusion. Henceforth we should no longer
consider that Cd in uncontaminated (NOAEL sludge) sludges or MSW-
composts compnse any food-chain Cd risk to humans consuming Western
dieis.under any conditions.
Evaluation of the potential for Pb risk to children who ingest MSW-compost:
The risk from Pb in compost-amended soil or MSW-compost
products ingested by children provides the basis for limiting compost Pb
concentration. This limit will require management and planning in the MSW-
compost community. Research on lead poisoning of children has shown that
children live in a dusty environment. We and our pets and environmental
processes like mud on shoes and dust blowing in a window, bring dust (soil-
derived environ mental dust) into our homes. We bring soil into our homes on
our shoes, it dries, is crushed, and becomes pan of the housedust pool, When
automotive exhaust was high in lead, children got about four times more lead
from the dust they'ingested than from the inhalation of Pb in air1 directly, The
dust was always more important, it just took us decades to understand the role
ofPbindust(US-DHEW, 1991).
We have all heard about Pb poisoning of children from paint chips.
However, other sources, such as.soil ingested by children, can be a significant
-------
Chancy and Ryan 471
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472 Science and Engineering of Composting'
source if the soils are highly con laminated. House side soil cancontaJn uptc
57c lead (50,000 ug Pb/g) around old painied houses (Chancy and Mielke
1986; Chaney,' Mielke, and Sterreu, 1989), whereas there are backgrounc
levels (10-20 ug Pb/g) in soils around newer houses.
All children ingest some soil by norm aJ hand-to-mouth play (CaJabrese
etai, 1989; Calabrese and Stanek, 1991; Davis, 1990;.Binder ei a!., 1986.
Clausing ei ai, 1987; Van NVijnen et a!., 1990; Stanek and Calabrese, 1991).
But when we consider Pb risk 10 children eating soil, we must consider pica
children because these children consume the most soil (pica is the consump-
tion of non-food items). Many of these studies of middle class children found
children with pica for soil. Thus, we need to protect pica children from sources
of Pb which could provide excessive bioavailable Pb if ingested.. As long as
we protect thai child, everybody else is protected.
An example of the clearest demonstration of the risk to children from
Pb in dusi was found at a Pb-battery recycling factory in Memphis, TiN (Baker
ei ai, 1977), At this factory, the workers did not change their clothing and
shower before going home (as since has been required by OSHA). They
carried highly contaminated smeller dust into their homes. The children of
the smelier workers were shown to have lead poisoning but their neighbor's
children did not, Blood Pb.concentration in the workers' children was related
io the concentration of lead in the house dust of their home. Most of these
children had very high blood Pb levels, due to the industrial dust exposure, and
required medicaJ treatment to remove Pb from their bodies. This result
illustrates the principal that if you bring a high-lead dust or product into the
home, n could be a risk io children who have high ingesu'on of dust. Other
research, summarized in Chaney andMielke (1986) and Chaney eial. (1989)
has shown thai for children exposed to Pb-rich dusts, the blood Pb concentra-
tion rises quickly after the children start crawling, reaches a peak at about 18
months with the peak of hand-to-mouth play, and declines until lower blood
Pb levels are reached by about 4-6 years of age when mouthing generally
reaches low levels.
Another reason we have such concern about Pb in children is the
demonstration over the last decade that blood Pb levels above 10-15 ug/dL (dl
= deciliter = 100 mL) can significantly reduce IQ and learning ability in
children. This .phenomenon has been labeled "neuro-behavioral impair-
ment", and appears to result from Pb interference with nerve growth during
brain development in children. Adults are much less sensitive to blood Pb
because they are not undergoing brain development. Previous limits for
acceptable blood Pb were 25 ug/dL, but the Center for Disease Control has
now lowered the recommended maximum blood Pb concentration to 10 ug/
dl_ (US-DHEW, 1991). If blood Pb is above this level, parents and public
officials are advised to identify the source(s) of Pb, reduce the Pb exposure,
and to improve nutrition to prevent Pb absorption, etc.
Because of the reduction of Pb in automotive emissions, and
reduction of Pb in food due to change in canning technology (both food and
-------
Chancy and Ryan 473
automotive emission Pb levels have decreased nearly 10 fold in the lasi 15
years) (Bolgerefa(., 1991), median blood Pb level sin suburban children have
fallen from aboul 20-25 ug/dL in 1970 to about 3-4 ug/dL in 1990. With the
normal variance (and varied amounts from Pb in plumbing systems, etc.),
some suburban children exceed the 15ug/dL. Butover 50% of children in the
center city exceeded 15 ug Pb/dL limit (ATSDR, 1988). Children exposed to
high levels of soil and dusi Pb have been found to have high blood Pb in
numerous cases (reviewed in Chaney and Mielke, 1986; Chancy, Mielke, and
Sierreti, 1989).. In other cases, social factors or soil chemical factors aJiered
ihe exposure or bioavailability of the soil Pb and little or no increase in blood
Pb was observed even with soils containing 5000 mg Pb/kg (Cotter-Howells
and Thornton, 1991).
In order to better understand ihe hsk from Pb in soil, feeding studies
were conducted with rats. Previous work summarized in Chaney et al. (1989)
showed thai less Pb was absorbed from soil than from soluble Pb salts or palm
,chip powder. Thus, rat feeding studies were conducted 10 determine the
bioavailability of lead in garden,soils. They found 1) compared to Pb acetate
(a soluble Pb salt considered to be 100% bioavailable in diets) added to
purified diets, bone Pb was increased only 53% as much in a diet containing
5% control low Pb soil as in the diet without soil (ihe added diet Pb and soil
v.ere equivalent to adding a soil with 1,000 ug Pb/g dry soil); and 2) If the rats
v-ere fed urban garden soils with about 1000 pg Pb/g, bone Pb was only about
20% as high as when equivalent Pb acetate was added to the control diet, while
one soil with 10,200 ug Pb/g caused bone Pb to be 707c as high as with Pb
acetaie. So we have to consider lead in soil as being partially bioavailable.
We now interpret these findings as indicating ihat soil Pb bioavailability
increases with increasing soil Pb concentration because of weaker Pb adsorp-
tion by the soil at higher Pb concentration (Chaney ei al., 1989).
Besides the effect of compost chemical properties on ihe bioavailability
of Pb in compost, new findings on the effect of "soil dose" (g soil ingested per
day) on absorption of soil.Pb are also very important in assessing this risk,
Based on our model of sludge/compost chemistry controlling the activity of
free me Lai ions in the equilibrium solution, we would expect that as the amount
of soil ingested increases, blood Pb concentration should approach a plateau
because soil is present to adsorb soil-Pb in the intestine. Because adsorption
controls Pb solubility, the solution concentration of Pb should be nearly
independent of theg soil/mL of intestine contents. In short, this is the linear
versus plateau response concept we found with plant uptake of Cd from sails
vs. from sludge. This concept had not been tested until November 1990, when
results were reported by Freeman et al. (1991). They found that lead acetate
in purified diet caused a huge smooth increase in bone and blood Pb, but two
different soils with up to 3,000 ug Pb/g.caused tissue Pb to increase up to a
plateau, far below that from equal Pb from ihe Pb acetate (Figure 3). This work
says soil Pb has both a low bioavailability and a non-linear or plateauing dose-
response, Thus, the pica child is protected much more than we previously
-------
474 Science and Engineering of Composting
believed because soil continues to adsorb Pb in the intestine and reduces,
absorpuon of Pb into blood.
