Organohalogenated contaminants in domestic cats' plasma in relation to spontaneous acromegaly and type 2 diabetes mellitus: A clue for endocrine disruption in humans?

Environment International

Volumn 57-58, Issue , 2013, Pages 60-67

  Dirtu, Alin C ^a   Niessen, Stijn J M ^b   Jorens, Philippe G ^a   Covaci, Adrian ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Acromegaly; Cat; Diabetes mellitus; Metabolism; Organohalogenated contaminants; PCBs

Indexed keywords

METABOLISM; METABOLITES; PLASMAS; POLYCHLORINATED BIPHENYLS;

ACROMEGALY; CAT; DIABETES MELLITUS; ORGANOCHLORINE PESTICIDES; PCBS; POLYBROMINATED DIPHENYL ETHER (PBDES); POLYCHLORINATED BIPHENYL (PCBS); TYPE 2 DIABETES MELLITUS;

ORGANIC POLLUTANTS;

ESTROGEN; ORGANOCHLORINE PESTICIDE; ORGANOHALOGEN DERIVATIVE; POLYBROMINATED DIPHENYL ETHER; POLYCHLORINATED BIPHENYL; XENOBIOTIC AGENT;

BIOACCUMULATION; CHEMICAL POLLUTANT; ENDOCRINE DISRUPTOR; FELID; METABOLISM; ORGANIC POLLUTANT; ORGANOHALOGEN; PCB; PLASMA; POLLUTION EXPOSURE;

ACROMEGALY; ARTICLE; BLOOD LEVEL; CARCINOGENESIS; CAT; CONTAMINATION; CONTROLLED STUDY; DOMESTIC ANIMAL; ENDOCRINE DISEASE; ENDOCRINE DISRUPTION; FEMALE; HYDROXYLATION; HYPOPHYSIS TUMOR; MALE; METABOLITE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; SPECIES DIFFERENCE;

EID: 84877805266     PISSN: 01604120     EISSN: 18736750     Source Type: Journal    
DOI: 10.1016/j.envint.2013.04.004     Document Type: Article

References (59)

