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Dietary intake of cadmium in the United States: 1920–1975
ENVIRONMENTAL
RESEARCH
27, l-9
Dietary
(1982)
Intake of Cadmium in the United States: 1920- 1975’ C. C. TRAVIS
Techrwlogy
Assessments National
AND E. L. ETNIER
Section. Heulth urd Safety Research Division. Lobomtory.’ Oak Ridge. Temessee 37830 Received
September
Oak
Ridge
15, 1980
Long-term changes in both per capita consumption rates of specific food categories and the concentration of cadmium in the foodstuffs were investigated for their effects on total dietary intake of cadmium. Results show that, under the assumption of historically constant levels of cadmium in foodstuffs, changes in dietary consumption patterns in the United States resulted in a decline in total cadmium intake of about 20% between 1945 and 1975. Even if historically increasing levels of cadmium in foodstuffs are assumed, the decline in consumption rates for food items with the highest concentrations resulted in an approximate steady state of cadmium intake from 1945 to 1975.
INTRODUCTION
Cadmium is a relatively rare, but widely distributed, element that has come to be recognized as a highly toxic and dangerous environmental pollutant. Excessive accumulation of cadmium in man results in a variety of maladies ranging from gastroenteritis and renal tubular dysfunction (I, 2) to a possible association with hypertension and cardiovascular disease (2-4). It is now generally accepted that food constitutes the principal environmental source of cadmium for the nonsmoking human population. Estimates of the average daily intake of cadmium via food in various foreign countries vary between 10 and 85 pg/day (5, 6). Values of lo-20 &day in Sweden, IS-35 &day in the United Kingdom, and as high as 215 &day in a polluted area of Japan have been reported (5). Estimates of daily intake reported for the United States vary between 20 and 70 &day (5, 6). Absorbed cadmium is stored mainly in the liver and kidneys, with the renal cortex recognized as the critical organ in long-term, low-level human exposure. It is estimated that renal damage can occur at cadmium concentrations of 200 ,ug/g wet wt in the kidney cortex (1, 7). Using this concentration as a limit, a tolerable daily intake of cadmium from foodstuffs can be estimated to be about 70 p.g/day (8). The average daily intake of cadmium via food is a function of both diet composition and concentration of cadmium in foodstuffs. The aim of this study was to investigate the effect on total dietary intake of cadmium of time-dependent changes in both diet composition and the concentration of cadmium in the foodstuffs. Food consumption patterns in the United States have changed dra* The U.S. Government’s right to retain a nonexclusive royalty-free license in and to the copyright covering this paper, for governmental purposes, is acknowledged. 2 Operated by Union Carbide Corporation under Contract W-7405.eng-26 for the U.S. Department of Energy.
0013-9351/82/010001-09$02.00/O Copyright Q 1982 by Academic Press. Inc. All rights of reproduction in any form reserved.
2
TRAVIS
AND
ETNIER
matically during the past 50 years. For example, it is estimated that per capita consumption of dairy products in the United States declined 22% from 1956 to the present (9). During the IO-year period between 1955 and 1965, per capita consumption of green or yellow vegetables decreased 19% while consumption of soft drinks, punches, and prepared desserts increased 79% (10). Such large changes in the eating habits of the U.S. population could result in temporal changes in total dietary intake of cadmium. Two direct methods for measuring daily cadmium intake have been reported in the literature. One is based on estimation of the cadmium content of various foodstuffs and surveys of the average daily intake of these foodstuffs (the market basket technique). The other is based on cadmium analysis of duplicates of all food eaten by an individual during one or more days (the total diet collection technique). In the present study, a form of the market basket technique was employed. Per capita food consumption statistics for the United States during the period 1920- 1975 (11, 12) were used to estimate apparent U.S. per capita consumption of six major food categories. Cadmium levels characteristic of these specific food categories were determined from the literature and were assumed to remain constant during the period 1920- 1975. Per capita consumption data were used to determine historical changes in average daily intake of cadmium. Results of the study show that if all other factors are held constant, changes in per capita dietary consumption patterns resulted in a decline of about 20% in the average daily intake of cadmium in the United States between 1945 and 1975. There is some question concerning whether the concentration of cadmium in foodstuffs has remained historically constant. It is generally agreed that the amount of cadmium available in the environment for plant and animal uptake is increasing. Between 1920 and 1975, cadmium production in the United States increased from 59 to 1989 metric tons (1969 was the peak production year at 5736 metric tons) (13). Total emissions of cadmium to the environment from all sources in the United States in 1968 were estimated to be greater than 3600 metric tons (14). Cadmium has a variety of industrial uses, principal among which are electroplating (coating steel, iron, copper, brass, and other objects with cadmium confers resistance to corrosion) and use as a pigment in plastics, ceramics, paints, textiles, rubber, glass, enamels, and printing inks. Phosphate fertilizers, atmospheric fallout, and sewage sludge continually add cadmium to the soil, where it enters the terrestrial food