Increase in dietary cadmium as a result of application of sewage sludge to The maximum acceptable dietary intake of cadmium i3 70 pglday. The FDA estimate of cadmium in the median American diet is 39 pglday, so a 30 pglday increase in dietary cadmium would keep Cd ingestion within the limit. When sludges are applied to gardens andfields, an annual application limit of 0.5 kg Cdlha should protect public health
Lewis M. Naylor Raymond C . Loehr Cornell Uniuersify
Ithara, N.Y. 14853 Application of sewage sludge to land can be beneficial because it adds organic matter, nitrogen, phosphorus, and trace minerals to the soil. However, when managed improperly, these sludges can result in potential health risks. Uptake of cadmium by crops grown on sludge-amended soils is one of the risks that the Environmental Protection Agency (EPA) and other organizations have examined extensively. Chronically excessive concentrations of cadmium in the diet are known to cause toxicity and health
effects and any increase in dietary cadmium should be minimized. EPA has recognized the need for a critical assessment of cadmium-related health issues, especially as these issues relate to application of sewage sludge to the land. Accordingly, during development of sludge management guidelines published Sept. 13,1979, in the Federal Register ( I ) , EPA considered a great deal of evidence related to dietary cadmium exposure. Based on this evidence, guidelines were developed to provide margins of safety associated with the agricultural utilization of sewage sludges. The guidelines established an acceptable maximum increase of 30 pg cadmium per day from foods grown on sludge-amended soil. This increase was
based upon assumptions o f protection of high-risk individuals specific diet scenarios expected health effects. This review explains how EPA arrived at this increase and, using data on the characteristics of municipal sludges in New York, considers implications of the guidelines. Health effects-dietary Cd exposure Extensive epidemiological evidence of the toxic effects of dietary cadmium has accrued from Japanese studies of the ltai-itai disease (2). Symptoms of this disease are the fracturing of bones and skeletal deformation due to softening of bone tissue. These symptoms are caused by impaired calcium me-
L
0013-936X/81/0915-0881$01.25/0
@ I981 American Chemical Society
Volume 15, Number 8. August 1981
881
tabolism, calcium deficiency, and impaired regulation of the calciumphosphorus balances in the body (36). In the Japanese studies, the cause of the disease was determined to be high concentrations of cadmium in the drinking water and diet (particularly in rice) of affected individuals. The source of the cadmium was contamination of the Jintsu River, caused by acid drainage from a Iead-zinc-cadmium mine upstream of the endemic area. Water from the river was used for drinking, cooking, and irrigation of rice paddies. Of 149 patients diagnosed as having Itai-itai disease in the affected area, 146 were women. The median age of the affected persons was 65-75. The symptoms occurred most frequently in women above 40 years of age who had borne several children. All affected individuals had consumed cadmiumcontaminated rice as a dietary staple. The dietary cadmium intake from food and water in the endemic area has been estimated at 300-600 &day (2). The reason that those affected severely were primarily women over 40 years of age, and especially those who had borne several children, was believed due to a combination of factors. The individuals’ diets contained relatively low amounts of calcium and fat-soluble vitamins, such as vitamin D. Losses of bone minerals in connection with pregnancy and lactation constituted a further contributing factor ( 5 ) . Iron deficiency and pregnancy increase calcium requirements and cadmium absorption. Itai-itai disease is the most severe manifestation of cadmium poisoning. Lesser symptoms include proteinuria and glucosuria brought on by injury of the proximal renal tubules. The prevalence of these symptoms was higher among women than men (2). While these incidents tragically demonstrate the toxic effects of high levels of cadmium in food and water as a result of a massive cadmium pollution incident, they do not necessarily indicate the type or the degree of hazards that are likely to be encountered by individuals who obtain all or part of their diet from food that has been grown on sludge-amended soils. Population at risk In order to avoid deleterious health effects due to cadmium in sludges applied to cropland, EPA reviewed evidence on municipal sludge characteristics, the quantities and characteristics of sludges applied to land, and uptake of cadmium by crops. The agency 882
Environmental Science a Technology
considered diet scenarios relating food intake and cadmium exposure, and models suggesting potential effects of various levels of cadmium exposure. Its conclusion (I) was that the high-risk individual, Le., one who might receive the greatest cadmium exposure from air, water and diet, should not have an increase in dietary cadmium intake greater than 30 pg/day. A higher intake in the average diet was considered clearly unacceptable by those who developed the guidelines. The high-risk individual was identified as one who receives 50% of a vegetable diet from sludge-amended soils for 40-50 years. The individual also was considered to be a chainsmoker (three packs/day for 50 years) since tobacco smoke is known to contain substantial amounts of cadmium, of which 40-50% is absorbed by the body, as contrasted to about 4-8% from dietary sources. Obviously, everyone is not likely to be exposed to the same environmental sources of cadmium or to ingest the same dose. The nutritional status of the individual at risk also is important when evaluating absorption of cadmium from dietary sources. Adequate and balanced dietary intake of iron, zinc, calcium, copper, protein, and vitamins D and C reduce absorption of cadmi, um ( 4 ) . Persons who eat food grown on sludge-amended soils might indeed consume adequate amounts of these nutrients.
