Current Diabetes Reports

, 17:132 | Cite as

Persistent Organic Pollutants as Risk Factors for Obesity and Diabetes

  • Chunxue Yang
  • Alice Pik Shan Kong
  • Zongwei CaiEmail author
  • Arthur C.K. ChungEmail author
Diabetes Epidemiology (NM Maruthur, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Diabetes Epidemiology


Purpose of review

The rising prevalence of obesity and diabetes cannot be fully explained by known risk factors, such as unhealthy diet, a sedentary lifestyle, and family history. This review summarizes the available studies linking persistent organic pollutants (POPs) to obesity and diabetes and discusses plausible underlying mechanisms.

Recent findings

Increasing evidence suggest that POPs may act as obesogens and diabetogens to promote the development of obesity and diabetes and induce metabolic dysfunction. POPs are synthesized chemicals and are used widely in our daily life. These chemicals are resistant to degradation in chemical or biological processes, which enable them to exist in the environment persistently and to be bio-accumulated in animal and human tissue through the food chain. Increasingly, epidemiologic studies suggest a positive association between POPs and risk of developing diabetes.


Understanding the relationship of POPs with obesity and diabetes may shed light on preventive strategies for obesity and diabetes.


persistent organic pollutants obesity diabetes metabolic diseases 



This work was supported by grants from Mr. Kwok Yat Wai and Madam Kwok Chung Bo Fun Graduate School Development Fund, Hong Kong Baptist University; National Natural Science Foundation of China (General Program 21577115 and 21477101); the Research Grant Council of Hong Kong (RGC GRF 463612 and 14104314, 12300114); Faculty Research Grants from the Hong Kong Baptist University (FRG2/15-16/067; FRG2/16-17/049); Hong Kong Health and Medical Research Fund (HMRF/ 03144376); and HKASO research grant 2015-16.