chains. Concentrations of cadmium in coal (0.02 to 10 pg/g) and in heating oil (0.53 to 10.4 pg/g) (15) also contribute to environmental levels of cadmium. No abatement is expected in the foreseeable future since it is estimated that domestic utilization of cadmium in the United States will increase at a 4% annual rate until the year 2000 (14). The increasing availability of cadmium in the environment may have resulted in increased cadmium concentrations in foodstuffs. To assess the consequences of this possibility, the market basket technique was also used to estimate the average daily intake of cadmium under the assumption of historical increases in the cadmium content of foodstuffs. Taking this possible increase into account, the market basket technique yields an approximately constant average daily intake of cadmium over the period 1945 through 1975. Thus, even though environmental levels
DIETARY
CADMIUM
IN
THE
UNITED
3
STATES
of cadmium have been increasing in the United States since 1945, changes in dietary composition patterns may have resulted in a fairly constant total per capita intake of cadmium via food. METHODS AND RESULTS The U.S. Food and Drug Administration has a continuing program to monitor the levels of various heavy metals, including cadmium, in food. The monitoring protocol is that of the Total Diet Study (16), in which “market baskets” of typical foods and beverages consumed by 15- to 20-year-old American males are collected in various geographical locations at regular intervals during the year, divided into food classes, and analyzed. For purposes of the present study, six broad food categories were selected from those used in the Total Diet Study: dairy products; meat, fish, and poultry; grain and cereal: potatoes: vegetables; and fruits. Selection of categories was determined by availability of data on temporal dietary consumption patterns for the United States over the period 1920- 1975. The chosen categories represent 80% of the contribution to total dietary intake of cadmium as reported by Mahaffey er af. (17). An additional 12.7% of the dietary intake of cadmium results from consumption of beverages (tea, cocoa, drinking water, coffee, and soft drinks). However, this category could not be included in the study due to insufficient historical consumption data. The six categories included in the present study represent 91.6% of total intake of cadmium from solid food. Concentrations of cadmium in the selected food categories are shown in Table 1. Food consumption data for the selected food categories, except that of grain and cereal, were taken from the U.S. Department of Agriculture’s “Historical Statistics of the United States” ( 1 I), which covers the years 1920- 1970. Data on grain and cereal consumption were obtained from “Agricultural Statistics” (12). Historical dairy product consumption data (11) were combined to represent as closely as possible the category described in Mahaffey et al, (17). This includes fluid milk and cream, condensed and evaporated milk, cheese, ice cream, margarine, and butter. Potato consumption data included both white and sweet potatoes. Data from 1970-1975 were taken from the “U.S. Statistical Abstract” (18).
CONCENTRATION
Food
OFCADMIUM
category
Grain and cereal products Fruits Potatoes Dairy products Vegetables Meat, fish, and poultry ” Adapted
from
Mahaffey
et al. (I2).
TABLE 1 IN SELECTED
Foon
CATEGORIEV
Concentration (PLg cw 0.032 0.042 0.045 0.005 0.026 0.009
in food
4
TRAVIS
AND
ETNIER
Estimated U.S. per capita consumption of the six selected food categories over the period 1920- 1975 is shown graphically in Figs. l-3. Per capita consumption of meat and vegetables rose during this period, while consumption of grain and cereal products, dairy products, fruits, and potatoes declined. The most dramatic changes occurred in consumption of grain and cereal products and of potatoes (82 and 58% decline, respectively). The significance of these declines can be seen in the fact that these two categories accounted for 40.1% of the total dietary intake of cadmium in the 1973 Total Diet Survey (17). Vegetable as well as meat, fish, and poultry consumption increased (72 and 3!X%, respectiveiy); however, these two categories accounted for only 13.4% of the total dietary intake of cadmium reported in 1973 (17). Combining daily per capita consumption data with data on concentration of cadmium in the various food categories results in an estimate of total intake of cadmium from the six categories. Figure 4 shows this intake over the period 1920- 1975. The figure was constructed under the assumption that concentrations of cadmium in the six food categories have remained constant over time. It suggests that the average daily per capita intake of cadmium in the United States remained approximately constant over the period 1920- 1945 and then declined about 200/o to present levels. The assumption that cadmium concentrations in the six food categories have remained constant over time is probably incorrect. We have already cited evidence supporting the hypothesis of an increase in environmental levels of cadmium. This hypothesis gains further support from the only empirical study avail-
250
--4910 FIG. 1. Apparent 1909- 1975 (lb/year),
FRESH, CANNED AND - FROZEN VEGETABLES
20 30 40 50 60 70 (9x)
30 40 50 60 70
U.S. per capita meat consumption (beef, pork, and vegetable consumption (fresh, canned, frozen),
lamb, chicken, and 1919% 1975 (lb/year).
fish),
DIETARY
CADMIUM
IN THE
UNITED I
I
5
STATES I
I
I
GRAIN
(920 FIG. 2. Apparent 1900- 1975 (lb/year).
U.S.
30
per capita
40 milk
50
60
70 (920 30
consumption,
WHITE AND SWEET POTATOES
1920-
i
4910 20 30 40 50 60 70 FIG. 3. Apparent ion (fresh, canned,
U.S. dried,
per capita potato consumption, frozen), 1909- 1975 (lb/year).
