Environmental Research Section A 80, S207—S212 (1999) Article ID enrs.1998.3912, available online at http://www.idealibrary.com on
PCB Congener Patterns in Rats Consuming Diets Containing Great Lakes Salmon: Analysis of Fish, Diets, and Adipose Tissue1 Scott A. Jordan2 and M. Mark Feeley Chemical Health Hazard Assessment Division, Health Canada, Postal Locator 2204 D1, Tunney’s Pasture, Ottawa, Ontario, Canada K1A 0L2 Received December 22, 1997
occurred at higher levels in the rats (3.4 vs. 0.3% of the total PCB concentration, respectively). Although adipose tissue from the rats fed diets containing Great Lakes salmon had up to two orders of magnitude higher concentrations of PCBs compared to average human values, with the exception of some lower chlorinated congeners, similar major congeners tended to be present in both the rats in the present study and humans. Key Words: polychlorinated biphenyls; congener specific; adipose; bioaccumulation; rat; Great Lakes fish.
As part of a multidisciplinary toxicological investigation into Great Lakes contaminants, chinook salmon were collected from Lake Huron (LH) and Lake Ontario (LO) and incorporated (as lyophilized fillets) into standard rat diets as 20 or 100% of the protein complement (5 or 20%, w/w diet—LH5, LH20, LO5, and LO20 diets). Final PCB concentrations in the experiment ranged from 3.15 ng/g in the control diet to 1080 ng/g in the high-dose (20%) LO diet, with maximal estimated daily consumption by the rats of 82 lg PCBs/kg body wt in the LO20 dietary group. Seventeen PCB congeners, PCB 85, 99, 101, 105, 110, 118, 128, 129, 132, 138, 149, 153, 170, 177, 180, 187, and 199, occurred at 53.0% of the total PCBs in the fish with no major site differences. Cumulatively, these 17 congeners accounted for up to 75% of the total PCBs in the fish compared to 44 and 54% in two commercial Aroclors, 1254 and 1260, respectively. PCB 77 was the major ‘‘dioxin-like’’ congener in the fish, followed by PCB 126 and then PCB 169. All major dietary congeners bioaccumulated in the adipose tissue of the rats with the exception of PCB congeners 101, 110, 132, and 149. The group of 17 major congeners accounted for up to 71% of the total PCBs in adipose tissue samples collected from the rats following up to 19 weeks of diet ingestion. Of the coplanar PCB congeners, PCB 77 appeared to bioaccumulate to a lesser extent compared to PCBs 126 and 169. When comparing PCBs in the rat adipose tissue to PCB congeners in Canadian breast milk, PCBs 44, 49, 74, and 137 tended to occur in higher amounts in the human samples (contributing together 18.4 vs. 1.4% of the total PCB concentration), whereas PCB 129
INTRODUCTION
Various federal health agencies in North America provide risk assessment advice with regard to chemical contaminants in the food supply. In turn, provincial/state agencies have developed guidelines concerning the consumption of sport fish from recreational waters. Fish consumption advisories for the public continue to be issued in the Great Lakes Basin due to the presence of a variety persistent contaminants. In particular, 95% of the fish advisories issued by the U.S. EPA in 1996 dealt with PCBs, chlordane, dioxins, and DDT (USEPA, 1996). Although manufacturing and use restrictions have been in effect for PCBs in many industrialized countries, they continue to be found in all trophic levels of the environment. Worldwide production of PCBs has been estimated at up to 1.3 million tons (Lang, 1992). Continued environmental input through improper storage and disposal techniques, combined with their various physicochemical properties, has resulted in extreme environmental persistence and PCBs being considered as true global pollutants (Pearson et al., 1996). For Great Lakes anglers, detectable residues (blood, adipose, breast milk) of PCBs and other organic contaminants can
1
This study was funded internally by the Great Lakes Health Effects Program of Health Canada. The animals used in this study were treated in accordance with Health Canada guidelines and the guidelines of the Canadian Council of Animal Care, for the humane treatment of experimental animals. 2 To whom correspondence should be addressed. S207
