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Exposure to persistent organic pollutants as potential risk factors for developing diabetes

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  • Special Topic · Research Progress of Persistent Organic Pollutants
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Abstract

Persistent organic pollutants (POPs), such as dioxins, polychlorinated biphenyls (PCBs), and organochlorine pesticides (OCPs), which are synthetic chemicals or by-products with an intrinsic resistance to natural degradation processes, are released into the environment, resulting in the widespread dispersal and accumulation in the environment, as well as in human and ecological food chains. Due to their ubiquity in the environment and lipophilic properties, there is emerging concern over the potential risks of human exposure to POPs. Extensive growing evidence indicated that exposure to POPs might be strongly associated with increased risk of a worldwide epidemic of diabetes, especially type 2 diabetes, suggesting that POPs might play a key role in their pathogenesis. Based on summary of the related studies, this paper reviews the epidemiologic and experimental data that addresses the association between increased risk of diabetes and POP exposure, including dioxins, PCBs, OCPs, polybrominated flame retardants (PBFRs), and some environmental estrogens. The potential mechanisms whereby POPs cause diabetes were discussed, such as alterations in lipid metabolism, in glucose transport, in insulin signaling pathway, in steroid metabolism, and disruption of endocrine system, induction of tumor necrosis factor-α (TNF-α). However, with respect to diabetes, some of the evidence on POPs linked to risk of diabetes was suggestive of a direct or indirect association but was limited or inconclusive. Future research is urgently needed for determining the relative contribution of POPs to diabetes and elucidating the exact mechanisms.

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References

  1. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care, 2004, 27(5):1047–1053

    Article  Google Scholar 

  2. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Practice, 2010, 87:4–14

    Article  CAS  Google Scholar 

  3. Hu FB, Manson JE, Stampfer MJ, Colditz G, Liu S, Soloman CG, Willett WC. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med, 2001, 345(11):790–797

    Article  CAS  Google Scholar 

  4. Kriska AM, Saremi A, Hanson RL, Bennett PH, Kobes S, Williams DE, Knowler WC. Physical activity, obesity, and the incidence of type 2 diabetes in a high-risk population. Am J Epidemiol, 2003, 158:669–675

    Article  Google Scholar 

  5. O’Rahilly S, Barroso I, Wareham NJ. Genetic factors in type 2 diabetes: the end of the beginning? Science, 2005, 307(5708):370–373

    Article  CAS  Google Scholar 

  6. Morgan DP, Lin LI, Saikaly HH. Morbidity and mortality in workers occupationally exposed to pesticides. Arch Environ Contam Toxicol, 1980, 9(3):349–382

    Article  CAS  Google Scholar 

  7. Kimbrough RD, Linder RE, Gaines TB. Morphological changes in livers of rats fed polychlorinated biphenyls: light microscopy and ultrastructure. Arch Environ Health, 1972, 25:354–364

    CAS  Google Scholar 

  8. Wassermann D, Wassermann M, Lemesch C. Ultrastructure of beta cells of the endocrine pancreas in rats receiving polychlorinated biphenyls. Environ Physiol Biochem, 1975, 5(5):322–340

    CAS  Google Scholar 

  9. Novelli M, Piaggi S, Tata VD. 2,3,7,8-Tetrachlorodibenzo-p-dioxininduced impairment of glucose-stimulated insulin secretion in isolated rat pancreatic islets. Toxicology Lett, 2005, 156:307–314

    Article  CAS  Google Scholar 

  10. 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):352–359

    Article  Google Scholar 

  11. Everett CJ, Frithsen IL, Diaz VA, Koopman RJ, Simpson WM Jr, Mainous AG 3rd. Association of a polychlorinated dibenzo-p-dioxin, a polychlorinated biphenyl, and DDT with diabetes in the 1999–2002 National Health and Nutrition Examination Survey. Environ Res, 2007, 103(3):413–418

    Article  CAS  Google Scholar 

  12. Lee DH, Lee IK, Jin SH, Steffes M, Jacobs Jr DR. Extended analyses of the association between serum concentrations of persistent organic pollutants and diabetes. Diabetes Care, 2007a, 30:1596–1598

    Article  Google Scholar 

  13. Wang SL, Tsai PC, Yang CY, Leon Guo Y. Increased risk of diabetes and polychlorinated biphenyls and dioxins: a 24-year follow-up study of the Yucheng cohort. Diabetes Care, 2008, 31(8):1574–1579

    Article  Google Scholar 

  14. Turyk M, Anderson H, Knobeloch L, Imm P, Persky V. Organochlorine exposure and incidence of diabetes in a cohort of Great Lakes Sport Fish Consumers. Environl health perspect, 2009, 117(7):1076–1082

    CAS  Google Scholar 

  15. Turyk M, Anderson HA, Knobeloch L, Imm P, Persky VW. Prevalence of diabetes and body burdens of polychlorinated biphenyls, polybrominated diphenyl ethers, and p,p′-diphenyldichloroethene in Great Lakes sport fish consumers. Chemosphere, 2009, 75(5):674–679