40
50
60
70
1975 (lb/year),
FRESH, CANNED, FROZEN AND DRIED
_
and grain
FRUIT
consumption
i
1910 20 30 40 50 60 70 1909-1975
(lb/year).
and fruit
consump-
6
TRAVIS
AND
ETNIER
FIG. 4. Average daily intake of cadmium in the U.S., 1920-1975 (based on the assumption of historically constant levels of cadmium in foodstuffs).
able on historical levels of cadmium in foodstuffs. Kjellstrom er al. (19) found that cadmium concentrations in Swedish wheat and barley increased in an almost linear fashion from 1920 to 1972. Results of their study on wheat are shown in Fig. 5. The data show a clear increase in cadmium concentrations in wheat since 1920. Measurements prior to 1920 indicate the possibility that cadmium concentrations in food remained constant until that time. On the basis of these data, it was decided to incorporate a linear increase in cadmium concentration in foodstuffs into our calculations. If X represents the calendar year, then Y, as given by Y = 0.0065X -
(1)
11.818,
represents the assumed ratio for the given year of cadmium concentrations in the various food categories relative to the 1972 values. In this equation, X is restricted to values greater than 1920. Function (1) was constructed so that the rate of increase of cadmium concentration in U.S. foodstuffs coincides with the average rate of increase for spring and fall wheat as reported by Kjellstrom et al. (19). Figure 6 shows the average daily intake of cadmium (from the six food
. FALL WHEAT, o FALL WHEAT, REGRESSION
-----
UPPSALA OTHER AREAS LINE, UPPSALA
1N SWEDEN
. .
0 .
.
. .
0
0
.
l .
. c-
c--
0 . --z .
“•;
-r
8
---
-em-‘:. .
.
p’#.ee.* .
11IIrIllrl u370 00
90
0 1900
., 1ilIIIrIr IO
20
30
40
50
60
70
I30
YEAR FIG. 5. Concentration of cadmium in Swedish wheat as a function of time. Data from Kjellstrbm e/ (II. (19).
DIETARY
IiJk +o
CADMIUM
IN THE UNITED
7
STATES
:: 5 -
15 1920
I
I 1930
I
I 1940
I
I 1950
I
I I960
I
I I970
FIG. 6. Average daily intake of cadmium in the United States, 1920- 1975 (based on the assumption of historically increasing levels of cadmium in foodstuffs).
categories) in the United States over the period 1920- 1975 under the assumption of time-dependent concentrations of cadmium in foodstuffs. It can be seen that the assumed rise in cadmium concentrations in foodstuffs resulted in an approximate 34% increase in the daily intake of cadmium in the United States during the period 1920- 1945. However, from 1950 to 1965, the rise in foodstuff concentrations was balanced by a decline in consumption rates for food items with the highest cadmium concentrations, with the result that the average daily intake of cadmium remained approximately constant. From 1965- 1975, the average daily intake of cadmium increased slightly (about 9%), a direct result of the assumed increase in environmental levels of cadmium (compare Fig. 6 with Fig. 4 for the period 1965- 1975). Overall, however, the data suggest that even if environmental levels of cadmium have been increasing, changes in per capita food consumption patterns have caused the average daily intake of cadmium in the United States to remain approximately constant since 1945. DISCUSSION
Eating habits in the United States have changed considerably since the turn of the century. Changes in per capita consumption rates of specific food categories could result in a change in the total intake of cadmium. Using data on per capita consumption rates in the United States over the period 1920- 1975, this hypothesis was investigated under two different assumptions: (1) historically constant environmental levels of cadmium and (2) historically increasing environmental levels of cadmium. Our findings indicate that under the assumption of constant cadmium content in foodstuffs, changes in food consumption patterns caused total dietary intake of cadmium to decrease about 20% between 1945 and 1975. If one assumes increasing concentrations of cadmium in foodstuffs during this period, dietary intake of cadmium remained fairly constant. Thus, our findings indicate that even though environmental levels of cadmium may have increased over the past 30 to 40 years, it is possible that changes in food consumption patterns caused total dietary intake of cadmium to remain constant or decline slightly. Evidence to support this conclusion was found in the Total Diet Survey program. Although changes in cadmium concentrations in successive crops of certain plant foods
8
TRAVIS
AND
ETNIER
have been documented (19), no temporal trend of increasing cadmium exposure in the diet was apparent in the Total Diet Survey from 1968 through 1974 (17). The constancy of the dietary intake of cadmium over the period 1950- 1975 has implications concerning the observed age dependency of cadmium body burdens in man. Human autopsy studies show a definite time-dependent pattern in renal cadmium levels as a function of age (20, 21). Starting from near zero in infancy, kidney concentrations increase steadily with age until about 45 years of age, and thereafter they decline. Friberg rt crl. (l), Kjellstrom (22), Travis and Haddock (23), and others have discussed possible explanations for this observed decrease in renal concentrations of cadmium in older age groups. Factors considered were: (a) age-related exposure variations caused