Polybrominated diphenyl ether (PBDE) neurotoxicity: a systematic review and meta-analysis of animal evidence

References

• Biesemeier, J. A., M. J. Beck, H. Silberberg, N. R. Myers, J. M. Ariano, A. Radovsky, L. Freshwater, D. W. Sved, S. Jacobi, D. G. Stump, M. L. Hardy, and T. Stedeford. 2011. An oral developmental neurotoxicity study of decabromodiphenyl ether (DecaBDE) in rats. Birth Defects Research Part B Developmental and Reproductive Toxicology 92:17–35. doi:10.1002/bdrb.20280.
   PubMedGoogle Scholar
• Blanco, J., M. Mulero, L. Heredia, A. Pujol, J. L. Domingo, and D. J. Sánchez. 2013. Perinatal exposure to BDE-99 causes learning disorders and decreases serum thyroid hormone levels and BDNF gene expression in hippocampus in rat offspring. Toxicology 308:122–28. doi:10.1016/j.tox.2013.03.010.
   PubMed Web of Science ®Google Scholar
• Bowers, W. J., P. M. Wall, J. S. Nakai, A. Yagminas, M. Wade, and N. Li. 2015. Behavioral and thyroid effects of in utero and lactational exposure of Sprague-Dawley rats to the polybrominated diphenyl ether mixture DE71. Neurotoxicology and Teratology 52:127–42. doi:10.1016/j.ntt.2015.08.002.
   PubMed Web of Science ®Google Scholar
• Bradman, A., R. Castorina, A. Sjödin, L. Fenster, R. S. Jones, K. G. Harley, J. Chevrier, N. T. Holland, and B. Eskenazi. 2012. Factors associated with serum polybrominated diphenyl ether (PBDE) levels among school-age children in the CHAMACOS cohort. Environmental Science and Technology 46:7373–81. doi:10.1021/es3003487.
   PubMed Web of Science ®Google Scholar
• Bramwell, L., S. V. Glinianaia, J. Rankin, M. Rose, A. Fernandes, S. Harrad, and T. Pless-Mulolli. 2016. Associations between human exposure to polybrominated diphenyl ether flame retardants via diet and indoor dust, and internal dose: A systematic review. Environment International 92-93:680–94. doi:10.1016/j.envint.2016.02.017.
   PubMed Web of Science ®Google Scholar
• Buratovic, S., H. Viberg, A. Fredriksson, and P. Eriksson. 2014. Developmental exposure to the polybrominated diphenyl ether PBDE 209: Neurobehavioural and neuroprotein analysis in adult male and female mice. Environmental Toxicology and Pharmacology 38:570–85. doi:10.1016/j.etap.2014.08.010.
   PubMed Web of Science ®Google Scholar
• Butryn, D. M., M. S. Gross, L. H. Chi, A. Schecter, J. R. Olson, and D. S. Aga. 2015. “One-shot” analysis of polybrominated diphenyl ethers and their hydroxylated and methoxylated analogs in human breast milk and serum using gas chromatography-tandem mass spectrometry. Analytica Chimica Acta 892:140–47. doi:10.1016/j.aca.2015.08.026.
   PubMed Web of Science ®Google Scholar
• Cantón, R. F., D. E. Scholten, G. Marsh, P. C. de Jong, and M. van Den Berg. 2008. Inhibition of human placental aromatase activity by hydroxylated polybrominated diphenyl ethers (OH-PBDEs). Toxicology and Applied Pharmacology 227:68–75. doi:10.1016/j.taap.2007.09.025.
   PubMed Web of Science ®Google Scholar
• Cantón, R. F., J. T. Sanderson, R. J. Letcher, A. Bergman, and M. van Den Berg. 2005. Inhibition and induction of aromatase (CYP19) activity by brominated flame retardants in H295R human adrenocortical carcinoma cells. Toxicological Sciences 88:447–55. doi:10.1093/toxsci/kfi325.