Compliance with Ethics Guidelines

Conflict of Interest

Chunxue Yang, Alice Pik Shan Kong, Zongwei Cai, and Arthur C.K. Chung declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Chan DS, Norat T. Obesity and breast cancer: not only a risk factor of the disease. Current treatment options in oncology. 2015;16(5):1–17.CrossRefGoogle Scholar
  2. 2.
    Maggio AB. Obesity-related complications in children: University of Geneva; 2016.Google Scholar
  3. 3.
    Cawley J, Meyerhoefer C. The medical care costs of obesity: an instrumental variables approach. J Health Econ. 2012;31(1):219–30.CrossRefPubMedGoogle Scholar
  4. 4.
    Elobeid MA, Padilla MA, Brock DW, Ruden DM, Allison DB. Endocrine disruptors and obesity: an examination of selected persistent organic pollutants in the NHANES 1999–2002 data. International journal of environmental research and public health. 2010;7(7):2988–3005.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Baillie-Hamilton PF. Chemical toxins: A hypothesis to explain the global obesity epidemic. J Altern Complem Med. 2002;8(2):185–92.CrossRefGoogle Scholar
  6. 6.
    Kelishadi R, Poursafa P, Jamshidi F. Role of environmental chemicals in obesity: a systematic review on the current evidence. J Environ Public Health. 2013;2013:896789.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Shaw SD, Harris JH, Berger ML, Subedi B, Kannan K. Brominated flame retardants and their replacements in food packaging and household products: uses, human exposure, and health effects. Toxicants in Food Packaging and Household Plastics: Springer; 2014. p. 61-93.Google Scholar
  8. 8.
    Kotthoff M, Müller J, Jürling H, Schlummer M, Fiedler D. Perfluoroalkyl and polyfluoroalkyl substances in consumer products. Environmental Science and Pollution Research. 2015;22(19):14546–59.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Vojta Š, Bečanová J, Melymuk L, Komprdová K, Kohoutek J, Kukučka P, et al. Screening for halogenated flame retardants in European consumer products, building materials and wastes. Chemosphere. 2017;168:457–66.CrossRefPubMedGoogle Scholar
  10. 10.
    Hong N, Kim K, Lee I, Lind P, Lind L, Jacobs D, et al. The association between obesity and mortality in the elderly differs by serum concentrations of persistent organic pollutants: a possible explanation for the obesity paradox. International journal of obesity. 2012;36(9):1170–5.CrossRefPubMedGoogle Scholar
  11. 11.
    Lyche JL, Nourizadeh-Lillabadi R, Karlsson C, Stavik B, Berg V, Skåre JU, et al. Natural mixtures of POPs affected body weight gain and induced transcription of genes involved in weight regulation and insulin signaling. Aquatic Toxicology. 2011;102(3):197–204.CrossRefPubMedGoogle Scholar
  12. 12.
    Lim J-S, Lee D-H, Jacobs DR. Association of brominated flame retardants with diabetes and metabolic syndrome in the US population, 2003–2004. Diabetes care. 2008;31(9):1802–7.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Grun F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology. 2006;147(6):s50–s5.CrossRefPubMedGoogle Scholar
  14. 14.
    Kong AP, Xu G, Brown N, So WY, Ma RC, Chan JC. Diabetes and its comorbidities--where East meets West. Nat Rev Endocrinol. 2013;9(9):537–47.CrossRefPubMedGoogle Scholar
  15. 15.
    Dawson J. Impacts of long-range transport of persistent organic pollutants on human health and ecosystems. Air Pollution Studies. 2013:167–84.Google Scholar
  16. 16.
    Hung H, MacLeod M, Guardans R, Scheringer M, Barra R, Harner T, et al. Toward the next generation of air quality monitoring: Persistent organic pollutants. Atmospheric Environment. 2013;80:591–8.CrossRefGoogle Scholar
  17. 17.
    Geyer HJ, Rimkus GG, Scheunert I, Kaune A, Schramm K-W, Kettrup A, et al. Bioaccumulation and occurrence of endocrine-disrupting chemicals (EDCs), persistent organic pollutants (POPs), and other organic compounds in fish and other organisms including humans. Bioaccumulation–New Aspects and Developments: Springer; 2000. p. 1-166.Google Scholar