1. Addinsoft XLStat-Pro 2012, version 2012.6.08, 28 West 27th Street, Suite 503, New York, NY 10001, United States of America.
2. Ali N., Malik R.N., Mehdi T., Eqani S.A.M.A.S., Javeed A., Neels H. Organohalogenated contaminants (OHCs) in the serum and hair of pet cats and dogs: biosentinels of indoor pollution. Sci Total Environ 2013, 449:29-36.
3. AMAP (The Arctic Monitoring and Assessment Program) Ring Test Institute National de Sauté Publique Quebéc, Centre de Toxicologie, Reports 2012 2012.
4. Bennett N. Monitoring techniques for diabetes mellitus in the dog and the cat. Clin Tech Small Anim Pract 2002, 17:65-69.
5. Bräuner E.V., Mayer P., Gunnarsen L., Vorkamp K., Raaschou-Nielsen O. Occurrence of organochlorine pesticides in indoor dust. J Environ Monit 2011, 13:522-526.
6. Dirtu A.C., Covaci A. Estimation of daily intake of organohalogenated contaminants from food consumption and indoor dust ingestion in Romania. Environ Sci Technol 2010, 44:6297-6304.
7. Dirtu A.C., Jaspers V.L.B., Cernat R., Neels H., Covaci A. Distribution of PCBs, their hydroxylated metabolites, and other phenolic contaminants in human serum from two European countries. Environ Sci Technol 2010, 44:2876-2883.
8. Dirtu A.C., Ali N., Van den Eede N., Neels H., Covaci A. Country specific comparison for profile of chlorinated, brominated and phosphate organic contaminants in indoor dust. Case study for Eastern Romania, 2010. Environ Int 2012, 49:1-8.
9. Dye J.A., Venier M., Zhu L., Ward C.R., Hites R.A., Birnbaum L.S. Elevated PBDE levels in pet cats: sentinels for humans?. Environ Sci Technol 2007, 41:6350-6356.
10. Erratico C.A., Moffatt S.C., Bandiera S.M. Comparative oxidative metabolism of BDE-47 and BDE-99 by rat hepatic microsomes. Toxicol Sci 2011, 123:37-47.
11. Erratico C.A., Szeitz A., Bandiera S.M. Oxidative metabolism of BDE-99 by human liver microsomes: predominant role of CYP2B6. Toxicol Sci 2012, 129:280-292.
12. Forcada Y., Holder A., Jepson R., Church D., Catchpole B. A missense mutation in the coding sequence of MC4R (MC4R:C.92 C>T) is associated with diabetes mellitus in DSH cats. J Vet Intern Med 2011, 25:681-682.
13. Frederiksen M., Vorkamp K., Thomsen M., Knudsen L.E. Human internal and external exposure to PBDEs-a review of levels and sources. Int J Hyg Environ Health 2009, 212:109-134.
14. Garcia M.M., Kapcala L.P. Growth of a microprolactinoma to a macroprolactinoma during estrogen therapy. J Endocrinol Invest 1995, 18:450-455.
15. Gerber H., Peter H., Ferguson D.C., Peterson M.E. Etiopathology of feline toxic nodular Goiter. Vet Clin North Am Small Anim Pract 1994, 24:541-565.
16. Gooren L.J.G., Assies J., Asscheman H., de Slegte R., van Kessel H. Estrogen-induced prolactinoma in a man. J Clin Endocrinol Metab 1988, 66:444-446.
17. Guo W.H., Park J.S., Wang Y.Z., Gardner S., Baek C., Petreas M., et al. High polybrominated diphenyl ether levels in California house cats: house dust a primary source?. Environ Toxicol Chem 2012, 31:301-306.
18. Harley K.G., Marks A.R., Chevrier J., Bradman A., Sjödin A., Eskenazi B. PBDE concentrations in women's serum and fecundability. Environ Health Perspect 2010, 118:699-704.
19. Harrad S., Ibarra C., Diamond M., Melymuk L., Robson M., Douwes J., et al. Polybrominated diphenyl ethers in domestic indoor dust from Canada, New Zealand, United Kingdom and United States. Environ Int 2008, 34:232-238.
20. Hectors T.L., Vanparys C., van der Ven K., Martens G.A., Jorens P.G., Van Gaal L.F., et al. Environmental pollutants and type 2 diabetes: a review of mechanisms that can disrupt beta cell function. Diabetologia 2011, 54:1273-1290.
21. Ishibashi M., Yamaji T. Effects of hypophysiotropic factors on growth-hormone and prolactin secretion from somatotroph adenomas in culture. J Clin Endocrinol Metab 1985, 60:985-993.
