Levels of Polychlorinated Biphenyls (PCBs) in Fish: The Influence on Local Decision Making About Fish Consumption.

Abstract

In 1989, the level of Aroclor 1254 (a mixture of polychlorinated biphenyls with 42 percent chlorine by weight) in fish collected from a recreational pond in Toledo, Ohio, was reported to be 44.4 milligrams per kilogram (mg/kg), prompting local health officials to declare a "no fishing advisory" for the pond. A second study conducted in 1990 did not identify elevated levels of polychlorinated biphenyls (PCBs) in fish tissue. In other words, the two studies gave conflicting results. The purpose of this study was to determine the level of Aroclor in fish tissues and then evaluate whether consumption of fish from the pond would pose a serious health risk. Fish samples collected on several occasions in 1998 and 1999 were filleted, and tissues were analyzed, as composite or individual samples, with gas chromatography. The levels of Aroclor 1254 ranged from 0.2 mg/kg in white crappies to 1.0 mg/kg in carp. These levels, while far less than the level reported in 1989, nevertheless were greater than 0.05 mg/kg, which is the maximum level established by the Great Lakes Fish Advisory Task Force for "no restriction in fish consumption." Levels of other Aroclor formulations ranged from less than the 0,02 mg/kg (the minimum detectable limit) to 0.1 mg/kg. Given current knowledge about the potential health consequence of exposure to PCBs and the results of this study, the authors have recommended that local health officials develop a new fish consumption guideline for PCBs. Any decisions about maintaining or lifting the restrictions on the pond, however, should be based on additional studies that determine the levels of other chemicals that are present in the pond and deemed hazardous to human health.

Introduction

Polychlorinated biphenyls (PCBs) are groups of synthetic chlorinated organic compounds. They comprise mixtures of distinct chlorinated biphenyls referred to as congeners. There are 209 congeners. In the United States, Monsanto Company has manufactured different mixtures of PCBs, the most widely used mixtures being Aroclors 1016, 1242, 1248, 1254, and 1260. The different mixtures have different numbers of chlorine atoms. For example, Aroclor 1254 has 42 percent chlorine by weight, while Aroclor 1260 has 54 percent chlorine by weight [1].

Because of their chemical stability and low flammability, polychlorinated biphenyls (PCBs) were widely used in electric transformers, capacitors, hydraulic fluids, protective coatings, paints, plastics, rubber, and many other products [2]. Thus, PCBs were commercially valuable, but they also posed health risks to humans. Because of potential toxicity, the manufacturing and use of PCBs were banned in the United States in 1979.

In general, most PCBs are insoluble in water, are soluble in fats, and resist biological and chemical degradation. They bioaccumulate in lipid-rich tissues, in the organs of animals, and in sediments of water bodies [1]. Therefore, animals at the top of an aquatic food chain (e.g., fish-eating birds) can accumulate more PCBs than organisms at the bottom of the food chain (e.g., zooplanktons) [3]. The number of chlorine atoms and the position of their attachment determine the level of toxicity of the mixtures, and PCBs with high chlorine content appear to resist biological and chemical degradation better than PCBs with lower chlorine content [4]. In spite of the global ban on their manufacturing and use, PCBs are still ubiquitous in the environment and remain a significant health risk to animals, including humans [5].

In rats, PCBs have caused liver and thyroid cancer, reduced sperm count and increased numbers of abnormal sperm cells, low-frequency hearing deficit, reduced levels of thyroid hormones, and serum concentrations of some pituitary hormones [6-10]. In chickens, PCBs have reduced egg production and hatching, caused weight loss, and increased mortality and neurological problems in chicks [11]. In barbels, PCBs have caused liver disease and egg and larval mortality, while among harbor porpoises, suppressed immune systems have resulted in increased mortality [12,13]. Concentrations of PCBs used in most of these studies were higher, however, than environmental PCB levels.

