Is the bone tissue of ring-billed gulls breeding in a pollution hotspot in the St. Lawrence River, Canada, impacted by halogenated flame retardant exposure?

Chemosphere

Volumn 93, Issue 10, 2013, Pages 2333-2340

  Plourde, Stéphanie Pellerin ^a   Moreau, Robert ^a   Letcher, Robert J ^b   Verreault, Jonathan ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b CARLETON UNIVERSITY   (Canada)

Author keywords

Alkaline phosphatase; Bird; Bone mineral density; Calcium; Flame retardant; Inorganic phosphate

Indexed keywords

BIRDS; BONE; CALCIUM; FLAME RETARDANTS; HALOGENATION; LIVING SYSTEMS STUDIES; METABOLISM; MINERALS; PALLETS; PHOSPHATASES; SALES; TISSUE;

ALKALINE PHOSPHATASE; BONE MINERAL DENSITY; BROMINATED DIPHENYL ETHERS; HALOGENATED FLAME RETARDANT; INORGANIC PHOSPHATES; MINERAL COMPOSITION; ORGANOHALOGEN CONTAMINANTS; ST. LAWRENCE RIVER;

RIVER POLLUTION;

CALCIUM; FLAME RETARDANT; PHOSPHATE; ALKALINE PHOSPHATASE; DIPHENYL ETHER DERIVATIVE; POLLUTANT;

BIRD; BONE; BREEDING; CALCIUM; ETHER; MALE; METABOLISM; NESTING; ORGANOHALOGEN; PHOSPHATE; POLLUTION; POLLUTION EXPOSURE;

ANIMAL TISSUE; ARTICLE; BONE DEMINERALIZATION; BONE DENSITY; BONE MASS; BONE METABOLISM; BONE STRUCTURE; BONE TISSUE; CALCIUM BLOOD LEVEL; CANADA; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; FEMALE; LARUS DELAWARENSIS; MALE; NONHUMAN; PHOSPHATE BLOOD LEVEL; RIVER; WATER BIRD; WATER POLLUTION; ANIMAL; BONE; CHARADRIIFORMES; METABOLISM; POLLUTANT; TOXICITY;

CANADA; MONTREAL; QUEBEC [CANADA]; SAINT LAWRENCE RIVER;

AVES; LARUS DELAWARENSIS;

ALKALINE PHOSPHATASE; ANIMALS; BONE AND BONES; CANADA; CHARADRIIFORMES; ENVIRONMENTAL POLLUTANTS; FLAME RETARDANTS; HALOGENATED DIPHENYL ETHERS; MALE; RIVERS;

EID: 84886950624     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2013.08.030     Document Type: Article

References (53)