The effect of exposure to high soil Pb on blood Pb of individual
children is highly variable, and appears 10 be related 10 social, nutritional,
beha\ioral, and soil chemical factors. Pb in mining soils appears 10 have lower
bioavailabiliiy than Pb in urban dusts (Steeleer al., 1990; Freeman etal., 1991;
Davis ei al., 1992; Ruby ei al., 1992). In particular, the least soluble known
compound of Pb in soil's is pyromorphite [(Pb5(PO4)3Cl],and thiscompound
has been found in the'weathering products of galena (PbS) in mine waste
contaminated soil, Couer-Howells and Thornton (1991) report low blood Pb
levels in children living in an area with soils (about 5000 mg Pb/kg) derived
from Pb mining wastes. High levels of soil phosphate may be required to
facilitate formation ofpyromorphiie from other forms of soil Pb.
Bioavailabiliiy of Pb in sludge and compost:
Because Pathway 2F is most limiting for compost-Pb, and because
human feeding studies with Pb-rich soil or compost have not been reponed,
we. musiconsiderihe available information on bioavailabiliiy of Pb in sludges
and compost. Studies1 have been conducted to assess the bioavailability of
metals in many different sew-age sludges ingested by livestock. In many of
these studies, no increase was found in bone Pb under conditions relevant to
pica children (Decker eial. ,1980), Their studies involved sludge compost that
had215ugPb/gdry weight, at 0, 3.3 and 10% of diet for 180 days. With this
sludge compost, there was no significant change in the indicator ussue lead
levels even though the fecal analyses show that the animals ingested greatly
increased amounts of Pb (Table 4). However, in comparable studies by
Kienholz ei al. (1979), tissue Pb was significantly increased by ingesting 12%
of a sludge containing 780 ug Pb/g (Table 4).
One laboratory conducted cattle feeding experiments with amaterial
similar to MSW-compost, in the early 1970's. UUey ei al. (1972) fed 20%
"digested garbage" and found that Pb accumulated in kidney and liver.
Johnson ei al (1975) fed 17.5% compost (prepared from pre-separaied MS W
using the Fairfield digester (containing about 152 mg Pb/kg DW), This
experiment found a small increase in Pb in liver and kidney, but the
significance was noi evaluated; bone Pb is a much better indicator of absorbed
Pb during chronic feeding studies (this compost contained low Fe and P, which
may have allowed Pb absorpuon to be higher than found with typical sewage
sludge materials), These studies were conducted at a time when Pb analyses
were less reliable than those of today, and the mixed diet Pb concentration does
not agree with the compost Pb level and amount of compost in the diets.
Unfortunately, bones (the best indicator of chronic Pb absorption) were not
analyzed. Interestingly, there has never been evidence of Pb accumulation in.
animal fat even when diets are high in Pb. However, Johnson et al. (1975)
reported a significantly higher level of Pb in fat (<2.0 in control vs. 3.58 ug/
g F\V in the garbage diet). This indicates they suffered Pb analysis problems
-------
Chancy and Ryan 475
b/brf 'qd
m
CN
CN
O
O
CN
ID
o
in
in
CN
O
o
o
in
in
CN
o o o o o o o o
CD
CD
_Q
QL
CD
CD
m CD
13
CO
D
CD
Figure 3. Effect of increasing soil dose (g soil ingesied per day) on response..
of Pb in bone of rats fed two soils and Pb acetate for 30 days (Freeman ei ai,
1991). Statistical analysis indicated thai bone Pb in the soil fed animals
approached a plateau with increasing soil dose.
-------
476 Science and Engineering of Composting
common 10 ihai era, Thus, these studies are not reliable evidence that Pb ir
MSW-composts comprises a risk to children. We believe that Pb in the
colored waste paper fed by Heffronf/a/. (1977)iscomparabletothe "digestec
garbage" studies of Utley and Johnson. Heffron ei al fed 23% colored paper
(538 ppm Pb) to sheep for a long period, and found increased Pb in tissues
which accumulate Pb (liver, kidney, bone), but not in other tissues.
Based on all the available research involving ingestion of sludge or
compost (grazing or controlled feeding studies), our best judgemeni now is
that limiting sludge and compost products to 300 ugPb/g dry weight will aJlow
adsorption of lead by the compost material to be strong enough so that it does
not significantly contribute to blood lead increase, even for the pica child (see
Table3)(ChaneyandRyan, 1991). WebelievethatthePbadsorptioncapacity
(due to Fe oxides and organic matter), Ca, and phosphate of sludges can
strongly bind Pb and reduce Pb absorption by animals which ingest sludges
or composts, Increasing Fe (and possibly increasing P) in MSW-composts
may further reduce bioavailability of compost Pb, although Pb levels in most
MS W-composts:are low enough that compost Pb comprises insignificant risk.
Because present MS W-composi prepared from MSW separated at a.
central facility often contains about 200-500 mg Pb/kg dry weight, there will
need 10 be an improvement in Pb diversion from the compost stream. Old
painted wood, Pb-batteries, Pb caps from wine bottles, bullet residues, etc.,
must be diverted to household hazardous waste collections rather than be put
in the MS W, This will require extensive education efforts. Cessation of using
Pb-soldered cans for foods has reduced one source of Pb compared'to 1980,
but discarded electronic equipment has lots of solder which can be leached
during hauling and separation. Some central separation facilities produce
MS W-compost with < 300 mg PbAg. Thus, it may not be necessary to require
pre-separauon of the compostable or "green wastes" at the home in order to
allow production of acceptable quality MS W-compost for marketing.
Evaluation of potential food-chain risks through mushrooms produced on
media containing MSW-composl:
Commercial mushrooms are usually produced on special "mush-
room composts", and these have been considered one possible market for
MSW-composi. Some research has been conducted to determine if mush-
rooms grown on media which include MSW-compost or sludge cause high
transfer of metaJs to edible mushrooms. Some mushroom species accumulate
Hg or Cd to concentrations higher than the media on which they are grown.
Uptake of Hg by vascular plants and transport to edible plant tissues is so small
that diets are not enriched in Hg when soils would provide appreciable
bioavailable Hg to animals which ingest soil. Thus, the unusual Hg food-chain
of compost -> media -> mushrooms •> humans requires consideration.
-------
Chancy and Ryan 477
Table 4. Effect of ingesting sewage sludges, composts, or similar materials
with different properties on the concentration of Pb in bones of livestock.
Study Sludge Pb Concn. Sludge
Source in
1.
2.
3
3.
