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SEDIMENT CONTAMINATION AND MARINE ECOSYSTEMS: POTENTIAL RISKS TO HUMAN HEALTH Donald C. Malins Pacific Northwest Research Foundation ABSTRACT It is recognized that exposure of aquatic organ- isms to contaminated sediments results in the bioaccu- mulation of toxic chemicals (Capuzzo et al., 1988~. Toxic ~ ~~ ~ ~ ~ ~~ ~ . responses may occur at the biochem~cal-cellular, organismal, population, and community levels and range from metabolic impairment to changes in community structure and function (Capuzzo et al., 1988; Buhler and Williams, 19881. The toxic insults are not limited to the initial organisms impacted, but may extend throughout the food web and include the human consumer of seafood. Contamination of the sediment is especially significant because of the host of benthic species that inhabit the ocean floor--species that serve as initial contaminant reservoirs and are food for a variety of organisms. Thus, the sediment is the starting point for the transfer of toxic chemicals through wide expanses of the food web (Malins et al., 1984; U.S. EPA, 1985). Many gaps exist in our understanding of the far ranging effects of sediment contamination on the myriad organisms that inhabit rivers, estuaries, and coastal areas. ~ ~ ~ ~ ~ ~~ iney vary trom a ~ emoted understanding of synergistic/antagonistic interactions to a shallow perspective of chronic effects. Knowledge about mechanisms that mediate chemical accumulations, metabolic changes and biological effects have been especially elusive. Yet, we know far more about the impacts of sediment contamination on aquatic species than on the human consumer. Simply stated, our understanding of events and processes that lead to potential human health effects from the consumption of contaminated seafood are virtually unknown, as is the extent of the impact on human populations (Swain, 1988; Friberg, 1988~. Many of the chemicals that contaminate fish and shellfish in polluted environments are transferred to humans through the diet prawns er a.., troy. Onus, numans are ~og~cai~y viewed as an intimate part of marine food webs. Metabolically resistant (refractory) chemicals, such as PCBs, DDT derivatives, and other halogenated compounds are readily transferred from the sediments to benthic species, such as worms, clams. and bottom-feeding fish ~ %. ~ ~ . ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ 155 r

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156 (Malins et al., 1984~. Thus, the potential exists for their transfer and bioconcentration through the food web. Compounds that are actively metabolized, such as the aromatic hydrocarbons, are not readily transferred through aquatic food webs, although they do accumulate in organisms, such as shellfish, that have a limited ability to metabolize them (Malins et al., 1986~. Thus, with fish the readily metabolized compounds may be of less concern for the human consumer than the refractory compounds, some of which are known to accumulate in the edible muscle (MacLeod et al., 1981; Romberg et al., 1984; Table 1~. The same conclusion cannot be drawn with respect to shellfish contaminated with xenobiotics. Overall, however, it is important to remember, as indicated, that little is known about the propensity for humans to accumulate and bioconcentrate through the diet the thousands of different parent chemicals and metabolites arising from contamination of sediments (Malins et al., 1986~. Also, only a paucity of information exists about the nature and extent of the human health effects. Having broadly delineated some of the complex problems that can be attributed to one of the "original sins" of chemical contamination-- pollution of the sediments--several specific questions will now be addressed: TABLE 1 Concentration (ppm, Wet Weight) of PCBs, DDT and AHs in Edible Tissues of Striped Bass and Salmon PCBs EDDT EAHs Striped bass (Hudson River, New York) 7.00 Striped bass (Montauk, Long Island) 0.80 Striped bass (Orient Point, New York Bight) 3.00 0.73 Chinook salmon (Denny Way, Seattle) 1.35 Chinook salmon (Richmond Beach, Seattle) NOTES: aTrace bPhenanthrene identified SOURCE: MacLeod et al., 1.01 ta 0.11 t O . 01 PHNb 0.23 0.01 PHN 1981 and Romberg et al., 1984.