Sludge may not only contain high cadmium concentrations but also greater amounts of most essential and nonessential elements than the soil. As a result, crops grown on sludgeamended soil, which might contain above-average content of cadmium, also are likely to contain higher levels of calcium. zinc, copper, and iron. To significantly increase dietary cadmium intake, one would have to consume large quantities of grains and vegetables. Consequently, they would also consume adequate amounts of protein, vitamins, and other essential nutrients, and would probably have a balanced diet with adequate caloric intake
(7). Diet scenarios During consideration of cadmium health effects that may result from sludge in soil, EPA evaluated several scenarios in which humans might be exposed to dietary cadmium. It considered both the diet of the typical American (8) and a vegetarian diet (Loma Linda University vegetarian diet) (9). Cadmium contributions from food classes for each of these diets are shown in Table I . In the scenarios, it was assumed that home gardens, grain crops, or animal feed crops received the full impact of the total municipal sludge produced in the U S . That is, all the sludge produced in the U S . was considered to be applied to gardens, grain crops, or
consumption and cadmium intake for
Dairy products Meat. fish, PDUlby Grain and cereal products
mevegetables
5.7 15.3 23.2
584
40.5 6.2
252 166
10.0
110
203
shortenings
Sugars and adjuncts Beverages Totals
3.0
10.2
8umBd that thm are no controls on
land aDDlication of waste (municioal
animal feed crops, and an individual or animal obtained its entire diet from sludge grown crops. In reality, this is unlikely. Sludge would bedistributed through various types of land application systems, including nonagricultural land. Thus, perhaps one third of the sludge applied on land might affect any one scenario. An additional safety margin is provided because probably no more than half the nation's sludge would be so applied. (Currently about 25% of municipal sludge is applied to land.) These possibilities would lessen the impact to about one-sixth of that projected in the scenarios. It should be noted that each scenario included conservative assumptions about cadmium uptake by crops grown on soils of the specified pH, Le., all food crops within each food class accumulate cadmium as efficiently as the most sensitive in the class. Health effect models Several models have been developed that relate dietary cadmium intake to specific health effects. These models focus on chronic long-term (50-year) dietary intake of cadmium, in contrast to occasional, acute, short-term exposure. The acute toxicity level of cadmium appears to be at least 1000 times that of the chronic toxicity level (2). Chronic health effects are generally the result of cadmium intake through diet. The kidney is the target organ for chronic exposure to cadmium because
when the cadmium content of the renal cortex reaches 200-300 pg/g (10.11) wet weight, damage to renal tubules results in proteinuria and loss of cadmium from the kidney (2). This condition is manifested by the excretion of betaz-microglobulin (Bz-MG) which is early discernible laboratory evidence of organ damage, although Bz-MG in the urine also has been shown to correlate closely with age (12). Small increases in Bz-MG are not considered a severe health impact, but rather a biochemical sign that continued cadmium exposure could lead to more severe health impacts. Data collected in the US. on cadmium in the kidney cortex of individuals not exposed to industrial sources of cadmium indicate that the mean concentration is about 20-35 pg/g wet weight. Results for apparently normal
adults from several studies are presented in Table 2. Only 0.6% of the results exceed 100 pg/g and none were close to the 200 pg/g level. The studies indicate that the average smoker has 70- 100%higher cadmium concentrations in the kidney cortex than the average nonsmoker (9). Various metabolic models have been developed to project cadmium exposure levels necessary to produce the critical cadmium concentration in the kidney. Using a model developed by Kjellstrom and Nordberg (13),EPA concluded that the cadmium concentration in the renal cortex of half of the nonsmokers would reach 200 pg/g wet weight in 50 years at an average daily dietary intake of 440 pg cadmium. A dose-response model developed by Kjellstrom ( 1 4 ) related the appearance of Bz-MG in the urine to daily total cadmium intake for a range of exposures from 0-400 pg Cd. The model is a log-normal model which indicates that a small incidence of renal dysfunction would be observed in a population even at very low exposure