Environ. Sci. Technol. 2008, 42, 685–691
Regional Trend and Tissue Distribution of Brominated Flame Retardants and Persistent Organochlorines in Raccoon Dogs (Nyctereutes procyonoides) from Japan †
TATSUYA KUNISUE, NOZOMI TAKAYANAGI,† TOMOHIKO ISOBE,† SHIN TAKAHASHI,† SUSUMU NAKATSU,‡ TOSHIO TSUBOTA,§ KEISUKE OKUMOTO,| S U M I O B U S H I S U E , | KAZUYUKI SHINDO,| AND 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, Nakatsu Veterinary Surgery Hospital, Shorinji-cho nishi 2-2-15, Sakai 590-0960, Japan, Laboratory of Wildlife Biology, Department of Environmental Veterinary Medicine, Graduate School of Veterinary Medicine, Hokkaido University, Kita18, Nishi 9, Kita-ku, Sapporo 060-0818, Japan, and Ehime Prefectural Institute of Public Health and Environmental Science, Sanban-cho 8-234, Matsuyama 790-0003, Japan
Received June 26, 2007. Revised manuscript received November 8, 2007. Accepted November 9, 2007.
The present study investigated concentrations and patterns of brominated flame retardants, such as polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs), and persistent organochlorines (OCs) in liver and adipose tissues of raccoon dogs (RD: Nyctereutes procyonoides) collected from two metropolises and a local prefecture in Japan during 2001–2006. Relatively high concentrations of PBDEs were found in RD livers, while HBCD levels were the lowest among the measured organohalogen compounds. Among PBDE congeners, BDE 209 was predominant in RDs from all the regions, indicating that pollution derived from the technical decaBDE product is extensive across Japan. On the other hand, concentrations of tetra- to nona-BDE congeners in RDs from a metropolis were significantly higher than those from the other two regions, implying that there were regional differences in the past usage of the technical tetraBDE and octaBDE products. Such a regional difference was also observed for HBCD levels. Lipid-normalized concentration ratios of liver to adipose tissue (L/A ratio) for tri to hepta-BDE congeners were lower than 1.0 in the investigated eight RDs, suggesting lipid-dependent accumulation. However, the L/A ratios of BDE 209 exceeded 1.0 in all the specimens, suggesting hepatic retention of this compound. In addition, lipid-dependent accumulation of * Corresponding author phone: +81-89-927-8171; fax: +81-89927-8171; e-mail:
[email protected]. † Ehime University. ‡ Nakatsu Veterinary Surgery Hospital. § Hokkaido University. | Ehime Prefectural Institute of Public Health and Environmental Science. 10.1021/es071565z CCC: $40.75
Published on Web 12/29/2007
2008 American Chemical Society
R-HBCD was observed, but the L/A ratios of γ-HBCD were greater than 1.0 in some specimens. These results indicate that Japanese RDs have been recently exposed to BDE 209 and γ-HBCD and accumulated both these compounds preferentially in blood-rich organs, probably due to their binding to proteins and/or rapid biotransformation, as reported in experimental rodents.
Introduction In recent years, environmental pollution by polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs), which are in use as brominated flame retardants (BFRs), has been drawing international attention. As in the case of organochlorines (OCs) such as dioxins and PCBs, these BFRs are persistent in the environment and have bioaccumulative nature (1–3). Although the detailed information on toxic effects are still lacking, it has been reviewed that PBDEs potentially cause adverse effects, such as clinical, morphological, immunological, and behavioral changes, disturbance of thyroid hormone homeostasis, and enzyme induction in in vivo and in vitro studies using experimental mammals and human cell lines (4–6). Toxic data on HBCDs are very scarce compared with PBDEs (6, 7). However, an in vitro study has suggested that HBCDs might cause neurotoxic effects (8). Thus, in North America and Europe, a large number of studies have been conducted on BFRs contamination in human and wildlife (see refs 1 and 3). Studies on temporal trends showed that since the late 1990s no significant change was observed for PBDEs and HBCDs in guillemot (Uria algae) eggs from Baltic Sea and PBDEs in blubber of California sea lion (Zalphophus californianus), but HBCD levels in blubber of California sea lion increased (9, 10). While many reports on BFRs contamination in wildlife inhabiting aquatic environment and polar regions are available (see refs 1 and 3), studies on terrestrial wild animals, especially on HBCDs, are very limited. In Japan, the technical tetraBDE and octaBDE products were used as flame retardants until 1990 and 1999, respectively, and the technical decaBDE product is still in use (11). PBDEs have been detected in various Japanese environmental media and biota such as air, sediment, and fish (11). Hence, investigations on residue levels of PBDEs in Japanese human milk, blood, and adipose tissues have been recently conducted to assess human exposure to these contaminants (12–17). In time trend studies, it was shown that PBDE levels in Japanese human milk and adipose tissues increased from 1973 to 2004 (12, 13) and from 1970 to 2000 (16), respectively, indicating recent increase in human exposure to these contaminants. In addition, a study on PBDEs in Japanese human blood showed regional differences in PBDE levels, indicating region-specific human exposure (15). However, there is much less information available on the levels and toxicity of PBDEs in Japanese wildlife. While consumption of the technical decaBDE has been decreasing each year, recent increased usage of the technical HBCD have been reported in Japan (11). A recent study using sediment cores