    Article  CAS  Google Scholar 

  16. Poon BH, Leung CK, Wong CK, Wong MH. Polychlorinated biphenyls and organochlorine pesticides in human adipose tissue and breast milk collected in Hong Kong. Rev Environ Arch Environ Contam Toxicol, 2005, 49(2):274–282

    Article  CAS  Google Scholar 

  17. Johnson-Restrepo B, Kannan K, Rapaport DP, Rodan BD. Polybrominated diphenyl ethers and polychlorinated biphenyls in human adipose tissue from New York. Environ Sci Technol, 2005, 39(14):5177–5182

    Article  CAS  Google Scholar 

  18. Henriksen GL, Ketchum NS, Michalek JE, Swaby JA. Serum dioxin and diabetes mellitus in veterans of Operation Ranch Hand. Epidemiology, 1997, 8(3):252–258

    Article  CAS  Google Scholar 

  19. Lee DH, Lee IK, Song KE, Steffes M, Toscano W, Baker BA, Jacobs, DR Jr. A strong dose-response relation between serum concentrations of persistent organic pollutants and diabetes: results from the National Health and Examination Survey. Diabetes Care, 2006b, 29(7):1638–1644

    Article  CAS  Google Scholar 

  20. Rylander L, Rignell-Hydbom A, Hagmar L. A cross-sectional study of the association between persistent organochlorine pollutants and diabetes. Environ Health, 2005, 4(28):1–6

    Google Scholar 

  21. Hoppe AA, Carey GB. Polybrominated diphenyl ethers as endocrine disruptors of adipocyte metabolism. Obesity, 2007, 15(12):2942–2950

    Article  CAS  Google Scholar 

  22. Sharp D. Environmental toxins, a potential risk factor for diabetes among Canadian aboriginals. Int J Circumpolar Health, 2009, 68(4):316–326

    Google Scholar 

  23. Lee DH, Jacobs DR Jr, Porta M. Could low-level background exposure to persistent organic pollutants contribute to the social burden of type 2 diabetes? J Epidemiol Community Health, 2006a, 60(12):1006–1008

    Article  Google Scholar 

  24. Porta M. Persistent organic pollutants and the burden of diabetes. Lancet, 2006, 368(9535):558–559

    Article  Google Scholar 

  25. Carpenter DO. Environmental contaminants as risk factors for developing diabetes. Rev Environl Health, 2008, 23(1):59–74

    CAS  Google Scholar 

  26. Kouznetsova M, Huang X, Ma J, Lessner L, Carpenter DO. Increased rate of hospitalization for diabetes and residential proximity of hazardous waste sites. Environ Health Perspect, 2007, 115(1):75–79

    Article  CAS  Google Scholar 

  27. Fierens S, Mairesse H, Heilier JF, De Burbure C, Focant JF, Eppe G, De Pauw E, Bernard A. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers, 2003, 8(6):529–534

    Article  CAS  Google Scholar 

  28. Bertazzi PA, Consonni D, Bachetti S, Rubagotti M, Baccarelli A, Zocchetti C, Pesatori AC. Health effects of dioxin exposure: a 20-year mortality study. Am J Epidemiol, 2001, 153(11):1031–1044

    Article  CAS  Google Scholar 

  29. Uemura H, Arisawa K, Hiyoshi M, Satoh H, Sumiyoshi Y, Morinaga K, Kodama K, Suzuki T, Nagai M, Suzuki T. Associations of environmental exposure to dioxins with prevalent diabetes among general inhabitants in Japan. Environ Res, 2008, 108(1):63–68

    Article  CAS  Google Scholar 

  30. Needham LL, Barr DB, Caudill SP, Pirkle JL, Turner WE, Osterloh J, Jones RL, Sampson EJ. Concentrations of environmental chemicals associated with neurodevelopmental effects in US population. Neurotoxicology, 2005, 26(4):531–545

    Article  CAS  Google Scholar 

  31. Rignell-Hydbom A, Lidfeldt J, Kiviranta H, Rantakokko P, Samsioe G, Agardh CD, Rylander L. Exposure to p,p′-DDE: a risk factor for type 2 diabetes.PLoS ONE, 2009, 4(10):e7503

    Article  CAS  Google Scholar 

  32. King H, Aubert RE, Herman WH. Global burden of diabetes, 1995–2005: Prevalence, numerical estimates, and projections. Diabetes Care, 1998, 21:1414–1431

    Article  CAS  Google Scholar 

  33. Mensah GA, Mokdad AH, Ford E, Narayan KM, Giles WH, Vinicor F, Deedwania PC. Obesity, metabolic syndrome, and type 2 diabetes: emerging epidemics and their cardiovascular implications. Cardiol Clin, 2004, 22(4):485–504

    Article  Google Scholar 

  34. Lee DH, Lee IK, Porta M, Steffes M, Jacobs DR Jr. Relationship between serum concentrations of persistent organic pollutants and the prevalence of metabolic syndrome among non-diabetic adults: results from the National Health and Nutrition Examination Survey 1999–2002. Diabetologia, 2007c, 50(9):1841–1851