by age-dependent changes in caloric intake and smoking patterns; (b) cohort-related exposure variations caused by an increase in environmental levels of Cd; and (c) age-related elimination variations caused by functional and morphological changes in the renal cortex. Using a single compartment model for the human body, Travis and Haddock demonstrated that neither age-dependent changes in caloric intake and smoking patterns nor cohortrelated exposure variations due to increasing environmental levels of cadmium were the cause of the observed decrease. The most critical parameter in analyzing the effect on autopsy data of historical increase in environmental levels of cadmium was the rate of increase of cadmium concentrations in foodstuffs between 1950 and 1972. With these increased environmental levels, Travis and Haddock assumed the same rate of increase in cadium intake as that expressed in Eq. (1). They found that this rate of increase could not account for the magnitude of the decline in kidney cadmium levels observed in older age groups, and in fact did little to change the overall shape of kidney burden curves. This conclusion is strengthened even further by our observations concerning the effect of temporal changes in diet composition on total cadmium intake. Even if environmental levels of cadmium did increase somewhat faster than Travis and Haddock assumed, changes in consumption patterns would have moderated any increase in cadmium intake to the human body. Thus, age-related functional and morphological changes in the renal cortex seem to be the most likely explanation of the decline in renal cadmium levels of older age groups observed in autopsy studies. REFERENCES 1. Friberg, L., Piscator, M., Nordberg, G. F., and Kjellstrom, T. (1974). “Cadmium in the Environment,” 2nd ed., CRC Press, Cleveland. 2. Commission of the European Communities (1978). “Criteria (Dose/Effect Relationships) for Cadmium.” Pergamon, Elmsford, New York. 3. Schroeder, H. A., and Buckman, J. (1967). Cadmium hypertension. Arch. Envirorr. He&h 14, 693. 4. Schroeder, H. A., (1967). Cadmium, chromium and cardiovascular disease. Circu/afio/? 35, 570. 5. Drury, J. S., and Hammons, A. S. (1979). “Cadmium in Foods: A Review of the World’s Literature.” ORNWEIS-149, EPA-56012.78-007. 6. DiFerrante, E. (Ed.) (1977) Trace metals: Exposure and health effects. In “Proceedings Research Seminar held at the University of Surrey, Guildford, United Kingdom, July lo- 13, 1978,” p. 37 Pergamon, Oxford. 7. World Health Organization (1977) WHO environmental health criteria for cadmium. Atnbio 6, 287-290.
DIETARY
CADMIUM
IN THE UNITED
STATES
9
8. World Health Organization (1972) “Evaluation of Certain Food Additives and the Contaminates Mercury, Lead and Cadmium.” Geneva WHO Technical Report Series, No. 505. 9. Manchester, A. C. (1978) “Dairy Price Policy-Setting-Problems-Alternatives.” U.S. Department of Agriculture, Economics. Statistics, and Cooperative Service, Agricultural Economic Report No.
402.
10. U. S. Department of Agriculture (1965). Food and nutrient intake of individuals in the United States, Spring 1965. I/I “Household Food Consumption Survey 1965- 1966,” Report No. 11. 11. U.S. Department of Commerce. Bureau of the Census. “Bicentennial Edition-Historical Statistics of the United States. Colonial Times to 1970. Part I,” 93rd Congress, 1st Session, House Document No. 93-78 (pt. 1). 12. U.S. Department of Agriculture (1967) “Agricultural Statistics.” U.S. Govt. Printing Office. Washington, D.C. 13. Nriagu. J. 0. (1980). Production, uses, and properties of cadmium. 111“Cadmium in the Environment,” Part 1, “Ecological Cycling” (J. 0. Nriagu, Ed.). Wiley, New York. 14. Hammons, A. S.. Huff. J. E.. Braunstein, H. M., Drury, J. S.. Shriner. C. R., Lewis, E. B., Whitfield. B, L., and Towill, L. E. ( 1978). “Reviews of the Environmental Effects of Pollutants: IV Cadmium,” ORNUEIS-106, EPA-600/l-78-026. 15. Hiatt, V.. and Huff. J. E. (1975). The environmental impact of cadmium: An overview. Inr. J. EtrtYrotc.
Stud.,
7, 277 -285.
16. Food and Drug Administration (1974). “Total Diet Studies-Adult.” Compliance Program Guidance Manual 7320.08. FDA, Washington, D.C. 17. Mahaffey, K. R.. Corneliussen, P. E., Jelinek, C. F.. and Fiorino, J. A. (1975). Heavy metal exposure in foods. Entfrorl. Hrctlth Prrsp. 12, 63-69. 18. U.S. Department of Commerce. (1978). “Statistical Abstract of the United States, 1978,” 99th annual ed. USDOC and Bureau of the Census, Washington, D.C. 19. Kjellstrom. T.. Lind. B.. Linnman, L., and Elinder, C. (1975). Variation of cadmium concentration in Swedish wheat and barley. Arch. E/r~~iron. He~lrl7 30, 321-328. 20. Schroeder. H. A., Nasson. A. P., Tipton, I. H. and Balassa, J. J. (1967). Essential trace elements in man: Zinc. Relation to environmental cadmium. J. Chrouic Dis. 20, 179-210. 21. Hammer, D. I.. Colucci. A. V., Hasselbad, V.. Williams, M. E.. and Pinkerton, C. (1973). Cadmium and lead in autopsy tissues. J. Occirp. Md. 12, 956. 22. Kjellstrom, T. (1971) A mathematical model for the accumulation of cadmium in human kidney cortex. Non/. Hyg. Tic/s!+. 53, 111- 117. 23. Travis, C. C.. and Haddock, A. G. (1980). Interpretation of the observed age-dependency of cadmium body burdens in man. Entirotr. Rc~s. 22, 46-60.