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be related to history, quantity, and type of fish consumed. Lake Michigan anglers who consumed up to and greater than 10.91 kg of fish per year had upper serum PCB ranges almost 24-fold higher than nonconsumers of Great Lakes fish (25—366 ppb vs. less than 5—41 ppb, respectively) (Humphrey, 1987). Hazard characterization of PCB residues can be complicated by a number of factors. Technical or commercial PCBs are complex mixtures, manufactured on the basis of total chlorine content and can theoretically be comprised of up to 209 different congeners. In contrast, through various physical, chemical, and biological processes, trophic levels tend to accumulate specific PCB congeners which may not resemble any specific commercial sample. Following analysis of environmental biota (fish, turtles) and comparison to analysis of Aroclor mixtures comprised of between 42 and 60% chlorine, by principal components analysis, it was concluded that the biota sample’s congener pattern did not resemble either one individual Aroclor or a defined mixture of Aroclors (Schwartz and Stalling, 1987). Although commercial PCBs have been shown to be toxic to experimental animals and humans, extrapolating these findings to environmental PCBs may not be appropriate based on known congener differences. Currently, there is limited congener-specific PCB toxicological data available on which to attempt a hazard characterization of food chain or human PCB residues. In this current study, Great Lakes chinook salmon were collected and fed to rats as part of a multigeneration study. We describe here the PCB residues found in the fish and in rats following the consumption of the fish-containing diets as compared to major PCB congeners seen in the general Canadian population. MATERIALS AND METHODS
Full materials and methods are given in Feeley and Jordan (1998) and the study design is reported in Arnold et al. (1998). Briefly, Chinook salmon (Oncorhynchus tsawytscha) were collected, during the 1991 spawning run, from two sites—Lake Huron (LH, from the Sydenham River) and Lake Ontario (LO, from the Credit River). The salmon were filleted with the skin intact and the fillets were ground twice, lyophilized, and transported to Purina Mills, Inc. (Richmond, IN) where they were incorporated into Purina Basal Diet 5775 (20% protein derived from casein). Two different diets were prepared using fish from each of the two sites. These diets were produced by replacing appropriate amounts of the casein with the lyophilized fish in order to attain
diets composed of 5 or 20% fish (Feeley and Jordan, 1998). Diets were balanced for nutritional parameters including protein, calcium, phosphorus, and fat. Diets were fed ad libitum to male and female rats and breeding was allowed to occur to produce F1 pups. Upon weaning, these pups were placed on the diet of their dams and continued on diet until after breeding/gestation/lactation of an F2 generation. The F0 and F1 female animals were on diet for up to 19 weeks; however, the treated F1 animals were on the fish diets from an earlier age (21 days of age, after exposure in utero and via lactation) than were the F0 animals (4 weeks of age, after receipt and acclimatization). All analyses were performed by Wellington Laboratories (Guelph, Ontario, Canada). Samples of adipose were obtained during the sacrifice and autopsy of experimental animals at the scheduled termination times. Tissue samples from maternal animals were obtained from postlactation dams which had equal sized litters. Feed samples were analyzed individually (n"3/ group) for all contaminants. Tissue PCB analysis was performed on pooled samples (derived from five samples/group). The analytical method was as described in Feeley and Jordan (1998). PCB analysis was achieved by column chromatography and dual capillary column/dual electron capture detection (GC/ECD) for the nonplanar PCB congeners (about 130 congeners). For the coplanar PCB congeners, high resolution GC mass spectrometry (HRGC/ HRMS) using USEPA method 1613, modified to include these congeners, was employed. Appropriate 13 C-labeled internal standards were added prior to extraction and analysis. Unless stated, all results are given on a wet weight basis. Major PCB congeners in this study were defined as those that were present at concentrations of approximately 53% of total PCB concentration in the appropriate medium (feed or adipose tissue). RESULTS AND DISCUSSION
