Canine toys and training devices as sources of exposure to phthalates and bisphenol A: Quantitation of chemicals in leachate and in vitro screening for endocrine activity

Chemosphere

Volumn 93, Issue 10, 2013, Pages 2245-2253

  Wooten, Kimberly J ^a   Smith, Philip N ^a  

^a TEXAS TECH UNIVERSITY   (United States)

Author keywords

Bisphenol A; Dogs; Pet health; Phthalates; Toys

Indexed keywords

CHEMICALS; ELASTOMERS; ENDOCRINE DISRUPTERS; ENDOCRINOLOGY; LEACHING; PHENOLS;

BIS-PHENOL A; DI-2-ETHYLHEXYL PHTHALATE; DOGS; ENDOCRINE DISRUPTING CHEMICALS; ENVIRONMENTAL CHEMICALS; ESTROGENIC ACTIVITIES; PHTHALATES; TOYS;

ESTERS;

4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR; PHTHALIC ACID; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PHTHALIC ACID DIETHYL ESTER; PLASTIC; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

LEACHATE; PHTHALATE; POLLUTION EXPOSURE; SALIVA; TRAINING;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEVICES; DOG; ENDOCRINE FUNCTION; ENVIRONMENTAL EXPOSURE; IMMERSION; LEACHING; LIMIT OF DETECTION; SALIVA; ANALYSIS; ANIMAL; DRUG EFFECTS; ENDOCRINE SYSTEM; RECREATION; RISK ASSESSMENT; STATISTICS AND NUMERICAL DATA; TOXICITY;

CANIS FAMILIARIS;

ANIMALS; BENZHYDRYL COMPOUNDS; DIETHYLHEXYL PHTHALATE; DOGS; ENDOCRINE DISRUPTORS; ENDOCRINE SYSTEM; ENVIRONMENTAL EXPOSURE; PHENOLS; PLAY AND PLAYTHINGS; RISK ASSESSMENT;

EID: 84886953773     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2013.07.075     Document Type: Article

References (59)

