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Perfluoroalkyl Substances in the Blood of Wild Rats and Mice from 47 Prefectures in Japan: Use of Samples from Nationwide Specimen Bank

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Abstract

Numerous studies have reported on the global distribution, persistence, fate, and toxicity of perfluoroalkyl and polyfluoroalkyl substances (PFASs). However, studies on PFASs in terrestrial mammals are scarce. Rats can be good sentinels of human exposure to toxicants because of their habitat, which is in close proximity to humans. Furthermore, exposure data measured for rats can be directly applied for risk assessment because many toxicological studies use rodent models. In this study, a nationwide survey of PFASs in the blood of wild rats as well as surface water samples collected from rats’ habitats from 47 prefectures in Japan was conducted. In addition to known PFASs, combustion ion chromatography technique was used for analysis of total fluorine concentrations in the blood of rats. In total, 216 blood samples representing three species of wild rats (house rat, Norway rats, and field mice) were analyzed for 23 PFASs. Perfluorooctanesulfonate (PFOS; concentration range <0.05-148 ng/mL), perfluorooctane sulfonamide (PFOSA; <0.1–157), perfluorododecanoate (<0.05–5.8), perfluoroundecanoate (PFUnDA; <0.05–51), perfluorodecanoate (PFDA; <0.05–9.7), perfluorononanoate (PFNA; <0.05–249), and perfluorooctanoate (PFOA) (<0.05–60) were detected >80 % of the blood samples. Concentrations of several PFASs in rat blood were similar to those reported for humans. PFSAs (mainly PFOS) accounted for 45 % of total PFASs, whereas perfluoroalkyl carboxylates (PFCAs), especially PFUnDA and PFNA, accounted for 20 and 10 % of total PFASs, respectively. In water samples, PFCAs were the predominant compounds with PFOA and PFNA found in >90 % of the samples. There were strong correlations (p < 0.001 to p < 0.05) between human population density and levels of PFOS, PFNA, PFOA, and PFOSA in wild rat blood.

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References

  • Abbott BD, Wolf CJ, Das KP, Schmid JE, Lau CS (2007) The developmental toxicity of perfluorooetanoic acid (PFOA) in the mouse requires expression of peroxisome proliferator activated receptoralpha (PPAR). Birth defects research. Birth Defects Res A Clin Mol Teratol 79:370

    Google Scholar 

  • Ahrens L, Taniyasu S, Yeung LW, Yamashita N, Lam PK, Ebinghaus R (2010) Distribution of polyfluoroalkyl compounds in water, suspended particulate matter and sediment from Tokyo Bay, Japan. Chemosphere 79:266–272

    Article  CAS  Google Scholar 

  • Ceruti R, Ghisleni G, Ferretti E, Cammarata S, Sonzogni O, Scanziani E (2002) Wild rats as monitors of environmental lead contamination in the urban area of Milan, Italy. Environ Pollut 117:255–259

    Article  CAS  Google Scholar 

  • Chang SC, Das K, Ehresman DJ, Ellefson ME, Gorman GS, Hart JA et al (2008) Comparative pharmacokinetics of perfluorobutyrate in rats, mice, monkeys, and humans and relevance to human exposure via drinking water. Toxicol Sci 104:40–53

    Article  CAS  Google Scholar 

  • Conder JM, Hoke RA, De Wolf W, Russell MH, Buck RC (2008) Are PFCAs bioaccumulative? A critical review and comparison with regulatory lipophilic compounds. Environ Sci Technol 42:995–1003

    Article  CAS  Google Scholar 

  • Dai JY, Li M, Jin YH, Saito N, Xu MQ, Wei FW (2006) Perfluorooctanesulfonate and perfluorooctanoate in red panda and giant panda from China. Environ Sci Technol 40:5647–5652