  18. 18.
    Hedley A, Hui L, Kypke K, Malisch R, Van Leeuwen F, Moy G, et al. Residues of persistent organic pollutants (POPs) in human milk in Hong Kong. Chemosphere. 2010;79(3):259–65.CrossRefPubMedGoogle Scholar
  19. 19.
    Harrad S, Hazrati S, Ibarra C. Concentrations of polychlorinated biphenyls in indoor air and polybrominated diphenyl ethers in indoor air and dust in Birmingham, United Kingdom: implications for human exposure. Environmental Science & Technology. 2006;40(15):4633–8.CrossRefGoogle Scholar
  20. 20.
    Shoeib M, Harner T, Wilford BH, Jones KC, Zhu J. Perfluorinated sulfonamides in indoor and outdoor air and indoor dust: occurrence, partitioning, and human exposure. Environmental science & technology. 2005;39(17):6599–606.CrossRefGoogle Scholar
  21. 21.
    •• La Merrill M, Emond C, Kim MJ, Antignac JP, Le Bizec B, Clement K, et al. Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ Health Perspect. 2013;121(2):162-169. This review highlights adipose tissue is toxic pool to modulate the accumulated POPs to induce endocrine dysfunction, such as insulin resistance and T2D.Google Scholar
  22. 22.
    Wang T, Wang Y, Liao C, Cai Y, Jiang G. Perspectives on the Inclusion of Perfluorooctane Sulfonate into the Stockholm Convention on Persistent Organic Pollutants 1. Environmental science & technology. 2009;43(14):5171–5.CrossRefGoogle Scholar
  23. 23.
    Polder A, Gabrielsen G, Odland JØ, Savinova T, Tkachev A, Løken K, et al. Spatial and temporal changes of chlorinated pesticides, PCBs, dioxins (PCDDs/PCDFs) and brominated flame retardants in human breast milk from Northern Russia. Science of the Total Environment. 2008;391(1):41–54.CrossRefPubMedGoogle Scholar
  24. 24.
    Singh N, Chhillar N, Banerjee B, Bala K, Basu M, Mustafa M. Organochlorine pesticide levels and risk of Alzheimer’s disease in north Indian population. Human & experimental toxicology. 2013;32(1):24–30.CrossRefGoogle Scholar
  25. 25.
    Karlaganis G, Marioni R, Sieber I, Weber A. The elaboration of the ‘Stockholm convention’on persistent organic pollutants (POPs): a negotiation process fraught with obstacles and opportunities. Environmental Science and Pollution Research. 2001;8(3):216–21.CrossRefPubMedGoogle Scholar
  26. 26.
    Li Y, Chen L, Wen Z-H, Duan Y-P, Z-B L, Meng X-Z, et al. Characterizing distribution, sources, and potential health risk of polybrominated diphenyl ethers (PBDEs) in office environment. Environmental Pollution. 2015;198:25–31.CrossRefPubMedGoogle Scholar
  27. 27.
    Rotander A, Toms L-ML, Aylward L, Kay M, Mueller JF. Elevated levels of PFOS and PFHxS in firefighters exposed to aqueous film forming foam (AFFF). Environment international. 2015;82:28–34.CrossRefPubMedGoogle Scholar
  28. 28.
    Dirinck E, Jorens PG, Covaci A, Geens T, Roosens L, Neels H, et al. Obesity and persistent organic pollutants: possible obesogenic effect of organochlorine pesticides and polychlorinated biphenyls. Obesity. 2011;19(4):709–14.CrossRefPubMedGoogle Scholar
  29. 29.
    Carpenter DO. Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Reviews on environmental health. 2006;21(1):1–24.CrossRefPubMedGoogle Scholar
  30. 30.
    Codru N, Schymura MJ, Negoita S, Environment ATFot, Rej R, Carpenter DO. Diabetes in relation to serum levels of polychlorinated biphenyls and chlorinated pesticides in adult Native Americans. Environ Health Persp. 2007:1442-7.Google Scholar
  31. 31.
    Agudo A, Goñi F, Etxeandia A, Vives A, Millán E, López R, et al. Polychlorinated biphenyls in Spanish adults: determinants of serum concentrations. Environmental research. 2009;109(5):620–8.CrossRefPubMedGoogle Scholar
  32. 32.
    • Aminov Z, Haase R, Rej R, Schymura MJ, Santiago-Rivera A, Morse G, et al. Diabetes prevalence in relation to serum concentrations of polychlorinated biphenyl (PCB) Congener groups and three chlorinated pesticides in a native american population. Environ Health Persp. 2016;124(9):1376–83. This study provides epidemiological data to determine the relationship between serum PCBs and T2D.Google Scholar