Consumption estimations of total PCBs for this study are reported in Feeley and Jordan (1998) and ranged up to 82 lg PCB/kg body wt/day. Table 1 shows the major PCB congeners (equal to or greater than 3% of the total PCB concentration) present in the fresh fish as well as in the diets used in the study. If any congener was present in any diet at greater than or equal to 3% of the total PCB concentration, the level of this congener was given in all diets regardless of its concentration. Seventeen
PCB CONGENERS IN RATS CONSUMING GREAT LAKES FISH
TABLE 1 Concentration of PCB Congeners (ppb) in Fish and Feed Samples from the Great Lakes Multigeneration Study Congener Control LH (W)a LH5 Total PCB 3% of total" 85 99 101 105 110 118 128 129 132 138 149 153 170 177 180 187 199 77 (ppt) 126 (ppt) 169 (ppt) a b
LH20 LO (W) LO5 LO20
3.15
338.3
211
667
834.6
341
1080
0.095 0.08 NDb 0.10 ND 0.15 0.16 ND ND ND 0.19 0.08 0.15 ND ND 0.33 0.08 ND ND 0.39 0.35
10.1 13 5.5 4.2 ND 69 39 16 ND 14 28 15 18 7.2 9.9 6.2 5.9 3.1 810 330 ND
6.33 3.8 8.0 8.9 5.5 16.1 13.8 2.8 4.51 3.9 13.3 8.1 16.6 3.52 3.3 9.9 7.0 4.38 151 56.1 5.55
20.01 11.6 22.9 25.2 20.3 47.9 39.7 8.6 14.7 9.9 36.7 21.7 45.5 10.6 8.8 28.4 20.0 14.8 482 204 49.8
25.0 10.23 25 5.5 18 13 15.5 13.5 39 6.8 94 19.4 78.5 19.1 19.5 3.5 16.5 6.67 26 5.9 71.5 19.1 37.5 12.3 45 25.4 20 5.0 25.5 5.4 27 16.6 12 11 9.35 6.64 350 141 390 65.7 ND 5.7
32.4 18.4 45.9 46.4 23.5 62.2 57.7 11 22.4 18.7 58.9 38.9 76.3 18.3 17.2 55.2 35.7 23.3 489 245 32.3
W, wet (fresh) fish. ND, not detected.
congeners were identified as being present at levels of 3% or more of the total PCB concentration—PCB 85, 99, 101, 105, 110, 118, 128, 129, 132, 138, 149, 153, 170, 177, 180, 187, and 199. Combined, these 17 congeners accounted for up to 75% of the total PCB concentration (LO20 diet). This is in contrast to commercial Aroclor mixtures for which these congeners made up 44 and 54% of the total (Aroclor 1254 and 1260, respectively; Schulz et al., 1989). The predominant congeners present in both the fish and the diets were of the (in order of concentration) penta-, hexa-, and heptasubstituted homolog groups with the major congeners being 110, 118, 138, and 153. These particular congeners together comprised 46 and 35% of the total PCB concentration in LH and LO fish, respectively, and represented 28, 25, 24, and 24% of the total PCBs in the LH-5, LH-20, LO-5, and LO-20 diets, respectively. The lyophilization procedure concentrated the PCBs an average of six times over the concentrations in the fresh fish and produced a congener distribution pattern that was similar to that found in the fresh fish (data not shown). Also, the congener pattern in the fish from the two collection sites was very similar. The 20% diets had an average of 3.4 times the amount of the major PCBs
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compared to the 5% diets. In terms of the coplanar PCBs, congener 77 occurred in the highest concentration followed by PCB 126 and then PCB 169. This pattern was conserved in the fresh fish, lyophilized fish, and all diet groups. Other research has shown that this pattern of coplanar PCB concentration occurs in a wide variety of species such as lake trout from Lake Michigan, killer whale, and Baltic herring (summarized in Patterson et al., 1994). Gerstenberger et al. (1997) analyzed PCB congeners in Lake Superior walleye, pink salmon, siscowet trout, carp, and whitefish. The PCB congener pattern in walleye and siscowet was similar to the chinook salmon from the current study with congeners 138 and 153 predominating. The walleye and siscowet also had a similar homolog pattern compared to this study with penta-, hexa-, and hepta substituted congeners predominating. Carp and whitefish tended to have more lower chlorinated congeners. The pink salmon had the lowest total PCB concentrations of any of the species tested. The data in the current study correlates with those from a study of salmonid fish from Lake Ontario (Niimi and Oliver, 1989). These authors found that the homolog groups contributing the most to the PCB content of the fish were (in order of