RESEARCH
27, l-9
Dietary
(1982)
Intake of Cadmium in the United States: 1920- 1975’ C. C. TRAVIS
Techrwlogy
Assessments National
AND E. L. ETNIER
Section. Heulth urd Safety Research Division. Lobomtory.’ Oak Ridge. Temessee 37830 Received
September
Oak
Ridge
15, 1980
Long-term changes in both per capita consumption rates of specific food categories and the concentration of cadmium in the foodstuffs were investigated for their effects on total dietary intake of cadmium. Results show that, under the assumption of historically constant levels of cadmium in foodstuffs, changes in dietary consumption patterns in the United States resulted in a decline in total cadmium intake of about 20% between 1945 and 1975. Even if historically increasing levels of cadmium in foodstuffs are assumed, the decline in consumption rates for food items with the highest concentrations resulted in an approximate steady state of cadmium intake from 1945 to 1975.
INTRODUCTION
Cadmium is a relatively rare, but widely distributed, element that has come to be recognized as a highly toxic and dangerous environmental pollutant. Excessive accumulation of cadmium in man results in a variety of maladies ranging from gastroenteritis and renal tubular dysfunction (I, 2) to a possible association with hypertension and cardiovascular disease (2-4). It is now generally accepted that food constitutes the principal environmental source of cadmium for the nonsmoking human population. Estimates of the average daily intake of cadmium via food in various foreign countries vary between 10 and 85 pg/day (5, 6). Values of lo-20 &day in Sweden, IS-35 &day in the United Kingdom, and as high as 215 &day in a polluted area of Japan have been reported (5). Estimates of daily intake reported for the United States vary between 20 and 70 &day (5, 6). Absorbed cadmium is stored mainly in the liver and kidneys, with the renal cortex recognized as the critical organ in long-term, low-level human exposure. It is estimated that renal damage can occur at cadmium concentrations of 200 ,ug/g wet wt in the kidney cortex (1, 7). Using this concentration as a limit, a tolerable daily intake of cadmium from foodstuffs can be estimated to be about 70 p.g/day (8). The average daily intake of cadmium via food is a function of both diet composition and concentration of cadmium in foodstuffs. The aim of this study was to investigate the effect on total dietary intake of cadmium of time-dependent changes in both diet composition and the concentration of cadmium in the foodstuffs. Food consumption patterns in the United States have changed dra* The U.S. Government’s right to retain a nonexclusive royalty-free license in and to the copyright covering this paper, for governmental purposes, is acknowledged. 2 Operated by Union Carbide Corporation under Contract W-7405.eng-26 for the U.S. Department of Energy.
0013-9351/82/010001-09$02.00/O Copyright Q 1982 by Academic Press. Inc. All rights of reproduction in any form reserved.
2
TRAVIS
AND
ETNIER
matically during the past 50 years. For example, it is estimated that per capita consumption of dairy products in the United States declined 22% from 1956 to the present (9). During the IO-year period between 1955 and 1965, per capita consumption of green or yellow vegetables decreased 19% while consumption of soft drinks, punches, and prepared desserts increased 79% (10). Such large changes in the eating habits of the U.S. population could result in temporal changes in total dietary intake of cadmium. Two direct methods for measuring daily cadmium intake have been reported in the literature. One is based on estimation of the cadmium content of various foodstuffs and surveys of the average daily intake of these foodstuffs (the market basket technique). The other is based on cadmium analysis of duplicates of all food eaten by an individual during one or more days (the total diet collection technique). In the present study, a form of the market basket technique was employed. Per capita food consumption statistics for the United States during the period 1920- 1975 (11, 12) were used to estimate apparent U.S. per capita consumption of six major food categories. Cadmium levels characteristic of these specific food categories were determined from the literature and were assumed to remain constant during the period 1920- 1975. Per capita consumption data were used to determine historical changes in average daily intake of cadmium. Results of the study show that if all other factors are held constant, changes in per capita dietary consumption patterns resulted in a decline of about 20% in the average daily intake of cadmium in the United States between 1945 and 1975. There is some question concerning whether the concentration of cadmium in foodstuffs has remained historically constant. It is generally agreed that the amount of cadmium available in the environment for plant and animal uptake is increasing. Between 1920 and 1975, cadmium production in the United States increased from 59 to 1989 metric tons (1969 was the peak production year at 5736 metric tons) (13). Total emissions of cadmium to the environment from all sources in the United States in 1968 were estimated to be greater than 3600 metric tons (14). Cadmium has a variety of industrial uses, principal among which are electroplating (coating steel, iron, copper, brass, and other objects with cadmium confers resistance to corrosion) and use as a pigment in plastics, ceramics, paints, textiles, rubber, glass, enamels, and printing inks. Phosphate fertilizers, atmospheric fallout, and sewage sludge continually add cadmium to the soil, where it enters the terrestrial food chains. Concentrations of cadmium in coal (0.02 to 10 pg/g) and in heating oil (0.53 to 10.4 pg/g) (15) also contribute to environmental levels of cadmium. No abatement is expected in the foreseeable future since it is estimated that domestic utilization of cadmium in the United States will increase at a 4% annual rate until the year 2000 (14). The increasing availability of cadmium in the environment may have resulted in increased cadmium concentrations in foodstuffs. To assess the consequences of this possibility, the market basket technique was also used to estimate the average daily intake of cadmium under the assumption of historical increases in the cadmium content of foodstuffs. Taking this possible increase into account, the market basket technique yields an approximately constant average daily intake of cadmium over the period 1945 through 1975. Thus, even though environmental levels