   PubMed Web of Science ®Google Scholar
• Ceccatelli, R., O. Faass, M. Schlumpf, and W. Lichtensteiger. 2006. Gene expression and estrogen sensitivity in rat uterus after developmental exposure to the polybrominated diphenylether PBDE 99 and PCB. Toxicology 220:104–16. doi:10.1016/j.tox.2005.12.004.
   PubMed Web of Science ®Google Scholar
• Chen, A., K. Yolton, S. A. Rauch, G. M. Webster, R. Hornung, A. Sjödin, K. N. Dietrich, and B. P. Lanphear. 2014a. Prenatal polybrominated diphenyl ether exposures and neurodevelopment in U.S. children through 5 years of age: The HOME study. Environmental Health Perspectives 122:856–62. doi:10.1289/ehp.1307562.
   PubMed Web of Science ®Google Scholar
• Chen, L. J., E. H. Lebetkin, J. M. Sanders, and L. T. Burka. 2006. Metabolism and disposition of 2,2ʹ,4,4ʹ,5-pentabromodiphenyl ether (BDE99) following a single or repeated administration to rats or mice. Xenobiotica 36:515–34. doi:10.1080/00498250600674477.
   PubMed Web of Science ®Google Scholar
• Chen, Y. H., Z. H. Li, Y. Tan, C. F. Zhang, J. S. Chen, F. He, Y. H. Yu, and D. J. Chen. 2014b. Prenatal exposure to decabrominated diphenyl ether impairs learning ability by altering neural stem cell viability, apoptosis, and differentiation in rat hippocampus. Human and Experimental Toxicology. Feb 24. Epub ahead of print. doi:10.1177/0960327113509661.
   Google Scholar
• Cheng, J., J. Gu, J. Ma, X. Chen, M. Zhang, and W. Wang. 2009. Neurobehavioural effects, redox responses and tissue distribution in rat offspring developmental exposure to BDE-99. Chemosphere 75:963–68. doi:10.1016/j.chemosphere.2009.01.004.
   PubMed Web of Science ®Google Scholar
• Cornell, J. E., C. D. Mulrow, R. Localio, C. B. Stack, A. R. Meibohm, E. Guallar, and S. N. Goodman. 2014. Random effects meta-analysis of inconsistent effects: A time for change. Annals of Internal Medicine 160:267–70. doi:10.7326/M13-2886.
   PubMed Web of Science ®Google Scholar
• Costa, L. G., C. Pellacani, K. Dao, T. J. Kavanagh, and P. J. Roque. 2015. The brominated flame retardant BDE-47 causes oxidative stress and apoptotic cell death in vitro and in vivo in mice. Neurotoxicology 48:68–76. doi:10.1016/j.neuro.2015.03.008.
   PubMed Web of Science ®Google Scholar
• Cowens, K. R., S. Simpson, W. K. Thomas, and G. B. Carey. 2015. Polybrominated diphenyl ether (PBDE)-induced suppression of phosphoenolpyruvate carboxykinase (PEPCK) decreases hepatic glyceroneogenesis and disrupts hepatic lipid homeostasis. Journal of Toxicology and Environmental Health A 78:1437–49. doi:10.1080/15287394.2015.1098580.
   PubMed Web of Science ®Google Scholar
• Darnerud, P. O., M. Aune, L. Larsson, and S. Hallgren. 2007. Plasma PBDE and thyroxine levels in rats exposed to Bromkal or BDE-47. Chemosphere 67:S386–S392. doi:10.1016/j.chemosphere.2006.05.133.
   PubMed Web of Science ®Google Scholar
• Darnerud, P. O., and T. Sinjari. 1996. Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroxine and TSH blood levels in rats and mice. Organohalogen Compounds 29:316–19. PMID: 11482517.
   Google Scholar
• de-Miranda, A. S., S. N. Kuriyama, C. S. da-Silva, M. S. do-Nascimento, T. E. Parente, and F. J. Paumgartten. 2016. Thyroid hormone disruption and cognitive impairment in rats exposed to PBDE during postnatal development. Reproductive Toxicology 63:114–24. doi:10.1016/j.reprotox.2016.05.017.