    Article  CAS  Google Scholar 

  35. Lee DH, Lee IK, Jin SH, Steffes M, Jacobs DR Jr. Association between serum concentrations of persistent organic pollutants and insulin resistance among nondiabetic adults: results from the National Health and Nutrition Examination Survey 1999–2002. Diabetes Care, 2007a, 30:622–628

    Article  CAS  Google Scholar 

  36. Fujiyoshi PT, Michalek JE, Matsumura F. Molecular epidemiologic evidence for diabetogenic effects of dioxin exposure in US Air force veterans of the Vietnam War. Environ Health Perspect, 2006, 114(11):1677–1683

    CAS  Google Scholar 

  37. Dellinger JA, Meyers RM, Gebharft KJ, Hansen LK. The Ojibwa health study: fish residue comparisons for Lakes Superior, Michigan, and Huron. Toxicol Ind Health, 1996, 12(3–4):393–402

    CAS  Google Scholar 

  38. Poon BH, Leung CK, Wong CK, Wong MH. Polychlorinated biphenyls and organochlorine pesticides in human adipose tissue and breast milk collected in Hong Kong. Rev Environ Arch Environ Contam Toxicol, 2005, 49(2):274–282

    Article  CAS  Google Scholar 

  39. Baibergenova A, Kudyakov R, Zdeb M, Carpenter DO. Low birth weight and residential proximity to PCB-contaminated waste sites. Environ Health Perspect, 2003, 111(10):1352–1357

    Google Scholar 

  40. DeCaprio AP, Johnson GW, Tarbell AM, Carpenter DO, Chiarenzelli JR, Morse GS, Santigo-Rivera AL, Schymura MJ. Polychlorinated biphenyl (PCB) exposure assessment by multivariate statistical analysis of serum congener profiles in an adult Native American population. Environ Res, 2005, 98(3):284–302

    Article  CAS  Google Scholar 

  41. Huang X, Lessner L, Carpenter DO. Exposure to persistent organic pollutants and hypertensive disease. Environ Res, 2006, 102(1):101–106

    Article  CAS  Google Scholar 

  42. Vorhees DJ, Cullen AC, Altshul LM. Exposure to polychlorinated biphenyls in residential indoor air and outdoor air near a superfund site. Environ Sci Technol, 1997, 31(12):3612–3618

    Article  CAS  Google Scholar 

  43. Currado GM, Harrad S. Comparison of polychlorinated biphenyl concentrations in indoor and outdoor air and the potential significance of inhalation as a human exposure pathway. Environ Sci Technol, 1998, 32(20):3043–3047

    Article  CAS  Google Scholar 

  44. Cullen AC, Vorhees DJ, Altshul LM. Influence of harbor contamination on the level and composition of polychlorinated biphenyls in produce in greater New Bedford, Massachusetts. Environ Sci Technol, 1996, 30(5):1581–1588

    Article  CAS  Google Scholar 

  45. Longnecker MP, Klebanoff MA, Brock JW, Zhou H. Polychlorinated biphenyl serum levels in pregnant subjects with diabetes. Diabetes Care, 2001, 24(6):1099–1101

    Article  CAS  Google Scholar 

  46. Longnecker MP, Daniels JL. Environmental contaminants as etiologic factors for diabetes. Environ Health Perspect, 2001, 109(6):871–876

    Article  Google Scholar 

  47. Michalek JE, Akhtar FZ, Kiel JL. Serum dioxin, insulin, fasting glucose, and sex hormone-binding globulin in veterans of Operation Ranch Hand. J Clin Endocrinol Metab, 1999, 84(5):1540–1543

    Article  CAS  Google Scholar 

  48. Longnecker MP, Michalek JE. Serum dioxin level in relation to diabetes mellitus among Air Force veterans with background levels of exposure. Epidemiology, 2000, 11(1):44–48

    Article  CAS  Google Scholar 

  49. Institute of Medicine of the National Academies of Sciences (IOM). Veterans and Agent Orange: herbicide/dioxin exposure and Type 2 diabetes. Washington, DC: The National Academy Press, 2000

    Google Scholar 

  50. Enan E, Lasdley B, Stewart D, Overstreet J, Vandevoort. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) modulates function of human luteinizing granulosa cells via cAMP signaling and early reduction of glucose transporting activity. Reprod Toxicol, 1996, 10(3):191–198

    Article  CAS  Google Scholar 

  51. Ebner K, Brewster DW, Matsumura F. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on serum insulin and glucose levels in rabbits. J Environ Sci Health B, 1988, 23(5):427–438

    Article  CAS  Google Scholar 

  52. Remillards RB, Bunce VJ. Linking dioxins to diabetes: epidemiology and biologic plausibility. Enriron health Perpesct, 2002, 110(9):853–858

    Google Scholar 

  53. Bertazzi PA, Bernucci I, Brambilla G, Consonni D, Pesatori AC. The Seveso studies on early and long-term effects of dioxin exposure: a review. Environ Health Perspect, 1998, 106(2), 625–633