    Article  CAS  Google Scholar 

  • Ellis DA, Martin JW, De Silva AO, Mabury SA, Hurley MD, Andersen MPS et al (2004) Degradation of fluorotelomer alcohols: a likely atmospheric source of perfluorinated carboxylic acids. Environ Sci Technol 38:3316–3321

    Article  CAS  Google Scholar 

  • Emmett EA, Shofer FS, Zhang H, Freeman D, Desai C, Shaw LM (2006) Community exposure to perfluorooctanoate: relationships between serum concentrations and exposure sources. J Occup Environ Med 48:759–770

    Article  CAS  Google Scholar 

  • Ericson I, Nadal M, van Bavel B, Lindstrom G, Domingo JL (2008) Levels of perfluorochemicals in water samples from Catalonia, Spain: is drinking water a significant contribution to human exposure? Environ Sci Pollut Res 15:614–619

    Article  CAS  Google Scholar 

  • Fairley KJ, Purdy R, Kearns S, Anderson SE, Meade BJ (2007) Exposure to the immunosuppressant, perfluorooctanoic acid, enhances the murine IgE and airway hyperreactivity response to ovalbumin. Toxicol Sci 97:375–383

    Article  CAS  Google Scholar 

  • Giesy JP, Kannan K (2001) Global distribution of perfluorooctane sulfonate in wildlife. Environ Sci Technol 35:1339–1342

    Article  CAS  Google Scholar 

  • Guruge KS, Manage PM, Yamanaka N, Miyazaki S, Taniyasu S, Yamashita N (2008) Species-specific concentrations of perfluoroalkyl contaminants in farm and pet animals in Japan. Chemosphere 73:S210–S215

    Article  CAS  Google Scholar 

  • Harada KH, Koizumi A (2009) Environmental and biological monitoring of persistent fluorinated compounds in Japan and their toxicities. Environ Health Prev Med 14:7–19

    Article  CAS  Google Scholar 

  • Harada K, Saito N, Inoue K, Yoshinaga T, Watanabe T, Sasaki S et al (2004) The influence of time, sex and geographic factors on levels of perfluorooctane sulfonate and perfluorooctanoate in human serum over the last 25 years. J Occup Health 46:141–147

    Article  CAS  Google Scholar 

  • Harada K, Koizumi A, Saito N, Inoue K, Yoshinaga T, Date C et al (2007) Historical and geographical aspects of the increasing perfluorooctanoate and perfluorooctane sulfonate contamination in human serum in Japan. Chemosphere 66:293–301

    Article  CAS  Google Scholar 

  • Higgins CP, Field JA, Criddle CS, Luthy RG (2005) Quantitative determination of perfluorochemicals in sediments and domestic sludge. Environ Sci Technol 39:3946–3956

    Article  CAS  Google Scholar 

  • Hori H, Nagaoka Y, Yamamoto A, Sano T, Yamashita N, Taniyasu S et al (2006) Efficient decomposition of environmentally persistent perfluorooctanesulfonate and related fluorochemicals using zerovalent iron in subcritical water. Environ Sci Technol 40:1049–1054

    Article  CAS  Google Scholar 

  • Houde M, Martin JW, Letcher RJ, Solomon KR, Muir DCG (2006) Biological monitoring of polyfluoroalkyl substances: a review. Environ Sci Technol 40:3463–3473

    Article  CAS  Google Scholar 

  • Houde M, Gertje Czub G, Small JM, Backus S, Wang X, Alaee M et al (2008) Fractionation and bioaccumulation of perfluorooctane sulfonate (PFOS) isomers in a Lake Ontario food web. Environ Sci Technol 42:9397–9403

    Article  CAS  Google Scholar 

  • Ishizuka M, Takasuga T, Senthil Kumar K, Tanikawa T, Fujita S (2005) Accumulation of persistent organochlorine pollutants and polybrominated diphenyl ether in wild rats, and toxicogenomic analyses of their effects. Organohalogen Compd 67:2435–2436

