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Evaluation of spatial distribution and accumulation of novel brominated flame retardants, HBCD and PBDEs in an Italian subalpine lake using zebra mussel (Dreissena polymorpha)


Because of the reduction in the use of polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecane (HBCD), novel brominated flame retardants (NBFRs), including 1,2-bis(2,4,6-tribromophenoxy) ethane (BTBPE), decabromodiphenyl ethane (DBDPE), hexabromobenzene (HBB), and pentabromoethylbenzene (PBEB), started to be marketed as alternatives to the banned formulations. In this study, the spatial distribution and accumulation of NBFRs, PBDEs, and HBCD in the biota have been investigated in the littoral compartment of a large and deep subalpine lake (Lake Maggiore, Northern Italy), using zebra mussel Dreissena polymorpha and roach (Rutilus rutilus) as bioindicators. To our knowledge, this is the first study reporting the contamination of NBFRs in the freshwater invertebrate D. polymorpha. Contamination of zebra mussel due to PBEB, HBB, and BTBPE was low, ranging from 0.9 to 2.9 ng/g lipid weight, from 1.1 to 2.9 ng/g l.w., and from 3.5 to 9.5 ng/g l.w., respectively. PBEB and BTBPE in roach were always below the detection limit, while the contamination of HBB ranged from < limits of detection (LOD) to 1.74 ng/g l.w., indicating a weak contamination. DBDPE was < LOD in all the considered biological samples. Finally, HBCD was detected in all organic tissues with mean concentrations up to 74.4 ng/g l.w. PBDE results, supported by principal component analysis elaboration, suggested a possible contamination due to the congeners composing the penta- and deca-BDE technical formulations, which are present in the Lake Maggiore basin. The biomagnification factor values showed that tetra- and penta-BDE biomagnified, while octa-, nona-, and deca-BDE were still bioavailable and detectable in the fish muscles, but they do not biomagnified. Considering the other BFRs, only HBCD showed a moderate biomagnification potential.

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  1. Abdallah MA-E, Harrad S (2011) Tetrabromobisphenol-A, hexabromocyclododecane and its degradation products in UK human milk: relationship to external exposure. Environ Int 37(2):443–448

  2. Arias PA (2001) Brominated flame retardants—an overview. The Second International Workshop on Brominated Flame Retardants (BFR 2001), Stockholm, pp 17–19

  3. Arnot JA, Gobas FAPC (2006) A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ Rev 14(4):257–297

  4. Betts K (2008) New flame retardants detected in indoor and outdoor environments. Environ Sci Technol 42(18):6778

  5. Binelli A, Galassi S, Provini A (2001) Factors affecting the use of Dreissena polymorpha as a bioindicator: the PCB pollution in Lake Como (N. Italy). Water Air Soil Poll 125(1):19–32

  6. Binelli A, Guzzella L, Roscioli C (2008) Levels and congener profiles of polybrominated diphenyl ethers (PBDEs) in zebra mussels (D. polymorpha) from Lake Maggiore (Italy). Environ Pollut 153(3):610–617

  7. BSEF Bromine Science Environmental Forum (2013) http://www.bsef.com/regulation/international-regulations/what-are-the-united-nations-conventions

  8. Burreau S, Zebühr Y, Broman D, Ishaq R (2004) Biomagnification of polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) studied in pike (Esox lucius), perch (Perca fluviatilis) and roach (Rutilus rutilus) from the Baltic Sea. Chemosphere 55(7):1043–1052

  9. Camusso M, Balestrini R, Binelli A (2001) Use of zebra mussel (Dreissena polymorpha) to assess trace metal contamination in the largest Italian subalpine lakes. Chemosphere 44(2):263–270

  10. CIPAIS Commissione Internazionale per la Protezione delle Acque Italo-Svizzere (2012) Indagini su DDT e sostanze pericolose nell’ecosistema del Lago Maggiore. Rapporto annuale 2012 (in Italian)

  11. CIPAIS Commissione Internazionale per la Protezione delle Acque Italo-Svizzere (2013) Indagini su DDT e sostanze pericolose nell’ecosistema del Lago Maggiore. Rapporto annuale 2013 (in Italian)

  12. Covaci A, Voorspoels S, de Boer J (2003) Determination of brominated flame retardants, with emphasis on polybrominated diphenyl ethers (PBDEs) in environmental and human samples—a review. Environ Int 29(6):735–756