DIETARY
CADMIUM
IN
THE
UNITED
3
STATES
of cadmium have been increasing in the United States since 1945, changes in dietary composition patterns may have resulted in a fairly constant total per capita intake of cadmium via food. METHODS AND RESULTS The U.S. Food and Drug Administration has a continuing program to monitor the levels of various heavy metals, including cadmium, in food. The monitoring protocol is that of the Total Diet Study (16), in which “market baskets” of typical foods and beverages consumed by 15- to 20-year-old American males are collected in various geographical locations at regular intervals during the year, divided into food classes, and analyzed. For purposes of the present study, six broad food categories were selected from those used in the Total Diet Study: dairy products; meat, fish, and poultry; grain and cereal: potatoes: vegetables; and fruits. Selection of categories was determined by availability of data on temporal dietary consumption patterns for the United States over the period 1920- 1975. The chosen categories represent 80% of the contribution to total dietary intake of cadmium as reported by Mahaffey er af. (17). An additional 12.7% of the dietary intake of cadmium results from consumption of beverages (tea, cocoa, drinking water, coffee, and soft drinks). However, this category could not be included in the study due to insufficient historical consumption data. The six categories included in the present study represent 91.6% of total intake of cadmium from solid food. Concentrations of cadmium in the selected food categories are shown in Table 1. Food consumption data for the selected food categories, except that of grain and cereal, were taken from the U.S. Department of Agriculture’s “Historical Statistics of the United States” ( 1 I), which covers the years 1920- 1970. Data on grain and cereal consumption were obtained from “Agricultural Statistics” (12). Historical dairy product consumption data (11) were combined to represent as closely as possible the category described in Mahaffey et al, (17). This includes fluid milk and cream, condensed and evaporated milk, cheese, ice cream, margarine, and butter. Potato consumption data included both white and sweet potatoes. Data from 1970-1975 were taken from the “U.S. Statistical Abstract” (18).
CONCENTRATION
Food
OFCADMIUM
category
Grain and cereal products Fruits Potatoes Dairy products Vegetables Meat, fish, and poultry ” Adapted
from
Mahaffey
et al. (I2).
TABLE 1 IN SELECTED
Foon
CATEGORIEV
Concentration (PLg cw 0.032 0.042 0.045 0.005 0.026 0.009
in food
4
TRAVIS
AND
ETNIER
Estimated U.S. per capita consumption of the six selected food categories over the period 1920- 1975 is shown graphically in Figs. l-3. Per capita consumption of meat and vegetables rose during this period, while consumption of grain and cereal products, dairy products, fruits, and potatoes declined. The most dramatic changes occurred in consumption of grain and cereal products and of potatoes (82 and 58% decline, respectively). The significance of these declines can be seen in the fact that these two categories accounted for 40.1% of the total dietary intake of cadmium in the 1973 Total Diet Survey (17). Vegetable as well as meat, fish, and poultry consumption increased (72 and 3!X%, respectiveiy); however, these two categories accounted for only 13.4% of the total dietary intake of cadmium reported in 1973 (17). Combining daily per capita consumption data with data on concentration of cadmium in the various food categories results in an estimate of total intake of cadmium from the six categories. Figure 4 shows this intake over the period 1920- 1975. The figure was constructed under the assumption that concentrations of cadmium in the six food categories have remained constant over time. It suggests that the average daily per capita intake of cadmium in the United States remained approximately constant over the period 1920- 1945 and then declined about 200/o to present levels. The assumption that cadmium concentrations in the six food categories have remained constant over time is probably incorrect. We have already cited evidence supporting the hypothesis of an increase in environmental levels of cadmium. This hypothesis gains further support from the only empirical study avail-
250
--4910 FIG. 1. Apparent 1909- 1975 (lb/year),
FRESH, CANNED AND - FROZEN VEGETABLES
20 30 40 50 60 70 (9x)
30 40 50 60 70
U.S. per capita meat consumption (beef, pork, and vegetable consumption (fresh, canned, frozen),
lamb, chicken, and 1919% 1975 (lb/year).
fish),
DIETARY
CADMIUM
IN THE
UNITED I
I
5
STATES I
I
I
GRAIN
(920 FIG. 2. Apparent 1900- 1975 (lb/year).
U.S.
30
per capita
40 milk
50
60
70 (920 30
consumption,
WHITE AND SWEET POTATOES
1920-
i
4910 20 30 40 50 60 70 FIG. 3. Apparent ion (fresh, canned,
U.S. dried,
per capita potato consumption, frozen), 1909- 1975 (lb/year).