4
4
5,
6,
FL Collini
FL Collini
Denver
Denver
Washington, DC
Washington, DC
Lai Crucei •
Chicago
sludge Ji diet
mgAg
466
387
780
780
215
215
150
%
11.5
12.0
4.0
12.0
3.3
10,0
7.0
Dietary Pb Duration
COHL Tett Fed
-mfc/kg DW-
0.86
1,8
0.6
0.6
6.0
6.0
56.6
50.0,
26.
77.
11.2
19.9
+ 10.5
diyi
106
270
94
94
180
ISO
1440
Bone/Liver Pb
Control +Sludge
•-•ma/kg DW
B
B
B
B
B
B'
L
L:
:5.0
: 1,6
: 1,
: 1.
:3.7
•3-7
; .
. 7,2
<-3
4.
11,
4.7
3-4
..
• • •
•
•
NS
NS
NS
NS
Added after W. 1,70'Drocesi.
7.
8.
9,
10.
11.
12.
13.
14.
15.
16,
17,
18.
19.
20.
21
22
23,
24.
25
26,
WSSC, MD
WSSC, MD
WSSC, MD'
WSSC, MD
WSSC, MD
WSSC, MD
Pensacola
Pensacola
Chicago
Melbourne 56-24
Ohio
Fairfield
Furfield '
Chicago Dig
La: Cruces
Chicago
Netherlands
Netherlands
Colored Paper
Glenfield
190
185 '
380
250
257
215
397
397 '
774
l(soil)
557
163
169
937
'150 •
260
7
165
514
254
3.5
9,3
3,8
3.2
3.0.
1.0 ;•
2.7 -
5.2
6.0
<1,
22.0
17.5
3.5
50.!
7
10.0
23.0
4,3
4,3
5.6
56
6.0
6.0
08
0.8
1,4
34
45
4.8
3.6
4.
1.5
2.5
1.1
•1,1
9,07
• Bone or liver Pb concentration significantly
1,
Johnson ei al. (1981)
also by Boyer ei al,.
2.
3,
4.
Baxter ei at.
Kienholz ei
Decker ei at
(1982),
. Hereford steers
1981).
Cows
and steers.
120
22.4
192
11.2
13.6
74
11,0
20.5
40.0
12.
3.8
39.2
35.3
8.
+ 5.2
130.
8.0
13.0
138.
8.74
150
150
200
200
200
200
168
168
141
365
700
140
91 ,.
>1000
730
63
840
90
124
1800
B
B
B
B
B
B
L:
L:
L:
L:
L:
K
L:
L:
B
B:
K
K
K
B:
K
•5,7
;5,7'
4.1
4.1
•12.1
.12.1
0,32
0.32
0.10
0,93
0.40
•0.42
0.62
3,9
7,4
4.4
4.4
14.8
12.6
0.31
0.49
0.26
DW 1.12
ww 0.52
ww 0,72
w>v 3 96
<0.50 ww 1 60
1.8
21
;0.00
0.66
:026
2,6
:0.99
DW 0.6
DW 18,
w^OOO
ww 0,42
FW. 0,31
DW 19.0
DW 1.25
NS •
NS
NS
NS
NS
.NS
NS
NS
«
NS
NS
•
•
NS
NS
NS
NS
•
NS
•
*
increased by sludge ingestion.
. Selected samples analyzed
al. (1979). Fecdloi steers.
.(1980).
high in Fe and CaCO
5.
6.
Smith ei al.
Cows
j'
(1985) Sheep.
Harden ei al (1981).
.calves, and steers. Composted
No significant change of
Pbinl
sludge,
iver.
Foraging sows,
-------
478 Science and Engineering of Composting
Soil Pb in 504 mt/ha plot =131 mg/kg. while control plot soil was
37.7 mg Pb/kg. Feces were 7.9 and 41.7 mg Pb/lcg FW in March. Bone not
analyzed, but liver and kidney showed no significant change in tissue Pb.
7,8 Decker el al. (1979). Cows, calves, and steers graced on pastures with
spray applied sludge every 4 weeks; 7 is for sludge applied 21 -days before
grazing; 8 is for sludge applied 1 day before grazing. In the 1-day treatment,
high sludge Fe (11 %) caused induced Cu deficiency and severe toxicity and
weight loss, with higher liver Pb. Dietary sludge and Pb estimated at 50% of
fecal concentrations.
9-12 Decker et al. (1979. 1980a, 1980b). Cows, calves, and steers grazed on
pastures with spray applied sludge every 4 weeks (Nos, 9,11) with cattle
entering the paddocks 21 days after sludge application. Alternatively,
sludge compost was lopdressed on the pastures intermittently to provide
adequate N (Nos. 10, 12). In the second year of the study, compost was
applied only once because of residual N release.
13-14. Bertrand et al. (1980). Bahaigrass pastures spray applied repeatedly
during grazing season, 9 (No. 13) or 16 (No. 14) times. Blood, liver and
kidney Pb not increased by sludge application.
15. Bertrand et al. (1981). Chicago heat dried activated sludge mixed into
practical diet for steers.
16. Evans et al. (1979). Cattle grazed pastures which had received sewage
from Melbourne, Australia, for about 60 years. Soils had accumulated
high levels of me La Is in surface 2-5 cm. Cattle continuously grazed on ,
the pastures.
17 Reddy et al. (1985). Dewatered sludge surface applied in pastures, and
cattle grazed about 30 days later. Much less sludge ingestion than from
spray-applied sludge in other studies. Blood Pb was significantly higher
on sludged farms, 0.43 vs. 1.21 ug/dL in cows, but not calves; kidney
. Pb but not liver or blood Pb was sig. higher in calves; bone, kidney and
liver Pb unchanged in cows.
18. Utley et al. (1972). Fairfield "garbage digest" for 5 days, then dried
and pelletized. Fed to beef steers and cows.. Poor analysis. Report
significant increase in Pb in kidney and liver; no bone analysis. Milk
analyzed, but no Pb detected.
19. Johruon et al. (1975). Fairfield "garbage digest" fed to beef cattle for
91 days. Poor agreement between direct analysis of garbage (140 ppm .
Pb) and garbage as pan of feed (198 ppm Pb). Fat was reported to be
sign, increased in Pb (<2.0 vs. 3.58) in contrast with any other study of
Pb at chronic doses. Kidney reported to also be sig. increased.
20. Fitzgerald et at., 198S. Cows grazed up to 8 yr on pastures with spray
applied or incorporated Chicago fluid digested sludge. Liver, kidney,
and bone not increased in Pb.
21. Sanson et al.. 1984. Breeding ewes fed complete ration ± 3.5%
irradiated sludge for 2 yr. No changes found in tissue Pb levels. No
adverse effects of sludge in diet.
22. Osuna el al., 1981. Fed 50% Chicago dried activated sludge to weanling
swine for 63 days, compared to control and 79 ppm Cd as salt.
23. Vreman et al.t 1986. Cows fed salts v»,*|udge in indoor management
-------
Chaney and Ryan 479
vs. 8.0 ppm Pb. Few replications. Sludge caused smaller increase in
kidney Pb than did PbOAc [ 1,19 ug Pb/gFW (salt), 0.66 pg Pb/g
(sludge,)] . •
24 Veen and Vreman, 1986, Lambs fed abom 1100 g concentrate ind 225 g hay
DW for 90 days in an enclosed environment. Sludge included in concentrate
it iQ%for42day$,andihenreducedlo5% for the duration, Cain not reduced
by sludge addition.
