Environ. Scl. Technol. 1984, 18, 628-631
Mullin, M. D. (Large Lakes Research Station, U.S.EPA) “PCBs and Other Chlorinated Hydrocarbons in Lake Water, Fish, Human Blood and Human Milk A Qualitative Comparison Utilizing High Resolution Glass Capillary Gas Chromatography”. Presented at the LABCON ’81 Conference, Rosemont, IL, Sept 15-17, 1981. Nisbet, I. C. T.; Sarofim, A. F. EHP, Environ. Health
(20) Putnam, T. B.; Gulan, M. P.; Bills, D. D.; Libbey, L. M. Bull. Enuiron. Contam. Toxicol. 1974, 1 1 , 309. (21) Giam, C. S.; Atlas, E.; Chan, H. S.; Neff, G. S. Atmos. Environ. 1980, 14, 65. (22) “Lange’sHandbook of Chemistry”,11th ed.; McGraw-Hill: New York, 1973; pp 10-31 (Table 10-10).
Perspect. 1972, I , 21. Duce, R. A.; Duursma, E. K. Mar. Chem. 1977, 5, 319. Wingender, R. J.; Williams, R. M.; White, R. V.; Ely, R. S., submitted for publication in Atmos. Environ.
Received for review December 24, 1981. Revised manuscript received February 13,1984. Accepted February 23,1984. Work performed under the auspices of the U S . Environmental Protection Agency and the U.S. Department of Energy.
Comparison of the Carcinogenic Risks from Fish vs. Groundwater Contamination by Organic Compounds Michael Stewart Connor” Interdisciplinary Programs in Health, Harvard School of Public Health, Boston, Massachusetts 02 115
EPA’s carcinogenesis risk assessment methodology is used to compare the risks from trace organic contaminants in groundwater to those in freshwater and marine fishes. Lipophilic, biologically refractory organics are most often found in fish and soluble, volatile compounds in groundwater. Nationwide, known carcinogenic risks from fish consumption are at least as important as those from groundwater consumption, but both vary widely with location and consumption patterns. Introduction Water pollution can affect the general public’s intake of organic carcinogens through two major pathways: drinking contaminated groundwater and consuming fish from contaminated surface waters. Since people ingest about 100 times more water than fish (2 L per capita daily vs. 18.7 g), it seems sensible to focus on groundwater, which supplies about half of our drinking water (I), in controlling our exposure to hazardous organic chemicals. On the other hand, fish and shellfish are able to bioconcentrate organic compounds to levels thousands of times greater than the concentrations in the water in which they live (2-4). While our consumption of fish is small, their contamination by organic compounds can be large enough to make a sizable contribution to our intake of carcinogens. What is the relative importance of these two pathways? While the EPA considers both pathways in developing its water quality standards ( 5 ) ,the average risks of drinking groundwater have never been compared to consuming contaminated fish. Recent nationwide groundwater and fishery surveys allow us to make a rough estimate of the carcinogenic risks associated with fish and groundwater consumption. The most extensive groundwater and fisheries data are from Nassau County on Long Island, NY, and the nearby waters of the New York Bight, which allows a comparison of these risks for a specific location. Methods The National Oceanic and Atmospheric Administration (NOAA), National Marine Fisheries Service (NMFS), United States Fish and Wildlife Service (USFWS), and Food and Drug Administration (FDA) have all recently released reports summarizing their chemical monitoring of aquatic organisms. The most extensive collection of ~~~
~
*Address correspondence to this author at the Water Quality Branch, EPA Region I, Boston, MA 02203. 628
Environ. Sci. Technol., Vol. 18, No. 8, 1984