22. Jakobsson K., Fang J., Athanasiadou M., Rignell-Hydbom A., Bergman A. Polybrominated diphenyl ethers in maternal serum, umbilical cord serum, colostrum and mature breast milk. Insights from a pilot study and the literature. Environ Int 2012, 47:121-130.
23. Jeng Y.J., Watson C.S. Combinations of physiologic estrogens with xenestrogens alter ERK phosphorylation profiles in rat pituitary cells. Environ Health Perspect 2011, 119:104-112.
24. Johnson-Restrepo B., Kannan K. An assessment of sources and pathways of human exposure to polybrominated diphenyl ethers in the United States. Chemosphere 2009, 76:542-548.
25. Jones-Otazo A.H., Clarke J.P., Diamond M.L., Archbold J.A., Ferguson G., Harner T., et al. Is house dust the missing exposure pathway for PBDEs? An analysis of the urban fate and human exposure to PBDEs. Environ Sci Technol 2005, 39:5121-5130.
26. Jones-Otazo A.H., Maguire M.L., Griffin J.L. Environmental pollution and diabetes: a neglected association. Lancet 2008, 371:287-288.
27. Letcher R.J., Klasson-Wehler E., Bergman Å. Methyl sulfone and hydroxylated metabolites of polychlorinated biphenyls. The Handbook of Environmental Chemistry, Vol 3, Part K 2000, 315-359. Springer-Verlag, Berlin-Heidelberg. J. Paasivirta (Ed.).
28. Liem A.K.D., Furst P., Rappe C. Exposure of populations to dioxins and related compounds. Food Addit Contam 2000, 17:241-259.
29. Lloyd R.V. Estrogen-induced hyperplastia and neoplastia in the rat anterior-pituitary gland-an immunohistochemical study. Am J Pathol 1983, 113:198-206.
30. Löfstrand K., Athanassiadis I., Bergman Å., Asplund L. 6-Hydroxylated-2,2',4,4'-tetrabromodiphenyl ether in herring (Clupea harengus) plasma from the Baltic Sea. Organohalogen Compd 2008, 70:1625-1628.
31. Löfstrand K., Liu X., Lindqvist D., Jensen S., Asplund L. Seasonal variations of hydroxylated and methoxylated brominated diphenyl ethers in blue mussels from the Baltic Sea. Chemosphere 2011, 84:527-532.
32. Lorber M. Exposure of Americans to polybrominated diphenyl ethers. J Expo Sci Environ Epidemiol 2008, 18:2-19.
33. Meijer L., Weiss J., Van Velzen M., Brouwer A., Bergman Å., Sauerf P.J.J. Serum concentrations of neutral and phenolic organohalogens in pregnant women and some of their infants in the Netherlands. Environ Sci Technol 2008, 42:3428-3433.
34. Mensching D.A., Slater M., Scott J.W., Ferguson D.C., Beasley V.R. The feline thyroid gland: a model for endocrine disruption by polybrominated diphenyl ethers (PBDEs)?. J Toxicol Environ Health A 2012, 75:201-212.
35. Mizukawa H., Nomiyama K., Nakatsu S., Yachimori S., Hayashi T., Tashiro Y., et al. Species-specific differences in the accumulation features of organohalogen contaminants and their metabolites in the blood of Japanese terrestrial mammals. Environ Pollut 2013, 174:28-37.
36. Nguyen L.Q., Arseven O.K., Gerber H., Stein B.S., Jameson J.L., Kopp P. Cloning of the cat TSH receptor and evidence against an autoimmune etiology of feline hyperthyroidism. Endocrinology 2002, 143:395-402.
37. Niessen S.J.M. Feline acromegaly: an essential differential diagnosis for the difficult diabetic. J Feline Med Surg 2010, 12:15-23.
38. Niessen S.J.M., Petrie G., Gaudiano F., Khalid M., Smyth J.B., Mahoney P., et al. Feline acromegaly: an underdiagnosed endocrinopathy?. J Vet Intern Med 2007, 21:899-905.
39. Norrgran J., Jones B., Lindquist N.G., Bergman Å. Decabromobiphenyl, polybrominated diphenyl ethers, and brominated phenolic compounds in serum of cats diagnosed with the endocrine disease feline hyperthyroidism source. Arch Environ Contam Toxicol 2012, 63:161-168.
40. Olczak J., Jones B.R., Pfeiffer D.U., Squires R.A., Morris R.S., Markwell P.J. Multivariate analysis of risk factors for feline hyperthyroidism in New Zealand. N Z Vet J 2005, 523:53-58.