23. Heffron ei al., 1977. Colored paper from newspapers and magazines
fed at 23% of practical diet to sheep for 124 days. This could be
considered "uncomposted" MSW, similar to the poorly composted
Fairfield compost used by Utley el al. (1972) and Johnson et al. (1975).
All Pb accumulating tissues increased (control diet/colored paper diet):
Blood, 0.10.7 pg/gDW; kidney, 0.85/7.6 JJ|/|DW; liver. 0.45/5.0 ug/gDW.
26. Ross and Short, 1990. Managed to produce f*t lambs for 3 yr with 37.5
Mg/ha sludge DW applied each year. Details of waiting period not reported.
No adverse effects on ewes or lambs. Lamb kidney also significantly
lower on sludge amended paddocks, Daia not used due to internal
disagreement:
27, Beau'douin el al. (1980), Tissue Pb results varied in no pattern, with
control 2 mg Pb/kg and sludge fed swine have <0.0l mg Pb/kg in some
tissues, and reversed in others.
28; Cibulka et al. (1983). Tissue Pb levels increased without clear relationship
with increasing sludge level in diet, 0-4.5%. Muscle increased as much as
kidney, while other research did not observe increases in muscle with such
low diet Pb levels.
The potential of mushrooms to bioaecumylaie Hg has been demon-
strated both in compost- or sludge-amended media and in natural environ-
ments (Brunneri and Zadrazil, 1983; Enke, etal,, 1979; Frank, Rainforth, and
Sangster, 1974;Zabowskie?a/., 1990). Some mushroom species, especially
cellulolyiic species, accumulate very high levels of Hg compared to other
vegetable foods, even when grown on media which are not contaminated.
However, research has shown that only a small fraction of tfie total Hg in
mushrooms is in ihe form of methyl-Hg (D'Arrigo et al., 1984; Bargagli and
Baldi, 1984;Minagawae
-------
.480 Science and Engineering of Composting
mushrooms (Agaricus bisporus) which were grown on a mushroom compost
which included MSW+sludge compost at 0,25,50, and 75% of ihe medium
(the compost contained 2.4 mg total Hg/kg DW). The mushrooms grown on
media containing 50 or 75% compost contained slightly over 0.5 mg Hg/kg
FW, the US Food and Drug Administration numerical limit for Hg in fish. The
concern about Hg in MSW-compost and sludge-compost used in production
of mushrooms has not adequately taken into account the finding that methyl-
Hg was only a small fraction of total Hg in mushrooms. Further, the response
of increased Hg in mushrooms vs. fraction of MSW+sludge in the mixed
mushroom compost shown in the Domsch ft al. study is clearly plateauing
(same mushroom-Hg concentration for 50 and 75% MSW+sludge in the
mushroom compost). Thus, modern low Hg MSW compost materials appear
to comprise little risk lo persons who ingest unusual high quantities of
mushrooms. In forest ecosystems, the combination of low methyl-Hg in the
mushrooms, coupled with low annual ingestion, indicates that Hg should not
be a practical limit on forest utilization of compost (Zabowski et al., 1990).
Unfortunately, the bioavailability of Hg in mushrooms has not been reported,
and the effect of modem MSW-composts on mushroom Hg levels or
bioavailability have not been evaluated, so limits for Hg in MSW-compost
products can not be accurately estimated. Compost programs clearly need to
promote separate collection of Hg rich wastes (e.g. batteries).
Cd in mushrooms is only important in those species which
bioaccumulate high levels of Cd, which does not include the commercial
mushroom, Agaricus bisporus. Some Cd-accumulating mushroom species
contain over 50 ppm Cd DW on uncontaminated substrates. Rat feeding
studies have been conducted by Diehl and Schlemmer (1984) to test the
retention in animals of mushroom Cd; about 1% of diet Cd reached the kidney
and liver by the end of 6 weeks of feeding 15% mushroom diet with 3.9 ppm
total Cd. Human feeding studies have also been conducted, and over 90% of
ingested Cd was excreted within a few days (Schellmann et al., 1980,1984);
if normal retention of Cd in the intestine for a prolonged period is considered,
the human studies support very low bioavailability of mushroom Cd. Several
hypotheses have been suggested to explain the low bioavailability of mush-
room Cd: 1) the presence of chitin in mushrooms may adsorb Cd in the
intestine and reduce absorption; 2) Cd in mushrooms may be in the form of
Cd-phytochelatins or metallothioneins which have lower bioavailability; and/
or 3) presence of other nutrients in the m ushrooms may inhibit retention of Cd.
In any case, there is no evidence that mushroom Cd would be a significant
source of transfer of soil-compost mixture Cd to humans (forest worst case
scenario) compared to the worst case acidic garden scenario.
Evaluation of potential risks to wildlife.
Although the evidence summarized in this review paper has shown
that modem sludges and MSW-composts can be safely utilized in agriculture
and protect humans, plants, and livestock, there has been less research on the
-------
Chancy and Ryan 481
potential effects of sludge or compost-applied heavy metals and toxicorganics
on soil organisms and wi Idlife than on agricultural ecosystems. Ii is now clear
that soil fauna are particularly important in risk analysis because earthworms
have been found to bio-concentrate Cd and PCBs from soils (e.g., Ireland,
1983). Although most wildlife animals'consume seeds or forage materials, a
few mammaJs or birds ingest substantial amounts of earth worms and oihersoil
fauna which might serve to accumulate and transfer the toxic constituents
from soils when other food webs do not. Although some crops absorb Cd to
high concentrations, there is no evidence that herbivorous wildlife are at
higher risk from eating crops growing on Cd-rich sludge-amended soils than
are omnivorous wildlife eating earthworms living in the soils. Beyer (1986)
noted that there is little evidence for biomagnification of heavy meials (other
than meihyl-Hg) in food webs except for the earthworm pathway. Little
dietary Cd is retained over a lifetime, so the body contains little Cd when
consumed by the next higher trophic level. This situation makes the
earthworm pathway much more significant that plant based foods.
Studies of Cd in ecosystems has consistently shown that shrews are
"close to soil" regarding Cd, PCBs, and Pb risk. Ecologists studying metal
transfer and risk in smelter-contaminated soils, or in mine soils, repeatedly
showed thai animals which consumed earthworms comprised the most
exposed receptors for these contaminants. Comparison of other mammal
species to shrews orotherearthworm consuming mammaJs has shown thatCd,
Pb, or PCB transfer from soil is perhaps 10-fold higher for the shrew than for
mice, voles, or other non-earth worm consumers (Cookee/a/., 1990; Hegstrom
and West, 1989; Hunter et al., 1983; Ma, 1989; Scanlon, 1987). Studies of
other wildlife collected on sludge amended soils, or fed sludge-grown crops
(e.g. rabbits, deer, deer-mice, voles, pheasants etc.) (Alberici, et al. 1989;
Anderson et a!., 1982; Beardsley et al., 1978; Dressier ei al., 1986; Hinesly
ei al., 1982) failed to find appreciable contaminant transfer to wildlife. Often
the increase in plant biomass production on disturbed sites caused significant
increases in population density. The increased exposure to sod Pb by
earthworm consumers results from the high fraction of soil in this food source,
which causes higher soil ingestion than other behaviors.
