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Environ. Sci. Technol. 2010, 44, 3732–3738

Polychlorinated Biphenyls and Their Hydroxylated Metabolites (OH-PCBs) in the Blood of Toothed and Baleen Whales Stranded along Japanese Coastal Waters KEI NOMIYAMA,† SATOKO MURATA,† TATSUYA KUNISUE,‡ TADASU K YAMADA,§ HAZUKI MIZUKAWA,† SHIN TAKAHASHI,† A N D S H I N S U K E T A N A B E * ,† Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan, Wadsworth Center, New York State Department of Health, Empire State Plaza, P.O. Box 509, Albany, New York 12201-0509, and Department of Zoology, National Museum of Nature and Science, 3-23-1 Hyakunin-cho, Shinjuku-ku, Tokyo, 169-0073, Japan

Received February 4, 2010. Revised manuscript received April 15, 2010. Accepted April 20, 2010.

In this study, we determined the residue levels and patterns of polychlorinated biphenyls (PCBs) and hydroxylated PCBs (OH-PCBs) in the blood from eight species of toothed whales and three species of baleen whales stranded along the Japanese coast during 1999-2007. Penta- through heptachlorinated PCB congeners were the dominant homologue groups in all cetaceans. In contrast, specific differences in the distribution of dominant OH-PCB isomers and homologues were found among the cetacean species. In five species of toothed whales (melon-headed whale, Stejneger’s beaked whale, Pacific white-sided dolphin, Blainville’s beaked whale, and killer whale), the predominant homologues were OH-pentaPCBs followed by OH-tetra-PCBs and OH-tri-PCBs. The predominant homologues of finless porpoise and beluga whale were OH-penta-PCBs followed by OH-hexa-PCBs and OH-triPCBs. The predominant OH-PCB isomers were para-OHPCBs such as 4OH-CB26, 4′OH-CB25/4′OH-CB26/4OH-CB31, 4OHCB70, 4′OH-CB72, 4′OH-CB97, 4′OH-CB101/4′OH-CB120, and 4OH-CB107/4′OH-CB108 in toothed whales. In three baleen whales (common minke whale, Bryde’s whale, and humpback whale) and in sperm whale (which is a toothed whale), OHocta-PCB (4OH-CB202) was the predominant homologue group accounting for 40-80% of the total OH-PCB concentrations. The differences in concentrations and profiles of OH-PCBs may suggest species-specific diets, metabolic capability, and the transthyretin (TTR) binding specificity. These results reveal that the accumulation profiles of OH-PCBs in cetacean blood are entirely different from the profiles found in pinnipeds, polar bear, and humans. * Corresponding author phone: +81-89-927-8171; fax: +81-89927-8171; e-mail: [email protected] † Ehime University. ‡ New York State Department of Health. § National Museum of Nature and Science. 3732