The toxic effects of PCBs have been extensively investigated. Acute PCB poisoning can cause acnelike skin disruption (chloracne), skin and nail pigmentation, excessive eye discharge, swelling of eyelids, and distinctive hair follicles [1]. Ingestion of rice bran oil contaminated with PCBs caused skin disease in Japan in 1968 and in Taiwan in 1979 [14,15]. The long-term effect of PCBs on human health from occupational and environmental exposure is, however, still the subject of much controversy

Carpenter extensively reviewed the effects of PCBs on the functioning of human systems (including the immune, nervous, and endocrine systems) [5]. According to a review article by Cogliano, PCBs were responsible for increased mortality from liver, gall bladder, biliary-tract, and gastrointestinal-tract cancer and from malignant melanoma in capacitor-manufacturing workers [16]. Another study however, did not find significantly elevated mortality for any site-specific cancer in PCB-exposed workers 'as compared with unexposed workers [17].

In addition to the occupationally induced cancers reported above, environmental exposure to PCBs has been implicated in other forms of disease in adults and infants. Several studies have reported a significant association between PCB levels in breast adipose tissue and breast cancer [18-20]. The concentrations of some coplanar PCBs significantly increased in postmenopausal women with estrogen-receptor-positive tumors [21]. These studies, however, had small sample sizes and did not adjust for all confounding variables. In contrast, studies that adjusted for confounding variables and had large sample sizes did not find an association between serum PCB level and breast cancer [22-26].

Recent studies have shown that consuming fish from the Great Lakes could increase the human-body PCB burden [27-30]. Maternal consumption of Great Lakes fish has been said to increase the risk of prenatal exposure to high-chlorinated PCBs [31,32]. Exposure of infants to PCBs have been associated with low birth weight, reduced IQ scores, and performance impairment [33-35]. Studies showing this association between prenatal exposure and developmental impairment have, however, been criticized for methodological problems [36-38]. In addition, other contaminants interacting with the PCBs could have caused the reported neurobehavioral deficits in infants [39,40].

Because of the potential health risks posed by chemical contaminants in fish, state and local health officials in the Great Lake region periodically issue a fish consumption advisory based on the concentration of chemical contaminants, including PCBs, in fish tissue. In 1989, local health officials in Toledo issued a health advisory for the Hecklinger pond (a 10-acre body of water in east Toledo once used for sport fishing) because of a high PCB level in fish. The advisory was based on a study that determined the level of PCBs and other chemical contaminants in a composite tissue sample obtained from 373 fish of which carp accounted for 84.3 percent by weight. The concentration of Aroclor 1254 in the sample was 44.4 milligrams per kilogram (mg/kg); all other chemical contaminants evaluated were below levels considered hazardous to human health (unpublished report, Toledo Health Department).

Approximately a year later, another study was conducted, but no Aroclor 1254 PCBs were recovered. Only a few of the 209 chlorinated biphenyls were detected in four composite samples, each consisting of carp, rock bass, white crappies, and bluegills. The detected chlorinated biphenyls were tetra-chlorinated biphenyl (at levels ranging from 0.4 mg/kg in white crappies to 5.7 mg/kg in carp), pentachlorinated biphenyl and hexachlorinated biphenyl at concentrations approximately five times the minimum detectable limit (0.05 mg/kg) (unpublished report, Toledo Health Department). Levels of these chlorinated biphenyls were significantly lower than the level of Aroclor 1254 reported in the 1989 study Because the fish consumption advisory was based on total PCBs and not on congener levels, the 1990 PCB data were not useful for revising the 1989 "no fishing advisory"

Therefore, since results of the two studies were conflicting, and methods used for PCB analysis were not adequately elaborated, a third study was conducted to determine the level of PCBs in fish tissues. The authors report here the results of this study and their recommendation for revising the1989 health advisory on the basis of these results and current knowledge about the health consequences of PCBs.

Methods

Eighty-five fish, of which bluegills accounted for 71 percent of the samples, were analyzed for PCBs. Carp was by far the largest fish in the group, followed by white perch. The length and weight of white crappies are similar to those of bluegills. Of the 85 fish, 22 were sampled in fall 1998 and 63 in early spring 1999. The fish were kept frozen until the time of analysis. Each fish was measured, weighed, and skinned; excess fat was excised and discarded. Only the edible tissue of each fish was used in the PCB analysis. Depending on size, and therefore amount of fish tissue, samples were analyzed as composites or individually Because of their large size, carp (Cyprinus carpio) and white perch (Morone americana) were analyzed as individual samples, while the smaller fish, white crappies (Pomoxis annularis) and bluegills (Lepomis macrochirus), were analyzed as composite samples. The number of fish per composite sample was four to five for crappies and five to six for bluegills.