contaminant data is from surveys in the late 1970s for freshwater fish from USFWS’s nationwide survey (6, 7), and N O M S survey of marine fish from Puget Sound (8) and the New York Bight (9). More extensive geographic data for a few compounds have been collected for estuarine and coastal fisheries for 1981 (10, 11). In 1979, a marketplace survey of 768 fish products was conducted by the FDA (12). The concentrations reported in these field and marketplace surveys are in general agreement (13). A national survey of volatile organic compounds in groundwater has been conducted by the EPA (14). I have used data from their random survey of groundwater systems supplying more than 10000 people. The Nassau County groundwater data are based on several hundred samples from a 1980 groundwater quality assessment (15). These limited data for fish and groundwater concentrations fit both a normal and log-normal distribution. log-normal distributions are often used in risk assessment, but since the distribution of the groundwater data was so dependent on the chemical’s detection limit, I used means from the normal distribution to be conservative. Fish concentrations were treated similarly to be consistent. I have followed the methodology of the Environmental Protection Agency’s (EPA) Carcinogen Assessment Group (CAG),estimating human carcinogenic risk by multiplying a chemical’s carcinogenic potency factor, determined from animal feeding experiments and adjusted for humans, by the expected daily dose to humans from contaminated groundwater and fish (5). In determining the total risk of all the chemicals characterized in fish and drinking water for which a carcinogenic potency factor has been calculated, I have simply added the effects of the individual chemicals, ignoring any potential for synergistic effects. Carcinogenic potency factors published by the CAG were used in the calculations ( 5 ) . The CAG calculates dose for a 70-kg man with an average daily consumption of 2 L of drinking water and 6.5 g of estuarine and freshwater fish. Average U S . per capita daily consumption is 1.63 L of drinking water (16)and 18.7 g of all fish: 6.5 g of estuarine fish and shellfish, 2.0 g of freshwater fish, and 2.8 g of marine fish with the remainder tuna and unclassified imported fish (17). These assumed consumption rates used by EPA understate fish risks compared to groundwater risks since an upper bound of drinking water consumption is used. Fish risks would be 10 times greater if consumption rates at the 95% confidence interval, about 65 glday, were used. In using animal feeding tests to predict human risks from carcinogens, two conversions must be made: from
0013-936X/84/0918-0628$01.50/0
0 1984 American Chemical Society
the high doses in feeding tests to the low doses typical of human environmental exposure and scaling animal results to man. Few animal tumorigenesis studies have included enough animals to adequately define the shape of the dose-response relationship at low doses. Both extrapolation models used by the governmental regulatory agencies which conduct risk assessments (EPA, FDA, the Occupational Safety and Health Administration, and the Consumer Product Safety Commission), the one-hit linear model and the linearized multi-stage model, behave very similarly in the low-dose region (5,18-21). The very large ED01 study conducted to test this linear hypothesis did show linearity in the appearance of liver tumors in mice exposed to 2-(acety1amino)fluorenebut a sharply curvilinear pattern for bladder tumors in the same strain (22). These same regulatory agencies convert from animals to humans by assuming that species are equally sensitive relative to a particular measure of dose rate. Three scaling measures are commonly employed: daily intake per body weight (mg kg-l day-l) (18,19),amount in diet or air (ppm) (20,21), and daily intake per surface area (mg m-2 day-l) (5). Two studies have compared animal-generated cancer estimates to human epidemiological data, a National Academy of Sciences' analysis of six known human carcinogens (23) and a follow-up of those cases and nine additional ones by Crouch and Wilson (24). Taken together these studies indicated a log-log correlation between the potency of a carcinogen in animals and humans. Further analysis of these data (25,261 have shown that, of the three species extrapolation procedures, the mg kg-l day-' based animal projections always generate the lowest risk estimates, and the mg m-2 day-' approach the highest. All three methods have both overestimated and underestimated the risk of these known human carcinogens. Given the limited extent and variability of the data, the choice of species conversion method can be strongly influenced by agency philosophy. The CAG extrapolates by surface area to ensure the least likelihood of underestimating risk (5).