1. Altman, P.L., Katz, D.D. (Eds.), 1968. Metabolism; prepared under the auspices of the Committee on Biological Handbooks. Bethesda, MD: Federation of American Societies for Experimental Biology.
2. Banfield Pet Hospital, 2012. State of Pet Health: 2012 Report. Available: www.stateofpethealth.com. (accessed 15.10.12).
3. Ben-Jonathan N., Hugo E.R., Brandenbourg T.D. Effects of bisphenol A on adipokine release from human adipose tissue: implications for the metabolic syndrome. Mol. Cell. Endocrinol. 2009, 304:49-54.
4. Biedermann-Brem S., Biedermann M., Pfenninger S., Bauer M., Altkofer W., Rieger K., Hauri U., Droz C., Grob K. Plasticizers in PVC toys and childcare products: what succeeds the phthalates?. Chromatographia 2008, 68:227-234.
5. Bouma K., Schakel D.J. Migration of phthalates from PVC toys into saliva simulant by dynamic extraction. Food Addit. Contam. 2002, 19(6):602-610.
6. Bukowski J.A., Wartenberg D. An alternative approach for investigating the carcinogenicity of indoor air pollution: pets as sentinels of environmental cancer risk. Environ. Health Perspect. 1997, 105(12):1312-1319.
7. Christen V., Crettaz P., Oberli-Schrammli A., Fent K. Antiandrogenic activity of phthalate mixtures: validity of concentration addition. Toxicol. Appl. Pharmacol. 2012, 259(2):169-176.
8. Consumer Product Safety Improvement Act of 2008 (CPSIA), 2008. Public Law 110-314.
9. Desvergne B., Feige J.N., Casals-Casas C. PPAR-mediated activity of phthalates: a link to the obesity epidemic?. Mol. Cell. Endocrinol. 2009, 304(1-2):43-48.
10. 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(18):6350-6356.
11. Earls A.O., Axford L.P., Braybrook J.H. Gas chromatography-mass spectrometry determination of the migration of phthalate plasticisers from polyvinyl chloride toys and childcare articles. J. Chromatogr., A 2003, 983:237-246.
12. EWG (Environmental Working Group)., 2008. Polluted Pets. Available: http://www.ewg.org/reports/pets. (accessed 01.10.12).
13. Fabjan E., Hulzebos E., Mennes W., Piersma H. A category approach for reproductive effects of phthalates. Crit. Rev. Toxicol. 2006, 36:695-726.
14. Fisher J.S., Macpherson S., Marchetti N., Sharpe R.M. Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate. Hum. Reprod. 2003, 18(7):1383-1394.
15. Foster P.M.D., Thomas L.V., Cook M.W., Gangolli S.D. Study of the testicular effects and changes in zinc excretion produced by some n-alkyl phthalates in the rat. Toxicol. Appl. Pharmacol. 1980, 54:392-398.
16. Gavazza A., Presciuttini S., Barale R., Lubas G., Gugliucci B. Association between canine malignant lymphoma, living in industrial areas, and use of chemicals by dog owners. J. Vet. Intern. Med. 2001, 15(3):190-195.
17. Gayrard V., Lacroix M.Z., Collet S.H., Viguie C., Bousquet-Melou A., Toutain P.L., Picard-Hagen N. High bioavailability of bisphenol A from sublingual exposure. Environ. Health Perspect. 2013, 10.1289/ehp.1206339.
18. Gioiosa L., Fissore E., Ghirardelli G., Parmigiani S., Palanza P. Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Horm. Behav. 2007, 52(3):307-316.
19. Glickman L.T., Raghavan M., Knapp D.W., Bonney P.L., Dawson M.H. Herbicide exposure and the risk of transitional cell carcinoma of the urinary bladder in Scottish Terriers. J. Am. Vet. Med. Assoc. 2004, 224(8):1290-1297.
20. Grieco V., Riccardi E., Veronesi M.C., Giudice C., Finazzi A. Evidence of testicular dysgenesis syndrome in the dog. Theriogenology 2008, 70(1):53-60.
21. Guo W., Park J.S., Wang Y., Gardner S., Baek C., Petreas M., Hooper K. High polybrominated diphenyl ether levels in California house cats: house dust a primary source?. Environ. Toxicol. Chem. 2012, 31(2):301-306.
22. Hayes H.M., Wilson G.P., Pendergrass T.W., Cox V.S. Canine cryptorchidism and subsequent testicular neoplasia - case-control study with epidemiologic update. Teratology 1985, 32(1):51-56.
23. Howdeshell K.L., Rider C.V., Wilson V.S., Gray L.E. Mechanisms of action of phthalate esters, individually and in combination, to induce abnormal reproductive development in male laboratory rats. Environ. Res. 2008, 108(2):168-176.
24. Hunt P.A., Lawson C., Gieske M., Murdoch B., Smith H., Marre A., Hassold T., VandeVoort C.A. Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(43):17525-17530.
25. Ikeda G.J., Sapienza P.P., Couvillion J.L., Farber T.M., Vanloon E.J. Comparative distribution, excretion and metabolism of di-(2-ethylhexyl) phthalate in rats, dogs and miniature pigs. Food Cosmet. Toxicol. 1980, 18(6):637-642.
26. Kang J.H., Kondo F. Determination of bisphenol A in canned pet foods. Res. Vet. Sci. 2002, 73(2):177-182.
27. Kuiper G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg P., Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139(10):4252-4263.
28. Kunisue T., Nakanishi S., Watanabe M., Abe T., Nakatsu S., Kawauchi S., Sano A., Horii A., Kano Y., Tanabe S. Contamination status and accumulation features of persistent organochlorines in pet dogs and cats from Japan. Environ. Pollut. 2005, 136(3):465-476.
29. Latini G., Verrotti A., De Felice C. Di-2-ethylhexyl phthalate and endocrine disruption: a review. Curr. Drug Targets: Immune Endocr. Metabol. Disord. 2004, 4:37-40.
30. Lavy E., Goldberger D., Friedman M., Steinberg D. PH values and mineral content of saliva in different breeds of dogs. Isr. J. Vet. Med. 2012, 67(4):244-248.
31. Martino-Andrade A.J., Chahoud I. Reproductive toxicity of phthalate esters. Mol. Nutr. Food Res. 2010, 54:148-157.