PCB analysis followed U.S. Environmental Protection Agency (U.S. EPA) method 8082 [41]. A known mass of fish fillet was ground with anhydrous sodium sulfate and then extracted for 16 hours with a mixture of 50 percent acetone and 50 percent methylene chloride in a Soxhlet extractor. The extracts were then concentrated in a Kuderna Danish apparatus, solvent-exchanged into hexane, and afterward analyzed for the presence of PCBs with a gas chromatograph equipped with an electron capture detector.

For quality purposes, replicate portions of fish samples (one in every 10 samples) were spiked with 10 [micro]g each of Aroclor 1016 and Aroclor 1260, and the PCBs were later recovered with the procedure described above. The mixture of Aroclor 1016 and Aroclor 1260 contained a wide range of chlorinated biphenyls and was used to validate the analytical method. In addition, to determine the extraction efficiency of the analytical method, each fish sample was spiked with 1 [micro]g of decachlorobiphenyl (DCB) and 1 [micro]g of tetrachloro-m-xylene (TCMX), Surrogate recovery of these chemicals from fish samples were within an acceptable range for each sample (30 percent to 134 percent for DCB and 30 percent to 125 percent for TCMX).

Results

Similar patterns of peaks were observed in the chromatograms of all fish species analyzed for PCBs. There were no significant peaks at retention times of four minutes to eight minutes, indicating that low-chlorinated PCBs (i.e., Aroclors 1221, 1232, 1242, 1016, and 1248) were not present in any of the fish tissues. Significant peaks did, however, occur at retention times greater than eight minutes; this result was consistent with the elution times and peak area ratios associated with a mixture of Aroclor 1254 and Aroclor 1260.

It was suspected that Aroclor 1260 was present in all tissue extracts, since each of the chromatograms had triplet peaks at about 13.0, 13.2, and 13.3 minutes. This suspicion was confirmed when the retention times of the remainder peaks were compared with the peaks in Aroclor 1260 calibration standards. Since the peaks eluting prior to 12.5 minutes were, however, higher in area than the peaks eluting at 12.5 minutes (highest response of Aroclor 1260 is at 12.5 minutes), it also was suspected that Aroclor 1254 was present in all fish tissue samples. This suspicion was confirmed by comparison of the peak-area ratios in the retention times ranging from 8.7 minutes to 11.3 minutes. Peaks eluting at retention times of 8.7, 9.1, 9.8, 10.3, and 11.3 minutes confirmed the presence of Aroclor 1254. Figure 1 shows the applicable chromatograms.

Some of the PCB congeners present in Aroclor 1260 also were present in Aroclor 1254 and may have contributed to a slight bias in the analysis of Aroclor 1254 concentration. The bias was not considered to be significant, however, since the concentration of Aroclor 1254 was considerably higher than that of Aroclor 1260. By contrast, the congeners in Aroclor 1254 did not cause bias in the analysis of Aroclor 1260 concentrations, since the congeners used in the calibration of Aroclor 1260 were not present in Aroclor 1254 in significant concentrations.

Based on the chromatogram analysis, the levels of Aroclors 1221, 1232, 1242, 1016, and 1248 in all fish samples were less than the minimum detectable (0.02 mg/kg) level. Figure 2 shows the applicable chromatograms. The level of Aroclor 1260 ranged from 0.03 mg/kg in white perch to 0.1 mg/kg in carp. Aroclor 1254 was the predominant type of Aroclor found in all fish samples, at levels ranging from 0.19 [+ or -] 0.09 mg/kg in white perch to 0.33 [+ or -] 0.26 in carp (Table 1).