from Tokyo Bay demonstrated an increasing trend of HBCD levels until now and a consistency with increased consumption of the technical HBCD (18). Therefore, the growing input of HBCDs into the Japanese environment and subsequent exposure of various animals to these contaminants can be suspected. To our knowledge, no data on HBCDs in Japanese wildlife, and even in humans, is available. We have previously analyzed OCs in wild raccoon dogs (RD: Nyctereutes procyonoides) from a Japanese metropolis VOL. 42, NO. 3, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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and found elevated levels of polychlorinated dibenzo-pdioxins (PCDDs), dibenzofurans (PCDFs), and chlordane compounds (CHLs), indicating that significant pollution sources of these contaminants are still present in Japanese terrestrial environments (19, 20). Additionally, hepatic sequestration of PCDD/DFs and oxychlordane was observed in RDs (19, 20). While hepatic sequestration of PCDD/DF congeners has been demonstrated in experimental mice (21, 22), no data is available for oxychlordane, suggesting RD-specific accumulation of this compound (20). RD might be an interesting species for monitoring not only OCs but also BFRs, due to its limited habitat area and short life span. PBDEs and HBCDs are used in electronic and electrical equipments, thermal insulation foam, and upholstery in Japan. Although no investigation on the regional trend of BFRs has been conducted in the Japanese environment, higher levels of PBDEs in urban air and soil than in rural areas have been found in a recent UK study, probably due to high usage of furnishings, electronic goods, etc (23). Considering these observations, it can be suspected that wild RDs, which inhabit areas close to human activity, have been exposed to BFRs derived from in-use technical products and may show specific accumulation patterns such as hepatic sequestration of these contaminants. The present study attempted to elucidate the contamination levels and patterns of OCs and BFRs such as PBDEs and HBCDs in RDs collected from three Japanese regions. In addition, we addressed hepatic sequestration of BFRs by analyzing liver and adipose tissues of RDs to verify whether the same phenomenon as in case of PCDD/DFs and oxychlordane is observed.
Materials and Methods Samples. Liver samples of raccoon dogs (RD; Nyctereutes procyonoides) that died in traffic accidents during 2001–2003 were obtained from Kanagawa (n ) 10; males ) 5 and females ) 5), an eastern metropolis, and from Ehime (n ) 21; males ) 12 and females ) 9), a local prefecture. Additionally, liver and adipose tissue samples of RDs were obtained from Osaka (n ) 8; male ) 5, female ) 3), a western metropolis, during 2004–2006. The specimens from Osaka were the RDs which were caught by traps set up to prevent crop damage or avoid wild animals from entering indoors. These traps were not designed to kill the animals, but some of them had accidentally died before their release into the wild. Locations of these prefectures in Japan are shown in Supporting Information (SI) Figure S1. All the samples were stored in the Environmental Specimen Bank (es-BANK) for Global Monitoring, Ehime University (24) at -20 °C until analysis. Information on the systematics, food habit, life span, and activity area of RD were described previously (20). Chemical Analysis. Analysis of PBDEs (BDE 15, 28, 47, 99, 100, 153, 154, 183, 196, 197, 206, 207, and 209) and HBCDs (R-, β-, and γ-HBCD) in RD liver or adipose tissue was performed following the procedures described by Ueno et al. (25) and Isobe et al. (26) with slight modifications. The analytical method of OCs, such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane and its metabolites (DDTs), hexachlorocyclohexane isomers (HCHs), chlordane compounds (CHLs), and hexachlorobenzene (HCB), in RDs has been already described (20). In this study, data on OCs in RD livers from Kanagawa were cited from Kunisue et al. (20). The concentrations of organohalogen compounds were expressed on lipid weight basis. Detailed description of chemical analysis and QA/QC are given in the SI. Statistical Analysis. Mann–Whitney U test and Kruskal–Wallis test were employed to evaluate differences in organohalogen concentrations between sexes and regions, respectively. A p value of less than 0.05 was considered to indicate statistical significance. These analyses were executed 686
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using StatView (Version 5.0, SAS Institute Inc., U.S.). To compare regional PBDE profiles, principal component analysis (PCA) was performed using Excel Toukei 2000 (Social Survey Research Information Co., Ltd., Japan). For PCA, each congener concentration in the individual RD was normalized as a contribution ratio to the total PBDE concentrations.
Results and Discussion Residue Levels. Organohalogen compounds were detected in all the RD samples analyzed in this study (Table 1), while BDE 15 was below LOQ (data not shown). No significant difference was observed between concentrations of these contaminants in males and females, and this trend was similar to the results of previous studies (19, 20). This may be due to a short lactation period of RDs, as discussed in previous studies (19, 20). Therefore, concentrations of organohalogen compounds in males and females from each region were treated as one data set in the subsequent discussion. Concentrations of CHLs (range: 170–43000 ng/g) were dominant in RD livers, followed by PCBs (15–1700 ng/g), DDTs (0.45–290 ng/g) or HCHs (6.3–250 ng/g) or PBDEs (0.36–250 ng/g), HCB (0.54–61 ng/g), HBCDs (
