Persistent Organohalogens in Paired Fish Fillet and Eggs: Implications for Fish Consumption Advisories

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 14, 2016, Pages 2832-2840

  Zhang, Xianming ^a   Gandhi, Nilima ^a   Bhavsar, Satyendra P ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ONTARIO MINISTRY OF THE ENVIRONMENT   (Canada)

Author keywords

contaminant exposure; fish consumption advisory; human health; POPs; roe eggs; toxics

Indexed keywords

CONTAMINATION; FATTY ACIDS; HEALTH RISKS; IMPURITIES; LAKES; NAPHTHALENE; ORGANIC CHEMICALS; ORGANIC POLLUTANTS;

CONTAMINANT EXPOSURE; FISH CONSUMPTION; HUMAN HEALTH; POPS; ROE EGGS; TOXICS;

FISH;

DIPHENYL ETHER DERIVATIVE; POLYCHLORINATED BIPHENYL; WATER POLLUTANT;

ANALYSIS; ANIMAL; EGG; FISH; FISH PRODUCT; FOOD CONTAMINATION; HUMAN; PRODUCT SAFETY; UNITED STATES; WATER POLLUTANT;

ANIMALS; CONSUMER PRODUCT SAFETY; EGGS; FISH PRODUCTS; FISHES; FOOD CONTAMINATION; GREAT LAKES REGION; HALOGENATED DIPHENYL ETHERS; HUMANS; POLYCHLORINATED BIPHENYLS; WATER POLLUTANTS, CHEMICAL;

EID: 84964595237     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b00089     Document Type: Article

References (63)