  33. 33.
    Lee D-H, Lee I-K, Steffes M, Jacobs DR. Extended analyses of the association between serum concentrations of persistent organic pollutants and diabetes. Diabetes Care. 2007;30(6):1596–8.CrossRefPubMedGoogle Scholar
  34. 34.
    Vasiliu O, Cameron L, Gardiner J, DeGuire P, Karmaus W. Polybrominated biphenyls, polychlorinated biphenyls, body weight, and incidence of adult-onset diabetes mellitus. Epidemiology. 2006;17(4):352–9.CrossRefPubMedGoogle Scholar
  35. 35.
    Tanaka T, Morita A, Kato M, Hirai T, Mizoue T, Terauchi Y, et al. Congener-specific polychlorinated biphenyls and the prevalence of diabetes in the Saku Control Obesity Program (SCOP). Endocrine journal. 2011;58(7):589–96.CrossRefPubMedGoogle Scholar
  36. 36.
    Xu W, Wang X, Cai Z. Analytical chemistry of the persistent organic pollutants identified in the Stockholm Convention: A review. Analytica Chimica Acta. 2013;790:1–13.CrossRefPubMedGoogle Scholar
  37. 37.
    Schreck E, Geret F, Gontier L, Treilhou M. Neurotoxic effect and metabolic responses induced by a mixture of six pesticides on the earthworm Aporrectodea caliginosa nocturna. Chemosphere. 2008;71(10):1832–9.CrossRefPubMedGoogle Scholar
  38. 38.
    Montgomery M, Kamel F, Saldana T, Alavanja M, Sandler D. Incident diabetes and pesticide exposure among licensed pesticide applicators: Agricultural Health Study, 1993–2003. American journal of epidemiology. 2008;167(10):1235–46.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Shaub WM, Tsang W. Dioxin formation in incinerators. Environmental science & technology. 1983;17(12):721–30.CrossRefGoogle Scholar
  40. 40.
    McKay G. Dioxin characterisation, formation and minimisation during municipal solid waste (MSW) incineration: review. Chemical Engineering Journal. 2002;86(3):343–68.CrossRefGoogle Scholar
  41. 41.
    Stanmore B. The formation of dioxins in combustion systems. Combustion and flame. 2004;136(3):398–427.CrossRefGoogle Scholar
  42. 42.
    Geyer HJ, Schramm K-W, Feicht EA, Behechti A, Steinberg C, Brüggemann R, et al. Half-lives of tetra-, penta-, hexa-, hepta-, and octachlorodibenzo-p-dioxin in rats, monkeys, and humans––a critical review. Chemosphere. 2002;48(6):631–44.CrossRefPubMedGoogle Scholar
  43. 43.
    Milbrath MOG, Wenger Y, Chang C-W, Emond C, Garabrant D, Gillespie BW, et al. Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ Health Persp. 2009;117(3):417.CrossRefGoogle Scholar
  44. 44.
    Aylward LL, Collins JJ, Bodner KM, Wilken M, Bodnar CM. Elimination rates of dioxin congeners in former chlorophenol workers from Midland. Michigan. Environ Health Persp. 2013;121(1):39.Google Scholar
  45. 45.
    Milbrath MO, Wenger Y, Chang CW, Emond C, Garabrant D, Gillespie BW, et al. Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ Health Perspect. 2009;117(3):417–25.CrossRefPubMedGoogle Scholar
  46. 46.
    Chang J-W, Chen H-L, H-J S, Lee C-C. Abdominal Obesity and Insulin Resistance in People Exposed to Moderate-to-High Levels of Dioxin. PloS one. 2016;11(1):e0145818.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Uemura H, Arisawa K, Hiyoshi M, Kitayama A, Takami H, Sawachika F, et al. Prevalence of metabolic syndrome associated with body burden levels of dioxin and related compounds among Japan's general population. Environ Health Persp. 2009;117(4):568.CrossRefGoogle Scholar
  48. 48.
    Warner M, Mocarelli P, Brambilla P, Wesselink A, Samuels S, Signorini S, et al. Diabetes, metabolic syndrome, and obesity in relation to serum dioxin concentrations: the Seveso Women's Health Study. Environmental Health Perspectives (Online). 2013;121(8):906.CrossRefGoogle Scholar
  49. 49.
    Mandal PK. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. Journal of Comparative Physiology B. 2005;175(4):221–30.CrossRefGoogle Scholar
  50. 50.