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157 1. What is actually known about the dietary transfer to humans of toxic chemicals from contaminated fish and shell fish? 2. What are the human health implications? 3. How can the gaps in knowledge be filled? TRANSFER OF TOXIC CHEMICALS TO HUMAN POPULATIONS An almost singular emphasis has been placed on PCBs as a "model" for considering the exposure of humans to contaminants through marine food webs (U.S. EPA, 1985; Swain, 1988~. These studies suggest that refractory organic compounds have the potential for being transferred to human populations through consumption of contaminated sea food (U.S. EPA, 1985; Swain, 19881. For example, a study was conducted on the exposure of humans to PCBs through the consumption of fish from Lake Michigan (Humphrey, 1976~. In the 18 counties that border Lake Michi- gan, 381, 000 licensed sports fishermen caught 14 million pounds of trout and salmon annually. As a group, the fishermen and their fami lies consumed 36.6 pounds of fish per year (Humphrey, 1976, 1983), which is over three times the national average. Adults were used in a matched cohort study (MacLeod et al., 1981; Romberg et al., 1984) in which samples of serum from each group were analyzed for PCBs, then the results were compared with data obtained from interviews with each indi- vidual involved in the study. The findings generally revealed an increase in PCB serum levels with increased fish consumption (Humphrey, 1983; Table 2~. These data also provided evidence that the Michigan residents were exposed through the diet to levels of PCBs significantly above those for the average population ~ Swain, 1988 ~ . TABLE 2 PCBs in Human Serum as a Function of Fish Consumption and Geographic Location of Fish Source Amount consumed Sample Serum PCB (ug/kg) Source of fish (kg~a N Range Mean Median No source O 29 NDb-41 17.3 15 Lake St. Clair 5 - 66 . 8 15 ND- 38 19 .4 17 Lake Michigan 0-2.73 39 ND-41 18.5 20 Lake Michigan 10.91-118 90 25-366 72.7 56 NOTES: aPresumably kg/yr, though not so specified. bND ~ Not detected; detection limit specified as <5pg/kg. SOURCE: Humphrey, 1983.

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158 It was reasoned that additional groups especially at risk were pregnant women and their unborn and newborn offspring. Thus, a longitu- dinal study was designed to assess the impact of contaminated fish con- sumption on these groups (Jacobson et al., 1983~. Briefly, the study revealed that infants were exposed to PCBs in utero, as well as post- partum via the breast milk, when the mothers consumed contaminated fish. The above findings are not surprising. Evidence with rodents exposed to PCBs revealed essentially the same potential for bioaccu- mulation (see U.S. EPA, 1985~. In addition, a recent study with seals (Reijnders, 1988) showed that the consumption of PCB-contaminated fish resulted in substantial accumulations of these compounds. Comparable results were also obtained with mink fed PCB-contaminated fish (Reijnders, 1986~. The findings with the PCBs add an additional dimension to the con- cern expressed after the Minamata, Japan, mercury poisoning incident in the 1950s (Takeuchi, 1972~. ~ , ~ , or ~ ~ IN phi ~ BAND Pi ah were shown to he the source or methy~mercury exposure in humans seriously afflicted with neurological and other damage (Takeuchi, 1972~. Unfortunately, little or no information exists on the transfer to human populations of the wide variety of xenobiotics that exist together with the PCBs in edible tissues of aquatic life exposed to pollutants. It is not known, for r TABLE 3 DDTa concentrations (pg/gm, ppm Wet Weight) in Uncooked and Pan Fried White Croaker (Genyonemus lineatus) Fillets DDT (pg/g) Composite Percent original Pan fried number weight Uncooked Pan fried normalized 1 27 .8 0.202 0.247 0.069 2 35.7 0.167 0.184 0.066 3 35.2 1.110 0.844 0.297 4 33.2 1.070 0.531 0.176 5 31.8 0.410 0.506 0.161 Mean + SE 32 . 7 0. 57+0 . 20 0. 46+0 . 12 0 . 15+0 . 04 Mean percent loss of DDT due to frying 74 NOTE: aRefers to DDT, 000, and DOE. SOURCE: Puffer et al., 1982.

