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Accumulation Features of Pcbs and Hydroxylated Metabolites in the Blood of Terrestrial Mammals

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Accumulation Features of Pcbs and Hydroxylated Metabolites in the Blood of Terrestrial Mammals ACCUMULATION FEATURES OF PCBS AND HYDROXYLATED METABOLITES IN THE BLOOD OF TERRESTRIAL MAMMALS Hazuki Mizukawa1, Kei Nomiyama1, Susumu Nakatsu2, Terutake Hayashi3 and Shinsuke Tanabe1 1Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama, Ehime 790-8577, Japan 2Nakatsu Animal Hospital, 2-2-5, Rinsyoujityounishi, Sakai-ku, Sakai-shi, Osaka 590-0960, Japan 3Tochigi prefectural museum, 2-2, Mutsumi-cho, Utsunomiya, Tochigi 320-0865, Japan Introduction Hydroxylated PCBs (OH-PCBs) are formed by oxidative metabolism of PCBs by cytochrome P450 monooxygenases (CYP) in the liver after PCBs were ingested into the body. Then OH-PCBs undergo conjugation reactions (e. g. glucuronidation, glutathione conjugation, sulfoconjugation), and eliminated from the body. However, the structural similarity to thyroxine (T4) allows OH-PCBs to bind strongly with transthyretin (TTR) which is a thyroid hormone transport protein, and OH-PCBs are carried by blood to organs and tissues. OH-PCBs have been detected in the blood, liver and brain of various marine and terrestrial mammals, and birds1-6. Previous researches obviously indicate that the capacity to metabolize PCBs into OH-PCBs differ widely among animal species. Particularly, OH-PCBs levels were found to be higher than parent PCBs in the blood of carnivora species such as dog, cat and raccoon dog4. They presume toxicological risk of OH-PCBs to terrestrial mammals, especially carnivora species might be high. However, few studies have been reported on OH-PCBs in terrestrial mammals and accumulation features of these compounds but not the metabolic machanism of PCBs. The present study elucidates the accumulation pattern of PCBs and OH-PCBs, and specific difference in metabolic capacity by analyzing the blood samples of various terrestrial mammals such as cat, dog, raccoon dog, masked palm civet, fox, raccoon and badger collected from Japan. Furthermore, we attempted to assess the risk by PCBs metabolism in a comparative biological perspective and to estimate the potential adverse effect on animal health. Materials and Methods Blood samples of terrestrial mammals [cat (Felis silvestris catus); dog (Canis lupus); raccoon (Procyon lotor); fox (Vulpes vulpes japonica); raccoon dog (Nyctereutes procyonoides); masked palm civet (Paguma larvata); badgar (Meles meles)] were collected from various regions of Japan from 2006 to 2009. Animals collected in this study were caused by death including traffic accidents and mammalian pest control. The blood samples were collected directly from the heart. Organohalogen Compounds Vol. 72, 944-947 (2010) 944 Whole blood (10g) were denatured with 6 M HCl and homogenized with 2-propanol and 50% methyl t-butyl ether (MTBE)/hexane. The resultant mixture was extracted using ultrasonic wave. After centrifugation, 1M KOH in 50% ethanol/water was added and shaken for partition. The extract was passed through 6 g activated silica-gel packed in a column after the fat was removed by gel permeation chromatography (GPC) and eluted with 5% DCM/hexane and concentrated. The KOH solution phase was acidified with sulfuric acid and extracted twice with 50% MTBE/hexane. The organic fraction containing OH-PCBs was passed through a column packed with 3g inactivated silica-gel (5% H2O deactivated) and eluted with 50% dichloromethane (DCM)/hexane and derivatized overnight by using trimethylsilyldiazomethane. The derivatized solution was passed through 3 g activated silica-gel packed in a column after the fat was removed by GPC then eluted with 10% DCM/hexane and concentrated. Identification and quantification were made using a gas chromatograph (GC: 6890 series, Agilent) coupled with high resolution (10,000) mass spectrometer (HRMS: JMS-800D, JEOL). GC-HRMS was equipped with a capillary column (DB-5MS for OH-PCBs and DB-1MS for PCBs, J&W Scientific) and operated in electron impact and selected ion monitoring mode (EI-SIM). Results and Discussion PCBs and OH-PCBs were detected in the blood of all the terrestrial mammals analyzed in this study. The highest concentration (on a wet weight basis) of total PCBs was detected in cats (4600 pg/g), followed by raccoons (3500 pg/g), masked palm civets (370 pg/g), raccoon dogs (360 pg/g), foxes (250 pg/g), dogs (180 pg/g) and badgers (160 pg/g). Hexa- through octa-chlorinated PCBs congeners were predominant in the blood of all terrestrial mammals except that in raccoons (Fig. 1). The PCBs homolog pattern in raccoons was relatively having higher proportions of tri- through penta-chlorinated PCBs, showed species-specific accumulation feature. The homolog profiles of OH-PCB congeners were different among the terrestrial mammalian species (Fig. 2). The highest concentration (on a wet weight RaccoonRaccoon basis) of OH-PCBs was detected in the blood CatCat of raccoons (6900 pg/g), followed by foxes FoxFox (2300 pg/g), badgers (600 pg/g), cats (550 MaskedMasked palm palm civet civet pg/g), raccoon dogs (340 pg/g), dogs (260 DogDog pg/g) and masked palm civets (220 pg/g). Tri- RaccoonRaccoon dog dog through penta-chlorinated OH-PCB congeners BadgerBadger 0%0 20%20 40%40 60%60 80%80 100%100 were predominant in raccoon and cat bloods, TotalTotal T3CBsT3CBs TotalTotal T4CBsT4CBs TotalTotal P5CBsP5CBs TotalTotal H6CBsH6CBs and the contributions of these OH-PCBs to Total H7CBs Total O8CBs Total N9CBs Total D10CBs Total H7CBs Total O8CBs Total N9CBs Total D10CBs total OH-PCBs were above 50% (Fig. 2). The Composition (%) Fig. 1 Compositions of PCB homologues [Tri (T )-Deca (D )] in the blood accumulation of hexa- through 3 10 of terrestrial mammals collected from Japan. Organohalogen Compounds Vol. 72, 944-947 (2010) 945 octa-chlorinated OH-PCBs have been observed in RaccoonRaccoon other animals (Fig. 2). These results clearly show that CatCat the species-dependent congener profiles in terrestrial FoxFox mammals. It was reported that lower-chlorinated MaskedMasked palm palm civet civet OH-PCBs (less than penta-chlorinated OH-PCBs) has DogDog Raccoon dog weak binding affinity to TTR and/or easy to eliminate Raccoon dog BadgerBadger by phase II conjugation enzymes in terrestrial 0%0 20%20 40%40 60%60 80%80 100%100 mammals. However, the OH-PCB homolog pattern in TotalTotal OH-T3CBs OH-T3CBs TotalTotal OH-T4CBs OH-T4CBs TotalTotal OH-P5CBs OH-P5CBs 6 TotalTotal OH-H6CBs OH-H CBs TotalTotal OH-H7CBsOH-H CBs TotalTotal OH-O8CBsOH-O CBs raccoons and cats were similar to cetaceans , 6 7 8 Composition (%) suggesting species-specific accumulation pattern of lower-chlorinated OH-PCBs in the terrestrial Fig. 2 Compositions of OH-PCB homologues [Tri (T3)-Octa (O8)] in the blood of terrestrial mammals collected from Japan. mammals. Although PCB homolog pattern in cats was similar to that in dogs, raccoon dogs and masked palm civets, OH-PCB homolog pattern was quite different from these species. This suggests that cats have specific metabolic capacity. The concentration ratios of OH-PCBs to PCBs (OH-PCBs/PCBs) were calculated and the highest value was found in badger, followed by raccoons, raccoon dogs, dogs, foxes, masked palm civets, and cats (Fig. 3). The OH-PCBs/PCBs ratios in the blood of cats (0.12) and masked palm civets (0.59) were similar to that reported for human blood (0.22-0.37)4-5. Meanwhile, the ratios observed in other terrestrial mammals blood (1.0-9.1) were one order of magnitude higher than those in human4-5 and 2 to 4 orders of magnitude higher than marine mammals (0.0009-0.069)4,6,13, but the values were lower than those in polar bear blood (25)2. It is presumed that this could be due to higher metabolic capacity and/or binding affinity of OH-PCBs to TTR may be higher in these terrestrial mammals. Previous study reported pet dogs may have higher metabolic and elimination capacity for PCBs than pet cats7. In addition, it has been reported that raccoon dogs induce drug-metabolizing enzymes such as CYP families depending on the hepatic levels of contaminants and metabolize organohalogen compounds including PCBs8-10. Voorspoels et al. 11 also found high metabolic ability to transform PCBs in red fox, which belong to Canidae family. Especially, cats may preferentially metabolize lower chlorinated OH-PCBs and retain the metabolites in the blood4. But, they may not metabolize phenolic compounds due to lack of glucuronate conjugation ability12. This suggests that cats are at high risk for some phenolic compounds including halogenated metabolites. The present study reveals PCBs metabolic capacity in terrestrial mammals varies widely among species. Particularly, cats showed specific OH-PCBs accumulation feature which is different from other mammals, suggesting that they are sensitive to hydroxylated PCB metabolites. Further studies are needed to elucidate the metabolic mechanism and risk assessment of hydroxylated metabolites. Organohalogen Compounds Vol. 72, 944-947 (2010) 946 Marine mammals Acknowledgement Finless porpoise6 Pacific white-sided dolphin6 Killer whale6 This study was supported by Beluga whale6 Stejneger's beaked whale6 Byde's whale6 Grants-in-Aid for Scientific Research (S) Melon-headed whale6 Sperm whale6 (No. 2022103), Grants-in-Aid for Young Blainville's beaked whale6 Minke whale6 Scientists (B) (No. 22710064), Baikal seal13 Northern fur seal4 Exploratory Research (No. 21651024) and Terrestrial mammals Polar bear2 Global COE program from the Ministry of Human4 Human5 Education, Culture, Sports, Science and Pig (control site)14 Pig (dumping site)14 Technology (MEXT), Japan, and from Cat Masked palm civet Raccoon dog Japan Society for the Promotion of Dog Raccoon Science (JSPS). Badger Fox 0.001 0.01 0.1 1 10 100 OH-PCBs/PCBs concentration ratio Fig. 3 Concentration ratios of OH-PCBs to PCBs in the blood of terrestrial mammals Reference and marine mammals. 1. Kunisue T., Sakiyama T., Yamada KT., Takahashi S., Tanabe S. (2007); Mar Pollut Bull. 54: 963-973 2. Gebbink WA., Sonne C., Dietz R., Kirkegaard M., Giget FF., Born EW., Muir DCG., Letcher RJ.
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