Results and Discussion Carcinogenic risks from consuming freshwater fish are several times greater than for most marine fish (Figure lA), with the exception of striped bass caught in the tidal Hudson River whose consumption results in a lifetime per g of daily consumption. In cancer risk of 6 X general, freshwater and estuarine fish from industrialized regions present similar orders of magnitude of risk, about 10 times greater than less-developed estuaries and 50-100 times greater than offshore fisheries. Most known carcinogenic risk is due to PCB contamination, though DDT residues also account for 12-33%. Dieldrin, toxaphene, and chlordanes make only minor contributions, and the risks from residues of hexachlorobenzene and hexachlorobutadiene are 3-5 orders of magnitude less than the other chlorinated hydrocarbons. Contaminant concentrations in fish, and therefore corresponding risks, from these field surveys are in general agreement with data reported in FDA's marketplace surveys (13). Assuming average U.S. fish consumption rates (51, the lifetime cancer risk from fish consumption is about 4 X lo-' (Figure lB),20-40 times greater than the risk from average contaminant concentrations in US. groundwaters. Groundwaters can contain a number of halogenerated 1-3-carbon compounds. For those compounds for which carcinogenesis testing has been done, most of the risk is associated with chloroform and 1,l-dichloroethylene. These national trends can be modified by several factors. A comparison of the risks faced by Nassau County resi-
I 0- 3, OTHER
B DOT 0
FII HA HA
PCB
PSIPSUNE
FOAGH
Flgure i . Lifetime carcinogenic risk (A) per gram daily consumption of fish caught in different U S . waters and (B)at per capita daily consumption rates of fish and groundwater. Concentration data from ref 6-1 1 used in risk calculations as explained in text. (A) Fish risks reported for those areas for which most extensive survey information exists; these data are typical of contamination levels in other regions ( 73). Risks calculated for PCBs, DDT, and others-including dieldrin, chlordanes, hexachlorobenzene, benzo[a]pyrene, hexachlorobutadiene, and toxaphene. Symbols: FW, assuming average concentrations from 1979 freshwater fish survey for US.;HR, Hudson River striped bass; MA, Mid-Atlantic coastal fish and shellfish; PSI, bottom fish from industrialized and iess-developed(PSU) sections of Puget Sound; NE, New England offshore fishery. (B)Mean concentrations of contaminants reported from FDA marketplace survey ( 72) in fish multiplied by consumption rates to calculate a dose and the risk associated with that dose (FDA). Mean concentrations of contaminants from EPA random survey ( 7 4 ) in groundwater systems serving more than 10 000 people multiplled by per capita daily consumption of 2 L to calculate dose and the risk associated with that dose (GW). Symbols: CLF, chloroform; DCE, 1, l-dichloroethylene. Other compounds (OTH) include trichloroethylene, tetrachloroethylene, carbon tetrachloride, 1,2dichloroethane, benzene, and vinyl chloride. Because these compounds are usually below detection limits, the calculated risk is sensitive to assumptions made about the distribution of concentrations of these "undetected" compounds. Bar graph indicates risk assuming undetected compounds are not present: error bar indicates risk if all compounds are present at concentrations just below detection limit.
dents depends strongly on their fish consumption behavior (Table I). Fish and groundwater risks are similar for those people who eat fish at or below average U.S. rates and exclude striped bass, but for high fish consumers or striped bass eaters the carcinogenic risks posed by fish consumption can be from 10 to 100 times greater, respectively, than the groundwater risks. In recognition of these risks, New Jersey has issued an advisory concerning consumption of its coastal fish, and Long Island's commercial striped bass fishery has been closed for several years. When the carcinogenic risks posed by organic contaminants through fish or groundwater are compared, it is immediately apparent that these are very different sorts of organic compounds (Figure 1 and Table I). Low molecular weight, volatility, and high solubility are the characteristics that allow some of these organic compounds to be transported with groundwater (27). Larger, fatsoluble compounds are bioconcentrated by fish. Although we consume 100 times more water than fish, the fish pathway can be a more important source of organic carcinogens. The consumption difference is offset by the bioconcentration ability of fish-lipophilic compounds are present in the high ppb to low ppm range in fish, but drinking water contaminants are usually present in the low to mid ppb range-and the higher carcinogenic potency factors for the compounds found in fish. Environ. Sci. Technol., Vol. 18,
No. 8, 1984
620
Table I. Comparison of the Risks Presented by the Consumption of Contaminated Groundwater and Fish in Nassau County, Long Island“