    • Roh E, Kwak SH, Jung HS, Cho YM, Pak YK, Park KS, et al. Serum aryl hydrocarbon receptor ligand activity is associated with insulin resistance and resulting type 2 diabetes. Acta diabetologica. 2015;52(3):489–95. This study shows that a strong association between AhR ligand activities and T2D and log2-transformed TCDD levels were also significantly associated with the risk of T2D.CrossRefPubMedGoogle Scholar
  51. 51.
    Zhang Z, Li S, Liu L, Wang L, Xiao X, Sun Z, et al. Environmental exposure to BDE47 is associated with increased diabetes prevalence: Evidence from community-based case-control studies and an animal experiment. Scientific reports. 2016;6.Google Scholar
  52. 52.
    Jones-Otazo HA, Clarke JP, Diamond ML, Archbold JA, 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. Environmental science & technology. 2005;39(14):5121–30.CrossRefGoogle Scholar
  53. 53.
    Stapleton HM, Eagle S, Anthopolos R, Wolkin A, Miranda ML. Associations between polybrominated diphenyl ether (PBDE) flame retardants, phenolic metabolites, and thyroid hormones during pregnancy. Environ Health Persp. 2011;119(10):1454.CrossRefGoogle Scholar
  54. 54.
    Roberts SC. PBDE Metabolism and Effects on Thyroid Hormone Regulation in Human Astrocytes. 2014.Google Scholar
  55. 55.
    Airaksinen R, Rantakokko P, Eriksson JG, Blomstedt P, Kajantie E, Kiviranta H. Association between type 2 diabetes and exposure to persistent organic pollutants. Diabetes Care. 2011;34(9):1972–9.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Erkin-Cakmak A, Harley KG, Chevrier J, Bradman A, Kogut K, Huen K, et al. In utero and childhood polybrominated diphenyl ether exposures and body mass at age 7 years: the CHAMACOS Study. Environ Health Persp. 2015;123(6):636.Google Scholar
  57. 57.
    Pereira-Fernandes A, Dirinck E, Dirtu AC, Malarvannan G, Covaci A, Van Gaal L, et al. Expression of obesity markers and Persistent Organic Pollutants levels in adipose tissue of obese patients: reinforcing the obesogen hypothesis? PloS one. 2014;9(1):e84816.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Lau C, Anitole K, Hodes C, Lai D, Pfahles-Hutchens A, Seed J. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicological sciences. 2007;99(2):366–94.CrossRefPubMedGoogle Scholar
  59. 59.
    Nakamura H, Jinzu H, Nagao K, Noguchi Y, Shimba N, Miyano H, et al. Plasma amino acid profiles are associated with insulin, C-peptide and adiponectin levels in type 2 diabetic patients. Nutrition & diabetes. 2014;4(9):e133.CrossRefGoogle Scholar
  60. 60.
    Færch K, Højlund K, Vind BF, Vaag A, Dalgård C, Nielsen F, et al. Increased serum concentrations of persistent organic pollutants among prediabetic individuals: potential role of altered substrate oxidation patterns. The Journal of Clinical Endocrinology & Metabolism. 2012;97(9):E1705–E13.CrossRefGoogle Scholar
  61. 61.
    Conway B, Innes KE, Long D. Perfluoroalkyl Substances and Beta Cell Deficient Diabetes. Journal of Diabetes and its Complications. 2016;Google Scholar
  62. 62.
    Zhang C, Sundaram R, Maisog J, Calafat AM, Barr DB, Louis GMBA. prospective study of prepregnancy serum concentrations of perfluorochemicals and the risk of gestational diabetes. Fertility and sterility. 2015;103(1):184–9.CrossRefPubMedGoogle Scholar
  63. 63.
    Eriksen KT, Raaschou-Nielsen O, McLaughlin JK, Lipworth L, Tjønneland A, Overvad K, et al. Association between plasma PFOA and PFOS levels and total cholesterol in a middle-aged Danish population. PloS one. 2013;8(2):e56969.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Domazet SL, Grøntved A, Timmermann AG, Nielsen F, Jensen TK. Longitudinal Associations of Exposure to Perfluoroalkylated Substances in Childhood and Adolescence and Indicators of Adiposity and Glucose Metabolism 6 and 12 Years Later: The European Youth Heart Study. Diabetes Care. 2016:dc160269.Google Scholar
  65. 65.
    Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell. 2012;148(6):1145–59.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 2002;51(7):2005–11.CrossRefPubMedGoogle Scholar
  67. 67.
    Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. The Journal of clinical investigation. 2005;115(12):3587–93.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Lim S, Cho YM, Park KS, Lee HK. Persistent organic pollutants, mitochondrial dysfunction, and metabolic syndrome. Annals of the New York Academy of Sciences. 2010;1201(1):166–76.CrossRefPubMedGoogle Scholar
  69. 69.
    Griffin ME, Marcucci MJ, Cline GW, Bell K, Barucci N, Lee D, et al. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes. 1999;48(6):1270–4.CrossRefPubMedGoogle Scholar
  70. 70.
    Yu C, Chen Y, Cline GW, Zhang D, Zong H, Wang Y, et al. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem. 2002;277(52):50230–6.CrossRefPubMedGoogle Scholar
  71. 71.
    Lim S, Ahn SY, Song IC, Chung MH, Jang HC, Park KS, et al. Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance. PLoS One. 2009;4(4):e5186.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Wahlang B, Prough RA, Falkner KC, Hardesty JE, Song M, Clair HB, et al. Polychlorinated Biphenyl-Xenobiotic Nuclear Receptor Interactions Regulate Energy Metabolism, Behavior, and Inflammation in Non-alcoholic-Steatohepatitis. Toxicological Sciences. 2016;149(2):396–410.CrossRefPubMedGoogle Scholar
  73. 73.
    Park WH, Jun DW, Kim JT, Jeong JH, Park H, Chang YS, et al. Novel cell-based assay reveals associations of circulating serum AhR-ligands with metabolic syndrome and mitochondrial dysfunction. BioFactors (Oxford, England). 2013;39(4):494–504.CrossRefGoogle Scholar
  74. 74.
    Kurita H, Yoshioka W, Nishimura N, Kubota N, Kadowaki T, Tohyama C. Aryl hydrocarbon receptor-mediated effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on glucose-stimulated insulin secretion in mice. J Appl Toxicol. 2009;29(8):689–94.CrossRefPubMedGoogle Scholar
  75. 75.
    Novelli M, Piaggi S, De Tata V. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced impairment of glucose-stimulated insulin secretion in isolated rat pancreatic islets. Toxicol Lett. 2005;156(2):307–14.CrossRefPubMedGoogle Scholar
  76. 76.
    Lee HK. Mitochondrial dysfunction and insulin resistance: the contribution of dioxin-like substances. Diabetes & metabolism journal. 2011;35(3):207–15.CrossRefGoogle Scholar
  77. 77.
    Sales LB, Kamstra J, Cenijn P, Van Rijt L, Hamers T, Legler J. Effects of endocrine disrupting chemicals on in vitro global DNA methylation and adipocyte differentiation. Toxicology in vitro. 2013;27(6):1634–43.CrossRefGoogle Scholar
  78. 78.
    •• Kamstra JH, Hruba E, Blumberg B, Janesick A, Mandrup S, Hamers T, et al. Transcriptional and epigenetic mechanisms underlying enhanced in vitro adipocyte differentiation by the brominated flame retardant BDE-47. Environmental science & technology. 2014;48(7):4110-4119.This study uses highlights that BDE-47 enhanced adipocytes differentiation via demethylation of PPARγ2 promoter.Google Scholar
  79. 79.
    Aly HA, Domènech Ò. Cytotoxicity and mitochondrial dysfunction of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in isolated rat hepatocytes. Toxicol Lett. 2009;191(1):79–87.CrossRefPubMedGoogle Scholar
  80. 80.
    Liu HG, Wang Y, Lian L, Tributyltin XLH. induces DNA damage as well as oxidative damage in rats. Environmental toxicology. 2006;21(2):166–71.CrossRefPubMedGoogle Scholar
  81. 81.
    Groom A, Potter C, Swan DC, Fatemifar G, Evans DM, Ring SM, et al. Postnatal growth and DNA methylation are associated with differential gene expression of the TACSTD2 gene and childhood fat mass. Diabetes. 2012;61(2):391–400.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Volkmar M, Dedeurwaerder S, Cunha DA, Ndlovu MN, Defrance M, Deplus R, et al. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients. The EMBO journal. 2012;31(6):1405–26.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Rakyan VK, Beyan H. Down TA, Hawa MI, Maslau S, Aden D, et al. Identification of type 1 diabetes–associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet. 2011;7(9):e1002300.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Itoh H, Iwasaki M, Kasuga Y, Yokoyama S, Onuma H, Nishimura H, et al. Association between serum organochlorines and global methylation level of leukocyte DNA among Japanese women: a cross-sectional study. Sci Total Environ. 2014;490:603–9.CrossRefPubMedGoogle Scholar