   PubMed Web of Science ®Google Scholar
• Dingemans, M. M., M. van Den Berg, and R. H. Westerink. 2011. Neurotoxicity of brominated flame retardants: (In)direct effects of parent and hydroxylated polybrominated diphenyl ethers on the (developing) nervous system. Environmental Health Perspectives 119:900–07. doi:10.1289/ehp.1003035.
   PubMed Web of Science ®Google Scholar
• Dingemans, M.M., M. van den Berg, and R.H. Westerink. 2011. Neurotoxicity of brominated flame retardants: (in)direct effects of parent and hydroxylated polybrominated diphenyl ethers on the (developing) nervous system. Environmental Health Perspectives 119 (7):900-907. doi: 10.1289/ehp.1003035.
   PubMed Web of Science ®Google Scholar
• Driscoll, L. L., A. M. Gibson, and A. Hieb. 2009. Chronic postnatal DE-71 exposure: Effects on learning, attention and thyroxine levels. Neurotoxicology and Teratology 31:76–84. doi:10.1016/j.ntt.2008.11.003.
   PubMed Web of Science ®Google Scholar
• Driscoll, L. L., J. Kaplan, E. Bucuvalas, H. Allen, J. Kraut, and J. Fitzpatrick. 2012. Acute postnatal exposure to the pentaBDE commercial mixture DE-71 at 5 or 15 mg/kg/day does not produce learning or attention deficits in rats. Neurotoxicology and Teratology 34:20–26. doi:10.1016/j.ntt.2011.10.002.
   PubMed Web of Science ®Google Scholar
• Dufault, C., G. Poles, and L. L. Driscoll. 2005. Brief postnatal PBDE exposure alters learning and the cholinergic modulation of attention in rats. Toxicological Sciences 88:172–80. doi:10.1093/toxsci/kfi285.
   PubMed Web of Science ®Google Scholar
• EFSA (European Food Safety Authority). 2011. Scientific opinion on polybrominated diphenyl ethers (PBDEs) in food. EFSA Journal 9: 2156.
   Google Scholar
• EPA (U.S. Environmental Protection Agency). 2010. An Exposure Assessment of Polybrominated Diphenyl Ethers. EPA/600/R-08/086F. National Center for Environmental Assessment, Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC [online]. Available at: https://cfpub.epa.gov/ncea/risk/recordisplay.cfm?deid=210404 [accessed May 10, 2018].
   Google Scholar
• Eriksson, P., E. Jakobsson, and A. Fredriksson. 2001. Brominated flame retardants: A novel class of developmental neurotoxicants in our environment?. Environmental Health Perspectives 109:903–08. PMCID: PMC1240439. doi:10.1289/ehp.01109903.
   PubMed Web of Science ®Google Scholar
• Faass, O., R. Ceccatelli, M. Schlumpf, and W. Lichtensteiger. 2013. Developmental effects of perinatal exposure to pbde and pbc on gene expression in sexually dimorphic rat brain regions and female sexual behavior. General and Comparative Endocrinology 188:232-241. doi: 10.1016/j.ygcen.2013.04.008.
   PubMed Web of Science ®Google Scholar
• Fayiga, A., and M. Ipinmoroti. 2017. Detection of toxic flame retardants in aquatic and terrestrial environment: An emerging global concern. Electronic Journal of Biology 13:38–55.
   Google Scholar
• Fischer, C., A. Fredriksson, and P. Eriksson. 2008. Coexposure of neonatal mice to a flame retardant PBDE 99 (2, 2ʹ,4, 4ʹ,5-pentabromodiphenyl ether) and methyl mercury enhances developmental neurotoxic defects. Toxicological Sciences 101:275–85. doi:10.1093/toxsci/kfm271.
   PubMed Web of Science ®Google Scholar
• Fowles, J. R., A. Fairbrother, L. Baecher-Steppan, and N. I. Kerkvliet. 1994. Immunologic and endocrine effects of the flame retardant pentabromodiphenyl ether (DE-71) in C57BL/6J mice. Toxicology 86:49–61. PMID: 8134923.