    Article  CAS  Google Scholar 

  54. Pesatori AC, Consonni D, Bachetti S, Zochetti C, Bonzini M, Baccarelli A, Bertazzi PA. Short- and long-term morbidity and mortality in the population exposed to dioxin after the “Seveso Accident”. Ind Health, 2003, 41(3):127–138

    Article  CAS  Google Scholar 

  55. Vena J, Boffetta P, Becher H, Benn T, Bueno-de-Mesquita HB, Coggon D, Colin D, Flesch-Janys D, Green L, Kauppinen T, Littorin M, Lynge E, Mathews JD, Neuberger M, Pearce N, Pesatori AC, Saracci R, Steenland K, Kogevinas M. Exposure to dioxin and nonneoplastic mortality in the expanded IARC international cohort study of phenoxy herbicide and chlorophenol production workers and sprayers. Environ Health Perspect, 1998, 106(2):645–653

    Article  CAS  Google Scholar 

  56. Kim JS, Lim HS, Cho SI, Cheong HK, Lim MK. Impact of Agent Orange exposure among Korean Vietnam veterans. Ind Health, 2003, 41(3):149–157

    Article  Google Scholar 

  57. Wang SL, Tsai PC, Yang CY, Leon Guo Y. Increased risk of diabetes and polychlorinated biphenyls and dioxins: a 24-year follow-up study of the Yucheng cohort. Diabetes Care, 2008, 31(8):1574–1579

    Article  Google Scholar 

  58. Steenland K, Piacitelli L, Deddens J, Fingerhut M, Chang LI. Cancer, heart disease, and diabetes in workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Natl Cancer Inst, 1999, 91(9):779–786

    Article  CAS  Google Scholar 

  59. Vezina CM, Walker NJ, Olson JR. Subchronic exposure to TCDD, PeCDF, PCB126, and PCB153: effect on hepatic gene expression. Environ Health Perspect, 2004, 112(16):1636–1644

    CAS  Google Scholar 

  60. Nishizumi M, Higaki Y. Effect of PCBs on insulin sensitivity in rats. Fukuoka Igaku Zasshi, 1995, 86(5):241–246

    CAS  Google Scholar 

  61. Wicklund-Glynn A, Wolk A, Aune M, Atuma S, Zettermark S, Moehle-Schmid M, Darnerud PO, Becker W, Vessby B, Adani HO. Serum concentrations of organochlorines in men: a search for markers of exposure. Sci Total Environ, 2000, 263(1–3):197–208

    Article  CAS  Google Scholar 

  62. Richthoff J, Rylander L, Jönsson BA, Åkesson H, Hagmar L, Nilsson-Ehle P, Stridsberg M, Giwercman A. Serum Levels of 2,2′,4,4′,5,5′-Hexachlorobiphenyl (CB-153) in Relation to Markers of Reproductive Function in Young Males from the General Swedish Population. Environ Health Perspect, 2003, 111(4):409–414

    CAS  Google Scholar 

  63. Svensson BG, Nilsson A, Jonsson E, Schutz A, Akesson B, Hagmar L. Fish consumption and exposure to persistent organochlorine compounds, mercury, selenium and methylamines among Swedish fishermen. Scand J Work Environ Health, 1995, 21(2):96–105

    CAS  Google Scholar 

  64. Rignell-Hydbom A, Rylander L, Hagmar L. Exposure to persistent organochlorine pollutants and type 2 diabetes mellitus. Hum Exp Toxicol, 2007, 26(5):447–452

    Article  CAS  Google Scholar 

  65. Smeds A, Saukko P. Identification and quantification of polychlorinated biphenyls (PCBs) and some endocrine disrupting pesticides in human adipose tissue from Finland. Chemosphere, 2001, 44(6):1463–1471

    Article  CAS  Google Scholar 

  66. Pesatori AC, Zocchetti C, Guercilena S, Consonni D, Turrini D, Bertazzi PA. Dioxin exposure and non-malignant health effects: a mortality study. Occup Environ Med, 1998, 55(2):126–131

    Article  CAS  Google Scholar 

  67. Beard J, Sladden T, Morgan G, Berry G, Brooks L, McMichael A. Health impacts of pesticide exposure in a cohort of outdoor workers. Environ Health Perspect, 2003, 111(5):724–730

    CAS  Google Scholar 

  68. Lee DH, Jacobs DR Jr, Steffes M. Association of organochlorine pesticides with peripheral neuropathy in patients with diabetes or impaired fasting glucose. Diabetes, 2008a, 57(11):3108–3111

    Article  CAS  Google Scholar 

  69. Cox S, Niskar AS, Narayan KM, Marcus M. Prevalence of self-reported diabetes and exposure to organochlorine pesticides among mexican americans: hispanic health and nutrition examination survey, 1982–1984. Environ Health Perspect, 2007, 115(12):1747–1752