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Introduction Several polychlorinated biphenyl (PCB) congeners are known to affect endocrine systems and neurodevelopment in humans and wildlife (1-3). Despite the ban on their production in many developed countries in the late 1970s and a global ban on their usage and disposal in 2004 under the Stockholm Convention on persistent organic pollutants (POPs), PCBs are still found at elevated concentrations in higher trophic level animals such as marine mammals related to food-chain (4, 5). It has been reported that PCBs disrupt thyroid hormone (TH) homeostasis in animals (6). A possible mechanism involved in the disruption of TH homeostasis is competitive binding of PCBs with TH transport protein, transthyretin (TTR), in blood (6-8). It has been demonstrated that the binding affinity to TTR was much stronger for hydroxylated PCBs (OH-PCBs), which are formed by oxidative metabolism of PCBs by cytochrome P450 (CYP) monooxygenases enzyme system than for the parent PCBs, due to the structural similarity of OH-PCBs to thyroxine (T4) (6-8). The formation of OH-PCBs is, in general, via arene oxide, followed by 1,2-shift (9). Alternatively, OH-PCB metabolites can be formed via direct insertion of hydroxyl group to parent PCBs (10). If the hydroxyl group is on the para-position of a biphenyl structure and has adjacent chlorine atoms, the structure resembles T4 (11). This structural similarity allows OH-PCBs to bind with a strong affinity to TTR (7, 8), and disrupt TH homeostasis and retinol (vitamin A) transportation (12, 13). TH plays critical roles in the development of central nervous system and brain function (14). In a recent study using reporter gene assays, it was shown that extremely low doses of OH-PCBs (10-10 M) suppressed 3,5,5′-triiodothyronine (T3)-induced transcriptional activation of thyroid hormone receptor (15). Moreover, it has been reported that OH-PCBs could suppress T3/thyroid hormone receptor mediated transcription through partial dissociation of thyroid hormone receptor/retinoid X receptor of TH-responsive element (16). Thus, low levels of OH-PCBs can adversely affect gene expression in brains. OH-PCBs have been detected in the blood and tissues of humans (17-20) and several wildlife species (21-28), and those levels and patterns were shown to vary with species, possibly due to species-specific metabolic capacity by phase I CYP and/or phase II conjugation enzymes and binding affinity to TTR (29, 30). Such interesting observations suggest the need for studies on OH-PCB residue levels in biota. However, little is known on the patterns and levels of OHPCBs in cetaceans, which accumulate some of the highest concentrations of PCBs (26, 28, 31-36). Our preliminary study on penta- through hepta- chlorinated OH-PCB congeners in the blood of melon-headed whales (Peponocephala electra) and finless porpoises (Neophocaena phocaenoides) stranded along Japanese coastal waters showed that OH-penta-PCB/penta-PCB ratios were higher than the ratios for hexa- and hepta-chlorinated homologue groups (35). Moreover, considerably higher proportions of OH-penta-PCBs were found in melon-headed whales and finless porpoises than in humans (19, 20). These results clearly indicate preferential accumulation of OH-penta-PCBs and suggest accumulation of less-chlorinated OH-PCBs (3-4 chlorines) in cetacean blood. Such a pattern has been reported for toothed whales. OH-penta-PCB congeners accounted for 90% of the total OH-PCB concentrations in beluga whale (Delphinapterus leucus) livers from the Canadian Arctic and the St. Lawrence River (32). In addition, considerable levels of 3-5 chlorinated OH-PCB congeners 10.1021/es1003928

 2010 American Chemical Society

Published on Web 04/28/2010

FIGURE 1. Median concentrations of total PCBs and total OH-PCBs (pg/g wet wt in whole blood) in the blood of toothed and baleen whales stranded along Japanese coastal waters. Error bars indicate range (minimum to maximum concentrations). Concentration of total PCBs in humpback whale was lower than the limit of quantification (LOQ). were found in blood plasma of bottlenose dolphin (Tursiops truncatus) from the Western Atlantic and the Gulf of Mexico (33). More recently, OH-PCBs have been reported in the cerebrospinal fluid of short-beaked common dolphins (Delphinus delphis) and Atlantic white-sided dolphins (Lagenorhynchus acutus) from the western North Atlantic of the United States (28), and plasma of a captive killer whale (Orcinus orca) (36). However, comprehensive investigations on residue patterns of OH-PCBs encompassing a wide range of homologues, in cetaceans, are lacking. The present study elucidated residue levels and patterns of tri- through octachlorinated homologues of OH-PCB congeners, and examined correlations between OH-PCBs and PCBs in the blood from eight species of toothed whales and three species of baleen whales stranded along the Japanese coast during 1999-2007.

