Levels, Temporal Trends, and Tissue Distribution of Perfluorinated Surfactants in Freshwater Fish from Asian Countries

  • Michio Murakami
  • Nozomi Adachi
  • Mahua Saha
  • Chiaki Morita
  • Hideshige Takada
Article

Abstract

Perfluorinated surfactants (PFSs) in Asian freshwater fish species were analyzed to investigate tissue distribution, temporal trends, extent of pollution, and level of PFS exposure through food intake. Freshwater fish species, namely carp, snakehead, and catfish, were collected in Japan, Vietnam, India, Malaysia, and Thailand, and 10 PFSs, including perfluorooctanesulfonate (PFOS) and perfluorooctanoate, were analyzed by liquid chromatography–tandem mass spectrometry. PFSs in carp in Tokyo were more concentrated in kidneys (Σ10 PFSs = 257 ± 95 ng/g wet weight [ww]) and livers (119 ± 36 ng/g ww) than in ovaries (43 ± 2 ng/g ww) and muscles (24 ± 17 ng/g ww). Concentrations of PFOS and its precursor, perfluorooctane sulfonamide, in livers of carp and in waters in Tokyo showed a dramatic decrease during the last decade, probably because of 3 M’s phasing-out of the manufacture of perfluorooctanesulfonyl-fluoride-based products in 2000. In contrast, continuing contamination by long-chain perfluorocarboxylates (PFCAs) with ≥ 9 fluorinated carbons was seen in multiple media, suggesting that these compounds continue to be emitted. PFS concentrations in freshwater fish species in tropical Asian countries were generally lower than those in developed countries, such as Japan, e.g., for PFOS in muscle, Vietnam < 0.05–0.3 ng/g ww; India < 0.05–0.2 ng/g ww; Malaysia < 0.05–0.2 ng/g ww; Thailand < 0.05 ng/g ww; and Japan (Tokyo) = 5.1–22 ng/g ww. Daily intake of short-chain PFCAs with ≤ 8 fluorinated carbons from freshwater fish species in Japan was approximately one order of magnitude lower than that from drinking water, whereas daily intake of PFOS and long-chain PFCAs with ≥ 9 fluorinated carbons from freshwater fish species was comparable with or greater than that from drinking water. Because the risk posed by exposure to these compounds through intake of fish species is a matter of concern, we recommend the continued monitoring of PFS levels in Asian developing countries.

Notes

Acknowledgments

We thank laboratory members for their help in collecting the environmental samples. This work was supported in part by KAKENHI (Grant No. 19404001).