to cadmium. Tsvchiya et al. (12) found a strong correlation between Bl-MG in the urine and aging, which would seem to provide an empirical basis for the model. According to the Kjellstrom model, daily cadmium exposures in the range of 100-125 pg would produce biochemical evidence of renal dysfunction in 5-8% of the population after about 50 years of exposure. Although the Kjellstrom model has some shortcomings, EPA has accepted conclusions from its use. However, more data is desirable for validation. Allowable increases in dietary intake From the review and evaluation of cadmium dose-health effects models, EPA concluded that 200 pg Cd ingested daily over 45-50 years could result in a critical renal cortex concentration of 200 pg/g in susceptible
-.admium in the kldney cortex of U.S. adult population
lndraparasit et ai.. 1974
31-80
134
22
Gross et al.. 1976 Johnson et al., 1977
Hammer et ai., 1973
Volume 15. Number 8, August 1981 883
individuals. Among the more susceptible persons, this intake could result in renal dysfunction as exhibited by increases in Bz-MG in the urine. The 200 pg Cd/day limit assumed background exposure levels in air and no exposure from smoking. To minimize the risk of persons exposed to potentially toxic levels of cadmium, reasonable margins of safety were adopted to ensure that undesirable exposures do not occur from the application of sludges to land used for food chain crops. A maximum allowable exposure of 150 pg Cd/day (calculated in terms of dietary intake) was considered acceptable (9). Because the 200 pg Cd/day dietary intake does not include increased exposure due to smoking, the maximum allowable dietary intake was reduced by 75 pg Cd/day. Smoking one pack of cigarettes is equivalent to cadmium retention in the body of 25 pg as dietary intake. American cigarettes contain 1.5-2 pg Cd/cigarette, and about 70% of this ends up in the smoke. About 0.1-0.2 pg Cd are actually inhaled for each cigarette smoked ( I O ) . One package of 20 cigarettes will result in the inhalation of 3 pg Cd and of this, about 1.2 pg is absorbed by the body. This is equivalent to a typical absorption of 4.8% of 25 pg Cd from dietary sources. Because many individuals do smoke, the 150 pg Cd/day maximum allowable exposure from dietary sources was reduced to 75 pg Cd/day. In 1972 a joint Food and Agricultural Organization (FAO)/ World Health Organization (WHO) Expert Committee on Food Additives established provisional tolerable dietary intakes of cadmium at 57-71 pg/day, or about 1 pg/day per kilogram of body weight (15). Because the 75 pg Cd/day value was close to the WHO recommendation, EPA concluded that a level of 70 &day represented a reasonable limit on the maximum acceptable dietary intake of cadmium. EPA established the 30 &day increase in dietary cadmium by comparing current levels of dietary cadmium with the 70 &day limit. The Food and Drug Administration (FDA) indicates in total diet studies (8) that dietary cadmium intake has followed a saw-toothed pattern since 1968, with intake varying between 26-51 pg/day (Figure I). The 1974 averagedietary intake in the U S . was 33.5 pg/day (Table 3). The FDA estimate of cadmium in the median American's diet was 39 pglday. This concentration represents the mean of the median levels found in foods during the years 1968-1974 (Figure I). Based on this 884
Environmental Science 8 Technology
estimate, EPA concluded that a 30 pg/day increase in dietary cadmium would keep cadmium ingestion within the limit of 70 pg/day. The logic and assumptions used in arriving at this limit are summarized in Table 4. Establishing Cd application rates The data base for calculating acceptable cumulative loadings of cadmium was a set of field studies from landspreading sites where crops were grown at least two years after application of sludge. This approach was considered appropriate for setting maximum cumulative limits because guidelines and limits primarily are set with a consideration of possible future use of landspreading sites for home gardens or commercial agriculture. The diet scenario analysis described earlier was used to translate levels of plant uptake of cadmium into projections about the amount of cadmium entering the human food chain. Intake of various food classes followed the information in the FDA total diet studies (8). The cumulative 5 kg Cd/ha limit for sludges applied to acid soils (pH 6.5 or less) was established by relating the diet scenario analysis to the analysis of health effects. Using the data base noted earlier and summarized in Table 5, this correlation indicated that on mildly acid soils (pH = 5.8), the addition of 5 kg/ha of cadmium increased dietary cadmium by 22 pg/day, assuming that no more than