Shrews, moles, badgers, and red fox consume an appreciable amount
of earth worms (Macdonald, 1983; Ma, 1987), and might thus be at higher risk
thanothermammals. Although birds maybe exposed to soil PCBsandCddue
to eanhworm ingestion, few species are known to inhabit a small territory for
their lifetime which might provide them unusual exposure to high amounts of
earth worm-transferred sludge or compost contaminants from an amended site
similar to shrews. In one bird study (with red winged blackbirds, a species not
known to consume earth worms), little or no Cd accumulated in liver or kidney
in birds nesting on mine spoil amended with a very high rate of a high Cd
sludge compared 10 birds nesting on non-sludged areas(Caffney and Ellerston,
1979). Considering the lifetime exposure of wildlife species to sludge
contaminants, it is clear that the earthworm-consuming small mammals with
-------
482 Science and Engineering of Composting
limited territory must comprise the mosl exposed individuals rather than birds
which have much more limited exposure over time.
Earthworm accumulation of Cdfrom soils:
Because earthworms can bioaccumulate at least Cd and PCBs, and
some animals ingest earthworms with the worm digestive system full of soil,
ingestion of earthworms comprises a significant exposure route to metals in
soils amended, with sludges or composts. Research has characterized the
ability of earthworms to accumulate different metals. Many researchers
attempted to purge the worms of soil by allowing them to live in a moist
environment on filter paper. However, Helmke el al. (1979) found that traces
of soil remaining in the digestive system can explain nearly all of the residues
of many meials. They used neutron activation to measure many elements, and
then used non-absorbed elements to estimate soil contamination of the worm
samples. Soil explained most of the residue of most elements, but Cd.Au. and
a few other elements were bioaccumulated. Because soil normally comprises
45% of the dry weight of an intact non-purged worm (Beyer and Stafford,
1992), the soil can provide much more exposure to many elements than can
the worm tissues (except for Cd). Also, soil in the gut of an animal which
consumes an earthworm should provide ability to adsorb the metal in the
intestine and reduce bioavailability. Beyer et al. (1982; 1987) and Beyer and
Cromartie (1987) have shown many characteristics of earthworms on metal
salt or sludge amended soils. Ma (1982) examined earthworm accumulation
of elements from the long term MSW-compost plots described by Haan
(1981). He found only Cd and Zn were increased in purged worms from these
plots. The pattern found for worms from MSW-compost amended soils was
quite similar to that for the sludge amended soils described by Helmke ei al.
(1979) and Beyer ei al. (1982).
Estimating allowed soil or compost Cd which protects wildlife mammals
which consume earthworms:
Two separate approaches for estimating the maximum allowed soil-
sludge mixture Cd concentration protective of the most sensitive wildlife
(predator) species from lifetime excess Cd including bioaccumulation of Cd
by soil biota, were identified by Chaney and Ryan (1991): 1) The first
approach follows that of the original US-EPA (1989a) Technical Support
Document for the Clean Water Act-503 Regulation: A tolerable Cd level in
wildlife is divided by the slope for the (soil biota-Cd):(soil-Cd) ratio [the
increment in diet Cd due to sludge utilization]; fraction of earthworms in the
total diet must be taken into consideration, as well as bioavailability of Cd in
the biota (or biota with ingested soil) to the predator; or 2) The second
approach avoids the uncertainties of the Cd-bioaccumulation ratio for earth-
worms , the fraction of chronic wildlife diet comprised by earthworms, and the
bioavailability of Cd in earthworms to wildlife, by computing a direct ratio
between soil-Cd and tolerable Cd in the kidney cortex of earthworm-predator
-------
Chancy and Ryan 483
wildlife.
Approach 1: This analysis follows the suggestion of Beyer and
Stafford (1992). wiih adjusimems for factors used in calculations for other
elements in the revision of the CWA-503 risk analysis. They noted thai a
number of studies have found earthworms with high Cd levels due to use of
sewage sludge. On soils amended with high Cd sludges, earthworms may
contain as high as 100 ugCd/g earth worm DW for soil-purged worms. Their
work has shown that the worm:soil bioaccumulation ratio forCd is about 10
for soil-purged worms, or about 5-6 for non-purged worms (Beyer and
Stafford, 1992). For 10-fold enrichment in purged worms:soil (dry matter
basis), (non-purged worms contained 45% soil (DW basis)), the worm tissue
provides about 92.4% of the Cd and soil only 7.6%; for 10-fold increase in
purged worms, the increase in non-purged worms is only 6.0-fold.
Bioavailability must be taken into account, and the soil or soil-sludge mixture
in the earthworm gut should lower Cd bioavailability to animals which ingest
earthworms (in nearly all cases, worms are ingested intact with internal soil).
Readers should recall the errors in assessing risk of dietary metal sails
compared to sludge-borne metals. In study of the relative toxicity of sludge-
Cd and Cd-salt to pigs, Osuna et at. (1981) fed diets containing 50% high Cd
sludge (147 mg Cd/kg DW) or Cd-salt (79 mg Cd/kg DW). Cd-salts caused
severe anemia and toxicity, while the pigs fed 50% sludge had no anemia (the
low energy of the sludge containing diet reduced gain rates, but caused no
other ad verse effects). Kidney Cd was increased 21.4% as much by sludge-
Cd as salt-Cd per unit diet Cd. Further, in chronic feeding studies of the effect
of feeding earthworms to Japanese quail, Stoewsand et at. (1986) and
Pimentel etal. (1984) found no ad verse effects of feeding 60% control or 50%
Cd-enriched earthworms (dry matter basis); the accumulation of Gd in
kidneys showed that worm Cd had low bioavailability.
Based on a number of studies, caking into consideration the short
biological half life of Cd in rodents and birds (e.g. Freeman et al., 1983), 100
ug Cd/g diet DW can be tolerated by sensitive individuals [the 0.5 mg Cd/kg
diet recommended by the US National Research Council (1980) was set to
protect use of liver and kidney as human food, not the health of the livestock].
Using this as the lowest chronic toxic concentration, and 6 as the
bioaccumulaiion factor for whole earthworms (and assuming 50%
bioavailability [higher than the 21.4% from Osuna et al. 1981] or even lower
bioavailabiliiy based on Decker et al., [1980]), and assuming the diet con tains
at maximum 1/3 earthworms (non-purged) over a lifetime chronic exposure
period, the allowed soil Cd would be:
100 mg bioavailable-Cd t I k; diei DW = 300 me bioavallable eanhworm-Cd
kg diet DW 0.33 kg earthworm.DW kg earihworm-DW
• 1 mf lolal eanhworm-Cd • 1.0 mt soil-Cd
0.5 mg bioavailable worm-Cd 6 mg etnhworm loial-Cd
= 100 mg Cd/kg soil DW = 200 kg Cd/h«.