contribution to the total) the penta-, hexa-, tetra-, and heptachlorinated groups. Niimi and Oliver (1989) also found that the most common congeners in Great Lakes salmonids were 84, (87#97), 101, 110, 118, 138, 149, 153, and 180 and when summed these contributed between 52 and 60% of the total PCBs in muscle tissue (54 and 55% in coho salmon, specifically). These congeners in the chinook salmon used in the present study contributed 53 and 44% of the total PCB concentration in fish caught in Lake Huron and Lake Ontario, respectively. The salmon collected by Niimi and Oliver (1989) were caught in the Credit River as were the LO chinook salmon used in the present study, while the other salmonids were caught at various locations in the western part of Lake Ontario. In terms of the coplanar congeners determined in the 1989 study, 169 was not detected, 126 was only found in lake and rainbow trout, and 77 was present in all Lake Ontario salmonids measured. The present study also showed no detectable 169 in the fresh chinook salmon; however, both 126 and 77 were detectable with 77 predominating. Newsome and Andrews (1993) found that the penta- and hexa-substituted PCB congeners were the homolog groups present in the highest levels in a wide variety of fish from Lakes Ontario, Erie, and Superior. While salmon were not analyzed specifically, these authors found that the major PCB
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congeners in 11 different species of fish tended to be 90, 138, and 153. The predominant congeners in the present study, in chinook salmon collected from Lakes Ontario and Huron, were 110, 118, 138, and 153. These congeners were also identified in between 90 and 100% of samples from 14 different fish species collected from Lakes Michigan and Superior in 1986—1987 (Maack and Sonzogni, 1988). Table 2 presents the concentration and pattern of the major PCB congeners (53% of the total PCB concentration) detected in adipose tissue samples collected from female F0 and F1 rats exposed to the experimental diets for up to 19 weeks. The same pattern of PCB congener distribution was noted in all diet groups and between the two generations. The predominant congeners in the adipose tissue of these adult rats were 118, 138, 153, and 180. These predominant PCB congeners accounted for 32—37% of the total PCB concentration in this tissue. All major dietary congeners bioaccumulated in the adipose tissue of the rats with the exception of PCB 101, 110, 132, and 149, which made up a lower percentage of the total PCB concentration than they did in the diet groups (Table 3). Previously, both congeners 110 and 149 have been identified as major components of
various commercial PCB mixtures, but not in human tissues (Jones, 1988). Congener 132 has been reported not to occur to a large extent in environmental samples and to bioaccumulate only weakly in humans (McFarland and Clarke, 1989). The group of 17 major congeners accounted for between 65 (OS20, F0 generation) and 71% (OS5, F0 generation) of the total PCBs in adipose tissue samples collected from the rats. In the adipose tissue in the present study, the LO groups accumulated an average of 2.6 times the PCB concentration that the LH groups accumulated. This difference correlated with the higher total PCB concentration in the LO fish compared to the LH fish, and in the respective diets prepared with these fish. In human adipose tissue, different studies report varying primary congeners; however, 138, 153, and 180 tend to be the congeners present in the highest concentration, with 153 being the predominant congener, as in the present study (Focardi and Romei, 1987; Mes and Malcolm, 1992; Kannan et al., 1994). Other major congeners that have been detected in human adipose tissue surveys are 99 (Focardi and Romei, 1987), 146, 170/190, 177, and 187 (Kannan et al., 1994). In terms of total PCB concentrations, the adipose tissue in the rats was 45 times higher than in adipose tissue collected from residents
TABLE 2 Concentration of PCB Congeners (ng/g) in Adipose Samples from the Great Lakes Multigeneration Study: Adult Females LH5 Congener Total PCB 3% of total" 85 99 101 105 110 118 128 129 132 138 149 153 170 177 180 187 199 77 (pg/g) 126 (pg/g) 169 (pg/g) a
ND, not detected.