    Google Scholar 

  • ISO25101 (2009) Water quality—determination of perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA)—method for unfiltered samples using solid phase extraction and liquid chromatography/mass spectrometry. The International Organization for Standardization, Geneva, p 24

  • Kannan K (2011) Perfluoroalkyl and polyfluoroalkyl substances: current and future perspectives. Environ Chem 8:333–338

    Article  CAS  Google Scholar 

  • Kannan K, Choi JW, Iseki N, Senthil Kumar K, Kim DH, Masunaga S et al (2002) Concentrations of perfluorinated acids in livers of birds from Japan and Korea. Chemosphere 49:225–231

    Article  CAS  Google Scholar 

  • Kannan K, Corsolini S, Falandysz J, Fillmann G, Senthil Kumar K, Loganathan BG et al (2004) Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ Sci Technol 38:4489–4495

    Article  CAS  Google Scholar 

  • Kannan K, Tao L, Sinclair E, Pastva SD, Jude DJ, Giesy JP (2005) Perfluorinated compounds in aquatic organisms at various trophic levels in a Great Lakes food chain. Arch Environ Contam Toxicol 48:559–566

    Article  CAS  Google Scholar 

  • Keil DE, Mehlmann T, Butterworth L, Peden-Adams MM (2008) Gestational exposure to perfluorooctane sulfonate suppresses immune function in B6C3F1 mice. Toxicol Sci 103:77–85

    Article  CAS  Google Scholar 

  • Kudo N, Suzuki-Nakajima E, Mitsumoto A, Kawashima Y (2006) Responses of the liver to perfluorinated fatty acids with different carbon chain length in male and female mice: in relation to induction of hepatomegaly peroxisomal beta-oxidation and microsomal 1-acylglycerophosphocholine acyltransferase. Biol Pharm Bull 29:1952–1957

    Article  CAS  Google Scholar 

  • Lau C, Anitole K, Hodes C, Lai D, Pfahles-Hutchens A, Seed J (2007) Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol Sci 99:366–394

    Article  CAS  Google Scholar 

  • Li XM, Yeung LWY, Taniyasu S, Li M, Zhang HX, Liu D et al (2008) Perfluorooctanesulfonate and related fluorochemicals in the Amur tiger (Panthera tigris altaica) from China. Environ Sci Technol 42:7078–7083

    Article  CAS  Google Scholar 

  • Liu C, Gin KY, Chang VW, Goh BP, Reinhard M (2011) Novel perspectives on the bioaccumulation of PFCs—the concentration dependency. Environ Sci Technol 45:9758–9764

    Article  CAS  Google Scholar 

  • Liu S, Li R, Ni X, Cai Z, Zhang R, Sun X et al (2012) Perfluorocarbon-facilitated CNS oxygen toxicity in rats: Reversal by edaravone. Brain Res 1471:56–65

    Article  CAS  Google Scholar 

  • Loos R, Wollgast J, Huber T, Hanke G (2007) Polar herbicides, pharmaceutical products, perfluorooctanesulfonate (PFOS), perfluorooctanoate (PFOA), and nonylphenol and its carboxylates and ethoxylates in surface and tap waters around Lake Maggiore in Northern Italy. Anal Bioanal Chem 387:1469–1478

    Article  CAS  Google Scholar 

  • Mak YL, Taniyasu S, Yeung LWY, Lu GH, Jin L, Yang YL et al (2009) Perfluorinated compounds in tap water from China and several other countries. Environ Sci Technol 43:4824–4829

    Article  CAS  Google Scholar 

  • Miyake Y, Yamashita N, So MK, Rostkowski P, Taniyasu S, Lam PKS et al (2007) Trace analysis of TF in human blood using combustion ion chromatography for fluorine: a mass balance approach for the determination of known and unknown organofluorine compounds. J Chromatogr A 1154:214–221