41. Osto M., Zini E., Reusch C.E., Lutz T.A. Diabetes from humans to cats. Gen Comp Endocrinol 2012, [Online 12 December 2012]. 10.1016/j.ygcen.2012.11.019.
42. Prior J.C., Cox T.A., Fairholm D., Kostashuk E., Nugent R. Testosterone-related exacerbation of a prolactin-producing macroadenoma-possible role for estrogen. J Clin Endocrinol Metab 1987, 64:391-394.
43. Ren X.M., Guo L.H. Assessment of the binding of hydroxylated polybrominated diphenyl ethers to thyroid hormone transport proteins using a site-specific fluorescence probe. Environ Sci Technol 2012, 46:4633-4640.
44. Sadoul J.L., Thyss A., Freychet P. Invasive mixed growth-hormone prolactin secreting pituitary-tumor-complete shrinking by ocreotide and bromocriptine, and lack of tumor-growth relapse 20 months after ocreotide withdrawal. Acta Endocrinol 1992, 126:179-183.
45. Santillo D., Labunska I., Davidson H., Johnston P., Strutt M., Knowles O. Consuming chemicals: hazardous chemicals in house dust as an indicator of chemical exposure in the home: part I- UK. Greenpeace Research Laboratories Technical Note 01/2003 2003.
46. Scarlett J.M., Moise N.S., Rayl J. Feline hyperthyroidism-a descriptive and case-control study. Prev Vet Med 1988, 6:295-308.
47. Sierra-Santoyo A., Hernandez M., Albores A., Cebrian M.E. DDT increases hepatic testosterone metabolism in rats. Arch Toxicol 2005, 79:7-12.
48. Sjödin A., Jones R.S., Focant J.F., Lapeza C., Wang R.Y., McGahee E.E., et al. Retrospective time-trend study of polybrominated diphenyl ether and polybrominated and polychlorinated biphenyl levels in human serum from the United States. Environ Health Perspect 2004, 112:654-658.
49. Stapleton H.M., Dodder N.G., Offenberg J.H., Schantz M.M., Wise S.A. Polybrominated diphenyl ethers in house dust and clothes dryer lint. Environ Sci Technol 2005, 39:925-931.
50. Stapleton H.M., Eagle S., Sjödin A., Webster T.F. Serum PBDEs in a North Carolina toddler cohort: associations with handwipes, house dust, and socioeconomic variables. Environ Health Perspect 2012, 120:1049-1054.
51. Steinmetz R., Brown N.G., Allen D.L., Bigsby R.M., Ben-Jonathan N. The environmental estrogen bisphenol A stimulates prolactin release in vitro and in vivo. Endocrinology 1977, 138:1780-1786.
52. Thomas G.O., Wilkinson M., Hodson S., Jones K.C. Organohalogen chemicals in human blood from the United Kingdom. Environ Pollut 2006, 141:30-41.
53. To-Figueras J., Sala M., Otero R., Barrot C., Santiago-Silva M., Rodamilans M., et al. Metabolism of hexachlorobenzene in humans: association between serum levels and urinary metabolites in a highly exposed population. Environ Health Perspect 1997, 105:78-83.
54. US EPA (United States Environmental Protection Agency) Integrated Risk Information System (IRIS) database Available at URL:, [accessed December 2012]. http://www.epa.gov/ncea/iris/subst/2008.
55. Van den Berg K.J. Interaction of chlorinated phenols with thyroxine binding sites of human transthyretin, albumin and thyroid binding globulin. Chem Biol Interact 1990, 76:63-75.
56. Vijayakumar A., Novosyadlyy R., Wu Y., Yakar S., LeRoith D. Biological effects of growth hormone on carbohydrate and lipid metabolism. Growth Hormon IGF Res 2010, 20:1-7.
57. Voorspoels S., Covaci A., Maervoet J., Schepens P. Relationship between age and levels of organochlorine contaminants in human serum of a Belgian population. Bull Environ Contam Toxicol 2002, 69:22-29.
58. Watkins D.J., McClean M.D., Fraser A.J., Weinberg J., Stapleton H.M., Sjödin A., et al. Exposure to PBDEs in the office environment: evaluating the relationships between dust, handwipes, and serum. Environ Health Perspect 2011, 119:1247-1252.
59. Waxman D.J., O'Connor C. Growth hormone regulation of sex-dependent liver gene expression. Mol Endocrinol 2006, 20:2613-2629.