Control 34.7 1.04 0.692 1.78 0.655 3.78 NDa 5.18 ND ND ND 4.73 ND 6.82 ND ND 3.68 1.76 ND ND 7.4 2.5
F0 3415 103 55.5 126 54.2 131 42.4 277 56.2 153 8.87 301 32.7 401 78.3 77.9 275 184 163 454 1260 345
LH20 F1 3559 107 47.4 121 43.3 110 31 248 56.3 142 7.80 324 32.8 436 91.8 88.0 317 212 198 458 1290 451
LO5
LO20
F0
F1
F0
F1
F0
F1
8983 269 162 364 149 406 99.5 686 155 441 27.2 732 90.1 902 199 189 658 440 170 1270 4000 998
8315 249 139 333 122 363 82.5 628 141 318 22.3 725 96.1 888 190 182 628 422 395 1430 4230 1140
6275 188 103 250 107 201 68.9 442 91.3 213 24.5 512 81 691 158 161 553 350 281 672 1840 362
6121 184 98.8 260 99.3 201 56.9 424 89.2 225 20.0 528 73.8 682 163 158 549 336 269 1030 2020 387
15856 476 238 766 235 438 118 885 228 532 60.9 1182 215 1636 433 414 1374 880 788 2290 6100 1500
15149 454 239 759 258 457 126 873 220 507 58.8 1144 147 1597 401 387 1264 829 716 2220 6110 1260
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TABLE 3 Percentage Contribution of PBC Congeners, to the Total PCB Concentration, in the Diet and Adipose Tissue of Control and High-Dose Adult Female Rats Fed Lake Ontario Salmon Control Congener
% diet
% adipose
85 99 101 105 110 118 128 129 132 138 149 153 170 177 180 187 199 77 (ppt) 126 (ppt) 169 (ppt)
2.5 —a 3.2 — 4.8 5.1 — — — 6.0 2.5 4.8 — — 10.5 2.5 — — 0.01 0.01
2.0 5.1 1.9 10.9 — 14.9 — — — 13.6 — 19.7 — — 10.6 5.1 — — 0.02 0.007
a
LO 20% % diet 1.7 4.3 4.3 2.2 5.8 5.3 1.0 2.1 1.7 5.5 3.6 7.1 1.7 1.6 5.1 3.3 2.2 0.05 0.02 0.003
% adipose 1.6 5.0 1.7 3.0 0.8 5.8 1.5 3.3 0.4 7.6 1.0 10.5 2.6 2.6 8.3 5.5 4.7 0.01 0.04 0.008
Congener not detected.