    Article  CAS  Google Scholar 

  • Moody CA, Martin JW, Kwan WC, Muir DC, Mabury SA (2002) Monitoring perfluorinated surfactants in biota and surface water samples following an accidental release of fire-fighting foam into Etobicoke Creek. Environ Sci Technol 36:545–551

    Article  CAS  Google Scholar 

  • Murakami M, Takada H (2008) Perfluorinated surfactants (PFSs) in size-fractionated street dust in Tokyo. Chemosphere 73:1172–1177

    Article  CAS  Google Scholar 

  • Murakami M, Imamura E, Shinohara H, Kiri K, Muramatsu Y, Harada A et al (2008) Occurrence and sources of perfluorinated surfactants in rivers in Japan. Environ Sci Technol 42:6566–6572

    Article  CAS  Google Scholar 

  • Naile JE, Khim JS, Wang TY, Chen CL, Luo W, Kwon BO et al (2010) Perfluorinated compounds in water, sediment, soil and biota from estuarine and coastal areas of Korea. Environ Pollut 158:1237–1244

    Article  CAS  Google Scholar 

  • Nakata H, Kannan K, Nasu T, Cho HS, Sinclair E, Takemura A (2006) Perfluorinated contaminants in sediments and aquatic organisms collected from shallow water and tidal flat areas of the Ariake Sea, Japan: environmental fate of perfluorooctane sulfonate in aquatic ecosystems. Environ Sci Technol 40:4916–4921

    Article  CAS  Google Scholar 

  • Oakes KD, Sibley PK, Martin JW, MacLean DD, Solomon KR, Mabury SA et al (2005) Short-term exposures of fish to perfluorooctane sulfonate: acute effects on fatty acyl-CoA oxidase activity, oxidative stress, and circulating sex steroids. Environ Toxicol Chem 24:1172–1181

    Article  CAS  Google Scholar 

  • Paustenbach DJ, Panko JM, Scott PK, Unice KM (2007) A methodology for estimating human exposure to perfluorooctanoic acid (PFOA): a retrospective exposure assessment of a community (1951–2003). J Toxicol Environ Health A 70:28–57

    Article  CAS  Google Scholar 

  • Quinones O, Snyder SA (2009) Occurrence of perfluoroalkyl carboxylates and sulfonates in drinking water utilities and related waters from the United States. Environ Sci Technol 43:9089–9095

    Article  CAS  Google Scholar 

  • Raj B, Tanaka S, Fujii S, Hong LNP, Nozoe M, Kunacheva C et al (2011) Perfluorinated compounds (PFCs) in Yodo River system, Japan. Water Sci Technol 63:115–123

    Article  Google Scholar 

  • Scott JP (1966) Agonistic behavior of mice and rats: a review. Am Zool 6:683–701

    CAS  Google Scholar 

  • Seacat AM, Thomford PJ, Hansen KJ, Olsen GW, Case MT, Butenhoff JL (2002) Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys. Toxicol Sci 68:249–264

    Article  CAS  Google Scholar 

  • Senthil Kumar K (2005) Fluorinated organic chemicals: a review. Res J Chem Environ 9:50–79

    Google Scholar 

  • Senthil Kumar K, Takasuga T, Ishizuka M, Tanikawa T, Fujita S (2005a) Contamination profiles of UNEP POPs and PBDEs in brown rat collected from urban and rural regions of Japan. Organohalogen Compd 67:615–618

    Google Scholar 

  • Senthil Kumar K, Watanabe K, Takemori H, Iseki N, Masunaga S, Takasuga T (2005b) Analysis of UNEP priority POPs using HRGC-HRMS and their contamination profiles in livers and eggs of great cormorants (Phalacrocorax carbo) from Japan. Arch Environ Contam Toxicol 48:538–551

    Article  Google Scholar 

  • Senthil Kumar K, Ohi E, Sajwan KS, Takasuga T, Kannan K (2007) Perfluorinated compounds in water, sediment and biological samples from Kyoto, Japan. Bull Environ Contam Toxicol 79:427–431