    Article  CAS  Google Scholar 

  70. Eskenazi B, Chevrier J, Rosas LG, Anderson HA, Bornman MS, Bouwman H, Chen A, Cohn BA, de Jager C, Henshel DS, Leipzig F, Leipzig JS, Lorenz EC, Snedeker SM, Stapleton D. The pine river statement: human health consequences of DDT use. Environ Health Perspect, 2009, 117(9):1359–1367

    CAS  Google Scholar 

  71. Haffner SM. Epidemiology of type 2 diabetes: risk factors. Diabetes Care, 1998, 21(3):C3–6

    Google Scholar 

  72. Boada LD, Lara PC, Álvarez-León EE, Losada A, Zumbado ML, Limiñana-Cañal JM, Apolinario R, Serra-Majem L, Luzardo OP. Serum levels of insulin-like growth factor-I in relation to organochlorine pesticides exposure. Growth Hormone & IGF Research, 2007, 17(6):506–511

    Article  CAS  Google Scholar 

  73. Nomeir AA, Hajjar NP. Metabolism of chlordane in mammals. Rev Environ Contam Toxicol, 1987, 100:1–22

    CAS  Google Scholar 

  74. Sonawane BR. Chemical contaminants in human milk: an overview. Environ Health Perspect, 1995, 103(6):197–205

    Article  CAS  Google Scholar 

  75. Dougherty CP, Henricks Holtz S, Reinert JC, Panyacosit L, Axelrad DA, Woodruff TJ. Dietary exposures to food contaminants across the United States. Environ Res, 2000, 84(2):170–185

    Article  CAS  Google Scholar 

  76. Gaffney SH, Curriero FC, Strickland PT, Glass GE, Helzlsouer KJ, Breysse PN. Influence of geographic location in modeling blood pesticide levels in a community surrounding a US Environmental Protection Agency Superfund site. Environ Health Perspect, 2005, 113(12):1712–1716

    Article  CAS  Google Scholar 

  77. Glynn AW, Granath F, Aune M, Atuma S, Darnerud PO, Bjerselius R, Vainio H, Weiderpass E. Organochlorines in Swedish women: determinants of serum concentrations. Environ Health Perspect, 2003, 111(3):349–355

    CAS  Google Scholar 

  78. Langer P, Kočan A, Tajtaková M, Petrík J, Chovancová J, Drobná B, Jursa S, Rádiková Z, Koška J, Kšinantová L, Hučková M, Imrich R, Wimmerová S, Gašperíková D, Shishiba Y, Trnovec T, Šeböková E, Klimeš I. Fish from industrially polluted freshwater as the main source of organochlorinated pollutants and increased frequency of thyroid disorders and dysglycemia. Chemosphere, 2007, 67(9):S379–385

    Article  CAS  Google Scholar 

  79. Codru N, Schymura MJ, Negoita S, Akwesasne Task Force on the Environment, Rej R, Carpenter DO. Diabetes in relation to serum levels of polychlorinated biphenyls and chlorinated pesticides in adult native americans. Environ Health Perspect, 2007, 115(10):1442–1447

    CAS  Google Scholar 

  80. Rogers JM, Morelli L, Grabowski CT. Plasma glucose and protein concentrations in rat fetuses and neonates exposed to cataractogenic doses of mirex. Environ Res, 1984, 34(1):155–161

    Article  CAS  Google Scholar 

  81. Ervin MG, Yarbrough JD. Mirex-induced liver enlargement in rats is dependent upon an intact pituitary-adrenalcortical axis. Life Sci, 1985, 36(2):139–145

    Article  CAS  Google Scholar 

  82. Keller JM, Kucklick JR, Stamper MA, Harms CA, McClellan-Green PD. Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina, USA. Environ Health Perspect, 2004, 112(10):1074–1079

    CAS  Google Scholar 

  83. Schecter A, Päpke O, Tung KC, Joseph J, Harris TR, Dahlgren J. Polybrominated diphenyl ether flame retardants in the US population: current levels, temporal trends, and comparison with dioxins, dibenzofurans, and polychlorinated biphenyls. J Occup Environ, Hale RC, Alaee M, Manchester-Neesvig JB, Stapleton HM, Ikonomou MG. Polybrominated diphenyl ether flame retardants in the North American environment. Environ Int, 2003, 29(6):771–779

    Article  CAS  Google Scholar 

  84. Müllerová D, Kopecký J. White adipose tissue: storage and effector site for environmental pollutants. Physiol Res, 2007, 56(4):375–381

    Google Scholar 

  85. Rudel RA, Camann DE, Spengler JD, Korn LR, Brody JG. Phthalates, alkylphenols, pesticides, polybrominated diphenyl ethers, and other endocrine-disrupting compounds in indoor air and dust. Environ Sci Technol, 2003, 37(20):4543–4553

    Article  CAS  Google Scholar 

  86. Wilford BH, Harner T, Zhu J, Shoeib M, Jones KC. Passive sampling survey of polybrominated diphenyl ether flame retardants in indoor and outdoor air in Ottawa, Canada: implications for sources and exposure. Environ Sci Technol, 2004, 38(20):5312–5318