  85. 85.
    Kim K-Y, Kim D-S, Lee S-K, Kang J-H, Chang Y-S, Jacobs Jr DR, et al. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ Health Persp. 2010;118(3):370.Google Scholar
  86. 86.
    Lind L, Penell J, Luttropp K, Nordfors L, Syvanen AC, Axelsson T, et al. Global DNA hypermethylation is associated with high serum levels of persistent organic pollutants in an elderly population. Environ Int. 2013;59:456–61.CrossRefPubMedGoogle Scholar
  87. 87.
    Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Persp. 2008;116(11):1547.CrossRefGoogle Scholar
  88. 88.
    Zhang J, Wang C, Ha X, Li W, Xu P, Gu Y, et al. The DNA methylation of TNF-aplha, MCP-1, and adiponectin in visceral adipose tissue is related to type 2 diabetes in Xinjiang Uygur population. J Diabetes. 2016;Google Scholar
  89. 89.
    Ukropec J, Radikova Z, Huckova M, Koska J, Kocan A, Sebokova E, et al. High prevalence of prediabetes and diabetes in a population exposed to high levels of an organochlorine cocktail. Diabetologia. 2010;53(5):899–906.CrossRefPubMedGoogle Scholar
  90. 90.
    Howell G, Mangum L. Exposure to bioaccumulative organochlorine compounds alters adipogenesis, fatty acid uptake, and adipokine production in NIH3T3-L1 cells. Toxicology in Vitro. 2011;25(1):394–402.CrossRefPubMedGoogle Scholar
  91. 91.
    Bhaskar R, Mohanty B. Pesticides in mixture disrupt metabolic regulation: in silico and in vivo analysis of cumulative toxicity of mancozeb and imidacloprid on body weight of mice. General and comparative endocrinology. 2014;205:226–34.CrossRefPubMedGoogle Scholar
  92. 92.
    Eden PR, Meek EC, Wills RW, Olsen EV, Crow JA, Chambers JE. Association of type 2 diabetes mellitus with plasma organochlorine compound concentrations. Journal of Exposure Science and Environmental Epidemiology. 2016;26(2):207–13.CrossRefPubMedGoogle Scholar
  93. 93.
    Howell GE, Meek E, Kilic J, Mohns M, Mulligan C, Chambers JE. Exposure to p, p′-dichlorodiphenyldichloroethylene (DDE) induces fasting hyperglycemia without insulin resistance in male C57BL/6H mice. Toxicology. 2014;320:6–14.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Hines EP, White SS, Stanko JP, Gibbs-Flournoy EA, Lau C, Fenton SE. Phenotypic dichotomy following developmental exposure to perfluorooctanoic acid (PFOA) in female CD-1 mice: low doses induce elevated serum leptin and insulin, and overweight in mid-life. Molecular and cellular endocrinology. 2009;304(1):97–105.CrossRefPubMedGoogle Scholar
  95. 95.
    Wang L, Wang Y, Liang Y, Li J, Liu Y, Zhang J, et al. PFOS induced lipid metabolism disturbances in BALB/c mice through inhibition of low density lipoproteins excretion. Scientific reports. 2014;4Google Scholar
  96. 96.
    Xu J, Shimpi P, Armstrong L, Salter D, Slitt ALPFOS. induces adipogenesis and glucose uptake in association with activation of Nrf2 signaling pathway. Toxicology and applied pharmacology. 2016;290:21–30.CrossRefPubMedGoogle Scholar
  97. 97.
    Watkins AM, Wood CR, Lin MT, Abbott BD. The effects of perfluorinated chemicals on adipocyte differentiation in vitro. Molecular and cellular endocrinology. 2015;400:90–101.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Partner, State Key Laboratory of Environmental and Biological Analysis, and Department of ChemistryHong Kong Baptist UniversityKowloon TongChina
  2. 2.HKBU Institute for Research and Continuing EducationShenzhenChina
  3. 3.Department of Medicine and TherapeuticsThe Chinese University of Hong Kong, Prince of Wales HospitalHong KongChina
  4. 4.Li Ka Shing Institute of Health SciencesThe Chinese University of Hong Kong, Prince of Wales HospitalHong KongChina
  5. 5.Hong Kong Institute of Diabetes and ObesityThe Chinese University of Hong Kong, Prince of Wales HospitalHong KongChina

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