40
50
60
70
1975 (lb/year),
FRESH, CANNED, FROZEN AND DRIED
_
and grain
FRUIT
consumption
i
1910 20 30 40 50 60 70 1909-1975
(lb/year).
and fruit
consump-
6
TRAVIS
AND
ETNIER
FIG. 4. Average daily intake of cadmium in the U.S., 1920-1975 (based on the assumption of historically constant levels of cadmium in foodstuffs).
able on historical levels of cadmium in foodstuffs. Kjellstrom er al. (19) found that cadmium concentrations in Swedish wheat and barley increased in an almost linear fashion from 1920 to 1972. Results of their study on wheat are shown in Fig. 5. The data show a clear increase in cadmium concentrations in wheat since 1920. Measurements prior to 1920 indicate the possibility that cadmium concentrations in food remained constant until that time. On the basis of these data, it was decided to incorporate a linear increase in cadmium concentration in foodstuffs into our calculations. If X represents the calendar year, then Y, as given by Y = 0.0065X -
(1)
11.818,
represents the assumed ratio for the given year of cadmium concentrations in the various food categories relative to the 1972 values. In this equation, X is restricted to values greater than 1920. Function (1) was constructed so that the rate of increase of cadmium concentration in U.S. foodstuffs coincides with the average rate of increase for spring and fall wheat as reported by Kjellstrom et al. (19). Figure 6 shows the average daily intake of cadmium (from the six food
. FALL WHEAT, o FALL WHEAT, REGRESSION
-----
UPPSALA OTHER AREAS LINE, UPPSALA
1N SWEDEN
. .
0 .
.
. .
0
0
.
l .
. c-
c--
0 . --z .
“•;
-r
8
---
-em-‘:. .
.
p’#.ee.* .
11IIrIllrl u370 00
90
0 1900
., 1ilIIIrIr IO
20
30
40
50
60
70
I30
YEAR FIG. 5. Concentration of cadmium in Swedish wheat as a function of time. Data from Kjellstrbm e/ (II. (19).
DIETARY
IiJk +o
CADMIUM
IN THE UNITED
7
STATES
:: 5 -
15 1920
I
I 1930
I
I 1940
I
I 1950
I
I I960
I
I I970
FIG. 6. Average daily intake of cadmium in the United States, 1920- 1975 (based on the assumption of historically increasing levels of cadmium in foodstuffs).
categories) in the United States over the period 1920- 1975 under the assumption of time-dependent concentrations of cadmium in foodstuffs. It can be seen that the assumed rise in cadmium concentrations in foodstuffs resulted in an approximate 34% increase in the daily intake of cadmium in the United States during the period 1920- 1945. However, from 1950 to 1965, the rise in foodstuff concentrations was balanced by a decline in consumption rates for food items with the highest cadmium concentrations, with the result that the average daily intake of cadmium remained approximately constant. From 1965- 1975, the average daily intake of cadmium increased slightly (about 9%), a direct result of the assumed increase in environmental levels of cadmium (compare Fig. 6 with Fig. 4 for the period 1965- 1975). Overall, however, the data suggest that even if environmental levels of cadmium have been increasing, changes in per capita food consumption patterns have caused the average daily intake of cadmium in the United States to remain approximately constant since 1945. DISCUSSION
Eating habits in the United States have changed considerably since the turn of the century. Changes in per capita consumption rates of specific food categories could result in a change in the total intake of cadmium. Using data on per capita consumption rates in the United States over the period 1920- 1975, this hypothesis was investigated under two different assumptions: (1) historically constant environmental levels of cadmium and (2) historically increasing environmental levels of cadmium. Our findings indicate that under the assumption of constant cadmium content in foodstuffs, changes in food consumption patterns caused total dietary intake of cadmium to decrease about 20% between 1945 and 1975. If one assumes increasing concentrations of cadmium in foodstuffs during this period, dietary intake of cadmium remained fairly constant. Thus, our findings indicate that even though environmental levels of cadmium may have increased over the past 30 to 40 years, it is possible that changes in food consumption patterns caused total dietary intake of cadmium to remain constant or decline slightly. Evidence to support this conclusion was found in the Total Diet Survey program. Although changes in cadmium concentrations in successive crops of certain plant foods
8
TRAVIS
AND
ETNIER
have been documented (19), no temporal trend of increasing cadmium exposure in the diet was apparent in the Total Diet Survey from 1968 through 1974 (17). The constancy of the dietary intake of cadmium over the period 1950- 1975 has implications concerning the observed age dependency of cadmium body burdens in man. Human autopsy studies show a definite time-dependent pattern in renal cadmium levels as a function of age (20, 21). Starting from near zero in infancy, kidney concentrations increase steadily with age until about 45 years of age, and thereafter they decline. Friberg rt crl. (l), Kjellstrom (22), Travis and Haddock (23), and others have discussed possible explanations for this observed decrease in renal concentrations of cadmium in older age groups. Factors considered were: (a) age-related exposure variations caused