   PubMed Web of Science ®Google Scholar
• Gassmann, K., T. Schreiber, M. M. Dingemans, G. Krause, C. Roderigo, S. Giersiefer, J. Schuwald, M. Moor, K. Unfried, K. Bergman, R. H. Weterink, C. R. Rose, and E. Fritsche. 2014. BDE-47 and 6-oh-BDE-47 modulate calcium homeostasis in primary fetal human neural progenitor cells via ryanodine receptor-independent mechanisms. Archives of Toxicology 88:1537–48. doi:10.1007/s00204-014-1217-7.
   PubMed Web of Science ®Google Scholar
• Geyer, H. J., K. W. Schramm, P. O. Darnerud, M. Aune, E. A. Feicht, K. W. Fried, B. Henkelmann, D. Lenoir, P. Schmid, and T. A. McDonald. 2004. Terminal elimination half-lives of the brominated flame retardants TBBPA, HBCD, and lower brominated PBDEs in humans. Organohalogen Compounds 66:3820–25.
   Google Scholar
• Ghassabian, A., H. El Marroun, R. P. Peeters, V. W. Jaddoe, A. Hofman, F. C. Verhulst, H. Tiemeier, and T. White. 2014. Downstream effects of maternal hypothroxinemia in early pregnancy: Nonverbal IQ and brain morphology in school-age children. Journal of Clinical Endocrinology and Metabolism 99:2383–90. doi:10.1210/jc.2013-4281.
   PubMed Web of Science ®Google Scholar
• Gill, S., Y. Hou, N. Li, O. Pulido, and W. Bowers. 2016. Developmental neurotoxicity of polybrominated diphenyl ethers mixture de71 in Sprague-Dawley rats. Journal of Toxicology and Environmental Health A 79:482–93. doi:10.1080/15287394.2016.1182001.
   PubMed Web of Science ®Google Scholar
• Guyatt, G. H., A. D. Oxman, E. A. Akl, R. Kunz, G. Vist, J. Brozek, S. Norris, Y. Falck-Ytter, P. Glasziou, H. Debeer, R. Jaeschke, D. Rind, J. Meerpohl, P. Dahm, and H. J. Schunemann. 2011. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. Journal of Clinical Epidemiology 64:383–94. doi:10.1016/j.jclinepi.2010.04.026.
   PubMed Web of Science ®Google Scholar
• He, P., A. Wang, Q. Niu, L. Guo, T. Xia, and X. Chen. 2011. Toxic effect of PBDE-47 on thyroid development, learning, and memory, and the interaction between PBDE-47 and PCB153 that enhances toxicity in rats. Toxicology and Industrial Health 27:279–88. doi:10.1177/0748233710387002.
   PubMed Web of Science ®Google Scholar
• He, P., A. G. Wang, T. Xia, P. Gao, Q. Niu, L. J. Guo, and X. M. Chen. 2009. Mechanisms underlying the developmental neurotoxic effect of PBDE-47 and the enhanced toxicity associated with its combination with PCB153 in rats. Neurotoxicology 30:1088–95. doi:10.1016/j.neuro.2009.06.005.
   PubMed Web of Science ®Google Scholar
• He, Y. M. B., R. M. Murphy, M. H. Yu, L. M. Hecker, J. P. Giesy, R. S. Wu, and P. K. Lam. 2008. Effects of 20 PBDE metabolites on steroidogenesis in the H295R cell line. Toxicology Letters 176:230–38. doi:10.1016/j.toxlet.2007.12.001.
   PubMed Web of Science ®Google Scholar
• Hedges, L. V., J. Gurevitch, and P. S. Curtis. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–56. doi:10.2307/177062.