contaminant chloroform trichloroethylene tetrachloroethylene l,l,l-trichloroethane carbon tetrachloride 1,l-dichloroethylene l,2-dichloroethane vinyl chloride 1,1,2-trichloroethane total risk EPCBs EDDT dieldrin a-chlordane hexachlorobenzene total risk
solubility, mg L-’
concn, ppb
carcin potency, kg day mg-l
NO4
risk
Groundwater 8200 3.5-4.4 1100 5.7-6.5 150-200 5.3-6.1
0.18 0.013 0.040
480-4400
4.5-5.4
0
0
785
0.58-1.6
0.083
1.4-3.8
400
0.16-1.1
1.0
4.7-33
8690 2660 4500
1.2-2.1
0.037 0.017 0.057
1.3-2.2 0.8-1.2 0.1-1.8
1.6-2.5 0.09-1.1
18-23 2.1-2.4 6.0-7.0
34-74 Fish (Striped Bass) 4.3 0.003-0.4 120 (4200) 8.4 0.001-0.1 16 (610) 30 0.2 1.8 (1) 1.6 0.06-1 13 (120) 0.02 0.45 (1.1) 1.7
48 (1600) 12 (480) 4 (3) 0.5 (17) 0.07 (0.2) 65 (2100)
Carcinogenic risk calculated assuming a 70-kg person consumes 2 L of water daily or eats 6.5 g of estuarine fish (an equal mixture
of winter and windowpane flounder, lobster, and mussels) or striped bass alone (in parentheses). Carcinogenic potency, the ratio of the excess lifetime cancer incidence in a population caused by the carcinogen to the average daily dose received by the population, from EPA Carcinogen Assessment Group (5). Range of groundwater concentration and risk estimates represent values assuming undetected compounds are not present at the detection limits of the monitoring program.
These risk estimates include two major sources of uncertainty: the uncertainty of CAGs model for predicting human responses from animal data and the statistical variability associated with characterizing contaminant levels in fish and estimating our consumption of fish and drinking water. The uncertainty associated with estimating carcinogenic potency from feeding tests and extrapolating from potency in animals to man has been estimated to be greater than a factor of 5 (28). The coefficients of variation for these data for drinking water concentrations range from 100 to 500% and for fish concentrations from 25 to 100%. Despite the uncertainty surrounding these risk estimates, they demonstrate that fish contamination is an equally, if not more, important source of human exposure to organic carcinogens than groundwater contamination. It must be emphasized that this conclusion is drawn from the limited number of chemicals whose identity has been confirmed and for which animal testing has been done. It is estimated that only 10% of the chemicals in , recently nearly groundwater have been identified ( l ) and 500 chemicals were identified in Great Lakes fish (29). For instance, the brominated alkanes found in drinking water and dioxins found in fish are thought to be more carcinogenic than the contaminants characterized here (30),but they are present at much lesser concentrations (15, 31). In general, the chemicals considered here probably account for a major percentage of the contamination and risks, provided that none of the uncharacterized chemicals is both extraordinarily potent and abundant. In addition, 630
Environ. Sci. Technol., Vol. 18, No. 8, 1984
newly identified chemicals will certainly follow the general trends documented here-hydrophobic chemicals commonly presenting problems in fish and volatile organic compounds most commonly causing groundwater problems. The risks reported here mostly range between a lifetime risk of cancer of 10-4-10-6, which is the range of absolute risk normally of interest to regulators. Many of us are voluntarily exposed to much greater risks. For instance, the lifetime risk of cancer of British smokers has been estimated at 1.4 X lop2per cigarette smoked daily (32). EPA has argued that these sorts of models provide only a rough estimate of absolute risk and that they are most properly used in comparing carcinogens or means of exposure (33). Specific regulatory decisions concerning these compounds will often require a variety of risk assessment models to give a range of risk estimates. For instance, in i b risk assessment of PCBs, FDA has scaled doses by body weight which results in a carcinogenic potency factor 13 times lower than that used by CAG (19). In addition, further studies may be required to better ascertain health effects-some groups dispute that PCBs are a human carcinogen (34). In addition, risk estimates are only a part of the political process of regulation which considers the economic costs of regulation, availability of substitutes, and other benefits of the compound-much of the chloroform in drinking water results from chlorination to reduce pathogenic risks. While not always powerful enough for regulatory use, comparative risk assessments minimize the quantitative importance of the assumptions used in translating animal feeding data into human health risks and provide a means for quickly interpreting comprehensive tabulations of chemical concentration data, allowing us to set priorities for research and regulation to reduce the risks from carcinogens within and across sources of environmental exposure.