Experimental Section Collection of Blood from Toothed and Baleen Whales. The whole blood samples were collected from eleven species of cetaceans (n ) 55) including melon-headed whale (Peponocephala electra) (n ) 14: male ) 7, female ) 7), finless porpoise (Neophocaena phocaenoides) (n ) 7: male ) 4, female ) 3), Stejneger’s beaked whale (Mesoplodon stejnegeris) (n ) 12: male ) 5, female ) 7), Pacific white-sided dolphin (Lagenorhynchus obliquidens) (n ) 7: male ) 5, female ) 2), Blainville’s beaked whale (Mesoplodon densirostris) (n ) 4: male ) 2, female ) 2), killer whale (Orcinus orca) (n ) 3: female ) 2, unknown ) 1), beluga whale (Delphinapterus leucas) (n ) 1: male ) 1), sperm whale (Physeter macrocephalus) (n ) 2: male ) 2), Bryde’s whale (Balaenoptera brydei) (n ) 2: male ) 1, female ) 1), common minke whale (Balaenoptera acutorostrata) (n ) 2: male ) 1, female ) 1), and humpback whale (Megaptera novaengliae) (n ) 1: female ) 1) stranded along the Japanese coast during 1999-2007 (Supporting Information (SI) Figure S1). Blood samples were collected directly from the hearts with dissection of a cadaver of cetaceans. All the blood samples were collected in falcon polypropylene conical tube and stored in the Environmental Specimen Bank (es-BANK) of Ehime University, Japan, at -25 °C were used for analysis (37). Chemicals. The authentic reference standards of 62 PCB (mono- to deca-) and 52 OH-PCB (tri- to octa-) isomers used for identification and quantification are given in SI Table S1. Measurements of PCBs and OH-PCBs in Whole Blood. The extraction procedure used in this study is similar to the method described earlier (26, 27). PCBs and OH-PCBs were

extracted from blood sample (10 g) with 50% methyl t-butyl ether (MTBE)/hexane. The organic phase was partitioned into PCBs and OH-PCBs fractions by 1 M potassium hydroxide (KOH) in 50% ethanol/water. The organic phase (containing PCBs) was passed through the gel permeation chromatography (GPC) and activated silica-gel column chromatography. PCBs fraction was concentrated for gas chromatography/ mass spectrometry (GC/MS) analysis. The alkaline phase (containing OH-PCBs) was acidified with sulfuric acid, and then OH-PCBs were re-extracted with MTBE/hexane. The organic phases passed through nonactivated silica-gel column chromatography. OH-PCBs were derivatized by using trimethylsilyldiazomethane. The derivatized solution was passed through activated silica-gel column chromatography. Identification and quantification of MeO-PCBs were performed using high-resolution GC/MS (JEOL JMS-800D, Japan). A detailed description of the experimental procedures can be found in the SI. Quality Assurance and Quality Control. PCBs and OHPCBs were quantified using isotope dilution method to the corresponding 13C12-internal standards. A detailed description can be found in the SI. Statistical Analysis. The Mann-Whitney U-test was used to test group of significant differences. Spearman’s rank correlation coefficients were calculated to compare the concentrations of PCBs and OH-PCBs in each cetacean. The p-values 0.05), 4OH-CB70/CB70 (r ) 0.12, p > 0.05), 4′OH-CB101 + 120/CB101 (r ) 0.66, p < 0.001), 4OH-CB107 + 4′OH-CB108/CB105 + 118 (r ) 0.68, p < 0.001), 3′OH-CB118/CB118 (r ) 0.28, p < 0.01), 4OH-CB146/CB138 + 153 (r ) 0.32, p < 0.05), 3OH-CB153/CB153 (r ) 0.58, p < 0.05), 4′OH-CB172/CB170 + 180 (r ) 0.23, p > 0.05), 4OH-CB187/CB183 + 187 (r ) 0.31, p > 0.05), and 4OH-CB202/CB202. p values: Spearman’s rank correlation coefficients. the Lake trout (Salvelinus namaycush) from the Great Lakes (42). The specific fish prey of baleen whales may have higher accumulation of 4OH-CB202. Characteristic differences found in the homologue patterns of OH-PCBs in cetaceans suggest the need for further studies on the differences in exposure profiles metabolic capacities and toxic effects. Accumulation Features of OH-PCB Isomers. Among the OH-PCB isomers identified, 4OH-CB26, 4′OH-CB25/4′OHCB26/4OH-CB31, 4OH-CB70, 4′OH-CB72, 4′OH-CB97, 4′OHCB101/4′OH-CB120, and 4OH-CB107/4′OH-CB108 were the predominant ones in the blood of toothed whales (SI Table S3). These tri- through penta-chlorinated OH-PCB isomers were detected at relatively higher levels than the hexathrough octa-chlorinated OH-PCB isomers. In recent studies, 4OH-CB107, 4OH-CB146, 3OH-CB153, and 4OH-CB187 were detected as dominant isomers in blood of humans and wildlife (17-28). However, the predominant OH-PCB isomers detected in cetacean blood, in this study, were not similar in structure to T4. The predominant 3-4 chlorinated OH-PCB isomers in cetaceans had one chlorine atom adjacent to OHgroup on the phenyl rings (T3-like OH-PCBs), and the chemical structures of these OH-PCBs are different from those congeners reported as having high binding affinity to TTR (45). Concentrations of these OH-PCB isomers were 17-70% of the identified OH-PCB concentrations (SI Figure S2). This result indicates that the accumulation profiles of OH-PCB isomers in cetacean blood are clearly different from those in other mammals and birds (17-28). The OH-PCB isomers identified in cetaceans might be less persistent in the blood due to their further metabolic degradation and weak binding affinity to TTR. Further studies are needed to evaluate the factors affecting accumulation and toxicity of lowerchlorinated OH-PCBs found in toothed whales.