   Web of Science ®Google Scholar
• Higgins, J. P. T., and S. Green, eds. 2011. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration [online]. Available: www.handbook.cochrane.org [accessed May 10, 2018]
   Google Scholar
• Ho, K. L., M. S. Yau, M. B. Murphy, Y. Wan, B. M. Fong, S. Tam, J. P. Giesy, K. S. Leung, and M. H. Lam. 2015. Urinary bromophenol glucuronide and sulfate conjugates: Potential human exposure molecular markers for polybrominated diphenyl ethers. Chemosphere 133:6–12. doi:10.1016/j.chemosphere.2015.03.003.
   PubMed Web of Science ®Google Scholar
• Horn, S., and H. Heuer. 2010. Thyroid hormone action during brain development: More questions than answers. Molecular and Cellular Endocrinology 315:19–26. doi:10.1016/j.mce.2009.09.008.
   PubMed Web of Science ®Google Scholar
• IOM (Institute of Medicine). 2011. Finding What Works in Health Care: Standards for Systematic Review. Washington, DC: The National Academies Press.
   Google Scholar
• Karpeta, A., J. Barc, A. Ptak, and E. L. Gregoraszczuk. 2013. The 2,2ʹ,4,4ʹ-tetrabromodiphenyl ether hydroxylated metabolites 5-OH-BDE-47 and 6-OH-BDE-47 stimulate estradiol secretion in the ovary by activating aromatase expression. Toxicology 305:65–70. doi:10.1016/j.tox.2012.10.021.
   PubMed Web of Science ®Google Scholar
• Kilkenny, C., W. J. Browne, I. C. Cuthill, M. Emerson, and D. G. Altman. 2010. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biology 8:e1000412. doi:10.1371/journal.pbio.1000412.
   PubMed Web of Science ®Google Scholar
• Kim, K. H., D. D. Bose, A. Ghogha, J. Riehl, R. Zhang, C. D. Barnhart, P. J. Lein, and I. N. Pessah. 2011. Para- and ortho-substitutions are key determinants of polybrominated diphenyl ether activity toward ryanodine receptors and neurotoxicity. Environmental Health Perspectives 119:519–26. doi:10.1289/ehp.1002728.
   PubMed Web of Science ®Google Scholar
• Kodavanti, P. R., J. E. Royland, C. Osorio, W. M. Winnik, P. Oritz, L. Pei, R. Ramabhadran, and O. Alzate. 2015. Developmental exposure to a commercial PBDE mixture: Effects on protein networks in the cerebellum and hippocampus of rats. Environmental Health Perspectives 123:428–36. doi:10.1289/ehp.1408504.
   PubMed Web of Science ®Google Scholar
• Koenig, C. M., J. Lango, I. N. Pessah, and R. F. Berman. 2012. Maternal transfer of BDE-47 to offspring and neurobehavioral development in C57BL/6J mice. Neurotoxicology and Teratology 34:571–80. doi:10.1016/j.ntt.2012.09.005.
   PubMed Web of Science ®Google Scholar
• Lajeunesse, M. J. 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92:2049–55. PMID: 22164829.
   PubMed Web of Science ®Google Scholar
• Lam, J., B. Lanphear, D. Bellinger, D. A. Axelrad, J. McPartland, P. Sutton, L. Davidson, N. Daniels, S. Sen, and T. Woodruff. 2017. Developmental PBDE exposure and IQ/ADHD in childhood: A systematic review and meta-analysis. Environmental Health Perspectives 125:086001. doi:10.1289/EHP1632.
   PubMed Web of Science ®Google Scholar
• Lilienthal, H., A. Hack, A. Roth-Härer, S.W. Grande, and C.E. Talsness. 2006. Effects of developmental exposure to 2,2′,4,4′,5-pentabromodiphenyl ether (pbde-99) on sex steroids, sexual development, and sexually dimorphic behavior in rats. Environmental Health Perspectives 114 (2):194-201. doi: 10.1289/ehp.8391.
   PubMed Web of Science ®Google Scholar
• Linares, V., M. Bellés, and J. L. Domingo. 2015. Human exposure to PBDE and critical evaluation of health hazards. Archives of Toxicology 89:335–56. doi:10.1007/s00204-015-1457-1.
