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Characterizing PBDEs in fish, poultry, and pig feeds manufactured in China

  • Jing-Xin Wang
  • Lian-Jun Bao
  • Lei Shi
  • Liang-Ying LiuEmail author
  • Eddy Y. Zeng
Research Article
  • 73 Downloads

Abstract

A total of 53 feeds from 23 brands for four types of animals, i.e., fish, chicken, duck, and pig, as well as six types of raw materials, were bought from Guangxi, Hubei, Anhui, and Guangdong provinces in China and analyzed for polybrominated diphenyl ethers (PBDEs). The raw materials including super fish meal, ordinary fish meal, poultry ore, soybean, stone powder, and rapeseed were selected because they were added to all the animal feeds manufactured. The occurrence of PBDEs was ubiquitous in the feeds and raw materials, with BDE-209 as the most abundant congener. The average concentration of ∑8PBDE was 1.1 and 0.44 ng g−1 dry weight in feeds (range 0.25–5.7) and raw materials (range 0.27–0.84), respectively. No statistically significant differences in ∑8PBDE concentrations were observed among the four groups of animal feeds. Feeds from Yangzhiyuan Brand (n = 11) contained statistically (p < 0.01) lower ∑8PBDE concentrations than all other brands except for Baoshun Brand. Chicken was selected as a representative animal to assess health risk for human exposure to PBDEs via the consumption of chicken raised by the feeds under investigation. Hazard quotients based on per-capita consumption of chicken were all below 1, indicating low potential risk to humans consuming chicken raised with the feeds.

Graphical abstract

Keywords

Polybrominated diphenyl ethers Animal feed Raw material Dietary intake Risk assessment 

Notes

Acknowledgements

We thank all the participants from various provinces for help with sampling and sample shipment.

Funding

The present study was financially supported by the National Natural Science Foundation of China (Nos. 41390240 and 41329002).

Supplementary material

11356_2018_4057_MOESM1_ESM.doc (84 kb)
ESM 1 The Supplementary Material is available free of charge on the Springer Publications website at DOI: Date of sampling, brand, factory location, and lipid content (%) of feed and raw material samples (Table S1). Detailed concentration of each PBDE congener measured in feed and raw material samples (Table S2 and S3). Reference dose (RfDs) of PBDEs established by the US EPA (Table S4), calculated hazard quotients (HQ) of PBDEs via the consumption of chicken raised with chicken feeds investigated in this study (Table S5), and HQ values of PBDEs via “real” chicken meat (Table S6). (DOC 83 kb)