-------
484 Science and Engineering of Composting
Approach 2r This is the direct approach in which the kidney Cd
relationship with sludge-applied Cd is estimated for sludge-amended soils.
There are a few valid sludge Held data to allow calculation using the second
approach. A study by Hegstrom and West (38) looked at tissue metals in
several species of small mammals from forest sites which received sludge
applications. They collected insectivorous Towbridge's shrews (Sorex
lowbridgif) and shrew-moles (Neurotrichus gibbsi). and granivorous deer
mice (Peromyscus maniculaius) from sludge-treated and control sites at Pack
Forest, where Seattle sludge was surface applied at 51 Mg/ha several years
before the wildlife collections. Heavy metals were higher in tissues of
Towbridge's shrews from the sludge-treated areas than in control, and much
more accumulated in the shrews than in the other species.
A second collection of shrews was made from forested sites with much
higher cum ulative applications in order to identify any kidney or liver lesions
which may result from sludge use. Despite the high levels of heavy metals
found in kidney of Towbridge's shrews (mean = 126 mg Cd/kg DW), no
lesions were found in their organs. Of course, this concentration is far below
the level expected to cause the first health effect in mammals (696 mg Cd /
kg whole kidney DW, shown below).
To estimate transfer from soil to kidney as a basis for limiting sludge
Cd applications, the following information was used: 51 Mg dry sludge was
applied to forest sites where shrews were sampled. The sludge applied in the
studies contained 50 ppm Cd, 2000 ppm Zn, 900 ppm Cu, and 1200 ppm Pb.
The application of 51 Mg DW sludge/ha containing 50 mg Cd/kg DW applied
2,55 kg Cd/ha. The shrew whole kidney Cd concentrations were 33 (25-43,
N=66) on sludged plots, and 9 (8-10, N=50) on equivalent control forested
sites. The increment in kidney Cd due to sludge utilization was 24 mg CdAg
whole kidney-DW.
The concentration of Cd in the whole kidney has to be related to the
potential toxic level (200 ug Cd/g kidney cortex-FW; this value is considered
a measure of the lowest Cd concentration which can cause tubular dysfunction
in sensitive individuals for many animal species):
200 ug Cd < ( l.QOuy Cd ^ g kidney conexl _ 160pgCd
g kidney cortex-FW ' \ g whole kidney* 1.25 pg Cd J g whole kidney-FW
(based on using the conversion factor 1.25 for (kidney cortex-Cd concentra-
tion) : (whole kidney-Cd concentration) for humans from Svartengren el at.
[1986]).
To complete this calculation, one also needs to convert from kidney-
FW to kidney-DW. In the absence of data specifically for shrews, the mean
dry matter content of fresh beef, calf, hog, and lamb kidney from USDA
-------
Chancy and Ryan 485
Handbook 8 (Adams, 1975) was used, = 23% solids. Thus, (160 mg Cd/kg
FW) (1.00 g FW/0,23 g DW) = 696 mg Cd/kg whole kidney DW.
Then the slope for (shrew kidney-Cd):(soil-Cd) is divided imo the
tolerable whole kidney Cd concentration on a dry weight basis; 696 ug Cd/
g DW (maximum permissible Cd concentration in whole kidney) -r [(24 mg
Cd increase/kg whole kidney DW)/(2.55 kg Cd/ha)] = 74 kg Cd/ha when
sensitive shrews would be expected to reach their first health effect on kidney
function due to dietary Cd exposure. The disagreement between the estimates
for Approach 1 and Approach 2 might be due to the surface application of
sludge in the forest compared to the slopes obtained for earthworms which
•habiiaied soils with sludge mixed about 20 cm deep imo ihe soil. Different
earthworm species feed al different depths in the soil; ihe earthworm species
and feeding habit in the forest was not reported (Hegsirom and West, 1989),
The relationship of kidney Cd, or bone or kidney Pb, to survival of
shrew populations has been studied somewhat. In the study by Ma (1989) of
the Pb transfer to mammals at a shooting range, shrews with excessive organ
Pb had high population density. In the study by Hunter ei at. (1983), shrews
had evidence of excessive organ Cd, but the population was well established.
In studies by Beyer ei at. (1985), many animals were collected in areas where
vegetation persisted in the vicinity of aZn smeller; no evidence of excessive
kidney Cd or Cd heaJ th effects were seen, but high Pbcaused depressed AL AD
activity in some animals with high tissue Pb, Deer in the area suffered Zn-
inducedCu deficiency with loss of cartilage in joints of long bones, but kidney
Cd levels were not sufficient to indicate tubular dysfunction due to excessive
Cd (Sileo and Beyer, 1985). Based on these evaluations, it seems clear that
the acidic garden scenario for Cd, and children ingesting compost scenario for
Pb are much more restrict! veon sludge and compost metalconcentrations than
are wildlife scenarios.
Evaluation of potential risks to soil microbes: Starting in the 1980s,
studies by McGrath, Brookes, Ciller, and thcirassociatcs identified apparent
adverse effects of sludge-applied heavy metals on the soil microbial biomass
and on the Rhizobium strain which forms nodules in white clover and related
species (Brookes and McGraih, 1984; Brookes el al., 1986; Ciller ei al., 1989;
McGrath, Brookes and Ciller 1988; McGraih, Hirsch and Ciller, 1988). In a
long-term experiment (the Woburn Market Garden Experiment), about 766
Mg/ha of moderately high metal concentration sewage sludge (average metals
were about 3000 mg Zn/kg, 1300 mg Cu, 200 mg Ni, 100 mg Cd, 900 mg Pb,
and 1000 mg Cr/kg DW; McGrath, 1984) was applied to field plots of
vegetable crops on a sandy soil from 1942 to 1961, and the soil microbe
populations were examined more than 20 years after the last sludge applica-
tion. No legume had been grown since 1942. Their research found that the
historic sludge applications had caused selection in these soils of a strain of
Rhizobium leguminosarum biovar irifolii which formed nodules on white
clover, but the nodules were ineffective in fixing N. Although ihe sludge
-------
486 Science and Engineering of Composting
utilization practice caused selection of this ineffective Rhizobium strain, no
phytotoxicity occurred to white clover if N-fenilizer was added to the pots.
Further, inoculation of the plots with an effective strain allowed normal
nodulation of while clover, although the population of effective strains in the
soil declined after inoculation. Further, Rhizobia for other legume species
(other biovars) have not been found to be inhibited by soil metals levels below
those which cause significant phytotoxicity (soybean: Heckman et al.t 1986;
1987a; 1987b; Kinklee; al.. 1987; alfalfa: Angle and Chancy, 1991; Angle et
at., 1988; El-Aziz etal., 1991).
Besides the inhibition of N fixation by this strain of Rhizobium, N
fixation by blue-green algae was also inhibited on these plots and some other
high metals soils (Brookes, McGrath and Heijnen, 1986) and N fixation by free
living bacteria was also inhibited on high metal mine soils (Rother, Millbank
and Thornton, I982a).