1. Alvarez-Lloret P., Lind P.M., Nyberg I., Örberg J., Rodriguez-Navarro A.B. Effects of 3,3',4,4',5-pentachlorobiphenyl (PCB126) on vertebral bone mineralization and on thyroxin and vitamin D levels in Sprague-Dawley rats. Toxicol. Lett. 2009, 187:63-68.
2. Beard J., Marshall S., Jong K., Newton R., Triplett-Mcbride T., Humphries B., Bronks R. 1,1,1-trichloro-2,2-bis (p-chlorophenyl)-ethane (DDT) and reduced bone mineral density. Arch. Environ. Health 2000, 55:177-180.
3. Betts K. New flame retardants detected in indoor and outdoor environments. Environ. Sci. Technol. 2008, 42:6778.
4. Brouwer A., Morse D.C., Lans M.C., Schuur A.G., Murk A.J., Klasson-Wehler E., Bergman Å., Visser T.J. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol. Ind. Health 1998, 14:59-84.
5. Caron-Beaudoin, E., Gentes, M.-L., Patenaude-Monette, M., Hélie, J.-F., Giroux, J.-F., Verreault, J., 2013. Combined usage of stable isotopes and GPS-based telemetry to understand the feeding ecology of an omnivorous bird. Can. J. Zool. Published, online August 1st, 2013.
6. Chabot-Giguère B., Letcher R.J., Verreault J. In vitro biotransformation of decabromodiphenyl ether (BDE-209) and Dechlorane Plus flame retardants: a case study of ring-billed gull breeding in a pollution hotspot in the St. Lawrence River. Canada. Environ. Int. 2013, 55:101-108.
7. Chen D., Hale R.C. A global review of polybrominated diphenyl ether flame retardant contamination in birds. Environ. Int. 2010, 36:800-811.
8. Chen D., Letcher R.J., Burgess N.M., Champoux L., Elliott J.E., Hebert C.E., Martin P., Wayland M., Weseloh D.V.C., Wilson L. Flame retardants in eggs of four gull species (Laridae) from breeding sites spanning Atlantic to Pacific Canada. Environ. Pollut. 2012, 168:1-9.
9. Chen D., Letcher R.J., Martin P.A. Flame retardants in eggs of American kestrels and European starlings from southern Lake Ontario region (North America). J. Environ. Monit. 2012, 14:2870-2876.
10. Christenson R.H. Biochemical markers of bone metabolism: an overview. Clin. Biochem. 1997, 30:573-593.
11. Clarke B. Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephro. 2008, 3:S131-S139.
12. Covaci A., Gerecke A.C., Law R.J., Voorspoels S., Kohler M., Heeb N.Z., Leslie H., Allchin C.R., de Boer J. Hexabromocyclododecanes (HBCDs) in the environment and humans: a review. Environ. Sci. Technol. 2006, 40:3679-3688.
13. Covaci A., Harrad S., Abdallah M.A.E., Ali N., Law R.J., Herzke D., de Wit C.A. Novel brominated flame retardants: a review of their analysis, environmental fate and behaviour. Environ. Int. 2011, 37:532-556.
14. Cruess R.L. Physiology of bone formation and resorption. The Musculoskeletal System: Embryology, Biochemistry, and Physiology 1982, Churchill Livingstone, New York. R.L. Cruess (Ed.).
15. Darnerud P.O. Brominated flame retardants as possible endocrine disrupters. Int. J. Androl. 2008, 31:152-160.
16. de Wit C.A., Herzke D., Vorkamp K. Brominated flame retardants in the Arctic environment - trends and new candidates. Sci. Total Environ. 2010, 408:2885-2918.
17. Duncan Bassett J.H., Williams G.R. The molecular actions of thyroid hormone in bone. Trends Endocrin. Met. 2003, 14:356-364.
18. Environment Canada, 2011. Risk management of DecaBDE: Commitment to voluntary phase-out exports to Canada. http://www.ec.gc.ca/toxiques-toxics/default.asp?lang=En&n=F64D6E3B-1&xml=F64D6E3B-0328-4C11-A9E4-790D053E42A1.
19. European Parliament, 2003. Directive 2003/11/EC of the European Parliament and the Council of 6 February 2003 amending for the 24th time Council Directive 76/769/EEC relating marketing and use of certain dangerous substances and preparations (pentabromodiphenyl ether, octabromodiphenyl ether), Official Journal L 042.