32. Muller, A.K., Nielsen, E., Ladefoged, O., Dalgaard, M., Hass, U., 2006. Survey of Chemical Substances in Consumer Products No. 74: Evaluation of the health risk to animals playing with phthalates containing toys. (accessed 23.10.12). http://www2.mst.dk/udgiv/publications/2006/87-7052-192-1/pdf/87-7052-194-8.pdf.
33. Munoz-de-Toro M., Markey C.M., Wadia P.R., Luque E.H., Rubin B.S., Sonnenschein C., Soto A.M. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146(9):4138-4147.
34. Niino T., Asakura T., Ishibashi T., Itoh T., Sakai S., Ishiwata H., Yamada T., Onodera S. A simple and reproducible testing method for dialkyl phthalate migration from polyvinyl chloride products into saliva simulant. J. Food Hyg. Soc. Japan 2003, 44(1):13-18.
35. Norrgran J., Jones B., Lindquist N.G., Bergman A. Decabromobiphenyl, polybrominated diphenyl ethers, and brominated phenolic compounds in serum of cats diagnosed with the endocrine disease feline hyperthyroidism. Arch. Environ. Contam. Toxicol. 2012, 63:161-168.
36. Notch E.G., Mayer G.D. Wastewater treatment effluent alters nucleotide excision repair in zebrafish (Danio rerio). Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2009, 150(2):307-313.
37. Perez Alenza M.D., Pena L., del Castillo N., Nieto A.I. Factors influencing the incidence and prognosis of canine mammary tumours. J. Small Anim. Pract. 2000, 41:287-291.
38. Posnack N.G., Swift L.M., Kay M.W., Lee N.H., Sarvazyan N. Phthalate exposure changes the metabolic profile of cardiac muscle cells. Environ. Health Perspect. 2012, 120(9):1243-1251.
39. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., Vandenbergh J.G., Walser-Kuntz D.R., Vom Saal F.S.V. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 2007, 24(2):199-224.
40. Rose R.J., Priston M.J., Rigby-Jones A.E., Sneyd J.R. The effect of temperature on di(2-ethylhexyl) phthalate leaching from PVC infusion sets exposed to lipid emulsions. Anaesthesia 2012, 67:514-520.
41. Rubin B.S., Soto A.M. Bisphenol A: perinatal exposure and body weight. Mol. Cell. Endocrinol. 2009, 304:55-62.
42. Salian S., Doshi T., Vanage G. Perinatal exposure of rats to Bisphenol A affects the fertility of male offspring. Life Sci. 2009, 85(21-22):742-752.
43. Schecter A., Malik N., Hafner D., Smith S., Harris T.R., Paepke O., Birnbaum L. Bisphenol A (BPA) in U.S. food. Environ. Sci. Technol. 2010, 44:9425-9430.
44. Schmidt J.S., Schaedlich K., Fiandanese N., Pocar P., Fischer B. Effects of di(2-ethylhexyl) phthalate (DEHP) on female fertility and adipogenesis in C3H/N mice. Environ. Health Perspect. 2012, 120(8):1123-1129.
45. Skakkebaek N.E., Rajpert-De Meyts E., Main K.M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum. Reprod. 2001, 16(5):972-978.
46. Smeets-Peters M., Watson T., Minekus M., Havenaar R. A review of the physiology of the canine digestive tract related to the development of in vitro systems. Nutr. Res. Rev. 1998, 11:45-69.
47. Springer R., Labunska I., Santillo D., Johnston P., Siddorn J., Stephenson A. Concentrations of phthalate esters and identification of other additives in PVC children's toys. Environ. Sci. Pollut. Res. 2000, 7(1):27-36.
48. Steiner I., Scharf L., Fiala F., Washuttl J. Migration of di-(2-ethylhexyl) phthalate from PVC child articles into saliva and saliva simulant. Food Addit. Contam. 1998, 15(7):812-817.
49. Storelli M.M., Storelli A., Barone G., Franchini D. Accumulation of polychlorinated biphenyls and organochlorine pesticide in pet cats and dogs: assessment of toxicological status. Sci. Total Environ. 2009, 408(1):64-68.
50. Takashima-Uebelhoer B.B., Barber L.G., Zagarins S.E., Procter-Gray E., Gollenberg A.L., Moore A.S., Bertone-Johnson E.R. Household chemical exposures and the risk of canine malignant lymphoma, a model for human non-Hodgkin's lymphoma. Environ. Res. 2012, 112:171-176.
51. Takehisa H., Naoko E., Masahiko S., Katsuhide T., Moriyuki O., Keisog S., Mutsuko T., Kenji K., Shin'ichiro N., Toshio O. Release behavior of diethylhexyl phthalate from the polyvinyl-chloride tubing used for intravenous administration and the plasticized PVC membrane. Int. J. Pharm. 2005, 297:30-37.
52. Takeuchi S., Iida M., Kobayashi S., Jin K., Matsuda T., Kojima H. Differential effects of phthalate esters on transcriptional activities via human estrogen receptors alpha and beta, and androgen receptor. Toxicology 2005, 210(2-3):223-233.
53. Taylor J.A., Vom Saal F.S., Welshons W.V., Drury B., Rottinghaus G., Hunt P.A., Toutain P.L., Laffont C.M., VandeVoort C.A. Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ. Health Perspect. 2011, 119(4):422-430.
54. US EPA (United States Environmental Protection Agency), 2008. Child-Specific Exposure Factors Handbook. Available: (accessed 1.02.13). http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=199243#Download.
55. US E.P.A. Endocrine disruptor screening program (EDSP); Announcing the availability of the Tier 1 screening battery and related test guidelines. Notice. Fed. Reg. 2009, 74:54416-54422.
56. U.S. Food and Drug Administration (US FDA), 2012. Indirect Food Additives: Polymers. Final Rule. Fed Reg 77, 41899-41902.
57. Venier M., Hites R.A. Flame retardants in the serum of pet dogs and their food. Environ. Sci. Technol. 2011, 45:4602-4608.
58. Wilson V.S., Bobseine K., Lambright C.R., Gray L.E. A novel cell line, MDA-kb2, that stable expresses an androgen- and glucocorticoid-responsive reporter for the detection of hormone receptor agonists and antagonists. Toxicol. Sci. 2002, 66:69-81.
59. Xu L.C., Sun H., Chen J.F., Bian Q., Qian J., Song L., Wang X.R. Evaluation of androgen receptor transcriptional activities of bisphenol A, octylphenol and nonylphenol in vitro. Toxicology 2005, 216:197-203.