    Article  CAS  Google Scholar 

  87. Gouin T, Thomas GO, Cousins I, Barber J, MacKay D, Jones KC. Airsurface exchange of polybrominated diphenyl ethers and polychlorinated biphenyls. Environ Sci Technol, 2002, 36(7):1426–1434

    Article  CAS  Google Scholar 

  88. Domingo JL. Human exposure to polybrominated diphenyl ethers through the diet. J Chromatogr A, 2004, 1054(1–2): 321–326; Schecter A, Päpke O, Tung KC, Staskal D, Birnbaum L. Polybrominated diphenyl ethers contamination of United States food. Environ Sci Technol, 2004, 38 (20):5306–5311

    Article  CAS  Google Scholar 

  89. Allchin CR, Law RJ, Morris S. Polybrominated diphenylethers in sediments and biota downstream of potential sources in the UK. Environ Pollution, 1999, 105(2):197–207

    Article  CAS  Google Scholar 

  90. Lim JS, Lee DH, Jacobs DR Jr. Association of brominated flame retardants with diabetes and metabolic syndrome in the US population, 2003–2004. Diabetes Care, 2008, 31(9):1802–1807

    Article  Google Scholar 

  91. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic cell function in vivo and induces insulin resistance. Environ Health Perspect, 2006, 114(1):106–112

    Article  CAS  Google Scholar 

  92. Vom Saal FS, Myers JP. Bisphenol A and risk of metabolic disorders. JAMA, 2008, 300(11):1353–1355

    Article  Google Scholar 

  93. Ropero AB, Alonso-Magdalena P, García-García E, Ripoll C, Fuentes E, Nadal A. Bisphenol-A disruption of the endocrine pancreas and blood glucose homeostasis. Int J Androl, 2008, 31(2):194–200

    Article  CAS  Google Scholar 

  94. Alonso-Magdalena P, Ropero AB, Carrera MP, Cederroth CR, Baquié M, Gauthier BR, Nef S, Stefani E, Nadal A. Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS ONE, 2008, 3(4):e2069

    Article  CAS  Google Scholar 

  95. Sakurai K, Kawazuma M, Adachi T, Harigaya T, Saito Y, Hashimoto N, Mori C. Bisphenol A affects glucose transport in mouse 3T3-F442A adipocytes. Br J Pharmacol, 2004, 141(2):209–214

    Article  CAS  Google Scholar 

  96. Stahlhut RW, Wijngaarden EV, Dye TD, Cook S, Swan SH. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult US males. Environ Health Perspect, 2007, 115(6):876–882

    Article  CAS  Google Scholar 

  97. Rengarajan S, Parthasarathy C, Anitha M, Balasubramanian K. Diethylhexyl phthalate impairs insulin binding and glucose oxidation in Chang liver cells. Toxicol in Vitro, 2007, 21(1):99–102

    Article  CAS  Google Scholar 

  98. Zhang Z, Xu S. Molecular mechanisms of toxicity of dioxin-type chemicals. J Environ Health, 2000, 17(5):316–318

    CAS  Google Scholar 

  99. Long M, Andersen BS, Lindh CH, Hagmar L, Giwercman A, Manicardi GC, Bizzaro D, Spano M, Toft G, Pedersen HS, Zvyezday V, Bonde JP, Bonefeld-Jorgensen EC. Dioxin-like activities in serum across European and Inuit populations. Environ Health, 2006, 5:14

    Article  CAS  Google Scholar 

  100. Hansen LG. Stepping backward to improve assessment of PCB congener toxicities. Environ Health Perspect, 1998, 106(1):171–189

    Article  CAS  Google Scholar 

  101. Fletcher N, Wahlstrom D, Lundberg R, Nilissson CB, Nilsson KC, Stockling K, Hellnold H, Håkansson H. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters the mRNA expression of critical genes associated with cholesterol metabolism, bile acid biosynthesis, and bile transport in rat liver: A microarray study. Toxicol Appl Pharmacol, 2005, 207(1):1–24

    Article  CAS  Google Scholar 

  102. Croutch CR, Lebofsky M, Schramm KW, Terranova PJ, Rozman KK. 2,3,7,8-tetrachloro-dibenzo-p-dioxin (TCDD) and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin (HxCDD) alter body weight by decreasing insulin-like growth factor 1 (IGF-1) signaling. Toxicol Sci, 2005, 85(1):560–571

    Article  CAS  Google Scholar 

  103. Johnson CD, Balagurunathan Y, Tadesse MG, Falahatpisheh MH, Brun M, Walker MK, Dougherty ER, Ramos KS. Unraveling gene-gene interactions regulated by ligands of the aryl hydrocarbon receptor. Environ Health Perspect, 2004, 112(4):403–412

    CAS  Google Scholar 

  104. Sweeney MH, Calvert GM, Egeland GA, Fingerhut MA, Halperin WE, Piactitelli LA. Review and update of the results of the NIOSH medical study of workers exposed to chemicals contaminated with 2,3,7,8-tetra-chlorodibenzo-p-dioxin. Teratog Carcinog Mutagen, 1997, 17(4–5):241–247