Many other studies have shown that soil microbial activities were not
inhibited on sludge-amended soils, including ammonification of organic-N,
nitrification of NH4-N, mineralization of C and N, etc. (e.g., Minnich and
McBride, 1986; Rother, Millbank and Thornton, 1982b). These studies on
while clover Rhizobium vs. other soil microbes appear to be replicated well,
but to disagree regarding the toxicity of soil metals to soil microbes compared
to the toxicity of soil metals to higher plants. Angle and co-workers have
conducted some work loevaluate metal toleranceof US strains of white clover
Rhizobium and found these strains were less sensitive to metals than the UK
strains described by McGrath et a!. (Angle et a!., unpublished). We have
found effective strains in nodules of white and red clover growing in fanners
fields in the vicinity of thePalmenon.PA.Zn smelter, in soils with higher Zn
and Cd levels than in the Woburn study.
In attempting to explain the adverse effects of sludge application on
the Worburn plots, some workers have hypothesized that the finding that the
Rhizobium strain was more sensitive to soil metals than was the host plant, ma>
have resulted from the very light textureof thesoil studied, the somewhat high
level of metals in the sludge applied, or from the long period of exposure
without reinoculation of the soil. It is clear that simple inoculation of seed.
when sowing white clover can allow normal nodulation. The causal agent fo
selection of ineffective strains has not yet been identified. Few long-tern
sludge plots with very high cumulative sludge applications have beet
examined for this phenomenon, while some high metal mine spoils have beei
found to cause rapid decline in white clover Rhizobium populations (S.P
McGrath and K.C. Jones,personalcommunication;Rotheref a/., 1983). Ith
clear that further research is needed to establish whether the first ad verse effec
of very high cumulative applications of NOAEL .quality sludges will b<.
phytotoxicity to highly sensitive vegetable crop species when the soil \.
acidified, or decline in population of white clover Rhizobium strains. Clover
are not as sensitive to excessive Zn and other metals as lettuce, beet, chard
and some other well known highly sensitive species (e.g., Hewitt, 1954).
-------
Chancy and Ryan 487
EVALUATION OF RISKS FROM POTENTIALLY TOXIC
ORGANIC COMPOUNDS IN MSW-COMPOST
Reviews by Harms and Sauerbeck (1983), Chaney (1985), Jacobs et
fl/,(1987),0'Connore;c/,(1991),Chaneye(c/.(1991),andChaneyandRyan
(1991) cover the concepts and research data on the potential for risk of sludge
PCBs and other organics to humans, livestock, crops, or wildlife.-When the
W-170 Peer Review Committee used the Pathway Approach to make quan-
titative estimates of cumulative applications of PCBs, PAHs, and other
compounds, none were found to occur in sewage sludge at high enough levels
to be a risk to the most exposed individuals (Page ei al., 1989; Chaney ei al.,
1991; Chaney and Ryan, 1991). Table 5 shows the limits required for PCBs
to avoid risk under each Pathway for which quantitative estimates were
completed. Thus, Pathway 2 (ingestion by children), Pathway 4-Surface
(surface applied compost ingested by grazing livestock), and Pathway 9
(accumulation by earthworms which are ingested by wildlife as one-third of
the dry matter of their diet) are most limiting to application to persistent
potentially toxic organic compounds.
Interestingly, the amount of MSW-compost ingested by grazing
livestock would be expected to be significantly lower than found in the case
of surface applied fluid sludges. Although cattle grazing pastures to which
fluid sludge was applied 21-days before initiation of grazing consume about
2.5% sludge in their diet (dry matter basis), when dewatered sludge or sludge
composts were applied, sludge comprised only about 1% of diet dry matter or
less (Reddy et al.. 1985; Decker et al., I980a, 1980b).
Besides PCBs, phthalates, and many other chemicals, the family of
compounds called polycyclic aromatic hydrocarbons (PAHs) is known to
occur in sludges and MSW-composts. Many of the PAHs are carcinogenic,
and research has been conducted to clarify the potential risk from represen-
tative carcinogenic PAH compounds (e.g., benzo(a)pyrene). PAHs are
generated by combustion processes, and are strongly adsorbed by humic acids.
PAHs are biodegradable, although the rate of biodegradation of sludge-borne
PAHs is now known to be somewhat slower than previously estimated using
addition of pure compounds to soils (Wild ei a!., 1990, 1991). Plant uptake
of PAHs is significant only in the case of carrots, and nearly all the PAH in
carrot roots is in the peel (Wild ei al., 1992)
Feeding studies with PCBs indicated that sludge organic matter could
adsorb PCBs strongly enough to reduce absorption by cattle by about 50%
compared to pure PCBs in com oil (see Chaney ei al., 1991). Using theq,*
for benzo(a)pyrene =11.5 (mg/kg/day)•', the allowed compost concentration
would be 6.1 mg/kg D W in order to protect 1 -6 year old ch ildren who consume
0.2 g dry compost per day for 5 years (or 0.5 g/day for 2 years) and assuming
100%bioavailability. Ifbioavailability is lower due to adsorption by compost
organic matter, the allowed sludge concentration would be proportionally
-------
488 Science and Engineering of Composting
higher.
As noted by Chancy et al. (1991), the garden foods pathway (Pathway
IF) for PCBs comprises much lower risk than does Pathway 2. In the garden
food pathway, the potential for transfer of potentially toxic organics in
compost to humans is very dependent upon the ability of carrots to accumulate
the compounds from amended soils since carrot is nearly the only crop with
appreciable accumulation of PAH or PCS from sludge-amended soils. Much
like the case for metaJs being bound by the specific metal adsorption capacity
of sludges, organics are bound strongly by sludge and compost organic matter.
This reduces "uptake" (transfer to edible plant parts) by plants growing on
compost amended soils compared to soils which receive applications of pure
compounds without the adsorption capacity of compost, and makes the
response pattern a plateau in crop PAH or PCB with increasing sludge
application rate for a sludge. This was shown for PCBs by O'Connor et al.
(1990). For PAHs, Ellwardt (1977) and Wild and Jones (1992) have made
similar observations for plateau response to compost or sludge-borne PAH,
again with focus on carrot which accumulates lipophilic organic compounds
in the peel layer.
Table 5. Comparison of PCB application limits for each pathway from the 503
Proposed Rule (US-EPA, 1989b) with the corrected versions based on US-EPA
(1989a) and Chancy, Ryan, and O'Connor (1991). Units are changed in some
corrected versions.