1. Kris-Etherton, P. M.; Harris, W. S.; Appel, L. J. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease Circulation 2002, 106, 2747-2757 10.1161/01.CIR.0000038493.65177.94
2. Calder, P. C.; Yaqoob, P. Omega-3 polyunsaturated fatty acids and human health outcomes BioFactors 2009, 35, 266-272 10.1002/biof.42
3. Sidhu, K. S. Health benefits and potential risks related to consumption of fish or fish oil Regul. Toxicol. Pharmacol. 2003, 38, 336 10.1016/j.yrtph.2003.07.002
4. Domingo, J. L.; Bocio, A.; Falco, G.; Llobet, J. M. Benefits and risks of fish consumption Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants Toxicology 2007, 230, 219-26 10.1016/j.tox.2006.11.054
5. Health Canada. Canada's Food Guide; available onlineat http://www.hc-sc.gc.ca/fn-an/food-guide-aliment/index-eng.php (accessed December 2011).
6. Fish: What Pregnant Women and Parents Should Know; updated Fish Consumption Advice and Questions & Answers by FDA and EPA; available at http://www.fda.gov/food/foodborneillnesscontaminants/metals/ucm393070.htm (accessed October 2015).
7. American Heart Association. Fish and Omega-3 Fatty Acids;available tat http://www.heart.org/HEARTORG/GettingHealthy/NutritionCenter/HealthyDietGoals/Fish-and-Omega-3-Fatty-Acids-UCM-303248-Article.jsp.VkEdUGSrTfY (accessed October 2015).
8. Ziboh, V. A.; Miller, C. C. Essential fatty acids and polyunsaturated fatty acids: significance in cutaneous biology Annu. Rev. Nutr. 1990, 10, 433-450 10.1146/annurev.nu.10.070190.002245
9. Kannan, K.; Tanabe, S.; Williams, R. J.; Tatsukawa, R. Persistent organochlorine residues in foodstuffs from Australia, Papua New Guinea and the Solomon Islands: contamination levels and human dietary exposure Sci. Total Environ. 1994, 153, 29-49 10.1016/0048-9697(94)90099-X
10. Liem, A. K. D.; Furst, P.; Rappe, C. Exposure of populations to dioxins and related compounds Food Addit. Contam. 2000, 17, 241-259 10.1080/026520300283324
11. Ontario Ministry of the Environment and Climate Change;Guide to Eating Ontario Sport Fish, 2015-2016; available at http://www.ontario.ca/document/guide-eating-ontario-fish (accessed November 2015).
12. U.S. EPA. Thenational listing of fish advisories; availableonline at http://water.epa.gov/scitech/swguidance/fishshellfish/fishadvisories/index.cfm (accessed Dec 2011).
13. Murkin, E.; Cole, D. C.; Kearney, J. P.; Sheeshka, J.; Dawson, J. Project, F. W. N., Fish consumption practices among frequent consuming fishers of five Ontario Great Lakes areas of concern (AOCs) J. Great Lakes Res. 2003, 29, 436-447 10.1016/S0380-1330(03)70449-3
14. Bhavsar, S. P.; Awad, E.; Fletcher, R.; Hayton, A.; Somers, K. M.; Kolic, T.; MacPherson, K.; Reiner, E. J. Temporal trends and spatial distribution of dioxins and furans in lake trout or lake whitefish from the Canadian Great Lakes Chemosphere 2008, 73, S158-S165 10.1016/j.chemosphere.2007.05.100
15. Gewurtz, S. B.; Bhavsar, S. P.; Fletcher, R. Influence of fish size and sex on mercury/PCB concentration: importance for fish consumption advisories Environ. Int. 2011, 37, 425-434 10.1016/j.envint.2010.11.005
16. Gewurtz, S. B.; Bhavsar, S. P.; Jackson, D. A.; Fletcher, R.; Awad, E.; Moody, R.; Reiner, E. J. Temporal and spatial trends of organochlorines and mercury in fishes from the St. Clair River/Lake St. Clair corridor, Canada J. Great Lakes Res. 2010, 36, 100-112 10.1016/j.jglr.2009.12.008
17. Olsson, A.; Valters, K.; Burreau, S. Concentrations of organochlorine substances in relation to fish size and trophic position: a study on perch (Perca fluviatilis L.) Environ. Sci. Technol. 2000, 34, 4878-4886 10.1021/es991400t