References

  1. Ahrens L, Yamashita N, Yeung LWY, Taniyasu S, Horii Y, Lam PKS et al (2009) Partitioning behavior of per- and polyfluoroalkyl compounds between pore water and sediment in two sediment cores from Tokyo Bay, Japan. Environ Sci Technol 43:6969–6975CrossRefGoogle Scholar
  2. Apelberg BJ, Witter FR, Herbstman JB, Calafat AM, Halden RU, Needham LL et al (2007) Cord serum concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) in relation to weight and size at birth. Environ Health Perspect 115:1670–1676CrossRefGoogle Scholar
  3. Austin ME, Kasturi BS, Barber M, Kannan K, MohanKumar PS, MohanKumar SMJ (2003) Neuroendocrine effects of perfluorooctane sulfonate in rats. Environ Health Perspect 111:1485–1489CrossRefGoogle Scholar
  4. Biegel LB, Hurtt ME, Frame SR, O’Connor JC, Cook JC (2001) Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats. Toxicol Sci 60:44–55CrossRefGoogle Scholar
  5. Bossi R, Strand J, Sortkjaer O, Larsen MM (2008) Perfluoroalkyl compounds in Danish wastewater treatment plants and aquatic environments. Environ Int 34:443–450CrossRefGoogle Scholar
  6. Butenhoff J, Costa G, Elcombe C, Farrar D, Hansen K, Iwai H, Jung R, Kennedy G, Lieder P, Olsen G, Thomford P (2002) Toxicity of ammonium perfluorooctanoate in male cynomolgus monkeys after oral dosing for 6 months. Toxicol Sci 69:244–257CrossRefGoogle Scholar
  7. Butt CM, Mabury SA, Muir DCG, Braune BM (2007) Prevalence of long-chained perfluorinated carboxylates in seabirds from the Canadian arctic between 1975 and 2004. Environ Sci Technol 41:3521–3528CrossRefGoogle Scholar
  8. Conder JM, Hoke RA, Wolf WD, Russell MH, Buck RC (2008) Are PFCAs bioaccumulative? A critical review and comparison with regulatory criteria and persistent lipophilic compounds. Environ Sci Technol 42:995–1003CrossRefGoogle Scholar
  9. Furdui VI, Stock NL, Ellis DA, Butt CM, Whittle DM, Crozier PW et al (2007) Spatial distribution of perfluoroalkyl contaminants in lake trout from the Great Lakes. Environ Sci Technol 41:1554–1559CrossRefGoogle Scholar
  10. Giesy JP, Kannan K (2001) Global distribution of perfluorooctane sulfonate in wildlife. Environ Sci Technol 35:1339–1342CrossRefGoogle Scholar
  11. Harada K, Nakanishi S, Saito N, Tsutsui T, Koizumi A (2005) Airborne perfluorooctanoate may be a substantial source contamination in Kyoto area, Japan. Bull Environ Contam Toxicol 74:64–69CrossRefGoogle Scholar
  12. Hart K, Kannan K, Isobe T, Takahashi S, Yamada TK, Miyazaki N et al (2008) Time trends and transplacental transfer of perfluorinated compounds in melon-headed whales stranded along the Japanese coast in 1982, 2001/2002, and 2006. Environ Sci Technol 42:7132–7137CrossRefGoogle Scholar
  13. Hawley JK (1985) Assessment of health risk from exposure to contaminated soil. Risk Anal 5:289–302CrossRefGoogle Scholar
  14. Houde M, Bujas TAD, Small J, Wells RS, Fair PA, Bossart GD et al (2006a) Biomagnification of perfluoroalkyl compounds in the bottlenose dolphin (Tursiops truncatus) food web. Environ Sci Technol 40:4138–4144CrossRefGoogle Scholar
  15. Houde M, Martin JW, Letcher RJ, Solomon KR, Muir DCG (2006b) Biological monitoring of polyfluoroalkyl substances: a review. Environ Sci Technol 40:3463–3473CrossRefGoogle Scholar
  16. Kleszczynski K, Gardzielewski P, Mulkiewicz E, Stepnowski P, Skladanowski AC (2007) Analysis of structure-cytotoxicity in vitro relationship (SAR) for perfluorinated carboxylic acids. Toxicol In Vitro 21:1206–1211CrossRefGoogle Scholar
  17. Kumar KS, 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 58:621–629CrossRefGoogle Scholar
  18. Kuroda K (2010) Evaluation of potential uses of groundwater for the improvement of urban environments. Ph. D. Thesis. The University of Tokyo, Tokyo (in Japanese)Google Scholar
  19. Larsen BS, Kaiser MA, Botelho M, Wooler GR, Buxton WB (2005) Comparison of pressurized solvent and reflux extraction methods for the determination of perfluorooctanoic acid in polytetrafluoroethylene polymers using LC-MS-MS. Analyst 130:59–62CrossRefGoogle Scholar
  20. Llorca M, Farré M, Picó Y, Barveló D (2009) Development and validation of a pressurized liquid extraction liquid chromatography-tandem mass spectrometry method for perfluorinated compounds determination in fish. J Chromatogr A 1216:7195–7204CrossRefGoogle Scholar
  21. Martin JW, Mabury SA, Solomon KR, Muir DCG (2003) Bioconcentration and tissue distribution of perfluorinated acids in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 22:196–204Google Scholar
  22. Martin JW, Whittle DM, Muir DCG, Mabury SA (2004) Perfluoroalkyl contaminants in a food web from Lake Ontario. Environ Sci Technol 38:5379–5385CrossRefGoogle Scholar
  23. Minnesota Department of Health (2008) Health risk limits for perfluorochemicals: report to the Minnesota LegislatureGoogle Scholar
  24. Morikawa A, Kamei N, Harada K, Inoue K, Yoshinaga T, Saito N et al (2006) The bioconcentration factor of perfluorooctane sulfonate is significantly larger than that of perfluorooctanoate in wild turtles (Trachemys scripta elegans and Chinemys reevesii): an Ai river ecological study in Japan. Ecotoxicol Environ Safe 65:14–21CrossRefGoogle Scholar
  25. Moriwaki H, Takata Y, Arakawa R (2003) Concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) in vacuum cleaner dust collected in Japanese homes. J Environ Monit 5:753–757CrossRefGoogle Scholar