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159 example, whether synergistic or antagonistic interactions play an impor- tant part in the disposition in humans of xenobiotics derived from con- t~minated seafood. Moreover, little is known about the accumulation of metabolites in edible tissues, especially those compounds that are not detected by conventional analytical techniques. Although, as stated, there are indications that metabolites of aromatic hydrocarbons may not accumulate to a significant degree in the edible tissue of fish (Malins et al., 1987), substantive information on possible contamination from many other compounds s imply does not exist (Swain, 1988~. Clearly of significance is the finding that pan- fried fish tend to have a signi- ficantly lower concentration of ODT derivatives than the uncooked fish (Puffer et al., 1982; Table 3~; however, the influence of cooking on the concentrations of other contaminants is virtually unknown THE HUMAN HEALTH IMPLICATIONS Considerations of human health effects from the consumption of contaminated seafood have focused, for the most part, on the PCBs; however, some concern has been expressed about inorganic compounds (e.g. , arsenic) that accumulate in the muscle of fish (Friberg, 1988) . Some studies, for example, point to a possible threat from arsenic (Friberg, 1988~. While most of the arsenic in seafood is in the form of arsenobetaine, which is considered relatively atomic, "extreme consumption" of seafood may give rise to an intake of several hundred micrograms of inorganic arsenic per day--an exposure, which over a lifetime, may be associated with a "significant increase in skin cancer" (Friberg, 1988~. Unfortunately, related studies that focus tightly on cause - effect relationships have yet to be conducted. The daily intake of tin through the consumption of seafood is not particu- larly high; however, more studies need to be conducted on the potential toxicity of trimethyltin resulting from biochemical alkylation reac- tions. Also, despite regulations pertaining to methylmercury, groups having a "high" fish intake, or an intake of fish with a "high" methyl- mercury content, may exceed established tolerance levels. In this regard, a special concern exists about pregnant women (Friberg, 1988~. Results from the relatively large amount of research on PCBs sug- gests that these compounds may pose a significant problem for the con- sumer of fish from polluted areas. In Lake Michigan studies (Jacobson et al., 1983, 1984; Fein et al. , 1984), for example, effects observed among infants born to mothers in "high fish consumption" categories in- cluded delays in developmental maturation at birth (rein et al., 1984~. The infants were also smaller in physical size, and had a reduced head circumference and neuromuscular maturity (Table 4~. They also exhi- bited an altered lability of state, increased startle reflexes, and were classified by physicians to be within the "worrisome" neonatal category (Jacobson et al., 1984, 1988~. Swain (1988) makes the point that these observations suggest "an effect of contaminants upon the centers of higher integration in infants secondarily exposed via mater- nal circulation." A study conducted with rats (Hertzler and Daly, 1985) supports the conclusion that PCBs derived from fish indeed have