18. Gewurtz, S. B.; Backus, S. M.; Bhavsar, S. P.; McGoldrick, D. J.; de Solla, S. R.; Murphy, E. W. Contaminant biomonitoring programs in the Great Lakes region: review of approaches and critical factors Environ. Rev. 2011, 19, 162-184 10.1139/a11-005
19. Stow, C. A.; Qian, S. S. A size-based probabilistic assessment of PCB exposure from Lake Michigan fish consumption Environ. Sci. Technol. 1998, 32, 2325-2330 10.1021/es970840m
20. Zhang, X. M.; Gandhi, N.; Bhavsar, S. P.; Ho, L. S. W. Effects of skin removal on contaminant levels in salmon and trout filets Sci. Total Environ. 2013, 443, 218-225 10.1016/j.scitotenv.2012.10.090
21. Bayen, S.; Barlow, P.; Lee, H. K.; Obbard, J. P. Effect of cooking on the loss of persistent organic pollutants from salmon J. Toxicol. Environ. Health, Part A 2005, 68, 253-265 10.1080/15287390590895126
22. Bhavsar, S. P.; Zhang, X.; Guo, R.; Braekevelt, E.; Petro, S.; Gandhi, N.; Reiner, E. J.; Lee, H.; Bronson, R.; Tittlemier, S. A. Cooking fish is not effective in reducing exposure to perfluoroalkyl and polyfluoroalkyl substances Environ. Int. 2014, 66, 107-114 10.1016/j.envint.2014.01.024
23. Bledsoe, G.; Bledsoe, C.; Rasco, B. Caviars and fish roe products Crit. Rev. Food Sci. Nutr. 2003, 43, 317-356 10.1080/10408690390826545
24. Bledsoe, G.; Rasco, B. Caviar and fish roe. Handbook of Food Science, Technology, and Engineering; CRC Taylor and Francis: Boca Raton, FL, USA, 2005; Vol. 4
25. Monfort, M. C. Fish roe in Europe: Supply and Demand Conditions; Food and Agriculture Organization of the United Nations, GLOBEFISH, Fishery Industries Division, 2002.
26. A fish consumption survey of the Umatilla, Nez Perce, Yakama, and Warm Springs tribes of the Columbia River Basin, Columbia River Inter-Tribal Fish Commission, 1994; available at http://www.critfc.org/wp-content/uploads/2015/06/94-3report.pdf (accessed August 2013).
27. Awad, E. The Results of the 2003 Guide to Eating Ontario Sport Fish Questionnaire; Environmental Monitoring and Reporting Branch, Ontario Ministry of the Environment, 2006.
28. Kaitaranta, J. K. Lipids and fatty-acids of a whitefish (Coregonus albula) flesh and roe J. Sci. Food Agric. 1980, 31, 1303-1308 10.1002/jsfa.2740311213
29. MacKay, D.; Fraser, A. Bioaccumulation of persistent organic chemicals: mechanisms and models Environ. Pollut. 2000, 110, 375-391 10.1016/S0269-7491(00)00162-7
30. Landrum, P. F.; Fisher, S. W. Influence of lipids on the bioaccumulation and trophic transfer of organic contaminants in aquatic organisms. Lipids in Freshwater Ecosystems; Springer: New York, 1998; pp 203-234 10.1007/978-1-4612-0547-0-10.
31. Russell, R. W.; Gobas, F. A. P. C.; Haffner, G. D. Maternal transfer and in ovo exposure of organochlorines in oviparous organisms: a model and field verification Environ. Sci. Technol. 1999, 33, 416-420 10.1021/es9800737
32. Daley, J. M.; Leadley, T. A.; Drouillard, K. G. Evidence for bioamplification of nine polychlorinated biphenyl (PCB) congeners in yellow perch (Perca flavascens) eggs during incubation Chemosphere 2009, 75, 1500-1505 10.1016/j.chemosphere.2009.02.013
33. Bhavsar, S. P.; Gewurtz, S. B.; McGoldrick, D. J.; Keir, M. J.; Backus, S. M. Changes in mercury levels in Great Lakes fish between 1970s and 2007 Environ. Sci. Technol. 2010, 44, 3273-3279 10.1021/es903874x
34. Bhavsar, S. P.; Jackson, D. A.; Hayton, A.; Reiner, E. J.; Chen, T.; Bodnar, J. Are PCB levels in fish from the Canadian Great Lakes still declining? J. Great Lakes Res. 2007, 33, 592-605 10.3394/0380-1330(2007)33[592:APLIFF]2.0.CO;2
35. French, T. D.; Campbell, L. M.; Jackson, D. A.; Casselman, J. M.; Scheider, W. A.; Hayton, A. Long-term changes in legacy trace organic contaminants and mercury in Lake Ontario salmon in relation to source controls, trophodynamics, and climatic variability Limnol. Oceanogr. 2006, 51, 2794-2807 10.4319/lo.2006.51.6.2794