References

  1. Ábalos M, Parera J, Abad E, Rivera J (2008) PCDD/Fs and DL-PCBs in feeding fats obtained as co-products or by-products derived from the food chain. Chemosphere 71:1115–1126.  https://doi.org/10.1016/j.chemosphere.2007.10.034 CrossRefGoogle Scholar
  2. Airaksinen R, Hallikainen A, Rantakokko P, Ruokojärvi P, Vuorinen PJ, Mannio J, Kiviranta H (2015) Levels and congener profiles of PBDEs in edible baltic, freshwater, and farmed fish in Finland. Environ Sci Technol 49:3851–3859.  https://doi.org/10.1021/es505266p CrossRefGoogle Scholar
  3. Alonso MB, Eljarrat E, Gorga M, Secchi ER, Bassoi M, Barbosa L, Bertozzi CP, Marigo J, Cremer M, Domit C, Azevedo AF, Dorneles PR, Torres JPM, Lailson-Brito J, Malm O, Barceló D (2012) Natural and anthropogenically-produced brominated compounds in endemic dolphins from Western South Atlantic: another risk to a vulnerable species. Environ Pollut 170:152–160.  https://doi.org/10.1016/j.envpol.2012.06.001 CrossRefGoogle Scholar
  4. Baron CP, Børresen T, Jacobsen C (2007) Comparison of methods to reduce dioxin and polychlorinated biphenyls contents in fishmeal: extraction and enzymatic treatments. J Agric Food Chem 55:1620–1626.  https://doi.org/10.1021/jf061888z CrossRefGoogle Scholar
  5. Bellés M, Alonso V, Linares V, Albina ML, Sirvent JJ, Domingo JL, Sánchez DJ (2010) Behavioral effects and oxidative status in brain regions of adult rats exposed to BDE-99. Toxicol Lett 194:1–7.  https://doi.org/10.1016/j.toxlet.2010.01.010 CrossRefGoogle Scholar
  6. Berntssen MHG, Julshamn K, Lundebye A-K (2010) Chemical contaminants in aquafeeds and Atlantic salmon (Salmo salar) following the use of traditional- versus alternative feed ingredients. Chemosphere 78:637–646.  https://doi.org/10.1016/j.chemosphere.2009.12.021 CrossRefGoogle Scholar
  7. Bocio A, Llobet JM, Domingo JL, Corbella J, Teixidó A, Casas C (2003) Polybrominated diphenyl ethers (PBDEs) in foodstuffs: human exposure through the diet. J Agric Food Chem 51:3191–3195.  https://doi.org/10.1021/jf0340916 CrossRefGoogle Scholar
  8. Braekevelt E, Tittlemier SA, Tomy GT (2003) Direct measurement of octanol–water partition coefficients of some environmentally relevant brominated diphenyl ether congeners. Chemosphere 51:563–567.  https://doi.org/10.1016/S0045-6535(02)00841-X CrossRefGoogle Scholar
  9. CNPP (2018) Brand Credit Index and sales volume of animal feeds in China (in Chinese). http://www.china-10.com/best/1546.html. (accessed Dec 2018)
  10. Cohen JT, Bellinger DC, Connor WE, Kris-Etherton PM, Lawrence RS, Savitz DA, Shaywitz BA, Teutsch SM, Gray GM (2005) A quantitative ris-benefit analysis of changes in population fish consumption. Am J Prev Med 29:325–334.  https://doi.org/10.1016/j.amepre.2005.07.003 CrossRefGoogle Scholar
  11. de Wit CA (2002) An overview of brominated flame retardants in the environment. Chemosphere 46:583–624.  https://doi.org/10.1016/S0045-6535(01)00225-9 CrossRefGoogle Scholar
  12. Delgado CL (2003) Rising consumption of meat and milk in developing countries has created a new food revolution. J Nutr 133:3907S–3910S.  https://doi.org/10.1093/jn/133.11.3907S CrossRefGoogle Scholar
  13. Domingo JL (2017) Concentrations of environmental organic contaminants in meat and meat products and human dietary exposure: a review. Food Chem Toxicol 107:20–26.  https://doi.org/10.1016/j.fct.2017.06.032 CrossRefGoogle Scholar
  14. Fernandes AR, Mortimer D, Rose M, Smith F, Panton S, Garcia-Lopez M (2016) Bromine content and brominated flame retardants in food and animal feed from the UK. Chemosphere 150:472–478.  https://doi.org/10.1016/j.chemosphere.2015.12.042 CrossRefGoogle Scholar
  15. Food and Agriculture Organiztion of the United Nations (2015) World agriculture: towards 2015/2030. http://www.fao.org/docrep/005/y4252e/y4252e05b.htm. (accessed May 2018)
  16. Food and Agriculture Organiztion of the United Nations (2017) Food supply-livestock and fish primary equivalent. http://www.fao.org/faostat/en/#data/CL/visualize. (accessed May 2018)