Discussion

Among the fish collected from the Hecklinger pond, bluegills predominated. Although the size and weight of bluegills, white crappies, and white perch were smaller than normal, several members of these fish had eggs and milt, indicating that they were mature and in prespawning conditions. Ten years after the presence of Aroclor 1254 in composite fish tissue samples was first reported by the Toledo Health Department, Aroclor 1254 and Aroclor 1260 were still present in all fish tissue samples at levels greater than the minimum detectable limit (0.02 mg/kg). Levels of Aroclor 1260 in carp and Aroclor 1254 in all fish samples were greater than 0.05 mg/kg (the level recommended by the Great Lakes Fish Task Force advisory for "no restriction in fish consumption").

High chlorine content may be one reason for the presence of Aroclor 1254 in all fish samples. As already mentioned, the higher the chlorine content of the PCB is, the lower the rate of its metabolic degradation, and, therefore, the more persistent the PCB is in animal tissues. The concentration of Aroclor 1254 found in this study is significantly lower than that reported in the 1989 study. The authors could not find an adequate explanation for the high level of Aroclor 1254 reported in the 1989 study, but speculate that it could be related to the composition of fish species in the composite sample. In the 1989 study, all fish (small and large) were analyzed as one composite sample, while in this study, carp and white perch were analyzed individually with the remaining fish grouped by species and analyzed as composite samples of three to six fish per sample. Bottom feeders such as carp can be expected to carry higher PCB body burdens than other fish species. Carp accounted for 84.3 percent of the 1989 composi te sample by weight, and, if highly contaminated, may have skewed the result upward.

Conclusion and Recommendation

The levels of Aroclor 1254 in all fish tissue samples were below the FDA action level of 2 mg/kg but exceeded the no-consumption-restriction level of 0.05 mg/kg set by the Great Lakes Fish Advisory Task Force. If such fish are not consumed raw (cooking has been reported to substantially reduce the concentration of PCBs), it can be assumed that the low levels of PCBs would be reduced to even safer levels [42].

Humans can be exposed to PCBs through inhalation of PCB vapor, ingestion of water-soluble PCBs, or ingestion of PCB-contaminated food, particularly fish [43]. Because evaporating and water-soluble PCB congeners tend to have low chlorine content, exposure via inhalation and ingestion of contaminated water poses a low health risk. Ingestion of contaminated fish and other aquatic organisms pose a higher risk, because these organisms accumulate high-chlorinated PCBs [43]. According to the U.S. EPA sample PCB calculation, daily ingestion of 30 grams of contaminated fish tissue (0.11 mg/kg PCB) for 30 years by a person weighing 70 kilograms over a lifetime (70 years) poses a cancer risk of 4.5 X [10.sup.-5] [43].

None of the published epidemiological data located by the authors link PCBs, at levels reported in this study or considered to represent background levels in the environment, to serious adverse health effects to humans. Accordingly, the authors propose that the "no fish consumption" restriction be revised. The degree of the revision, however, must be determined according to the identities and levels of all other toxic chemical contaminants potentially present in fish tissues, and the "no fish consumption" restrictions must be lifted only after this analysis is made. The authors further recommend that the local health department provide information to the public about health risks associated with consumption of fish from the Hecklinger pond.

Corresponding Author: Michael S. Bisesi, Ph.D., Department of Public Health, Medical College of Ohio, 3015 Arlington Avenue, Toledo, Ohio 43614.

Acknowledgement: The authors appreciate the assistance from David Welch, who collected the fish, and from John Huffman, who conducted the analysis of fish tissues for PCBs.