    Article  CAS  Google Scholar 

  • Senthil Kumar K, Zushi Y, Masunaga S, Gilligan M, Pride C, Sajwan KS (2009) Perfluorinated organic contaminants in sediment and aquatic wildlife, including sharks, from Georgia, USA. Mar Pollut Bull 58:621–629

    Article  CAS  Google Scholar 

  • Sinclair E, Kannan K (2006) Mass loading and fate of perfluoroalkyl surfactants in wastewater treatment plants. Environ Sci Technol 40:1408–1414

    Article  CAS  Google Scholar 

  • Skutlarek D, Exner M, Farber H (2006) Perfluorinated surfactants in surface and drinking water. Environ Sci Pollut Res 13:299–307

    Article  CAS  Google Scholar 

  • So MK, Miyake Y, Yeung WY, Ho YM, Taniyasu S, Rostkowski P et al (2007) Perfluorinated compounds in the Pearl River and Yangtze River of China. Chemosphere 68:2085–2095

    Article  CAS  Google Scholar 

  • Takasuga T, Ishizuka M, Senthil Kumar K, Tanikawa R, Fujita S (2004) Accumulation of chlorinated and brominated persistent toxic substances (PTS) and their relationship to testosterone suppression in Norway rats from Japan. Organohalogen Compd 66:3057–3064

    Google Scholar 

  • Tang CYY, Fu QS, Robertson AP, Criddle CS, Leckie JO (2006) Use of reverse osmosis membranes to remove perfluorooctane sulfonate (PFOS) from semiconductor wastewater. Environ Sci Technol 40:7343–7349

    Article  CAS  Google Scholar 

  • Taniyasu S, Kannan K, Horii Y, Hanari N, Yamashita N (2003) A survey of perfluorooctane sulfonate and related perfluorinated organic compounds in water, fish, birds, and humans from Japan. Environ Sci Technol 37:2634–2639

    Article  CAS  Google Scholar 

  • Taniyasu S, Kannan K, So MK, Gulkowska A, Sinclair E, Okazawa T et al (2005) Analysis of fluorotelomer alcohols, fluorotelorner acids, and short- and long-chain perfluorinated acids in water and biota. J Chromatogr A 1093:89–97

    Article  CAS  Google Scholar 

  • Taniyasu S, Kannan K, Yeung LWY, Kwok KY, Lam PKS, Yamashita N (2008) Analysis of trifluoroacetic acid and other short-chain perfluorinated acids (C2–C4) in precipitation by liquid chromatography-tandem mass spectrometry: comparison to patterns of long-chain perfluorinated acids (C5–C18). Anal Chim Acta 619:221–230

    Article  CAS  Google Scholar 

  • UNEP (2008) Report of the persistent organic pollutants review committee on the work its fourth meeting. Addendum to the risk management evaluation for perfluorooctane sulfonate. UNEP/POPS/POPRCS.4/15/Add.6Width1.2008

  • Wang Y, Yeung LWY, Yamashita N, Taniyasu S, So MK, Murphy MB et al (2008) Perfluorooctane sulfonate (PFOS) and related fluorochemicals in chicken egg in China. Chin Sci Bull 53:501–507

    Article  CAS  Google Scholar 

  • Wang T, Wang Y, Liao C, Cai Y, Jiang G (2009) Perspectives on the inclusion of perfluorooctane sulfonate into the Stockholm Convention on Persistent Organic Pollutants. Environ Sci Technol 43:5171–5175

    Article  CAS  Google Scholar 

  • Wang T, Lu Y, Chen C, Naile JE, Khim JS, Giesy JP (2012) Perfluorinated compounds in a coastal industrial area of Tianjin, China. Environ Geochem Health 34:301–311