  17. Food and Agriculture Organization of the United Nations, Poultry and poultry products-risks for human health. http://www.fao.org/docrep/013/al743e/al743e00.pdf. (accessed Dec 2018)
  18. Foran JA, Good DH, Carpenter DO, Hamilton MC, Knuth BA, Schwager SJ (2005) Quantitative analysis of the benefits and risks of consuming farmed and wild salmon. J Nutr 135:2639–2643.  https://doi.org/10.1093/jn/135.11.2639 CrossRefGoogle Scholar
  19. Giulivo M, Capri E, Kalogianni E, Milacic R, Majone B, Ferrari F, Eljarrat E, Barceló D (2017) Occurrence of halogenated and organophosphate flame retardants in sediment and fish samples from three European river basins. Sci Total Environ 586:782–791.  https://doi.org/10.1016/j.scitotenv.2017.02.056 CrossRefGoogle Scholar
  20. Gong Y, Wen S, Zheng C, Peng X, Li Y, Hu D, Peng L (2015) Potential risk assessment of polybrominated diphenyl ethers (PBDEs) by consuming animal-derived foods collected from interior areas of China. Environ Sci Pollut Res 22:8349–8358.  https://doi.org/10.1007/s11356-014-3940-2 CrossRefGoogle Scholar
  21. Grob K, Biedermann M, Scherbaum E, Roth M, Rieger K (2006) Food contamination with organic materials in perspective: packaging materials as the largest and least controlled source? A view focusing on the European situation. Crit Rev Food Sci Nutr 46:529–535.  https://doi.org/10.1080/10408390500295490 CrossRefGoogle Scholar
  22. Guo Y, Yu H-Y, Zhang B-Z, Zeng EY (2009) Persistent halogenated hydrocarbons in fish feeds manufactured in South China. J Agric Food Chem 57:3674–3680.  https://doi.org/10.1021/jf803868b CrossRefGoogle Scholar
  23. Hites RA (2004) Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environ Sci Technol 38:945–956.  https://doi.org/10.1021/es035082g CrossRefGoogle Scholar
  24. Hites RA, Foran JA, Schwager SJ, Knuth BA, Hamilton MC, Carpenter DO (2004) Global assessment of polybrominated diphenyl ethers in farmed and wild salmon. Environ Sci Technol 38:4945–4949.  https://doi.org/10.1021/es049548m CrossRefGoogle Scholar
  25. Huang H, Zhang S, Christie P (2011) Plant uptake and dissipation of PBDEs in the soils of electronic waste recycling sites. Environ Pollut 159:238–243.  https://doi.org/10.1016/j.envpol.2010.08.034 CrossRefGoogle Scholar
  26. Huang J-k, Wei W, Cui Q, Xie W (2017) The prospects for China's food security and imports: will China starve the world via imports? J Integr Agric 16:2933–2944.  https://doi.org/10.1016/s2095-3119(17)61756-8 CrossRefGoogle Scholar
  27. Jacobs MN, Covaci A, Schepens P (2002) Investigation of selected persistent organic pollutants in farmed Atlantic salmon (Salmo salar), salmon aquaculture feed, and fish oil components of the feed. Environ Sci Technol 36:2797–2805.  https://doi.org/10.1021/es011287i CrossRefGoogle Scholar
  28. Kang CS, Lee J-H, Kim S-K, Lee K-T, Lee JS, Park PS, Yun SH, Kannan K, Yoo YW, Ha JY, Lee SW (2010) Polybrominated diphenyl ethers and synthetic musks in umbilical cord serum, maternal serum, and breast milk from Seoul. South Korea Chemosphere 80:116–122.  https://doi.org/10.1016/j.chemosphere.2010.04.009 Google Scholar
  29. Karl H, Lehmann I, Oetjen K (1998) Levels of chlordane compounds in fish muscle, -meal, -oil and -feed. Chemosphere 36:2819–2832.  https://doi.org/10.1016/S0045-6535(97)10224-7 CrossRefGoogle Scholar
  30. Kawashima A, Watanabe S, Iwakiri R, Honda K (2009) Removal of dioxins and dioxin-like PCBs from fish oil by countercurrent supercritical CO2 extraction and activated carbon treatment. Chemosphere 75:788–794.  https://doi.org/10.1016/j.chemosphere.2008.12.057 CrossRefGoogle Scholar
  31. Kim S, Park J, Kim H-J, Lee JJ, Choi G, Choi S, Kim S, Kim SY, Moon H-B, Kim S, Choi K (2013) Association between several persistent organic pollutants and thyroid hormone levels in serum among the pregnant women of Korea. Environ Int 59:442–448.  https://doi.org/10.1016/j.envint.2013.07.009 CrossRefGoogle Scholar