   PubMed Web of Science ®Google Scholar
• Llansola, M., M. Hernandez-Viadel, S. Erceg, C. Montoliu, and V. Felipo. 2009. Increasing the function of the glutamate-nitric oxide-cyclic guanosine monophosphate pathway increases the ability to learn a Y-maze task. Journal of Neuroscience Research 87:2351–55. doi:10.1002/jnr.22064.
   PubMed Web of Science ®Google Scholar
• Lorber, M. 2008. Exposure of Americans to polybrominated diphenyl ethers. Journal of Exposure Science and Epidemiology 18:2–19. doi:10.1038/sj.jes.7500572.
   PubMed Web of Science ®Google Scholar
• Meerts, I. A., J. J. Van Zanden, E. A. Luijks, I. Van Leeuwen-Bol, G. Marsh, E. Jakobsson, Å. Bergman, and A. Brouwer. 2000. Potent competitive interactions of some brominated flame retardants and related compounds with human transthyretin in vitro. Toxicological Sciences 56:95–104. PMID: 10869457.
   PubMed Web of Science ®Google Scholar
• Meerts, I. A., R. J. Letcher, S. Hoving, G. Marsh, A. Bergman, J. G. Lemmen, B. van der Burg, and A. Brouwer. 2001. In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PBDEs, and polybrominated bisphenol A compounds. Environmental Health Perspectives 109:399–407. PMCID: PMC1240281. doi:10.1289/ehp.01109399.
   PubMed Web of Science ®Google Scholar
• Mercado-Feliciano, M., and R. M. Bigsby. 2008. Hydroxylated metabolites of the polybrominated diphenyl ether mixture DE-71 are weak estrogen receptor-alpha ligands. Environmental Health Perspectives 116:1315–21. doi:10.1289/ehp.11343.
   PubMed Web of Science ®Google Scholar
• Modesto, T., H. Tiemeier, R. P. Peeters, V. W. Jaddoe, A. Hofman, F. C. Verhulst, and A. Ghassabian. 2015. Maternal mild thyroid hormone insufficiency in early pregnancy and attention-deficit/hyperactivity disorder symptoms in children. JAMA Pediatrics 169:838–45. doi:10.1001/jamapediatrics.2015.0498.
   PubMed Web of Science ®Google Scholar
• NCHS (National Center for Health Statistics). 2007. National Health And nutrition examination survey 2003-2004 [online]. Available: https://wwwn.cdc.gov/Nchs/Nhanes/2003-2004/L28PBE_C.htm [accessed September 7, 2018].
   Google Scholar
• NASEM (National Academies of Science, Engineering, and Medicine). 2017. Application of Systematic Review Methods in an Overall Strategy for Evaluating Low-Dose Toxicity from Endocrine Active Chemicals. Washington, DC: The National Academies Press.
   Google Scholar
• NTP (National Toxicology Program). 2015. Handbook for Conducting a Literature-Based Health Assessment Using OHAT Approach for Systematic Review and Evidence Integration. Office of Health Assessment and Translation, Division, National Toxicology Program, National Institute of Environmental Health Sciences. January 9, 2015 [online]. Available: http://ntp.niehs.nih.gov/ntp/ohat/pubs/handbookjan2015_508.pdf [accessed September 21, 2015].
   Google Scholar
• Ptak, A., G. Ludewig, H. J. Lehmler, A. K. Wojtowicz, L. W. Robertson, and E. L. Gregoraszczuk. 2005. Comparison of the actions of 4-chlorobiphenyl and its hydroxylated metabolites on estradiol secretion by ovarian follicles in primary cells in culture. Reproductive Toxicology 20:57–64. doi:10.1016/j.reprotox.2004.12.003.
   PubMed Web of Science ®Google Scholar
• Ptak, A., G. Ludewig, M. Kapiszewska, Z. Magnowska, H. J. Lehmler, L. W. Robertson, and E. L. Gregoraszczuk. 2006. Induction of cytochromes P450, caspase-3 and DNA damage by PCB3 and its hydroxylated metabolites in porcine ovary. Toxicology Letters 166:200–11. doi:10.1016/j.toxlet.2006.07.304.