36. Gandhi, N.; Bhavsar, S. P.; Tang, R. W. K.; Drouillard, K. G.; Arhonditsis, G. B. Significance of toxaphene in Great Lakes fish consumption advisories J. Great Lakes Res. 2014, 40, 71-79 10.1016/j.jglr.2013.12.017
37. Gewurtz, S. B.; Lega, R.; Crozier, P. W.; Whittle, D. M.; Fayez, L.; Reiner, E. J.; Helm, P. A.; Marvin, C. H.; Tomy, G. T. Factors influencing trends of polychlorinated naphthalenes and other dioxin-like compounds in lake trout (Salvelinus namaycush) from Lake Ontario, North America (1979-2004) Environ. Toxicol. Chem. 2009, 28, 921-930 10.1897/08-307.1
38. Ismail, N.; Gewurtz, S. B.; Pleskach, K.; Whittle, D. M.; Helm, P. A.; Marvin, C. H.; Tomy, G. T. Brominated and chlorinated flame retardants in Lake Ontario, Canada, lake trout (Salvelinus namaycush) between 1979 and 2004 and possible influences of food-web changes Environ. Toxicol. Chem. 2009, 28, 910-920 10.1897/08-162.1
39. Gandhi, N.; Tang, R. W. K.; Bhavsar, S. P.; Reiner, E. J.; Morse, D.; Arhonditsis, G. B.; Drouillard, K.; Chen, T. Is mirex still a contaminant of concern for the North American Great Lakes? J. Great Lakes Res. 2015, 41, 1114-1122 10.1016/j.jglr.2015.09.015
40. Ontario Ministry of the Environment. The determination ofpolychlorinated dibenzo-p-dioxins, polychlorinated furans and dioxin-likePCBs in environmental matrices by GC-HRMS; Laboratory Services BranchMethod DFPCB-E3418; Ontario Ministry of the Environment, Toronto, ON, Canada, 2005.
41. Ontario Ministry of the Environment. Thedetermination ofpolybrominated diphenyl ethers (PBDEs) in environmental matrices byGas Chromatography-High Resolution Mass Spectrometry (GC-HRMS); LaboratoryServices Branch Method BDE-E3430; Ontario Ministry of the Environment, Toronto, ON, Canada, 2005.
42. Ontario Ministry of the Environment. The determination ofpolychlorinated naphthalenes (PCNs) in environmental matrices by GasChromatography-High Resolution Mass Spectrometry (GC-HRMS); LaboratoryServices Branch Method PCN-E3431; Ontario Ministry of the Environment, Toronto, ON, Canada, 2010.
43. Van den Berg, M.; Birnbaum, L. S.; Denison, M.; De Vito, M.; Farland, W.; Feeley, M.; Fiedler, H.; Hakansson, H.; Hanberg, A.; Haws, L.; Rose, M.; Safe, S.; Schrenk, D.; Tohyama, C.; Tritscher, A.; Tuomisto, J.; Tysklind, M.; Walker, N.; Peterson, R. E. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds Toxicol. Sci. 2006, 93, 223-241 10.1093/toxsci/kfl055
44. Van den Berg, M.; Birnbaum, L.; Bosveld, A. T. C.; Brunstrom, B.; Cook, P.; Feeley, M.; Giesy, J. P.; Hanberg, A.; Hasegawa, R.; Kennedy, S. W.; Kubiak, T.; Larsen, J. C.; van Leeuwen, F. X. R.; Liem, A. K. D.; Nolt, C.; Peterson, R. E.; Poellinger, L.; Safe, S.; Schrenk, D.; Tillitt, D.; Tysklind, M.; Younes, M.; Waern, F.; Zacharewski, T. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife Environ. Health Perspect. 1998, 106, 775-792 10.1289/ehp.98106775
45. Safe, S. H. Development validation and problems with the toxic equivalency factor approach for risk assessment of dioxins and related compounds J. Anim. Sci. 1998, 76, 134-141
46. Kelly, B. C.; Gray, S. L.; Ikonomou, M. G.; Macdonald, J. S.; Bandiera, S. M.; Hrycay, E. G. Lipid reserve dynamics and magnification of persistent organic pollutants in spawning sockeye salmon (Oncorhynchus nerka) from the Fraser River, British Columbia Environ. Sci. Technol. 2007, 41, 3083-3089 10.1021/es061559n
47. Song, W. L.; Ford, J. C.; Li, A.; Sturchio, N. C.; Rockne, K. J.; Buckley, D. R.; Mills, W. J. Polybrominated diphenyl ethers in the sediments of the Great Lakes. 3. Lakes Ontario and Erie Environ. Sci. Technol. 2005, 39, 5600-5605 10.1021/es050631z