by age-dependent changes in caloric intake and smoking patterns; (b) cohort-related exposure variations caused by an increase in environmental levels of Cd; and (c) age-related elimination variations caused by functional and morphological changes in the renal cortex. Using a single compartment model for the human body, Travis and Haddock demonstrated that neither age-dependent changes in caloric intake and smoking patterns nor cohortrelated exposure variations due to increasing environmental levels of cadmium were the cause of the observed decrease. The most critical parameter in analyzing the effect on autopsy data of historical increase in environmental levels of cadmium was the rate of increase of cadmium concentrations in foodstuffs between 1950 and 1972. With these increased environmental levels, Travis and Haddock assumed the same rate of increase in cadium intake as that expressed in Eq. (1). They found that this rate of increase could not account for the magnitude of the decline in kidney cadmium levels observed in older age groups, and in fact did little to change the overall shape of kidney burden curves. This conclusion is strengthened even further by our observations concerning the effect of temporal changes in diet composition on total cadmium intake. Even if environmental levels of cadmium did increase somewhat faster than Travis and Haddock assumed, changes in consumption patterns would have moderated any increase in cadmium intake to the human body. Thus, age-related functional and morphological changes in the renal cortex seem to be the most likely explanation of the decline in renal cadmium levels of older age groups observed in autopsy studies. REFERENCES 1. Friberg, L., Piscator, M., Nordberg, G. F., and Kjellstrom, T. (1974). “Cadmium in the Environment,” 2nd ed., CRC Press, Cleveland. 2. Commission of the European Communities (1978). “Criteria (Dose/Effect Relationships) for Cadmium.” Pergamon, Elmsford, New York. 3. Schroeder, H. A., and Buckman, J. (1967). Cadmium hypertension. Arch. Envirorr. He&h 14, 693. 4. Schroeder, H. A., (1967). Cadmium, chromium and cardiovascular disease. Circu/afio/? 35, 570. 5. Drury, J. S., and Hammons, A. S. (1979). “Cadmium in Foods: A Review of the World’s Literature.” ORNWEIS-149, EPA-56012.78-007. 6. DiFerrante, E. (Ed.) (1977) Trace metals: Exposure and health effects. In “Proceedings Research Seminar held at the University of Surrey, Guildford, United Kingdom, July lo- 13, 1978,” p. 37 Pergamon, Oxford. 7. World Health Organization (1977) WHO environmental health criteria for cadmium. Atnbio 6, 287-290.
DIETARY
CADMIUM
IN THE UNITED
STATES
9
8. World Health Organization (1972) “Evaluation of Certain Food Additives and the Contaminates Mercury, Lead and Cadmium.” Geneva WHO Technical Report Series, No. 505. 9. Manchester, A. C. (1978) “Dairy Price Policy-Setting-Problems-Alternatives.” U.S. Department of Agriculture, Economics. Statistics, and Cooperative Service, Agricultural Economic Report No.
402.
10. U. S. Department of Agriculture (1965). Food and nutrient intake of individuals in the United States, Spring 1965. I/I “Household Food Consumption Survey 1965- 1966,” Report No. 11. 11. U.S. Department of Commerce. Bureau of the Census. “Bicentennial Edition-Historical Statistics of the United States. Colonial Times to 1970. Part I,” 93rd Congress, 1st Session, House Document No. 93-78 (pt. 1). 12. U.S. Department of Agriculture (1967) “Agricultural Statistics.” U.S. Govt. Printing Office. Washington, D.C. 13. Nriagu. J. 0. (1980). Production, uses, and properties of cadmium. 111“Cadmium in the Environment,” Part 1, “Ecological Cycling” (J. 0. Nriagu, Ed.). Wiley, New York. 14. Hammons, A. S.. Huff. J. E.. Braunstein, H. M., Drury, J. S.. Shriner. C. R., Lewis, E. B., Whitfield. B, L., and Towill, L. E. ( 1978). “Reviews of the Environmental Effects of Pollutants: IV Cadmium,” ORNUEIS-106, EPA-600/l-78-026. 15. Hiatt, V.. and Huff. J. E. (1975). The environmental impact of cadmium: An overview. Inr. J. EtrtYrotc.
Stud.,
7, 277 -285.
16. Food and Drug Administration (1974). “Total Diet Studies-Adult.” Compliance Program Guidance Manual 7320.08. FDA, Washington, D.C. 17. Mahaffey, K. R.. Corneliussen, P. E., Jelinek, C. F.. and Fiorino, J. A. (1975). Heavy metal exposure in foods. Entfrorl. Hrctlth Prrsp. 12, 63-69. 18. U.S. Department of Commerce. (1978). “Statistical Abstract of the United States, 1978,” 99th annual ed. USDOC and Bureau of the Census, Washington, D.C. 19. Kjellstrom. T.. Lind. B.. Linnman, L., and Elinder, C. (1975). Variation of cadmium concentration in Swedish wheat and barley. Arch. E/r~~iron. He~lrl7 30, 321-328. 20. Schroeder. H. A., Nasson. A. P., Tipton, I. H. and Balassa, J. J. (1967). Essential trace elements in man: Zinc. Relation to environmental cadmium. J. Chrouic Dis. 20, 179-210. 21. Hammer, D. I.. Colucci. A. V., Hasselbad, V.. Williams, M. E.. and Pinkerton, C. (1973). Cadmium and lead in autopsy tissues. J. Occirp. Md. 12, 956. 22. Kjellstrom, T. (1971) A mathematical model for the accumulation of cadmium in human kidney cortex. Non/. Hyg. Tic/s!+. 53, 111- 117. 23. Travis, C. C.. and Haddock, A. G. (1980). Interpretation of the observed age-dependency of cadmium body burdens in man. Entirotr. Rc~s. 22, 46-60.