Acknowledgments I am thankful for the helpful criticisms of D. F. Hornig, R. Shaikh, E. A. C. Crouch, A. Janetos, E. D. Goldberg, F. Morel, D. Burmaster, C. Werme, and two anonymous reviewers.
Literature Cited (1) Burmaster, D. E.; Harris, R. H. Technol. Rev. 1982,85 (5), 50-62. (2) Chiou, C. T.; Freed, V. H.; Schmedding, D. W.; Kohnert, R. L. Environ. Sci. Technol. 1977, 11, 475-478. (3) Veith, G. D.; DeFoe, D. L.; Bergstedt, B. V. J. Fish. Res. Board Can. 1979, 36,1040-1048. (4) Mackay, D. Environ. Sci. Technol. 1982, 16, 274-278. (5) Environmental Protection Agency Fed. Regist. 1980,45, 79318-79379. (6) Schmitt, C. J.; Ludke, J. L.; Walsh, D. F. Pestic. Monit. J. 1981, 14, 136-206. (7) Schmitt, C. J.; Ribick, M. A.; Ludke, J. L.; May, T. W. U.S., Fish Wildl. Serv. Res. Publ. 1983, 152, 1-62. (8) Malins, D. C.; McCain, B. B.; Brown, D. W.; Sparks, A. K.; Hodgins, H. 0. NOAA Tech. Memo. 1980, OMPA-2, 235-242. (9) MacLeod, W. D., Jr.; Ramos, L. S.; Friedman, A. J.; Burrows, D. G.; Prohaska, P. G.; Fisher, D. L.; Brown, D. W. NOAA Tech. Memo. 1981, OMPA-6,48-87. (10) Gadbois, D. F.; Maney, R. S. Fish. Bull. 1983,81, 389-396. (11) Boehm, P. D.; Hirtzer, P. NOAA Tech. Memo. 1982, NMFS-FJNEC-13, 44-89. (12) “FY 79 Pesticides and Metals in Fish Program”; FDA 7305.007: Washington, DC, 1982. (13) Connor, M. S. “Management of Wastes in the Ocean”; Wiley: New York; in press. (14) Westrick, J. J., unpublished results.
Envlron. Scl. Technol. 1984, 18, 631-632 (15) Nassau County Department of Health “Chemical Quality of Untreated Water from Community Supply Wells in Nassau County”; Nassau County: Mineola, NY, 1981. (16) National Research Council “Drinking Water and Health”; National Academy of Sciences: Washington, DC, 1977; p 11. (17) “Seafood Consumption Study, 1973-1974”; National Marine Fisheries Service: Washington, DC, 1976; p 146. (18) Food and Drug Administration Fed. Regist. 1979, 44, 38330-38340. (19) Occupational Safety and Health Administration Fed. Regist. 1983,48, 17284-17319. (20) Occupational Safety and Health Administration Fed. Regist. 1983,48,45956-46003. (21) Consumer Product Safety Commission Fed. Regist. 1982, 47, 14366-14419. (22) Staffa, J. A.; Mehlman, M. A., eds. J. Environ. Pathol. Toxicol. 1980, 3 (3), 1-250. (23) Consultative Panel on Health Hazards of Chemicals Pesticides ”Pest Control: An Assessment of Present and Alternative Technologies”; National Academy of Sciences: Washington, DC, 1975. (24) Crouch, E. A. C.; Wilson, R. J. Toxicol. Environ. Health 1978,5, 1095-1118. (25) Crump, K. S.; Howe, R. B. “Approaches to Carcinogenic, Mutagenic, and Teratogenic Risk Assessment”; U.S. Environmental Protection Agency: Washington, DC, 1980;
EPA Contract 68-01-5975, pp 1-160. (26) Hogan, M. D.; Hoel, D. G. In “Principles and Methods of Toxicology”;Hayes, A. W., Ed.; Raven Press: New York, 1982; pp 711-731. (27) Tinsley, I. J. “Chemical Concepts in Pollutant Behavior”; Wiley: New York, 1979. (28) Crouch, E. A. C.; Feller, J.; Fiering, M. B.; Hakanogly, E.; Wilson, R.; Zeise, L. “Non-Regulatory and Cost-Effectiveness Control of Carcinogenic Hazard”; Energy and Environmental Policy Center, Harvard University: Cambridge, MA, 1982. (29) Hesselberg, R. J.; Seelye, J. G. “Identification of Organic Compounds in Great Lakes Fishes by Gas Chromatography/Mass Spectrometry: 1977”; Great Lakes Fishery Lab: Ann Arbor, MI, 1982; p 3. (30) Crouch, E. A. C.; Wilson, R.; Zeise, L. J. Water Res. 19 (6), 1359-1375. (31) Chem. Week 1983,132 (16), 26-27. (32) Doll, R.; Hill, A. B. Br. Med. J . 1964, 1 , 1399. (33) Todhunter, J. A. Science (Washington, D.C.)1983,219,794. (34) Miller, S. Environ. Sci. Technol. 1983, 17, llA-14A.