50%of the vegetable diet was derived from sludge-fertilized soils. In contrast, a cumulative loading of 7 kg/ha on very acid soils (pH = 4.9) increased the dietary level by 21 1 &day. This latter increase, attributed to both higher cadmium application rates and lower soil pH, was clearly unacceptable. Therefore, EPA established the maximum cumulative limit at 5 kg Cd/ha for acid soils. EPA conducted similar analyses for application of cadmium to soils with a pH of 6.5 or greater and for soils used for production of only animal feed crops. Annual application rates on gardens or commercial farms were based on cadmium uptake by "accumulator" crops such as leafy vegetables and tobacco. This was done to assure that if a mix of crops is grown on sludgeamended gardens, no crop will have a cadmium content fikely to cause a significant negative health impact. From the data base noted earlier for the diet scenario analyses, it was determined that annual additions of 0.8 kg Cd/ha could lead to a dietary increase of 10.3 pg/day from leafy vegetables alone. Thus, EPA concluded that when sludges are applied to gardens or fields for production of accumulator crops, an annual application limit of 0.5 kg Cd/ha should protect thepublic health. When sludge is applied to soils growing a nonaccumulator crop, EPA limits the annual cadmium addition to 2 kg/ha. This is to be
FIGURE 1
Median dally cadmium Intakes (H/day) in total diet of 15-20-yaar-old
Mean of 7 yearly
madIan8
F 1968
Y
F
Y
1969
F
Y
1970
F
Y
1971
F
Y
1972
F
Y
1973
F
Y 1974
decreased gradually to 0.5 kg/ha by 19x7
It is unlikely that the 0.5 kg Cd/ ha-year limit would be applied to fields used for crop production. The maximum cadmium content of sludges that can be applied to soils for production of “accumulator” crops is 25 mg/kg. To protect groundwater from nitrate contamination, available nitrogen in the applied sludge should not exceed crop needs. Most municipal sewage sludges in New York state contain 3-5% total nitrogen (dry basis). About 20-30% of the organic nitrogen and all of the inorganic nitrogen in the applied sludge is available for plant use each year. This amount of nitrogen represents about I-2% of the sludge solids (dry basis). Therefore, if the sludge solids on a dry basis contain 1% of such available nitrogen, I O metric tons/ha (4.5 tons/acre) of sludge would provide 100 kg/ha (89 Ib/acre) nitrogen available for plant use. If the sludge contains 25 mg/kg cadmium, 0.25 kg/ha (0.22Ib/acre) would be added to the soil. In successive years, lower sludge and hence cadmium application rates would be required because of continuing mineralization of the organic nitrogen in the sludge initially applied. Should the sludge contain a larger percentage of available nitrogen, the application rate required to meet the crop nitrogen needs would decrease and, as a consequence, smaller quantities of cadmium would be added to the soil. In New York state, 50% of the municipal sludges contain less than 6-8 mg/kg cadmium (Table 6). The annual cadmium application rate for these sludges when they are applied as a nitrogen fertilizer would be about 0.07 kg/ha (less than one-seventh the annual limit of 0.5kg/ha). To reach a cumulative cadmium application of 5 kg/ha would take about 70 years. This analysis is summarized in Table 6 and indicates that at the low level of cadmium additions to the soil that would result from use of EPA criteria and guidelines, it would take a considerable period of time to reach the allowable cumulative cadmium applications. During this time, periodic monitoring of the crop would provide ample opportunity to review the sludge utilization program and determine if potential health or other problems are occurring. Although the regulations for applying sludge to land were promulgated by EPA, FDA and the U S . Department of Agriculture reviewed these regulations and their inputs were incorporated. Early in 1981 the three
. . Gewraphls Numbwol Lead Cadmium Urn &% SalmIlum Uncuy rW-PII d d a y ) IwfdaY) I W d W 1 d d . Y ) (#@day) (IrgldaY)
Northeast Southeast Central West
10 7 6 7 -
~
105.5 75.7 105.5 69.7
Average
32.1 24.1 35.5 43.3 33.5
90.2
19.2 18.7 18.3 17.7_ _ 18.6
Background
31.3 11.4 4.4 28.6_ _ 20.7
146.9 154.1 197.8 -190.5 188.9
2.39 3.84 3.59 1.85 2.84
LOglC
The critical concentration of Cd in the kidney wrtex is 200 pglg wet weight, and the mean concentration is 20-35 pglg wet weight. The mean
AttemDt to nrotecl senslthre M i viduals. Provide a margin of safety; a m t to have no more than 150 pcg Cdl day ingested rather than 200 pa
concentration includes data from smokers who have higher concentrations than nonsmokers.