of the Canadian Great Lakes basin (Mes and Malcolm, 1992). In terms of the coplanar PCB congeners in the adipose tissue, 126 was the predominant congener followed by 77 and 169. This is in contrast to the fish diets where 77 was the predominant congener followed by 126 and 169. Other studies show variations in the relative contribution of the coplanar PCB congeners in the adipose tissue of humans. Japanese adipose sample have shown that 126 and 77 are similar in concentration with 169 being present in lower concentrations (Kannan et al., 1988), while a study in five cities in the Canadian Great Lakes basin reported that 126 was the predominant coplanar followed by 169, with 77 usually being nondetected in the majority of samples (Williams and LeBel, 1991). Very similar percent contributions of the coplanar PCB congeners to the total PCB concentration (less than 0.1% contribution in all cases) were noted between the generations in the treated groups of the present study. Table 4 compares levels of the main PCB congeners in Canadian human breast milk (Newsome and Andrews, 1995) with the concentrations found in the adipose tissue of animals from the LO20
group. Congeners 44, 49, 74, and 137 tended to be lower in the adipose of the treated rats than in the human breast milk samples (1.4% vs. 18.4% of total PCBs, respectively), whereas congener 129 was present at higher levels in the rat tissue compared to breast milk (3.3% vs. 0.3% of total PCBs, respectively). Some of the differences between the rat adipose tissue and human breast milk may be due to analytical differences between the studies; however, as fish represent only one food commodity responsible for human PCB exposure, the possibility exists that congeners 44, 49, 74, and 137 may be represented in other foods which humans consume (Duarte— Davidson and Jones, 1994). The concentration of total PCB in the adipose tissue of the LO high dose group was 76 times greater than that in human milk fat from residents of the Canadian Great lakes basin (Mes and Malcolm, 1992). Even though the actual PCB concentrations differed greatly between the adipose of rats and the human milk fat, the distribution of the major PCB congeners and the specific congeners present in both was similar. CONCLUSIONS
The lyophilization procedure used to concentrate the contaminants in this study did not alter the PCB
TABLE 4 Comparison between PCB Congeners in the Adipose Tissue of F0 Female Rats Fed Fish Diets from Lake Ontario and Human Breast Milk a % total (wet weight) PCB congener 28 44 49 74 99 105 118 129 137 138 153 156 170 180 187 199 Total %
F0 LO20 (adipose) 1.6 Not detected 0.14 0.29 5.0 3.0 5.8 3.3 0.93 7.6 10.5 1.1 2.6 8.3 5.5 4.7 60.4
Breast milk 1.9 2.9 4.9 5.7 5.7 2.1 7.0 0.3 4.9 11.7 16.1 2.7 3.9 8.7 3.7 Not available 82.2
a Canadian human breast milk data (1992) taken from Newsome et al., 1995.
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congener profile present in the fish collected from Lakes Ontario or Huron. This congener pattern was also conserved in the diets fed to the experimental animals. Although some differences exist, the fish used in this study had very similar congener profiles, both in homolog groups and in predominant congeners, to other Great Lakes fish species caught in various locations. The profile of PCB accumulation in the adipose tissue of the rats fed the Great Lakes fish diets was the same in all the dose groups in both generations. While the congener profile in adipose tissue was similar to that in the diets, some congeners did not accumulate in adipose, likely due to less bioavailability or to increased metabolism compared to the other congeners. The adipose PCB patterns in the rats were similar to that observed in human populations in terms of the predominant congeners and the same was noted in comparisons with human milk fat residues. With the exception of a group of lower chlorinated congeners, the rats fed diets composed of Great Lakes salmon exhibited similar PCB congener profiles to that observed in the general human population. REFERENCES Arnold, D. L., Stapley, R., Bryce, F., and Mahon, D. (1998). A multigeneration study to ascertain the toxicological effects of Great Lakes salmon fed to rats: Study overview and design. Reg. Toxicol. Pharmacol. 27(1), S1—S7. Duarte-Davidson, R., and Jones, K. C. (1994). Polychlorinated biphenyls (PCBs) in the U.K. population: Estimated intake, exposure and body burden. Sci. Tot. Environ. 151, 131—152. Feeley, M. M., and Jordan, S. A. (1998). Dietary and tissue residue analysis and contaminant intake estimations in rats consuming diets composed of Great Lakes salmon: a Multigeneration study. Reg. Toxicol. Pharmacol. 27(1), S8—S17. Focardi, S., and Romei, R. (1987). Fingerprint of polychlorinated biphenyl congeners in samples of human subcutaneous adipose tissue. Chemosphere 16(10—12), 2315—2320. Gerstenberger, S. L., Gallinat, M. P., and Dellinger, J. A. (1997). Polychlorinated biphenyl congeners and selected organochlorines in Lake Superior fish, USA. Environ. Toxicol. Chem. 16(11), 2222—2228. Humphrey, H.E.B. (1987). The human population—an ultimate receptor for aquatic contaminants. Hydrobiologia 149, 75—80. Jones, K. C. (1988). Determination of polychlorinated biphenyls in human foodstuffs and tissues: Suggestions for a selective congener analytical approach. Sci. Tot. Environ. 68, 141—159.