20. Fernie K.J., Shutt J.L., Mayne G., Hoffman D., Letcher R.J., Drouillard K.G., Ritchie I.J. Exposure to polybrominated diphenyl ethers (PBDEs): changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). Toxicol. Sci. 2005, 88:375-383.
21. Fernie K.J., Laird Shutt J., Letcher R.J., Ritchie I.J., Bird D.M. Environmentally relevant concentrations of DE-71 and HBCD alter eggshell thickness and reproductive success of American kestrels. Environ. Sci. Technol. 2009, 43:2124-2130.
22. Fox G.A., Lundberg R., Wejheden C., Lind L., Larsson S., Örberg J., Lind M. Health of herring gulls (Larus argentatus) in relation to breeding location in the early 1990s. III. Effects on the bone tissue. J. Toxicol. Environ. Heal. A 2008, 71:1448-1456.
23. Franceschi R.T., Xiao G., Jiang D., Gopalakrishnan R., Yang S., Reith E. Multiple signaling pathways converge on the Cbfa1/Runx2 transcription factor to regulate osteoblast differentiation. Connect. Tissue Res. 2003, 44(Suppl 1):109-116.
24. Gauthier L.T., Potter D., Hebert C.E., Letcher R.J. Temporal trends and spatial distribution of non-polybrominated diphenyl ether flame retardants in the eggs of colonial populations of Great Lakes herring gulls. Environ. Sci. Technol. 2008, 43:312-317.
25. Gentes M.L., Letcher R.J., Caron-Beaudoin É., Verreault J. Novel flame retardants in urban-feeding ring-billed gulls from the St. Lawrence River. Canada. Environ. Sci. Technol. 2012, 46:9735-9744.
26. Glynn A.W., Michaëlsson K., Lind P.M., Wolk A., Aune M., Atuma S., Darnerud P.O., Mallmin H. Organochlorines and bone mineral density in Swedish men from the general population. Osteoporosis Int. 2000, 11:1036-1042.
27. Guerra P., Fernie K., Jiménez B., Pacepavicius G., Shen L., Reiner E., Eljarrat E., Barceló D., Alaee M. Dechlorane plus and related compounds in peregrine falcon (Falco peregrinus) eggs from Canada and Spain. Environ. Sci. Technol. 2011, 45:1284-1290.
28. Guyton A.C., Hall J.E. Parathyroid hormone, calcitonin, calcium and phosphate metabolism, vitamin D, bone and teeth. Textbook of Medical Physiology 2006, Elsevier, Saunders, Philadelphia. eleventh ed. A.C. Guyton, J.E. Hall (Eds.).
29. Hodgson S., Thomas L., Fattore E., Lind M., Alfven T., Hellström L., Hakansson H., Carubelli G., Fanelli R., Jarup L. Bone mineral density changes in relation to environmental PCB exposure. Environ. Health Perspect. 2008, 116:1162-1166.
30. Karga H., Papapetrou P.D., Korakovouni A., Papandroulaki F., Polymeris A., Pampouras G. Bone mineral density in hyperthyroidism. Clin. Endocrinol. 2004, 61:466-472.
31. Lind P.M., Bergman A., Olsson M., Örberg J. Bone mineral density in male Baltic grey seal (Halichoerus grypus). Ambio 2003, 32:385-388.
32. Lind P.M., Milnes M.R., Lundberg R., Bermudez D., Örberg J.A., Guillette L.J. Abnormal bone composition in female juvenile American alligators from a pesticide-polluted lake (Lake Apopka, Florida). Environ. Health Perspect. 2004, 112:359-362.
33. Lind P.M., Wejheden C., Lundberg R., Alvarez-Lloret P., Hermsen S.A.B., Rodriguez-Navarro A.B., Larsson S., Rannug A. Short-term exposure to dioxin impairs bone tissue in male rats. Chemosphere 2009, 75:680-684.
34. Lind P.M., Gustafsson M., Hermsen S.A.B., Larsson S., Kyle C.E., Örberg J., Rhind S.M. Exposure to pastures fertilized with sewage sludge disrupts bone tissue homeostasis in sheep. Sci. Total Environ. 2009, 407:2200-2208.
35. Lind P.M., Öberg D., Larsson S., Kyle C.E., Örberg J., Rhind S.M. Pregnant ewes exposed to multiple endocrine disrupting pollutants through sewage sludge-fertilized pasture show an anti-estrogenic effect in their trabecular bone. Sci. Total Environ. 2010, 408:2340-2346.
36. Lundberg R., Lyche J.L., Ropstad E., Aleksandersen M., Rönn M., Skaare J.U., Larsson S., Örberg J., Lind P.M. Perinatal exposure to PCB 153, but not PCB 126, alters bone tissue composition in female goat offspring. Toxicology 2006, 228:33-40.