In three baleen species (common minke whales, Bryde’s whales, and humpback whale) and in sperm whales (which is a toothed whale), 4OH-CB202 was detected as a major congener at concentrations 1-2 orders of magnitude higher than that found in other toothed whales (SI Table S3). Previous study (46) on the activities of phenobarbital (PB)-type isozymes and 3-methylcholanthrene (MC)-type isozymes indicated that common minke whales have relatively high PB type (CYP 2B and 2C type) activity. A few studies have shown that CYP2B enzyme activity is minimal or inactive in toothed whales (43, 44). Buckman et al. (47) showed that rainbow trout exposed to a mixture of PCBs (including CB202) and resulted in bioformed OH-PCB (including 4OH-CB202) congeners through the catalytic activity of CYP1B and/or CYP2B enzymes. Elevated 4OH-CB187/CB183 + 187 and 4′OH-CB199/CB199 ratios were recently reported in blood of polar bears and it was suggested that these PCB metabolites were formed through the catalytic activity of CYP2B and/or CYP2D enzymes (48). Moreover, it is demonstrated that PBtype isozymes, CYP2B and/or CYP2C subfamilies, play a primary role in the metabolism of CB153 in dogs (49). Based on these findings, it is likely that CYP2C-type enzymes are responsible for the metabolism of higher-chlorinated OHPCBs in baleen whales and sperm whales. However, the differences in the activities of drug-metabolizing enzymes between sperm whales and other toothed whales have not been clarified so far. Nikaido et al. (50) reported that a small population of common ancestors of all toothed whales ultimately diverged into the lineages of sperm whales and other dolphins. This may suggest that drug-metabolizing enzymes of sperm whales are related to the evolution process and are different from other toothed whales. Sperm whales and baleen whales may have similar metabolic capacity VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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pounds in the blood of cetaceans. In sperm whales and baleen whales, the ratio of 4OH-CB202/CB202 was greater than 1, implying that these animals can metabolize CB202 and/or 4OH-CB202 via their preys and retain the metabolite in the blood. This study revealed that the accumulation profiles of OHPCBs in cetacean blood are entirely different from the profiles reported in pinnipeds, birds and humans. In future, further studies on the metabolism and toxicity of OH-PCBs in various cetaceans using fresh liver and also on the phylogenetic evolution of TTR in marine mammals are needed.