48. Hale, R. C.; Alaee, M.; Manchester-Neesvig, J. B.; Stapleton, H. M.; Ikonomou, M. G. Polybrominated diphenyl ether flame retardants in the North American environment Environ. Int. 2003, 29, 771-779 10.1016/S0160-4120(03)00113-2
49. Schrap, S. M.; Opperhuizen, A. Relationship between bioavailability and hydrophobicity-reduction of the uptake of organic-chemicals by fish due to the sorption of particles Environ. Toxicol. Chem. 1990, 9, 715-724 10.1002/etc.5620090604
50. Ramos, E. U.; Meijer, S. N.; Vaes, W. H. J.; Verhaar, H. J. M.; Hermens, J. L. M. Using solid-phase microextraction to determine partition coefficients to humic acids and bioavailable concentrations of hydrophobic chemicals Environ. Sci. Technol. 1998, 32, 3430-3435 10.1021/es980274a
51. Tomy, G. T.; Palace, V. P.; Halldorson, T.; Braekevelt, E.; Danell, R.; Wautier, K.; Evans, B.; Brinkworth, L.; Fisk, A. T. Bioaccumulation, biotransformation, and biochemical effects of brominated diphenyl ethers in juvenile lake trout (Salvelinus namaycush) Environ. Sci. Technol. 2004, 38, 1496-1504 10.1021/es035070v
52. Gandhi, N.; Bhavsar, S. P.; Gewurtz, S. B.; Tomy, G. T. 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. 2011, 37, 170-177 10.1016/j.envint.2010.08.013
53. van Leeuwen, S. P. J.; van Velzen, M. J. M.; Swart, C. P.; van der Veen, I.; Traag, W. A.; de Boer, J. Halogenated contaminants in farmed salmon, trout, tilapia, pangasius, and shrimp Environ. Sci. Technol. 2009, 43, 4009-4015 10.1021/es803558r
54. Voorspoels, S.; Covaci, A.; Schepens, P. Polybrominated diphenyl ethers in marine species from the Belgian North Sea and the Western Scheidt Estuary: levels, profiles, and distribution Environ. Sci. Technol. 2003, 37, 4348-4357 10.1021/es034503r
55. Bhavsar, S. P.; Fletcher, R.; Hayton, A.; Reiner, E. J.; Jackson, D. A. Composition of dioxin-like PCBs in fish: an application for risk assessment Environ. Sci. Technol. 2007, 41, 3096-3102 10.1021/es062402y
56. Bhavsar, S. P.; Hayton, A.; Reiner, E. J.; Jackson, D. A. Estimating dioxin-like polychlorinated biphenyl toxic equivalents from total polychlorinated biphenyl measurements in fish Environ. Toxicol. Chem. 2007, 26, 1622-1628 10.1897/06-621R.1
57. Bhavsar, S. P.; Reiner, E. J.; Hayton, A.; Fletcher, R.; MacPherson, K. Converting toxic equivalents (TEQ) of dioxins and dioxin-like compounds in fish from one toxic equivalency factor (TEF) scheme to another Environ. Int. 2008, 34, 915-921 10.1016/j.envint.2008.02.001
58. Blankenship, A. L.; Kannan, K.; Villalobos, S. A.; Villeneuve, D. L.; Falandysz, J.; Imagawa, T.; Jakobsson, E.; Giesy, J. P. Relative potencies of individual polychlorinated naphthalenes and halowax mixtures to induce Ah receptor-mediated responses Environ. Sci. Technol. 2000, 34, 3153-3158 10.1021/es9914339
59. Hanberg, A.; Stahlberg, M.; Georgellis, A.; Dewit, C.; Ahlborg, U. G. Swedish Dioxin Survey-evaluation of the H-4-Ii E bioassay for screening environmental-samples for dioxin-like enzyme-induction Pharmacol. Toxicol. 1991, 69, 442-449 10.1111/j.1600-0773.1991.tb01327.x
60. U.S. Department of Agriculture. NationalNutrient Databasefor Standard Reference Release 28-Basic Report: 15207, Fish,roe, mixed species, cooked, dry heat; available at http://ndb.nal.usda.gov/ndb/foods/show/4685?format=Full&reportfmt=pdf&pdfQvs=%7B%7D.
61. Endo, S.; Escher, B. I.; Goss, K. U. Capacities of membrane lipids to accumulate neutral organic chemicals Environ. Sci. Technol. 2011, 45, 5912-5921 10.1021/es200855w
62. Kaitaranta, J. K. Lipids and fatty acids of a whitefish (Coregonus albula) flesh and roe J. Sci. Food Agric. 1980, 31, 1303-1308 10.1002/jsfa.2740311213
63. Thomann, R. V. Bioaccumulation model of organic-chemical distribution in aquatic food-chains Environ. Sci. Technol. 1989, 23, 699-707 10.1021/es00064a008