  32. Labunska I, Harrad S, Wang M, Santillo D, Johnston P (2014) Human dietary exposure to PBDEs around e-waste recycling sites in eastern China. Environ Sci Technol 48:5555–5564.  https://doi.org/10.1021/es500241m CrossRefGoogle Scholar
  33. Liu D, Lin T, Shen K, Li J, Yu Z, Zhang G (2016) Occurrence and concentrations of halogenated flame retardants in the atmospheric fine particles in chinese cities. Environ Sci Technol 50:9846–9854.  https://doi.org/10.1021/acs.est.6b01685 CrossRefGoogle Scholar
  34. Luo X-J, Liu J, Luo Y, Zhang X-L, Wu J-P, Lin Z, Chen S-J, Mai B-X, Yang Z-Y (2009) Polybrominated diphenyl ethers (PBDEs) in free-range domestic fowl from an e-waste recycling site in South China: levels, profile and human dietary exposure. Environ Int 35:253–258.  https://doi.org/10.1016/j.envint.2008.06.007 CrossRefGoogle Scholar
  35. Luo XJ, Wu JP, Chen DJ, Mai BX (2013) Research progress on accumulation and mechanism for biological diversity of PBDEs, HBDEs and DPs. Science China 43:291–304 (In chinese) Google Scholar
  36. Meng X-Z, Zeng EY, Yu L-P, Guo Y, Mai B-X (2007) Assessment of hman exposure to polybrominated diphenyl ethers in China via fish consumption and inhalation. Environ Sci Technol 41:4882–4887.  https://doi.org/10.1021/es0701560 CrossRefGoogle Scholar
  37. Minh NH, Minh TB, Kajiwara N, Kunisue T, Iwata H, Viet PH, Tu NPC, Tuyen BC, Tanabe S (2006) Contamination by polybrominated diphenyl ethers and persistent organochlorines in catfish and feed from Mekong River Delta,Vietnam. Environ Toxicol Chem 25:2700–2708.  https://doi.org/10.1897/05-600R.1 CrossRefGoogle Scholar
  38. Ministry of Agriculture of the People's Republic of China (2004) Feeding standard of chicken. NY/T 33–2004 (in Chinese). http://www.docin.com/p-8340200.html. (accessed Dec 2018)
  39. Ministry of Agriculture of the People's Republic of China (2015) The total feed output of China exceeded 200 million tons in 2015 and 83.5 million tons of pig feed fell 3% year-on-year (in Chinese). http://bbs.pinggu.org/k/news/1392053.html. (accessed May 2018)
  40. Montory M, Barra R (2006) Preliminary data on polybrominated diphenyl ethers (PBDEs) in farmed fish tissues (Salmo salar) and fish feed in southern Chile. Chemosphere 63:1252–1260.  https://doi.org/10.1016/j.chemosphere.2005.10.030 CrossRefGoogle Scholar
  41. Ni H-G, Ding C, Lu S-Y, Yin X-L, Samuel SO (2012) Food as a main route of adult exposure to PBDEs in Shenzhen, China. Sci Total Environ 437:10–14.  https://doi.org/10.1016/j.scitotenv.2012.07.056 CrossRefGoogle Scholar
  42. Ni K, Lu Y, Wang T, Shi Y, Kannan K, Xu L, Li Q, Liu S (2013) Polybrominated diphenyl ethers (PBDEs) in China: policies and recommendations for sound management of plastics from electronic wastes. J Environ Manag 115:114–123.  https://doi.org/10.1016/j.jenvman.2012.09.031 CrossRefGoogle Scholar
  43. Olli JJ, Breivik H, Mørkøre T, Ruyter B, Johansen J, Reynolds P, Thorstad O, Berge G (2010) Removal of persistent organic pollutants from Atlantic salmon (Salmo salar L.) diets: influence on growth, feed utilization efficiency and product quality. Aquaculture 310:145–155.  https://doi.org/10.1016/j.aquaculture.2010.09.044 CrossRefGoogle Scholar
  44. Pirard C, De Pauw E (2007) Absorption, disposition and excretion of polybrominated diphenyl ethers (PBDEs) in chicken. Chemosphere 66:320–325.  https://doi.org/10.1016/j.chemosphere.2006.04.086 CrossRefGoogle Scholar
  45. Reverte I, Domingo JL, Colomina MT (2014) Neurodevelopmental effects of decabromodiphenyl ether (BDE-209) in APOE transgenic mice. Neurotoxicol Teratol 46:10–17.  https://doi.org/10.1016/j.ntt.2014.08.003 CrossRefGoogle Scholar
  46. Su G, Liu X, Gao Z, Xian Q, Feng J, Zhang X, Giesy JP, Wei S, Liu H, Yu H (2012) Dietary intake of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) from fish and meat by residents of Nanjing, China. Environ Int 42:138–143.  https://doi.org/10.1016/j.envint.2011.05.015 CrossRefGoogle Scholar
  47. Suominen K, Hallikainen A, Ruokojärvi P, Airaksinen R, Koponen J, Rannikko R, Kiviranta H (2011) Occurrence of PCDD/F, PCB, PBDE, PFAS, and organotin compounds in fish meal, fish oil and fish feed. Chemosphere 85:300–306.  https://doi.org/10.1016/j.chemosphere.2011.06.010 CrossRefGoogle Scholar