REFERENCES

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                   Mean [a] Body Length, Body Weight,
                   and Level of Aroclor 1254 in Fish
                   Tissue Samples from the Hecklinger
                          Pond in Toledo, Ohio
Type of Fish                       Sample Size (%)
Common Carp (Cyprinus carpio)           7 (8.2)
White Perch (Morone americana)          4 (4.8)
White Crappie (Pomoxis annularis)      14 (16)
Bluegill (Lepomis macrochirus)         60 (71)
Type of Fish                       Body Length (cm)
Common Carp (Cyprinus carpio)      44.14 [+ or -] 8.89
White Perch (Morone americana)     16.83 [+ or -] 0.69
White Crappie (Pomoxis annularis)  13.12 [+ or -] 0.50
Bluegill (Lepomis macrochirus)     10.93 [+ or -] 1.57
Type of Fish                       Body Weight (g)
Common Carp (Cyprinus carpio)      1154.30 [+ or -] 500
White Perch (Morone americana)       56.78 [+ or -] 4.80
White Crappie (Pomoxis annularis)    23.75 [+ or -] 1.91
Bluegill (Lepomis macrochirus)       24.73 [+ or -] 12.16
Type of Fish                       Aroclor 1254 (mg/kg)
Common Carp (Cyprinus carpio)       0.33 [+ or -] 0.26
White Perch (Morone americana)      0.19 [+ or -] 0.09
White Crappie (Pomoxis annularis)   0.27 [+ or -] 0.004 [b]
Bluegill (Lepomis macrochirus)      0.21 [+ or -] 0.07 [c]
(a.)plus or minus standard deviation.
(b.)n = 3 composite samples (4-5 fish per sample).
(c.)n = 11 composite samples (5-6 fish per sample).

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Practical Stuff!

Levels of Polychlorinated Biphenyls (PCBs) in Fish: The Influence On Local Decision Making About Fish Consumption

* Polychlorinated biphenyls (PCBs) are groups of synthetic chlorinated organic compounds.

* They comprise mixtures of distinct chlorinated biphenyls referred to as congeners.

* Because of chemical stability and low flammability, PCBs once were used in electric transformers, capacitors, hydraulic fluids, protective coatings, paints, plastics, and rubber.

* In the United States, Monsanto Company manufactured different mixtures, the most common being Aroclors 1016, 1242, 1248, 1254, and 1260.

* Because of potential toxicity, the manufacturing and use of PCBs were banned in the United States in 1979.

* Acute PCB poisoning can cause acnelike skin disruption (chloracne), skin and nail pigmentation, excessive eye discharge, swelling of eyelids, and distinctive hair follicles.

* The long-term effect of PCBs on human health from occupational and environmental exposure is still the subject of much controversy.

* The number of chlorine atoms and the position of their attachment determine the level of toxicity.

* Most PCBs are insoluble in water and soluble in fats. They resist biological and chemical degradation.

* PCBs bioaccumulate in lipid-rich tissues, in the organs of animals, and in the sediments of water bodies.

* Animals at the top of an aquatic food chain accumulate more PCBs than organisms at the bottom of the food chain.

* PCBs with high chlorine content appear to resist biological and chemical degradation better than PCBs with lower chlorine content.

* In spite of a global ban on their manufacturing and use, PCBs are still ubiquitous in the environment.

* Because of the potential health risks, health officials in the Great Lake regions periodically issue fish consumption advisories.

* In 1989, local health officials in Toledo, Ohio, issued a health advisory for the Hecklinger pond (a 10-acre body of water once used for sport fishing).

* The level of Aroclor 1254 in fish from the pond had been reported to be 44.4 milligrams per kilogram (mg/kg).

* A second study conducted in 1990 did not identify elevated levels of PCBs.

* The purpose of the current study was to determine Aroclor levels in fish tissues and evaluate whether consumption would pose a serious health risk.

* Fish samples collected in 1998 and 1999 were filleted, and tissues were analyzed with gas chromatography.

* The levels of Aroclor 1254 ranged from 0.2 mg/kg in white crappies to 1.0 mg/kg in carp.

* These levels, while far less than the level reported in 1989, nevertheless were greater than 0.05 mg/kg, which is the maximum level established by the Great Lakes Fish Advisory Task Force for "no restriction in fish consumption."

* The authors speculate that the significantly higher level of Aroclor 1254 reported in the 1989 study could be related to the composition of fish species in the samples.

* Bottom feeders such as carp can be expected to carry higher PCB body burdens than other fish species.

* Carp accounted for 84.3 percent of the 1989 sample by weight.

* The authors have recommended that local health officials develop a new fish consumption guideline for PCBs.

* Any decisions about maintaining or lifting the restrictions on the pond, however, should be based on additional studies that determine levels of other hazardous chemicals present in the pond.