Cd1day. To protect heavy smokers, subtract 75 pg Cdlday (equlvalent dletary intake from smoking three packsof
Objective To avoid reaching 200 pg Cdlg in kidney cortex: The Kjellstrom-Nordberg model indicates that ingestion of 440 pg Cdlday for 50 years will result in 50% of the population achieving 200 pg Cdlg in the kidney cortex. while the Friberg model indicates that ingestion of 200 .ua- Cdldav for 50 vears will result in
cigaretteslday). Establish maximum advisable intake: 57-71 pg Cdlday (WO). Consider 70 pg Cdlday as the maximum dietaty intake. Consider the a v e w “background“ dietary intake as 39 pg Cdlday (FDA).
Therefore, consider the maximum
the FDA vegetable diel is derived from crops grown on a site which had previously received sewage sludge [old sit data; two years after sludge application ( 76)] klQeaW k d W r y M
Cumulative
cd .pp11.=.tlon
N A USDA
5 7
.FmdCUlWmWl ’
nohQpmnt.o.olth. di.1 Is det1v.d hom
SOH
soli
CEC
5.8 4.9
NIA
O I b imake. dv
8
44.6 422.3
wt lsarns
.
22.2 211.0
11.1 105.5
4.5 42.2
4.95 osrden hits. 13.1: mlatm
Volume 15. Number 8. August 1981 885
sludge is used as a nitrogen fertilizer
cd cont.nt
content of me New YaX s
agencies formalized federal policy and guidance for the controlled application of municipal sewage sludge to land used for the production of fruits and vegetables (17). These guidelines state that the use of high-quality sludges in agriculture, combined with proper management procedures, should safeguard the consumer from contaminated crops and minimize any potential adverse effect on the environment. The federal guidelines are conservative but environmentally sound and are based on substantial field research conducted by federal agencies and other research institutions. A key element in the guidelines is the use of “high-quality sludges” at rates not to exceed crop nutrient needs. Sludges containing no more than 25 mg/kg cadmium, 1000 mg/kg lead, and 10 mg/kg PCB are considered to be of high quality under the federal guidelines. As noted in Table 6, highquality sludges applied as a nitrogen fertilizer could be applied annually to the same field for as much as 200 years before reaching the maximum cumulative cadmium loading allowable for acid soils. The federal guidance (17) notes that even though the maximum cumulative cadmium loading may eventually be reached, the soil would remain suitable for production of food crops, including fruits and vegetables.
Conclusions EPA guidelines for application of solid waste and sludges to land have resulted from an extensive review and evaluation of many studies correlating cadmium in soil with crop uptake and dietary cadmium intake with health effects. The guidelines have been re888
Environmental Science 8 Technology
viewed by FDA and USDA. Their conclusions have been summarized in a statement of unified federal policy and guidance which states that adherence to the guidelines will assure the safety and wholesomeness of fruit and vegetable crops grown on sludgeamended soils.
Acknowledgment Before publication, this article was commented on for technical accurac by Dr Robert H. Miller, Department o f Agron: omy, The Ohio State University, Columbus, Ohio 43210, and Dr. Lee E. Sommen, Professor of Agronomy, Purdue University, West Lafayette, Ind. 47907.
(ijj’iAo/wHo ~ x p e r t c o m m i t t e e o n~
a ~ Additives. “Evaluation of Certain Food Additives and the Contaminants Mercury, Lead, and Cadmium,” WHO Tech. Report No.
50551-59,1972. (16) US. EPA Background Document: Cu-
mulative Cadmium Application Rates, Criteria for Classification of Solid Waste Disp a l Facilities 40 CFR 257, U.S.EPA OEce of Solid Waste, 1979. (17) US. EPA, US. Food and Drug Administration: US. Deoartment of Amiculture. “Land Applicatidn of Municipd Scwagc Sludge for ihc Praductron of Fruits and Veertable A Statcrncnt of Federal Policv ._D andGuidance”; 1981.
References (1) Fed. Ren. 1919.9.41791.53438-53468.
(21, Friberg,-L.; Piicator, M.;Nordberg, G. Cadmium m the Environment”; CRC Press, Inc.:Cleveland. 1971.