    Article  CAS  Google Scholar 

  105. Enan E, Matsumura F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)-induced changes in glucose transporting activity in guinea pigs, mice, and rats in vivo and in vitro. J Biochem Toxicol, 1994, 9(2):97–106

    Article  CAS  Google Scholar 

  106. Liu PC, Matsumura F. Differential effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the “adipose-type” and “brain-type” glucose transporters in mice. Mol Pharmacol, 1995, 47(1):65–73

    CAS  Google Scholar 

  107. Olsen H, Enan E, Matsumura F. Regulation of glucose transport in the NIH 3T3 L1 preadipocyte cell line by TCDD. Environ Health Perspect, 1994, 102(5):454–458

    Article  CAS  Google Scholar 

  108. Minokoshi Y, Kahn CR, Kahn BB. Tissue-specific ablation of the GLUT4 glucose transporter or the insulin receptor challenges assumptions about insulin action and glucose homeostasis. J Biol Chem, 2003, 278(36):33609–33612

    Article  CAS  Google Scholar 

  109. Liu H, Biegel L, Narasimhan TR, Rowlands C, Safe S. Inhibition of insulin-like growth factor-I responses in MCF-7 cells by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Mol Cell Endocrinol, 1992, 87(1–3):19–28

    Article  CAS  Google Scholar 

  110. Fischer LJ, Wagner MA, Madhukar BV. Potential involvement of calcium, CaM kinase II, and MAP kinases in PCB-stimulated insulin release from RINm5F cells. Toxicol Appl Pharmacol, 1999, 159(3):194–203

    Article  CAS  Google Scholar 

  111. Kimbrough RD, Linder RE, Gaines TB. Morphological changes in livers of rats fed polychlorinated biphenyls: light microscopy and ultrastructure. Arch Environ Health, 1972, 25:354–364

    CAS  Google Scholar 

  112. Liu Z, Yu J, Xu S. Impact of environmental pollution on human and its countermeasures in China. Environ Protection, 2005 (4):31–34

  113. Jørgensen ME, Borch-Johnsen K, Bjerregaard P. A cross-sectional study of the association between persistent organic pollutants and glucose intolerance among Greenland Inuit. Diabetologia, 2008, 51(8):1416–1422

    Article  CAS  Google Scholar 

  114. Carvalho CR, Carvalheira JB, Lima MH, Zimmerman SF, Caperuto LC, Amanso A, Gasparetti AL, Meneghetti V, Zimmerman LF, Velloso LA, Saad MJ. Novel signal transduction pathway for luteinizing hormone and its interaction with insulin: activation of janus kinase/signal transducer and activator of transcription and phosphoinositol 3-kinase/akt pathways. Endocrinology, 2003, 144(2):638–647

    Article  CAS  Google Scholar 

  115. Lee DH, Steffes MW, Jacobs DR Jr. Can persistent organic pollutants explain the association between serum gamma-glutamyltransferase and type 2 diabetes? Diabetologia, 2008c, 51(3):402–407

    Article  CAS  Google Scholar 

  116. Wada K, Sakamoto H, Nishikawa K, Sakuma S, Nakajima A, Fujimoto Y, Kamisaki Y. Life style-related diseases of the digestive system: endocrine disruptor stimulate lipid accumulation in target cells related to metabolic syndrome. J Pharmacol Sci, 2007, 105(2):133–137

    Article  CAS  Google Scholar 

  117. Alonso-Magdalena P, Laribi O, Ropero AB, Fuentes E, Ripoll C. Low doses of Bisphenol A and Diethylstilbestrol Impair Ca2+ signals in pancreatic a-cells through a non-classical membrane estrogen receptor within intact islets of langerhans. Environ Health Perspect, 2005, 113(8):969–977

    Article  CAS  Google Scholar 

  118. Smith SA. Peroxisome proliferator-activated receptors and the regulation of mammalian lipid metabolism. Biochem Soc Transaction, 2001, 30(6):1086–1090

    Article  Google Scholar 

  119. Hokanson R, Miller S, Hennessey M, Flesher M, Hanneman W, Busbee D. Disruption of estrogen-regulated gene expression by dioxin: downregulation of a gene associated with the onset of non-insulin-dependent diabetes mellitus (type 2 diabetes). Hum Exp Toxicol, 2004, 23(12):555–564

    Article  CAS  Google Scholar 

  120. Marchand A, Tomkiewicz C, Marchandeau JP, Boitier E, Barouki R, Garlatti M. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces insulin-like growth factor binding protein-1 gene expression and counteracts the negative effect of insulin. Mol Pharmaco, 2005, 67(2):444–452

    Article  CAS  Google Scholar 

  121. Ferré P. The biology of peroxisome proliferator-activated receptors: relationship with lipid metabolism and insulin sensitivity. Diabetes, 2004, 53(1):43–50

    Article  Google Scholar 

  122. Latini G, Scoditti E, Verrotti A, De Felice C, Massaro M. Peroxisome proliferator-activated receptors as mediators of phthalate induced effects in the male and female reproductive tract: epidemiological ad experimental evidence. PPAR Res, 2008, 2008:359267