   PubMed Web of Science ®Google Scholar
• Qiu, X., M. Mercado-Feliciano, R. M. Bigsby, and R. A. Hites. 2007. Measurement of polybrominated diphenyl ethers and metabolites in mouse plasma after exposure to a commercial pentabromodiphenyl ether mixture. Environmental Health Perspectives 115:1052–58. doi:10.1289/ehp.10011.
   PubMed Web of Science ®Google Scholar
• Raudenbush, S.W. 2009. Analyzing effect sizes: Random-effects models. Pp. 295-315 in The Handbook of Synthesis Research and Meta-Analysis, 2nd Ed., H. Cooper, L.V. Hedges, and J.C. Valentine, eds. New York: Russell Sage Foundation.
   Google Scholar
• Reverte, I., A. Pujol, J. L. Domingo, and M. T. Colomina. 2014. Thyroid hormones and fear learning but not anxiety are affected in adult apoE transgenic mice exposed postnatally to decabromodiphenyl ether (BDE-209). Physiology and Behavior 133:81–91. doi:10.1016/j.physbeh.2014.05.013.
   PubMed Web of Science ®Google Scholar
• Reverte, I., A. B. Klein, J. L. Domingo, and M. T. Colomina. 2013. Long term effects of murine postnatal exposure to decabromodiphenyl ether (BDE-209) on learning and memory are dependent upon APOE polymorphism and age. Neurotoxicology and Teratology 40:17–27. doi:10.1016/j.ntt.2013.08.003.
   PubMed Web of Science ®Google Scholar
• Rice, D. C., W. D. Thompson, E. A. Reeve, K. D. Onos, M. Assadollahzadeh, and V. P. Markowski. 2009. Behavioral changes in aging but not young mice after neonatal exposure to the polybrominated flame retardant decaBDE. Environmental Health Perspectives 117:1903–11. doi:10.1289/ehp.11814.
   PubMed Web of Science ®Google Scholar
• Rooney, A. A., A. L. Boyles, M. S. Wolfe, J. R. Bucher, and K. A. Thayer. 2014. Systematic review and evidence integration for literature-based environmental health assessments. Environmental Health Perspectives 122:711–18. doi:10.1289/ehp.1307972.
   PubMed Web of Science ®Google Scholar
• Siddiqi, M. A., R. H. Laessig, and K. D. Reed. 2003. Polybrominated diphenyl ethers (PBDEs): New pollutants-old diseases. Clinical Medicine and Research 1:281–90. PMCID: PMC1069057.
   PubMedGoogle Scholar
• Stapleton, H. M., S. M. Kelly, R. Pei, R. J. Letcher, and C. Gunsch. 2009. Metabolism of polybrominated diphenyl ethers (PBDEs) by human hepatocytes in vitro. Environmental Health Perspectives 117:197–202. doi:10.1289/ehp.11807.
   PubMed Web of Science ®Google Scholar
• Staskal, D. F., H. Hakk, D. Bauer, J. J. Diliberto, and L. S. Birnbaum. 2006. Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicological Sciences 94:28–37. doi:10.1093/toxsci/kfl091.
   PubMed Web of Science ®Google Scholar
• Ta, T. A., C. M. Koenig, M. S. Golub, I. N. Pessah, L. Qi, P. A. Aronov, and R. F. Berman. 2011. Bioaccumulation and behavioral effects of 2,2ʹ,4,4ʹ-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice. Neurotoxicology and Teratology 33:393–404. doi:10.1016/j.ntt.2011.02.003.
   PubMed Web of Science ®Google Scholar
• Thuresson, K., P. Höglund, L. Hagmer, A. Sjödin, Å. Bergman, and K. Jakobsson. 2006. Apparent half-lives of hepta- to decabrominated diphenyl ethers in human serum as determined in occupationally exposed workers. Environmental Health Perspectives 114:176–81. PMCID: PMC1367828. doi:10.1289/ehp.8350.