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161 an effect on the nervous system. It was shown, for example, that rats maintained on a diet of PCB-contaminated salmon from Lake Ontario devel- oped behavioral anomalies, compared to controls, in relation to brain concentrations of PCBs. Such a finding can be compared with results obtained from the previously mentioned study of seals exposed to PCBs through their fish diet (Reijnders, 1986~. The reproductive process was shown to be "disrupted in the post-ovulation phase." Another study with mink (Reijnders, in press, and 1986) also supported the proposi- tion the PCBs derived from a fish diet have an effect on reproduction at "very low (25 fig per day) levels." Overall, a limited number of studies have indicated that signifi- cant changes in health status may occur in humans consuming contami- nated fish; however, obviously many factors impinge on the exact nature of the threat--so many, in fact, that the present findings are best viewed as a stimulus to study the issue in greater detail through care- fully controlled field and laboratory investigations. FILLING THE GAPS IN KNOWLEDGE Information required for a minimal understanding of the impacts of toxic environmental chemicals on aquatic species and human health sub- stantially exceeds the information available. Important areas for future research include obtaining more knowledge about the nature and extent of exposure on an individual, population, and geographic bases. In addition, biochemical/toxicological data on the scores of chemicals that have the potential to accumulate in edible tissues are also impor- tant to obtain, as is information on chronic effects. Moreover, pos- sible human health effects associated with the loss of volatile sedi- ment chemicals to the atmosphere, such as from contaminated subtidal areas, is well worth studying. The problem of human risk assessment is formidable when one consi- ders that marine life is often exposed to complex mixtures of chemicals in contaminated areas. Moreover, in some cases, assessments conducted thus far with contaminated fish have projected clearly unacceptable human cancer risks (Brown, 1985; Table 5~. In addition, the present reliance on PCBs and a small number of other compounds for risk assess- ment is clearly inadequate. More work needs to be undertaken to make risk assessment more meaningful from a public health point of view, such as by taking into account the fact that complex mixtures of poten- tially toxic chemicals are likely to be present in edible tissues of fish from polluted areas. Studies in which laboratory animals are fed a diet of contaminated fish tissue or a diet containing extractable, environmentally derived chemicals may well prove to be a useful approach. Finally, one can only hope that future work will consider a variety of biological end points as indicators of human health effects, rather than focus on the few (e g., cancer and neurological impairment) that have been studied thus far.

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162 TABLE 5 Contaminant Concentration and Risk Assessment for Consumption of Southern California Fish at Average U.S. Consumption Ratea Concentration (mg/wet kg) Risk White Point White Croakers DDTs 7.6 3.4/10,000 PCBs 0.38 2.2/20.000 Total 8.0 5.6/10,000 Rockfish DDTs 0.44 2.0/100,000 PCBs 0.057 3.3/100.000 Total 0.50 5.3/100,000 P. Mackeral DDTs 0.051 2.3/1,000,000 PCBs 0.014 8.0/1.000. 000 0.065 1.0/100, 000 Santa Monica Bay White Croakers DDTs 0.57 2 . 6/100, 000 PCBs 0.20 1.1/10. 000 Total 0 . 77 1. 4/10, 000 Rockfish DDTs 0.22 9. 9/1, 000, 000 PCBs 0.12 6 . 9/100. 000 Total 0.34 7 . 9/100, 000 P. Mackeral DDTs 0.057 2 . 6/1, 000, 000 PCBs 0.015 8.6/1.000. 000 0.072 1. 1/100, 000 NOTE: a9.3 g/day consumption of domestic estuarine and marine fish. SOURCE: Brown, 1985. REFERENCES Brown, D. 1985. Personal Communication. Based on work conducted while at the Southern California Coastal Water Research Project (S.C.W.R.P.), Long Beach, CA. Buhler, D. R. and D. E. Williams. 1988. The role of biotransformation toxicity in fish. Aquat. Toxicol. 11:303-311. Capuzzo, J. M., M. N. Moore, and J. Widdows. 1988. Effects of toxic chemicals in the marine environment: Predictions of impacts from r