    Google Scholar 

  123. Hurst CH, Waxman DJ. Activation of PPARalpha and PPARgamma by environmental phthalate monoesters. Toxicol Sci, 2003, 74(2):297–308

    Article  CAS  Google Scholar 

  124. Latini G, Marcovecchio ML, Del Vecchio A, Gallo F, Bertino E, Chiarelli F. Influence of environment on insulin sensitivity. Environ International, 2009, 35(6):987–993

    Article  CAS  Google Scholar 

  125. Uysal KT, Wiesbrock SM, Marino MW, Hotam-isligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature, 1997, 389(6651):610–614

    Article  CAS  Google Scholar 

  126. Kern PA, Dicker-Brown A, Said ST, Kennedy R, Fonseca VA. The stimulation of tumor necrosis factor and inhibition of glucose transport and lipoprotein lipase in adipose cells by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Metabolism, 2002, 51(1):65–68

    Article  CAS  Google Scholar 

  127. Ruan H, Hacohen N, Golub TR, Van Parijs L, Lodish HF. Tumor necrosis factor-alpha suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-alpha is obligatory. Diabetes, 2002, 51(5):1319–1336

    Article  CAS  Google Scholar 

  128. Agency for Toxic Substances and Disease Registry. Toxicological Profile for DDT, DDE, and DDD. Atlanta, GA: Agency for Toxic Substances and Disease Registry. 2002

  129. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev, 2007, 87(2):507–520

    Article  CAS  Google Scholar 

  130. Almind K, Bjørbaek C, Vestergaard H, Hansen T, Echwald S, Pedersen O. Amino acid polymorphisms of insulin receptor substrate-1 in noninsulin-dependent diabetes mellitus. Lancet, 1993, 342(8875):828–832

    Article  CAS  Google Scholar 

  131. Baroni MG, Oelbaum RS, Pozzilli P, Stocks J, Li SR, Fiore V, Galton DJ. Polymorphisms at the GLUT1 (HepG2) and GLUT4 (muscle/adipocyte) glucose transporter genes and non-insulin-dependent diabetes mellitus (NIDDM). Hum Genet, 1992, 88(5):557–561

    Article  CAS  Google Scholar 

  132. Langer P, Tájtáková M, Guretzki H, Kocan A, Petrik J, Chovancová J, Drobná B, Jursa S, Pavúk M, Trnovec T, Seböková E, Klimes I. High prevalence of anti-glutamic acid decarboxylase (anti-GAD) antibodies in employees at a polychlorinated biphenyl production factory. Arch Environ Health, 2002, 57:412–415

    Article  CAS  Google Scholar 

  133. Mazzetti MB, Taira MC, Lelli SM, Dascal E, Basabe JC, de Viale LC. Hexachlorobenzene impairs glucose metabolism in a rat model of porphyria cutanea tarda: a mechanistic approach. Arch Toxicol, 2004, 78(1):25–33

    Article  CAS  Google Scholar 

  134. Michalek JE, Ketchum NS, Tripathi RC. Diabetes mellitus and 2,3,7,8-tetrachlorodibenzo-p-dioxin elimination in veterans of Operation Ranch Hand. J Toxicol Environ Health A, 2003, 66(3):211–221

    Article  CAS  Google Scholar 

  135. Wong MH, Leung AO, Chan JK, Choi MP. A review on the usage of POP pesticides in China, with emphasis on DDT loadings in human milk. Chemosphere, 2005, 60(6):740–752

    Article  CAS  Google Scholar 

  136. Fu J, Mai B, Sheng G, Zhang G, Wang X, Peng P, Xiao X, Ran R, Cheng F, Peng X, Wang Z, Tang UW. Persistent organic pollutants in environment of the Pearl River Delta, China: an overview. Chemosphere, 2003, 52(9):1411–22

    Article  CAS  Google Scholar 

  137. Wang B, Fukuya I, Yu G, Huang J, Wei Y, Yamazaki N, Chen J, Chen X, Jiang W, Morita M. HRGC/HRMS analysis of mirex in soil of Liyang and preliminary assessment of mirex pollution in China. Chemosphere, 2010, 79:299–304

    Article  CAS  Google Scholar 

  138. Zhang P, Song J, Yuan H. Persistent organic pollutant residues in the sediments and mollusks from the Bohai Sea coastal areas, North China: an overview. Environ International, 2009, 35:632–646

    Article  CAS  Google Scholar 

  139. Hu G, Dai J, Mai B, Luo X, Cao H, Wang J, Li F, Xu M. Concentrations and accumulation features of organochlorine pesticides in the baiyangdian lake freshwater food web of North China. Arch Environ Contam Toxicol, 2009, DOI 10.1007/s00244-009-9400-1

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Wang, C., Xu, S., Lv, Z. et al. Exposure to persistent organic pollutants as potential risk factors for developing diabetes. Sci. China Chem. 53, 980–994 (2010). https://doi.org/10.1007/s11426-010-0157-1

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