Kannan, N., Tanabe, S., and Tatsukawa, R. (1988). Potentially hazardous residues of non-ortho chlorine substituted coplanar PCBs in human adipose tissue. Arch. Environ. Health 43(1), 11—14. Kannan, N., Schulz-Bull, D. E., Petrick, G., Duinker, J. C., Macht-Hausmann, M., and Wasserman, O. (1994). Toxic chlorobiphenyls in adipose tissue and whole blood of an occupationally/accidentally exposed man and the general population. Arch. Environ. Health 49(5), 375—382. Lang, V. (1992). Polychlorinated biphenyls in the environment. J. Chromat. 595, 1—43. Maack, L., and Sonzogni, W. C. (1988). Analysis of polychlorobiphenyl congeners in Wisconsin fish. Arch. Environ. Contam. Toxicol. 17, 711—719. McFarland, V. A., and Clarke, J. U. (1989). Environmental occurrence, abundance, and potential toxicity of polychlorinated biphenyl congeners: considerations for a congener-specific analysis. Environ. Health Perspect. 81, 225—239. Mes, J., and Malcolm, S. (1992). Comparison of chlorinated hydrocarbon residues in human populations from the Great Lakes and other regions of Canada. Chemosphere 25(3), 417—424. Newsome, W. H., and Andrews, P. (1993). Organochlorine pesticides and polychlorinated biphenyl congeners in commercial fish from the Great Lakes. J. AOAC. Int. 76(4), 707—710. Newsome, W. H., and Andrews P. (1995). PCB and organochlorine pesticides in Canadian human milk—1992. Chemosphere 30(11), 2143—2153. Niimi, A. J., and Oliver, B. G. (1989). Distribution of polychlorinated biphenyl congeners and other halocarbons in whole fish and muscle among Lake Ontario salmonids. Environ. Sci. Technol. 23, 83—88. Patterson, D. G. Jr., Todd, G., Turner, W. E., Maggio, V., Alexander, L. R., and Needham, L. L. (1994). Levels of non-orthosubstituted (coplanar), mono- and di-ortho-substituted polychlorinated biphenyls, dibenzo-p-dioxins, and dibenzofurans in human serum and adipose tissue. Environ. Health Perspect. 102 (suppl. 1), 195—204. Pearson, R. F., Hornbuckle, K. C., Eisenreich, S. J., and Swackhamer, D. L. (1996). PCBs in Lake Michigan water revisited. Environ. Sci. Technol. 30, 1429—1436. Schulz, D. E., Petrick, G., and Duinker, J. C. (1989). Complete characterization of polychlorinated biphenyl congeners in commercial Aroclor and Clophen mixtures by multidimensional gas chromatography—electron capture detection. Environ. Sci. Technol. 23(7), 852—859. Schwartz, T. R., and Stalling, D. L. (1987). Are polychlorinated biphenyl residues adequately described by Aroclor mixture equivalents? Isomer-specific principal components analysis of such residues in fish and turtles. Environ. Sci. Technol. 21, 72—76. USEPA (1996). Listing of Fish and Wildlife Advisories (EPA-823C-97-005). Williams, D. T., and LeBel, G. L. (1991). Coplanar polychlorinated biphenyl residues in human adipose tissue samples from Ontario municipalities. Chemosphere 22(11), 1019—1028.