Pathway
Proposed 503 Rule
Limit Units Limit value
Corrected Approach
Limit Units Limit value
1
IF
2F
2D&M
3
4-Surface Application
4-Mixed With Soil
9
kg/ha • yr
kg/ha • yr
kg/ha • yr
kg/ha • yr
kg/ha • yr
kg/ha • yr
kg/ha • yr
kg/ha • yr
kg/ha • yr
4.14
0.264
2.31
7.26
7.26
0.0056
0.0192
0.0192
•
mg/kg soil max.
mg/kg soil max.
mg/kg sludge DW
mg/kg soil max.
kg/ha «yr
mg/kg sludge DW
mg/kg soil max.
kg/ha soil max.
kg/ha • yr
mg/kg soil max.'
kg/ha soil max.
kg/ha • yr
17.2
9.09
9.09
18.3
2.46
2.23
2.23
4.46
0.299
4.06
8.12
0.545
Annual applications based on 10 year half-life for PCBs in soil. Fraction of dietary
meat and milk products from sludge/compost amended soil presumed to be 45%
(Chaney, Ryan, and O 'Connor, 1991); reassessment of this fraction indicates that only
15% may now come from "homegrown" livestock based on more recent dietary
-------
Chancy and Ryan 489
surveys. This would increase the allowed PCBs in sludge, or kg/ha • yr by about 3-
fold for Pathways 3, 4, 5, and 6.
Besides these considerations, there is the possibility that PAH com-
pounds will be biodegraded during composting of MSW. Little degradation
was observed by Muller and Korte (1976) in a model system. This question
has not been unequivocally sealed for sludge or MSW at this time. The
decreased microbial diversity in composting organic materials compared to
mesophilic populations may prevent enhanced destruction of some organics
during composting, and management at lower temperatures may favor
biodegradation of some persistent organics.
RESEARCH NEEDS FOR MSW-COMPOST:
In order for MSW-composting and distribution and marketing of
MSW-compost to win the degree of public acceptance and marketability
desired by the industry, research and demonstrations will be required.
Research on fate and effects of nutrients, metals, and organics in sewage
sludge were critical in winning public acceptance, and provided the data
needed to prepare appropriate regulations. Demonstration projects were
required in many locations to convince citizens that local agencies could
utilize sludges within the regulations. We conclude that the most important
research needs or questions remaining for MSW-composting and MSW-
compost marketing include:
1) Will higher Fe concentration in MSW-compost persistently increase
the specific metal adsorption capacity of compost and thereby reduce
the potential for risk from compost metals, particularly focusing on:
A) Unavailability of compost Pb to monogastric animals
which ingest compost;
B) Phyto-availability of compost Cd at pH > 5.5 as indicated
by reduced height of the plateau above the control, or slope
for plam:soil relationship;
C) Phytotoxicityofsludge-appliedZri,Cu,andNiatpH>5.5.
D) Effects on white clover Rhizobium.
2) Does addition of MSW-compost to Pb-rich urban soils reduce the
bioavailability of soil Pb to monogastric animals?
3) Can compost be efficiently convened to organic-N fertilizer instead of
a low N soil conditioner? Can methods be established to determine the
first year mineralization of organic-N in MSW-compost (see Gilmour
and Clark, 1988)?
4) Can homogeneity of MSW-compost be improved by planned mixing
during processing?
-------
490 Science and Engineering of Composting
5) Does aeration during storage prevent formation of phytotoxic
biodegradaiion by-products in MS W-compost as required for compost
to be utilized as a large fraction of potting media?
6) Can any MSW-compost cause rneial phytotoxicity at pH 5.5 or above
to sensitive vegetable crops. We have no evidence that phytotoxicity
could result from MSW-compost use in short or long term. However,
high cumulative applications, studied after considerable time to allow
decomposition of organic mailer in the soil-compost mixture, and
adjusted to very low pH to comprise the "worst case", should be
examined.
7) How important is the potential for lime-induced Mn deficiency from
land application of MSW-compost compared to lime-treated sludges?
Can susceptible crops and soils be identified so that agronomic advice
to avoid Mn deficiency can be provided to MSW-compost users.
8) Do particular sources of compostable organics carry undesirable levels
of boron, Pb, Cd, or Zn, and what can be done lo keep materials rich in
potentially toxic constituents out of the compost stream.
9) Do present levels of Hg in MSW-compost or MSW+sludge compost
still prevent their use in mushroom production? Do mushrooms
produced on media including MSW-compost have increased Hg or
methyl-Hg? New studies are needed to clarify Hg limitations for this
use of MSW-compost.
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TECHNICAL REPORT DATA ,
(Please read Instrucf.ens on the rcvene before complci
1. REPORT NO.
EPA/600/A-94/030
4. TITLE AND SUBTITLE ,
Heavy Metals and Toxic Organic Pollutants in MSW-Com-
posts: Research Results on Phytoavailability, Bio-
availability, Fate, Etc.
5. REPORT DATE
6. PERFORMING ORGANIZATION CODE
1. AUTHOR(S)
James A. Ryan, Rufus L. Chaney
8. PERFORMING ORGANIZATION REPORT NO
9. PERFORMING ORGANIZATION NAME AND ADDRESS
RREL/US EPA—Cincinnati, OH
Environmental Chemistry Lab/USDA-Agricultural Research
Service—Beltsville, MD
10. PROGRAM ELEMENT NO.
1 I. CONTRACT/GRANT NO.
12. SPONSORING AGENCY NAME AND ADDRESS
Risk Reduction Engineering Laboratory
Office of Research and Development
U.S. Environmental Protection Agency
Cincinnati, OH 45268
13. TYPE OF REPORT AND PERIOD COVERED
Published Paper
14. SPONSORING AGENCY CODE
EPA/600/14
15. SUPPLEMENTARY NOTES
Project Officer = James A. Ryan (513) 569-7653; Proceedings of
the "Science and Engineering of Composting: Design, Environmental, Microbiological
and Utilization Aspects", 3/27-29/92, Columbus, OH, p:451-506
16. ABSTRACT This paper is a review and interpretation'of research which as been conducted
to determine the fate, transport, and potential effects of heavy metals and toxic
organic compounds in MSW-composts and sewage sludges. Evaluation of research findings
identified a number of Pathways by which these contaminants can be transferred from
MSW-compost or compost-amended soils to humans, livestock, or wildlife. The Pathways
consider direct ingestion of compost or compost-amended soil by livestock and children,
plant uptake by food or feed crops, and exposure to dust, vapor, and water to which
metals and organics have migrated. In research on these questions, the chemical
properties of sludges and composts were found to be very important in binding the
metals and toxic organics. The "bioavailability" of contaminants in MSW-composts
describes the potential for accumulation in animals of mebals or organics from ingested
sludges or composts, or from food/feed materials grown on sludge or compost amended
soils. Presently, it appears that the most limiting heavy metal in MSW-composts may be
Pb. MSW-compost may provide fertilizer and soil conditioner benefit in agriculture and
horticulture if compost manufacturers carefully reject Pb rich wastes.
7.
KEY WORDS AND DOCUMENT ANALYSIS
DESCRIPTORS
b.lDENTIFIERS/OPEN ENDED TERMS C. COSATI Field/Group
MSW-composts, sewage
sludges, heavy metals
8. DISTRIBUTION STATEMENT
RELEASE TO PUBLIC
19. SECURITY CLASS (Tills Report)
UNCLASSIFIED
21. NO. OF PAGES
56
20. SECURITY CLASS (Tills page!
UNCLASSIFIED
22. PRICE
EPA Form J220-1 (R«v. 4-77) PREVIOUS EDITION is OBSOLETE
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