  48. Tao F, Abou-Elwafa Abdallah M, Ashworth DC, Douglas P, Toledano MB, Harrad S (2017) Emerging and legacy flame retardants in UK human milk and food suggest slow response to restrictions on use of PBDEs and HBCDD. Environ Int 105:95–104.  https://doi.org/10.1016/j.envint.2017.05.010 CrossRefGoogle Scholar
  49. Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre GI, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P, Berntssen MHG (2008) Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285:193–200.  https://doi.org/10.1016/j.aquaculture.2008.08.025 CrossRefGoogle Scholar
  50. Triantafyllou VI, Akrida-Demertzi K, Demertzis PG (2007) A study on the migration of organic pollutants from recycled paperboard packaging materials to solid food matrices. Food Chem 101:1759–1768.  https://doi.org/10.1016/j.foodchem.2006.02.023 CrossRefGoogle Scholar
  51. US EPA (1989) Risk assessment guidance for superfund. Volume I: human health evaluation manual (part a). US EPA, Washington DCGoogle Scholar
  52. US EPA (2014) Technical fact sheet polybrominated diphenyl ethers (PBDEs) and polybrominated biphenyls (PBBs). http://www.epa.gov/sites/production/files/2014-03/documents/ffrrofactsheet_contaminant_perchlorate_january2014_final_0.pdf. (accessed Dec 2018)
  53. Usydus Z, Szlinder-Richert J, Polak-Juszczak L, Malesa-Ciećwierz M, Dobrzański Z (2009) Study on the raw fish oil purification from PCDD/F and dl-PCB-industrial tests. Chemosphere 74:1495–1501.  https://doi.org/10.1016/j.chemosphere.2008.11.039 CrossRefGoogle Scholar
  54. Wang JX, Bao LJ, Luo P, Shi L, Wong CS, Zeng EY (2017) Intake, distribution, and metabolism of decabromodiphenyl ether and its main metabolites in chickens and implications for human dietary exposure. Environ Pollut 231:795–801.  https://doi.org/10.1016/j.envpol.2017.08.084 CrossRefGoogle Scholar
  55. Wang J, Liu Q, Hou Y, Qin W, Lesschen JP, Zhang F, Oenema O (2018) International trade of animal feed: its relationships with livestock density and N and P balances at country level. Nutr Cycl Agroecosyst 110:197–211.  https://doi.org/10.1007/s10705-017-9885-3 CrossRefGoogle Scholar
  56. Workman D (2018) Animal Feeds Exporters by Country. http://www.worldstopexports.com/animal-feeds-exporters-by-country/. (accessed Dec 2018)
  57. Yang Y, Xie Q, Liu X, Wang J (2015) Occurrence, distribution and risk assessment of polychlorinated biphenyls and polybrominated diphenyl ethers in nine water sources. Ecotoxicol Environ Saf 115:55–61.  https://doi.org/10.1016/j.ecoenv.2015.02.006 CrossRefGoogle Scholar
  58. Zheng X-B, Luo X-J, Zheng J, Zeng Y-H, Mai B-X (2015) Contaminant sources, gastrointestinal absorption, and tissue distribution of organohalogenated pollutants in chicken from an e-waste site. Sci Total Environ 505:1003–1010.  https://doi.org/10.1016/j.scitotenv.2014.10.076 CrossRefGoogle Scholar
  59. Zhou P, Zhao Y, Li J, Wu G, Zhang L, Liu Q, Fan S, Yang X, Li X, Wu Y (2012) Dietary exposure to persistent organochlorine pesticides in 2007 Chinese total diet study. Environ Int 42:152–159.  https://doi.org/10.1016/j.envint.2011.05.018 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jing-Xin Wang
    • 1
    • 2
    • 3
    • 4
  • Lian-Jun Bao
    • 1
  • Lei Shi
    • 1
  • Liang-Ying Liu
    • 1
    Email author
  • Eddy Y. Zeng
    • 1
  1. 1.School of EnvironmentJinan UniversityGuangzhouChina
  2. 2.State Key Laboratory of Organic Geochemistry, Guangzhou Institute of GeochemistryChinese Academy of SciencesGuangzhouChina
  3. 3.Key Laboratory of Recreational Fisheries Research, Ministry of Agriculture and Ministry of Agriculture Laboratory of Quality & Safety Risky Assessment for Aquatic ProductPearl River Fisheries Research Institute, Chinese Academic of Fishery ScienceGuangzhouChina
  4. 4.University of Chinese Academy of SciencesBeijingChina

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