   PubMed Web of Science ®Google Scholar
• Verma, P., P. Singh, and B. S. Gandhi. 2013. Prophylactic efficacy of Bacopa monnieri on decabromodiphenyl ether (PBDE-209)-induced alterations in oxidative status and spatial memory in mice. Asian Journal of Pharmaceutical and Clinical Research 6:242–47.
   Google Scholar
• Verma, P., P. Singh, and B. S. Gandhi. 2014. Neuromodulatory role of Bacopa monnieri on oxidative stress induced by postnatal exposure to decabromodiphenyl ether (PBDE −209) in neonate and young female mice. Iranian Journal of Basic Medical Sciences 17:307–11. PMCID: PMC4046233.
   PubMed Web of Science ®Google Scholar
• Viberg, H., A. Fredriksson, and P. Eriksson. 2003. Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicology and Applied Pharmacology 192:95–106. PMID: 14550744.
   PubMed Web of Science ®Google Scholar
• Viberg, H., N. Johansson, A. Fredriksson, J. Eriksson, G. Marsh, and P. Eriksson. 2006. Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions of adult mice. Toxicological Sciences 92:211–18. doi:10.1093/toxsci/kfj196.
   PubMed Web of Science ®Google Scholar
• Viechtbauer, W. 2005. Bias and efficiency of meta-analytic variance estimators in the random-effects model. Journal Of Educational and Behavioral Statistics 30 (3):261-293. doi: 10.3102/10769986030003261.
   Web of Science ®Google Scholar
• Viechtbauer, W. 2010. conducting meta-analysis in r with the metafor package. Journal Of Statistical Software 36 (3):1-48. doi: 10.18637/jss.v036.i03.
   Web of Science ®Google Scholar
• Vorhees, C. V., and M. T. Williams. 2006. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nature Protocols 1:848–58. doi:10.1038/nprot.2006.116.
   PubMed Web of Science ®Google Scholar
• Wiseman, S. B., Y. Wan, H. Chang, X. Zhang, M. Hecker, P. D. Jones, and J. P. Giesy. 2011. Polybrominated diphenyl ethers and their hydroxylated/methoxylated analogs: Environmental sources, metabolic relationships, and relative toxicities. Marine Pollution Bulletin 63:179–88. doi:10.1016/j.marpolbul.2011.02.008.
   PubMed Web of Science ®Google Scholar
• Woodruff, T. J., and P. Sutton. 2014. The Navigation Guide systematic review methodology: A rigorous and transparent method for translating environmental health science into better health outcomes. Environmental Health Perspectives 122:1007–14. doi:10.1289/ehp.1307175.
   PubMed Web of Science ®Google Scholar
• Woods, R., R. O. Vallero, M. S. Golub, J. K. Suarez, T. A. Ta, D. H. Yasui, L. H. Chi, P. J. Kostyniak, I. N. Pessah, R. F. Berman, and J. M. LaSalle. 2012. Long-lived epigenetic interactions between perinatal PBDE exposure and Mecp2308 mutation. Human Molecular Genetics 21:2399–411. doi:10.1093/hmg/dds046.
   PubMed Web of Science ®Google Scholar
• Zhang, H., X. Li, J. Nie, and Q. Niu. 2013. Lactation exposure to BDE-153 damages learning and memory, disrupts spontaneous behavior and induces hippocampus neuron death in adult rats. Brain Research 1517:44–56. doi:10.1016/j.brainres.2013.04.014.
   PubMed Web of Science ®Google Scholar
• Zhao, W., J. Cheng, J. Gu, Y. Liu, M. Fujimura, and W. Wang. 2014. Assessment of neurotoxic effects and brain region distribution in rat offspring prenatally co-exposed to low doses of BDE-99 and methylmercury. Chemosphere 112:170–76. doi:10.1016/j.chemosphere.2014.04.011.
   PubMed Web of Science ®Google Scholar