    Article  CAS  Google Scholar 

  • Yamashita N, Kannan K, Taniyasu S, Horii Y, Petrick G, Gamo T (2005) A global survey of perfluorinated acids in oceans. Mar Pollut Bull 51:658–668

    Article  CAS  Google Scholar 

  • Yamashita N, Yeung LWY, Taniyasu S, Kwok KY, Petrick G, Gamo T et al (2012) Global distribution of PFOS and related chemicals. In: Loganathan BG, Lam PKS (eds) Global contamination trends of persistent organic chemicals. CRC Press, Boca Raton, pp 593–628

    Google Scholar 

  • Yeung LWY, Miyake Y, Wang Y, Taniyasu S, Yamashita N, Lam PKS (2009a) Total fluorine, extractable organic fluorine, perfluorooctane sulfonate and other related fluorochemicals in liver of Indo-Pacific humpback dolphins (Sousa chinensis) and finless porpoises (Neophocaena phocaenoides) from South China. Environ Pollut 157:17–23

    Article  CAS  Google Scholar 

  • Yeung LWY, Taniyasu S, Kannan K, Xu DZY, Guruge KS, Lam PKS et al (2009b) An analytical method for the determination of perfluorinated compounds in whole blood using acetonitrile and solid phase extraction methods. J Chromatogr A 1216:4950–4956

    Article  CAS  Google Scholar 

  • Yeung LWY, Miyake Y, Li P, Taniyasu S, Kannan K, Guruge KS et al (2009c) Comparison of total fluorine, extractable organic fluorine and perfluorinated compounds in the blood of wild and pefluorooctanoate (PFOA)-exposed rats: evidence for the presence of other organofluorine compounds. Anal Chim Acta 635:108–114

    Article  CAS  Google Scholar 

  • Zhang C, Li Z, Gu M, Deng C, Liu M, Li L (2010) Spatial and vertical distribution and pollution assessment of soil fluorine in a lead-zinc mining area in the Karst region of Guangxi, China. Plant Soil Environ 56:282–287

    CAS  Google Scholar 

  • Zushi Y, Masunaga S (2009) Identifying the nonpoint source of perfluorinated compounds using a geographic information system based approach. Environ Toxicol Chem 28:691–700

    Article  CAS  Google Scholar 

  • Zushi Y, Tamada M, Kanai Y, Masunaga S (2010) Time trends of perfluorinated compounds from the sediment core of Tokyo Bay, Japan (1950s–2004). Environ Pollut 158:756–763

    Article  CAS  Google Scholar 

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Acknowledgments

We thank to Paul Lam and staff in City University of Hong Kong for their support.

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Authors and Affiliations

  1. National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, 305-8569, Japan

    Sachi Taniyasu, Eriko Yamazaki & Nobuyoshi Yamashita

  2. Department of Natural Sciences, Savannah State University, Savannah, GA, 31404, USA

    Kurunthachalam Senthilkumar

  3. Department of Chemistry, University of Toronto, Toronto, ON, M5S 3H6, Canada

    Leo W. Y. Yeung

  4. Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, State University of New York, Albany, NY, 12201-0509, USA

    Kurunthachalam Kannan

  5. Safety Research Team, National Institute of Animal Health, Tsukuba, Ibaraki, 305-0856, Japan

    Keerthi S. Guruge

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  1. Sachi Taniyasu
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  2. Kurunthachalam Senthilkumar
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  3. Eriko Yamazaki
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  7. Nobuyoshi Yamashita
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Correspondence to Kurunthachalam Senthilkumar or Nobuyoshi Yamashita.

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Taniyasu, S., Senthilkumar, K., Yamazaki, E. et al. Perfluoroalkyl Substances in the Blood of Wild Rats and Mice from 47 Prefectures in Japan: Use of Samples from Nationwide Specimen Bank. Arch Environ Contam Toxicol 65, 149–170 (2013). https://doi.org/10.1007/s00244-013-9878-4

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