  13. Covaci A, Harrad S, Abdallah MA-E, Ali N, Law RJ, Herzke D et al (2011) Novel brominated flame retardants: a review of their analysis, environmental fate and behaviour. Environ Int 37(2):532–556

  14. de Wit CA (2002) An overview of brominated flame retardants in the environment. Chemosphere 46(5):583–624

  15. Directive 2003/11/EC of the European Parliament and of the Council of 6 February 2003 amending for the 24th time Council directive 76/769/EEC relating to restrictions on the marketing and use of certain dangerous substances and preparations (pentabromodiphenyl ether and octabromodiphenyl ether). Official Journal L042. 15/02/2003

  16. ESIS European Chemical Substance Information System European Commission, Joint Research Centre, European Chemicals Bureau (2010) http://esis.jrc.ec.europa.eu/.

  17. European Court of Justice (2008) Cases C-14/06 and C-295/06, Judgement of the Court, 1 April 2008, Directive 2002/95/EC and Commission Decision 2005/717/EC. http://curia.europa.eu/. Accessed July 2010

  18. Gandhi N, Bhavsar SP, Gewurtz SB et al (2011) Can biotransformation of BDE-209 in lake trout cause bioaccumulation of more toxic, lower-brominated PBDEs (BDE-47,-99) over the long term? Environ Int 37(1):170–177

  19. Gauthier LT, Hebert CE, Weseloh DVC, Letcher RJ (2007) Current-use flame retardants in the eggs of herring gulls (Larus argentatus) from the Laurentian Great Lakes. Environ Sci Technol 41(13):4561–4567

  20. Guerra P, Eljarrat E, Barcelò D (2010) Analysis and occurrence of emerging brominated flame retardants in the Llobregat River basin. Journal Hydrology 383(1–2):39–43

  21. Guzzella L, Roscioli C, Binelli A (2008) Contamination by plybrominated diphenyl ethers of sediments from the Lake Maggiore Basin (Italy and Switzerland). Chemosphere 73(10):1684–1691

  22. Hermanson MH, Isaksson E, Forsstrom S et al (2010) Deposition history of brominated flame retardant compounds in an ice core from Holtedahlfonna, Svalbard, Norway. Environ Sci Technol 44(19-SI):7405–7410

  23. Hoh E, Zhu L, Hites RA (2005) Novel flame retardants, 1,2-bis(2, 4, 6-ribromophenoxy)ethane and 2,3,4,5,6-pentabromoethylbenzene, in United States' environmental samples. Environ Sci Technol 39(8):2472–2477

  24. Hu G, Dai J, Xu Z et al (2010) Bioaccumulation behavior of polybrominated diphenyl ethers (PBDEs) in the freshwater food chain of Baiyangdian Lake, North China. Environ Int 36(4):309–315

  25. Isobe T, Ogawa SP, Ramu K, Sudaryanto A, Tanabe S (2012) Geographical distribution of non-PBDE-brominated flame retardants in mussels from Asian coastal waters. Environ Sci Pollut R 19(8):3107–3117

  26. Kierkegaard A, Bjorklund J, Friden U (2004) Identification of the flame retardant decabromodiphenyl ethane in the environment. Environ Sci Technol 38(12):3247–3253

  27. Klosterhaus SL, Stapleton HM, La Guardia MJ, Greig DJ (2012) Brominated and chlorinated flame retardants in San Francisco Bay sediments and wildlife. Environ Int 47:56–65

  28. Kohler M, Zennegg M, Bogdal C et al (2008) Temporal trends, congener patterns, and sources of octa-, nona-, and decabromodiphenyl ethers (PBDE) and hexabromocyclododecanes (HBCD) in Swiss lake sediments. Environ Sci Technol 42(17):6378–6384

  29. La Guardia MJ, Hale RC, Harvey E (2007) Evidence of debromination of decabromodiphenyl ether (BDE-209) in biota from a wastewater receiving stream. Environ Sci Technol 41(19):6663–6670

  30. La Guardia MJ, Hale RC, Harvey E, Matteson Mainor T, Ciparis S (2012) In situ accumulation of HBCD, PBDEs, and several alternative flame-retardants in the bivalve (Corbicula fluminea) and gastropod (Elimia proxima). Environ Sci Technol 46(11):5798–5805