  26. Murakami M, Takada H (2008) Perfluorinated surfactants (PFSs) in size-fractionated street dust in Tokyo. Chemosphere 73:1172–1177CrossRefGoogle Scholar
  27. 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 42:6566–6572CrossRefGoogle Scholar
  28. Murakami M, Shinohara H, Takada H (2009) Evaluation of wastewater and street runoff as sources of perfluorinated surfactants (PFSs). Chemosphere 74:487–493CrossRefGoogle Scholar
  29. Nakayama S, Harada K, Inoue K, Sasaki K, Seery B, Saito N et al (2005) Distributions of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) in Japan and their toxicities. Environ Sci 12:293–313Google Scholar
  30. Ohmori K, Kudo N, Katayama K, Kawashima Y (2003) Comparison of the toxicokinetics between perfluorocarboxylic acids with different carbon chain length. Toxicology 184:135–140CrossRefGoogle Scholar
  31. Paul AG, Jones KC, Sweetman AJ (2009) A first global production, emission, and environmental inventory for perfluorooctane sulfonate. Environ Sci Technol 43:386–392CrossRefGoogle Scholar
  32. Peng H, Wei QW, Wan Y, Giesy JP, Li LX, Hu JY (2010) Tissue distribution and maternal transfer of poly- and perfluorinated compounds in Chinese sturgeon (Acipenser sinensis): implications for reproductive risk. Environ Sci Technol 44:1868–1874CrossRefGoogle Scholar
  33. Prevedouros K, Cousins IT, Buck RC, Korzeniowski SH (2006) Sources, fate and transport of perfluorocarboxylates. Environ Sci Technol 40:32–44CrossRefGoogle Scholar
  34. Sasaki K, Harada K, Saito N, Tsutsui T, Nakanishi S, Tsuzuki H, Koizumi A (2003) Impact of airborne perfluorooctane sulfonate on the human body burden and the ecological system. Bull Environ Contam Toxicol 71:408–413CrossRefGoogle Scholar
  35. 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 68:249–264CrossRefGoogle Scholar
  36. Senthilkumar K, Ohi E, Sajwan K, Takasuga T, Kannan K (2007) Perfluorinated compounds in river water, river sediment, market fish, and wildlife samples from Japan. Bull Environ Contam Toxicol 79:427–431CrossRefGoogle Scholar
  37. Sinclair E, Mayack DT, Roblee K, Yamashita N, Kannan K (2006) Occurrence of perfluoroalkyl surfactants in water, fish, and birds from New York State. Arch Environ Contam Toxicol 50:398–410CrossRefGoogle Scholar
  38. So MK, Taniyasu S, Lam PKS, Zheng GJ, Giesy JP, Yamashita N (2006) Alkaline digestion and solid phase extraction method for perfluorinated compounds in mussels and oysters from south China and Japan. Arch Environ Contam Toxicol 50:240–248CrossRefGoogle Scholar
  39. Stockholm Convention on Persistent Organic Pollutants (POPs) (2009) http://www.chm.pops.int/Programmes/NewPOPs/The9newPOPs/tabid/672/language/en-US/Default.aspx. Accessed 2009
  40. 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 37:2634–2639CrossRefGoogle Scholar
  41. United Nations Environment Programme (2008) Consideration of new information on perfluorooctane sulfonate (PFOS) http://www.unon.org/confss/doc/unep/pops/POPRC_04/POPRC_4_INF_17/K0841478%20POPRC-4-INF17.pdf. Accessed 2008
  42. United States Environmental Protection Agency (2009) Long-Chain Perfluorinated Chemicals (PFCs) Action Plan. http://www.epa.gov/oppt/existingchemicals/pubs/actionplans/pfcs.html. Accessed 2009
  43. Van de Vijver KI, Hoff P, Das K, Brasseur S, Van Dongen W, Esmans E et al (2005) Tissue distribution of perfluorinated chemicals in harbor seals (Phoca vitulina) from the Dutch Wadden Sea. Environ Sci Technol 39:6978–6984CrossRefGoogle Scholar
  44. Vanden Heuvel JP, Kuslikis BI, Van Rafelghem MJ, Peterson RE (1991) Disposition of perfluorodecanoic acid in male and female rats. Toxicol Appl Pharmacol 107:450–459CrossRefGoogle Scholar
  45. Yeung LWY, Yamashita N, Taniyasu S, Lam PKS, Sinha RK, Borole DV et al (2009) A survey of perfluorinated compounds in surface water and biota including dolphins from the Ganges River and in other waterbodies in India. Chemosphere 76:55–62CrossRefGoogle Scholar
  46. Yoo H, Yamashita N, Taniyasu S, Lee KT, Jones PD, Newsted JL et al (2009) Perfluoroalkyl acids in marine organisms from Lake Shihwa, Korea. Arch Environ Contam Toxicol 57:552–560CrossRefGoogle Scholar
  47. Zushi Y, Feng Y, Masunaga S, Motegi M, Nojiri K, Hosono S, et al (2010a) Survey of perfluorinaetd compound (PFC) pollution in the basin of Tokyo Bay–application of the simultaneous analysis method for 38 types of PFCs-[in Japanese]. Paper presented at the Forty-Fourth Annual Conference of the Japanese Society on Water Environment (Fukuoka, Japan; 15–17 Mar 2010)Google Scholar
  48. Zushi Y, Tamada M, Kanai Y, Masunaga S (2010b) Time trends of perfluorinated compounds from the sediment core of Tokyo Bay, Japan (1950 s–2004). Environ Pollut 158:756–763CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Michio Murakami
    • 1
  • Nozomi Adachi
    • 2
  • Mahua Saha
    • 2
  • Chiaki Morita
    • 2
  • Hideshige Takada
    • 2
  1. 1.“Wisdom of Water” (Suntory), Corporate Sponsored Research Program, Organization for Interdisciplinary Research ProjectsThe University of TokyoTokyoJapan
  2. 2.Laboratory of Organic Geochemistry, Institute of Symbiotic Science and TechnologyTokyo University of Agriculture and TechnologyTokyoJapan

Personalised recommendations