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163 laboratory studies. Aquat. Toxicol. 11:19-28. Fein, G. G., J. L. Jacobson, S. W. Jacobson, P. W. Schwartz, and J. K. Dowler. 1984. Prenatal exposure to polychlorinated biphenyls: Effects on birth size and gestational age. Pediatr. 105:315-320. Friberg, L. 1988. The GESAMP evaluation of potentially harmful sub- stances in fish and other seafood with special reference to carcinogenic substances. Aquat. Toxicol. 11:379-393. Hertzler, D. R. and H. B. Daly. 1985. Ingestion of neurotoxic Lake Ontario salmon influences behaviors of laboratory rats. Meeting of Psychonomic Society, Boston, Mass . Humphrey, H. E. B. 1983 . Population studies of PCBs in Michigan Residents. In PCBs: Human and environmental hazards, F. M. D'itri and M. A. Kamrin, eds. Boston: Butterworth Publishers. pp. 299-310. Humphrey , H. E. B. 1976. Evaluation of Changes of the Level of Polychlorinated Biphenyls (PCB) in Human Tissue. Final report on W. S. FDA contract. Lansing: Michigan Department of Public Health. p. 86. Jacobson, J. L., S. W. Jacobson, P. M. Schwartz, G. G. Fein,, and J. K. Dowler. 1984. Prenatal exposure to an environmental toxin: A test of the multiple effects model. Dev. Psychol. 20:523-532. Jacobson, S. W., J. L. Jacobson, P. M. Schwartz, and G. G. Fein. 1983. Intrauterine exposure of human newborns to PCBs: Measures of exposure. In PCBs: Human and Environmental hazards, F. M. D'itri and M. A. Kamrin, eds. Boston: Butterworth Publishers. pp. 311-343. MacLeod, W. D., Jr., L. S. Ramos, A. J. Friedman, D. G. Burrows, P. G. Prohaska, D. L. Fisher, and D. W. Brown. 1981. Analysis of residual chlorinated hydrocarbons, aromatic hydrocarbons and related compounds in selected sources, sinks, and biota of the New York Bight. NOAA Technical Memorandum OMPA-6. Seattle, Wash.: National Oceanic and Atmospheric Administration. Malins, D. C., B. B. McCain, D. W. Brown, S-L. Chan. 1984. Toxic chemicals in marine environments: Food-chain transfers and biological effects. In health and Environmental Research on Complex Organic Mixtures, R. H. Gray, E. K. Chess, P. J. Mellinger, R. G. Riley, and D . L. Springer, eds . Richland , Wash .: Battelle Memorial Institute, Pacific Northwest Laboratory. pp. 591-609. Malins, D. C., U. Varanasi, D. W. Brown, M. M. Krahn, and S-L. Chan. 1986. Biological transport of contaminants in marine environments: Bioavailability and biotransformations. Rapp. P.-v. Reun. Cons. Int. Explor. Mer. 186:442-448. Mal ins, D . C ., B . B . McCain, D. W. Brown , S - L . Chan . M . S . Myers, J . T . Landahl, P . G . Prohaska, A. J . Friedman, L. D . Rhodes, D . G . Burrows, W. D . Gronlund, and H . O . Hodgins . 1984 . Chemical pollutants in sediments and diseases in bottom-dwelling fish in Puget Sound, Washington. Environ. Sci. Technol. 18: 705-713 . Puffer , H . W., M. J . Duda , and S . P . Azen. 1982 . Potential health hazards from consumption of fish caught in polluted coastal waters of Los Angeles County . N. Am. J . Fish. Manage . 2: 74- 79 . Reijnders, P. J. H. 1986. Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324: 456-4S7 Romberg, G. P., S. P. Pavlou, R. F. Stokes, U. Hom, E. A. Crecelius,

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164 P. Hamilton, J. T. Gunn, R. D. Meunch, and J. Vinelli. 1984. Toxicant Pretreatment Planning Study Technical Report CI: Presence, Distribution and Fate of Toxicants in Puget Sound and Lake Washington. Seatle, Wash.: Municipality of Metropolitan Seattle. Swain, W. R. 1988. Human health consequences of consumption of fish contaminated with organochlorine compounds. Aquat. Toxicol. 11:357-377. Takeuchi, T. 1972. Distribution of mercury in the environment of Minamata Bay and the inland Ariake Sea. In Environmental Mercury Contamination, R. hartung and B. D. Dinaman, eds. Ann Arbor, Mich. Ann Arbor Science. pp. 79-81. Environmental Protection Agency (U.S. EPA). 1985. Assessment of Human Health Risk from Ingesting Fish and Crabs from Commencement Bay. Final Report. Seattle, Wash.: U. S . Environmental Protection Agency. U.S.