  31. Law K, Halldorson T, Danell R, Stern G, Gewurtz S, Alaee M (2006) Bioaccumulation and trophic transfer of some brominated flame retardants in a lake Winnipeg (Canada) food web. Environ Toxicol Chem 25(8):2177–2186

  32. OSPAR Commission. OSPAR List of Chemicals for Priority Action. http://www.ospar.org/content/content.asp?menu=00120000000074_000000_0000002001. Update 2007

  33. Ross PS, Couillard CM, Ikonomou MG et al (2009) Large and growing environmental reservoirs of deca-BDE present an emerging health risk for fish and marine mammals. Mar Pollut Bull 58(1):7–10

  34. Söderström G, Sellström U, de Wit CA, Tysklind M (2004) Photolytic debromination of decabromodiphenyl ether (BDE 209). Environ Sci Technol 38(1):127–132

  35. Stapleton HM, Brazil B, Holbrook RD, Mitchelmore CL, Benedict R, Konstantinov A, Potter D (2006) In vivo and in vitro debromination of decabromodiphenyl ether (BDE-209) by juvenile rainbow trout and common carp. Environ Sci Technol 40:4653–4658

  36. Tomy GT, Pleskach K, Oswald T et al (2008) Enantioselective bioaccumulation of hexabromocyclododecane and congener-specific accumulation of brominated diphenyl ethers in an eastern Canadian Arctic marine food web. Environ Sci Technol 42(10):3634–3639

  37. Verreault J, Gebbink W, Gauthier LT, Gabrielsen GW, Letcher RJ (2007) Brominated flame retardants in glaucous gulls from the Norwegian arctic: more than just an issue of polybrominated diphenyl ethers. Environ Sci Technol 41(14):4925–4931

  38. Viganò L, Roscioli C, Guzzella L (2011) Decabromodiphenyl ether (BDE-209) enters the food web of the River Po and is metabolically debrominated in resident cyprinid fishes. Sci Total Environ 409(23):4966–4972

  39. Volta P, Jepsen N (2008) The recent invasion of roach (Pisces: Cyprinidae) in a large South-Alpine Lake. Journal of Limnology 67(2):163–170

  40. Volta P, Grimaldi E, Calderoni A, Polli B (2013) Andamento della pesca professionale sul Lago Maggiore nel periodo 1979-2011. Commissione italo-svizzera per la Pesca (CISPP) 20pp (in Italian) (in press)

  41. Voorspoels S, Covaci A, Schepens P (2003) Polybrominated diphenyl ethers in marine species from the Belgian North Sea and the Western Scheldt estuary, levels, profiles and distribution. Environ Sci Technol 37(19):4348–4357

  42. Watanabe I, Sakai S (2003) Environmental release and behaviour of brominated flame retardants. Environ Int 29(6):665–682

  43. Wei H, Aziz-Schwanbeck AC, Zou Y, Corcoran MB, Poghosyan A, Li A, Rockne KJ, Christensen ER, Sturchio NC (2012) Polybromodiphenyl ethers and decabromodiphenyl ethane in aquatic sediments from Southern and Eastern Arkansas, United States. Environ Sci Technol 46(15):8017–8024

  44. Wei H, Zou Y, Li A, Christensen ER, Rockne KJ (2013) Photolytic debromination pathway of polybrominated diphenyl ethers in hexane by sunlight. Environ Pollut 174:194–200

  45. Yu YX, Zhang SH, Huang NB, Li JL, Pang YP, Zhang XY, Yu ZQ, Xu ZG (2012) Polybrominated diphenyl ethers and polychlorinated biphenyls in freshwater fish from Taihu Lake, China: their levels and the factors that influence biomagnification. Environ Toxicol Chem 31(3):542–549

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The authors thank Commissione Internazionale per la Protezione delle Acque Italo-Svizzere (CIPAIS) for having economically partially supported this study.

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Correspondence to Giulia Poma.

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Responsible editor: Roland Kallenborn

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Poma, G., Binelli, A., Volta, P. et al. Evaluation of spatial distribution and accumulation of novel brominated flame retardants, HBCD and PBDEs in an Italian subalpine lake using zebra mussel (Dreissena polymorpha). Environ Sci Pollut Res 21, 9655–9664 (2014). https://doi.org/10.1007/s11356-014-2826-7

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  • Novel brominated flame retardants (NBFRs)
  • Polybrominated diphenyl ethers (PBDEs)
  • Hexabromocylododecane (HBCD)
  • Lake Maggiore
  • Zebra mussel
  • Common roach