Received for review June 20,1983. Revised manuscript received October 31, 1983. Accepted March 7, 1984. This work was partially supported by Grant CR-807809 to the Interdisciplinary Programs in Health from the EPA. The contents of this paper do not necessarily reflect the views and policies of the EPA.
CORRESPONDENCE Comment on Comment on “Acid Precipitation in Historical Perspective” and “Effects of Acid Precipitation” SIR: Apparently, soil scientists have difficulties in accepting that lakes and stream waters have become acid due to acid rain, because the natural production of acidity in ecosystems is large compared to the contribution from acid rain. Richter (1) concludes that “many of the reported changes, where real, may well result from natural processes with relatively minor contributions from acid precipitation”. This conclusion is not based on scientific evidence documented in his letter. Richter does not even try to explain why regional acidification is only reported from areas receiving acid precipitation. If he believed his hypothesis, he should look for areas in the world not receiving acid precipitation where acid clear water lakes have been reported. If acid precipitation was only a small contributor, regional acidification should occur in all areas undergoing natural ecological changes. I assume Richter does not believe that natural acidification processes only take place in areas receiving acid precipitation? Natural acidification processes are well-known also to water chemists and lead to an excess of hydrogen ions in the soil where the base saturation is reduced. If the hydrogen ion concentration in the runoff water also increases because of natural acidification, this increase can be compensated either by an increased concentration of anions (organic anions) or by an equivalent decrease in cations. In the first case increased concentrations of organic carbon (more colored waters) should be found. In the latter case the H+ increase must be compensated by a decreased leaching of basic cations from the soil, because its base 0013-936X/84/0918-0631$01.50/0
saturation is decreased. Thus, the formation of bicarbonate from COz is correspondingly reduced, and the net effect on the runoff water will be lower concentrations of Ca, Mg, and HCO,, and thus a decrease in pH (which in oligotrophic clear water lakes is a function of the HCO, concentration). In areas not receiving external acid inputs, the pH of lakes will most likely not be lower than about 5.5 because some HCO, will still be present. This process does not lead to any relative change in concentrations of Ca, Mg, and HCO,, and this change will be difficult to detect. Thus, increasing acidity of soil does not necessarily lead to increasingly acid lakes, merely to lakes with lower alkalinity. We believe that the latter process dominates for natural acidification processes, because in sensitive areas both receiving and not receiving acid precipitation, clear water lakes are dominant. Krug and Frink (3) recently suggested that SO4 from acid rain is exchanged with organic anions originally present in the water, leaving pH essentially unchanged. This implies that all clear water lakes that are strong acid dominated today (and they are found in areas receiving acid precipitation) originally were acid dystrophic lakes with organic anion concentrations approximately equal to their present sulfate concentrations. To maintain the pH, the pK of the organic acid must have been the pK of H2S04! Their hypothesis is thus not acceptable, also because waters with organic anion as major anion are rather atypical. Harriman and Morrison (2)have compared the chemistry of a moorland stream with an adjacent forest stream in an area receiving acid precipitation (pH 4.3-4.4). They assumed that any differences in stream water chemistry would be due to afforestation of the catchment of the forest stream. Table I gives their results together with values
0 1984 American Chemical Society
Environ. Scl. Technol., Vol. 18, No. 8, 1984 831