37. Lundberg R., Jenssen B.M., Leiva-Presa À., Rönn M., Hernhag C., Wejheden C., Larsson S., Örberg J., Lind P.M. Effects of short-term exposure to the DDT metabolite p,p'-DDE on bone tissue in male common frog (Rana temporaria). J. Toxicol. Environ. Health A 2007, 70:614-619.
38. McNabb F.M.A. Biomarkers for the assessment of avian thyroid disruption by chemical contaminants. Avian Poult. Biol. Rev. 2005, 16:3-10.
39. Nøst T.H., Helgason L.B., Harju M., Heimstad E.S., Gabrielsen G.W., Jenssen B.M. Halogenated organic contaminants and their correlations with circulating thyroid hormones in developing Arctic seabirds. Sci. Total Environ. 2012, 414:248-256.
40. Risteli L., Risteli J. Biochemical markers of bone metabolism. Ann. Med. 1993, 25:385-393.
41. Roodman G.D. Cell biology of the osteoclast. Experiment. Hematol. 1999, 27:1229-1241.
42. Routti H., Nyman M., Jenssen B.M., Bäckman C., Koistinen J., Gabrielsen G.W. Bone-related effects of contaminants in seals may be associated with vitamin D and thyroid hormones. Environ. Toxicol. Chem. 2008, 27:873-880.
43. Sanderson T., van den Berg M. Interactions of xenobiotics with the steroid hormone biosynthesis pathway. Pure Appl. Chem. 2003, 75:1957-1971.
44. Sonne C., Dietz R., Born E.W., Riget F.F., Kirkegaard M., Hyldstrup L., Letcher R.J., Muir D.C.G. Is bone mineral composition disrupted by organochlorines in East Greenland polar bears (Ursus maritimus)?. Environ. Health Perspect. 2004, 112:1711-1716.
45. Sonne C., Bustnes J.O., Herzke D., Jaspers V.L.B., Covaci A., Eulaers I., Halley D.J., Moum T., Ballesteros M., Eens M., Ims R.A., Hanssen S.A., Erikstad K.E., Johnsen T.V., Rigét F.F., Jensen A.L., Kjelgaard-Hansen M. Blood plasma clinical-chemical parameters as biomarker endpoints for organohalogen contaminant exposure in Norwegian raptor nestlings. Ecotox. Environ. Safe. 2012, 80:76-83.
46. Ucán-Marín F., Arukwe A., Mortensen A., Gabrielsen G.W., Letcher R.J. Recombinant albumin and transthyretin transport proteins from two gull species and human: chlorinated and brominated contaminant binding and thyroid hormones. Environ. Sci. Technol. 2010, 44:497-504.
47. UNEP, 2010. The 9 new POPS: An introduction to the nine chemicals added to the Stockholm Convention by the Conference of the Parties at its fourth meeting. http://chm.pops.int/Programmes/New%20POPs/Publications/tabid/695/language/en-US/Default.aspx.
48. USEPA, 2009. DecaBDE Phase-out Initiative. http://www.epa.gov/oppt/existingchemicals/pubs/actionplans/deccadbe.html.
49. Van den Steen E., Eens M., Covaci A., Dirtu A.C., Jaspers V.L.B., Neels H., Pinxten R. An exposure study with polybrominated diphenyl ethers (PBDEs) in female European starlings (Sturnus vulgaris): toxicokinetics and reproductive effects. Environ. Pollut. 2009, 157:430-436.
50. Verreault J., Skaare J.U., Jenssen B.M., Gabrielsen G.W. Effects of organochlorine contaminants on thyroid hormone levels in Arctic breeding glaucous gulls. Larus hyperboreus. Environ. Health Perspect. 2004, 112:532-537.
51. Verreault J., Gebbink W.A., Gauthier L.T., Gabrielsen G.W., Letcher R.J. Brominated flame retardants in glaucous gulls from the Norwegian Arctic: more than just an issue of polybrominated diphenyl ethers. Environ. Sci. Technol 2007, 41:4925-4931.
52. Verreault J., Bech C., Letcher R.J., Ropstad E., Dahl E., Gabrielsen G.W. Organohalogen contamination in breeding glaucous gulls from the Norwegian Arctic: associations with basal metabolism and circulating thyroid hormones. Environ. Pollut. 2007, 145:138-145.
53. Verreault J., Helgason L.B., Gabrielsen G.W., Dam M., Braune B.M. Contrasting retinoid and thyroid hormone status in differentially-contaminated northern fulmar colonies from the Canada Arctic, Svalbard and the Faroe Island. Environ. Int. 2013, 52:29-40.