Acknowledgments

FIGURE 5. Concentrations ratios of predominant OH-PCB isomers and their potential parent PCB isomers in the blood of cetaceans: comparison of toothed whales and baleen whales. toward PCBs, especially CB202, and/or TTR of these species may have strong affinity to 4OH-CB202. Correlations Between Parent PCBs and OH-PCBs. Significant correlations between the most abundant OH-PCBs and their parent PCBs can indicate the origin of metabolites (19, 20, 45). Figure 4 shows correlation between the most abundant OH-PCBs and their potential parent PCBs in cetaceans studied. OH-penta-PCBs and parent penta-PCBs: 4′OH-CB101 + 120/CB101 (p < 0.001), 4OH-CB107 + 4′OHCB108/CB105 + 118 (p < 0.001), and 3′OH-CB118/CB118 (p < 0.01) showed significant positive correlation. OH-hexaPCBs and parent hexa-PCBs: 4OH-CB146/CB138 + 153 (p < 0.05), and 3OH-CB153/CB153 (p < 0.05) showed a weak, but significant correlation. In the lower-chlorinated PCBs, 4′OHCB18/CB18 and 4OH-CB70/CB70 showed no significant correlations (p > 0.05). This suggests that individuals with high levels of PCBs also contain high levels of OH-PCBs, supporting the fact that OH-PCBs have been formed via induction of CYPs. In the case of more highly chlorinated PCB congeners, no significant positive correlation between 4′OH-CB172/CB170 + 180, 4OH-CB187/CB183 + 187, and 4OH-CB202/CB202 were found (p > 0.05). Higher-chlorinated (6-8 chlorines) PCBs are less metabolizable, especially in cetaceans, having relatively lower metabolic capacity (4). Species Differences in the Accumulation Pattern of OH-PCBs. Concentration ratios of OH-PCBs to PCBs (OHPCBs/PCBs ratios) can indicate metabolic rates and patterns induced by a number of factors, including exposure to parent PCBs, sexuality, induction levels of hepatic enzymes, and TTR binding affinity (20). OH-PCBs/PCBs ratios were calculated based on the concentrations of OH-PCB and PCB congeners deemed as parent compounds of the dominant metabolites (Figure 5). The ratios were the highest for 4OHCB70/CB70, followed by 4′OH-CB18/CB18, 3′OH-CB118/ CB118, 4′OH-CB101 + 120/CB101, and 4OH-CB107 + 4′OH-CB108/CB105 + 118. Except for sperm whales, the ratios for lower-chlorinated OH-PCBs/PCBs were 2-3 orders higher than those of more highly -chlorinated congeners (4OH-CB146/CB138 + 153, 3OH-CB153/CB153, 4′OH-CB172/ CB170 + 180, and 4OH-CB187/CB183 + 187) in toothed whales. This result reiterates that lower-chlorinated PCBs are more readily metabolized than higher-chlorinated PCBs. Furthermore, lower-chlorinated OH-PCBs are retained in the blood of toothed whales. The accumulation of OH-PCBs is affected by phase I metabolizing enzymes (formation of OHPCBs from PCBs) and phase II conjugation enzymes (formation of OH-PCBs to (OH)2-PCBs and conjugation reaction) (45). Moreover, dietary exposure to PCBs and OH-PCBs can have some relation to the observed profiles of these com3736

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We deeply appreciate the generous cooperation on the sample collection provided by scientists and staffs of Aquarium Asamushi, Choshi Ocean Institute, Ehime University School of Medicine, Ibaraki Prefectural Oarai Aquarium, The Institute of Cetacean Research, Kagoshima City Aquarium, Izu Mito Sea Paradise, Joetsu Municipal Aquarium,KashiwazakiCityMuseum,KujukushimaAquarium, Kumamoto University, Kyusyu University, Marine World Umino-Nakamichi, Faculty of Bioresources, Mie University, Nagasaki Prefectural Government, Nagasaki University, Notojima Aquarium, Noto Marine Center, Oita Marine Palace Aquarium, Saga University, and Shimonoseki Marine Science Museum. We thank Dr. Kurunthachalam Kannan, Wadsworth Center, New York State Department of Health, Albany, New York and Dr. Annamalai Subramanian, Center for Marine Environmental Studies (CMES), Ehime university, Japan, for critical reading of this manuscript. This study was supported by Grants-in-Aid for Scientific Research (S) (No. 20221003), Exploratory Reseach (No. 21651024) and “Global COE Program” from the Ministry of Education, Culture, Sports, Science and Technology, Japan (MEXT) and Japan Society for the Promotion of Science (JSPS).

Supporting Information Available A detailed description of experimental procedures and reference standards list (Table S1), detailed information on concentrations of PCBs and OH-PCB congeners of all cetaceans (Tables S2 and S3), sampling locations of cetaceans stranded along the Japanese coast (Figure S1), and contribution of the structures of T3-like OH-PCBs and T4-like OHPCBs in the blood of toothed and baleen whales (Figure S2). This material is available free of charge via the Internet at http://pubs.acs.org.

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