Levels and Toxicokinetic Behaviors of PCDD, PCDF, and Coplanar

Jun 17, 2004 - determined in the liver and pectoral muscle of common cormorants ... Cormorant, a fish-eating bird, widely distributed in aquatic ...
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Environ. Sci. Technol. 2004, 38, 3853-3859

Levels and Toxicokinetic Behaviors of PCDD, PCDF, and Coplanar PCB Congeners in Common Cormorants from Lake Biwa, Japan A K I R A K U B O T A , † H I S A T O I W A T A , * ,† SHINSUKE TANABE,† KUMIKO YONEDA,‡ AND SACHIKO TOBATA‡ Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan, and Japan Wildlife Research Center, Shitaya 3-10-10, Taito City, Tokyo 110-8676, Japan

Concentrations of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and coplanar polychlorinated biphenyls (Co-PCBs) were determined in the liver and pectoral muscle of common cormorants (Phalacrocorax carbo) collected from Lake Biwa, Japan. To clarify the toxicokinetic behaviors and potential toxicities of these chemicals, the present study addresses life-stage- and tissue-specific accumulation of the congeners. Total 2,3,7,8-tetrachlorodibenzo-p-dioxin toxic equivalents (TEQs) were in the range of 360 to 50 000 pg/g lipid weight in the liver and 310 to 12 000 pg/g lipid weight in the pectoral muscle. Among congeners, for which toxic equivalency factors were assigned, PCB126, 2,3,4,7,8-P5CDF, and 1,2,3,7,8-P5CDD made a greater contribution to total TEQs in the liver. Hepatic concentrations of T4- to H6CDDs, P5- and H6CDFs, and Co-PCBs (except PCB77) significantly increased with growth of cormorants, leading to life-stage-related compositional changes. The concentration ratios of liver to pectoral muscle revealed preferential accumulation of higher chlorinated congeners in hepatic tissue. For most congeners, concentration ratios significantly increased with an increase in hepatic total TEQs, suggesting their concentration-dependent hepatic sequestration. These results imply the presence of hepatic binding protein(s) such as cytochrome P450, inducible by these chemicals, which may function as a binding species different from aryl hydrocarbon receptor. On the basis of these results, we conclude that the toxicokinetic behavior of each congener is life-stage-, tissue-, and concentrationdependent. TEQs in wildlife populations exposed to multiple congeners with varying concentrations should be used with caution for risk assessment, even within a species.

because of their worldwide distribution, high persistency, and lipophilic nature. Such chemical properties allow these chemicals to facilitate accumulation through the food web into higher trophic organisms. Cormorant, a fish-eating bird, widely distributed in aquatic environments at a higher trophic level, has been addressed as a suitable bioindicator species to understand the contamination and toxic effects of these chemicals. Previous reports indicated the impairments of reproductive performance and developmental deformities related to high accumulation of these congeners in the avian species (1). Toxicokinetic behavior is known to be dependent on factors including sex, life stage, tissue, and metabolic capacity of organisms. In addition, dose/concentration, exposure route, and absorption efficiency of certain chemicals may also be crucial factors, as reported in several laboratory studies (2). Therefore, the accumulation and toxic potential of each PHAH congener in wild populations may be affected by their toxicokinetics. Wildlife is chronically exposed to complex mixtures of PHAHs via the gastrointestinal tract, whereas laboratory animals, in most cases, are administered with single or repeated doses of a defined congener through various routes for a short period. The validity of such an experimental approach for PHAH toxicokinetics is completely unproven, and many questions still remain to be resolved. Because information on toxicokinetics from laboratory studies might cause false evaluation of risk in wildlife, congener-specific toxicokinetics of PHAHs need to be verified in wildlife. Nevertheless, most of the kinetic data available for wild avian species have been derived from a limited number of congeners in certain life stages and tissues (3). An earlier study reported only six Co-PCB congeners analyzed in the liver of common cormorants from Tokyo Bay, and life stage-dependent accumulation (4). Common cormorants residing around Lake Biwa, which is the largest freshwater lake in Japan, also exhibited considerable high levels of these chemicals (5). However, no comprehensive data are available on congener-specific toxicokinetics of PCDDs, PCDFs, and Co-PCBs, considering multiple factors to be involved. Our recent study isolated two distinct aryl hydrocarbon receptors (AHRs), through which the toxicity of PHAHs is mediated, in common cormorant (6). Although functions of these AHRs have not yet been evaluated, this may be a crucial factor affecting toxicokinetics of PHAHs in this species. Because Lake Biwa is a closed environment with a single outlet river and a few canals in contrast to more than 450 inlet rivers, it may work as a sink for pollutants. This study therefore clarifies the residue levels of congeners of PCDDs, PCDFs, and Co-PCBs in wild cormorant populations from Lake Biwa. The toxicokinetic behavior of each congener will be addressed, particularly focusing on factors including life stage, tissue, and residue concentration. Role of AHR and cytochrome P450 (CYP) in congener-specific accumulation will also be discussed.

Materials and Methods Introduction The planar halogenated aromatic hydrocarbons (PHAHs), including polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and coplanar polychlorinated biphenyls (Co-PCBs), have been of great concern * Corresponding author phone and fax: +81-89-927-8172; email: [email protected]. † CMES, Ehime University. ‡ Japan Wildlife Research Center. 10.1021/es0494858 CCC: $27.50 Published on Web 06/17/2004

 2004 American Chemical Society

Samples. Twenty-six common cormorants (Phalacrocorax carbo) captured under the license from Shiga Prefecture in May 2001 from the southern part of Lake Biwa were used for this study (Figure 1). Cormorants were immediately dissected onboard after measurements of biometry. Subsamples of liver and pectoral muscle were stored at -20 °C until chemical analysis. Growth stage of cormorants was determined from the development of reproductive organs. For nine female specimens, however, the growth stage could not be determined due to the involution of reproductive organ, as the VOL. 38, NO. 14, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 1. Geometric Mean Concentrations and TEQs of PCDDs, PCDFs, and Co-PCBs in the Liver and Pectoral Muscle of Common Cormorants from Lake Biwa, Japan liver (n ) 26)

congener lipid (%)

4.0 (2.2-5.2)

pectoral muscle (n ) 20) 4.6 (2.5-6.5)

PCDDs (pg/g lipid wt) 2,3,7,8-T4CDD 1,2,3,7,8-P5CDD 1,2,3,4,7,8-H6CDD 1,2,3,6,7,8-H6CDD 1,2,3,7,8,9-H6CDD 1,2,3,4,6,7,8-H7CDD 1,2,3,4,6,7,8,9-O8CDD

53 (6.8-470) 350 (50-4700) 130 (19-1200) 360 (29-4500) 43 (