Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: A systematic review and meta-analysis

Journal of Diabetes

Volumn 8, Issue 4, 2016, Pages 516-532

  Song, Yan ^a,b   Chou, Elizabeth L ^g   Baecker, Aileen ^a   You, Nai Chieh Y ^a   Song, Yiqing ^d   Sun, Qi ^e,f   Liu, Simin ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BROWN UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

^d INDIANA UNIVERSITY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

bisphenol A; diabetes; endocrine disrupting chemical; meta analysis; phthalate

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CHLORINATED PESTICIDE; DIOXIN; ENDOCRINE DISRUPTOR; PESTICIDE; PHTHALIC ACID; POLYCHLORINATED BIPHENYL; UNCLASSIFIED DRUG;

ARTICLE; BLOOD LEVEL; CROSS-SECTIONAL STUDY; DIABETES RELATED METABOLIC TRAIT; DISEASE ASSOCIATION; GENETIC TRAIT; HUMAN; IMPAIRED GLUCOSE TOLERANCE; INSULIN RESISTANCE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; RISK ASSESSMENT; SYSTEMATIC REVIEW; URINE LEVEL;

EID: 84973866680     PISSN: 17530393     EISSN: 17530407     Source Type: Journal    
DOI: 10.1111/1753-0407.12325     Document Type: Article

References (74)

1. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC et al. Endocrine-disrupting chemicals: An Endocrine Society scientific statement. Endocr Rev. 2009; 30: 293–342.
2. Alonso-Magdalena P, Quesada I, Nadal A. Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat Rev Endocrinol. 2011; 7: 346–353.
3. Calafat AM, Weuve J, Ye X et al. Exposure to bisphenol A and other phenols in neonatal intensive care unit premature infants. Environ Health Perspect. 2009; 117: 639–644.
4. Thayer KA, Heindel JJ, Bucher JR, Gallo MA. Role of environmental chemicals in diabetes and obesity: A National Toxicology Program workshop review. Environ Health Perspect. 2012; 120: 779–789.
5. Wu H, Bertrand KA, Choi AL et al. Persistent organic pollutants and type 2 diabetes: A prospective analysis in the Nurses' Health Study and meta-analysis. Environ Health Perspect. 2013; 121: 153–161.
6. Silverstone AE, Rosenbaum PF, Weinstock RS et al. Polychlorinated biphenyl (PCB) exposure and diabetes: Results from the Anniston Community Health Survey. Environ Health Perspect. 2012; 120: 727–732.
7. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7: 177–188.
8. Greenland S, Longnecker MP. Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am J Epidemiol. 1992; 135: 1301–1309.
9. Borenstein M, Hedges L, Higgins J, Rothstein H. Converting among effect sizes. In: Borenstein M, Hedges L, Higgins J, Rothstein H (eds). Introduction to Meta-Analysis. John Wiley & Sons, Chichester, 2009; 45–49.
10. Duval S, Tweedie R. Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000; 56: 455–463.
11. Calvert GM, Sweeney MH, Deddens J, Wall DK. Evaluation of diabetes mellitus, serum glucose, and thyroid function among United States workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Occup Environ Med. 1999; 56: 270–276.
12. Longnecker MP, Michalek JE. Serum dioxin level in relation to diabetes mellitus among Air Force veterans with background levels of exposure. Epidemiology. 2000; 11: 44–48.
13. Cranmer M, Louie S, Kennedy RH, Kern PA, Fonseca VA. Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is associated with hyperinsulinemia and insulin resistance. Toxicol Sci. 2000; 56: 431–436.
14. Fierens S, Mairesse H, Heilier JF et al. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: Findings in a population-based study in Belgium. Biomarkers. 2003; 8: 529–534.
15. Lee DH, Lee IK, Song K et al. A strong dose–response relation between serum concentrations of persistent organic pollutants and diabetes: Results from the National Health and Examination Survey 1999–2002. Diabetes Care. 2006; 29: 1638–1644.
16. Chen HL, Su HJ, Guo YL, Liao PC, Hung CF, Lee CC. Biochemistry examinations and health disorder evaluation of Taiwanese living near incinerators and with low serum PCDD/Fs levels. Sci Total Environ. 2006; 366: 538–548.
17. 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: 413–418.
18. Uemura H, Arisawa K, Hiyoshi M et al. Associations of environmental exposure to dioxins with prevalent diabetes among general inhabitants in Japan. Environ Res. 2008; 108: 63–68.
19. Chang JW, Chen HL, Su HJ, Liao PC, Guo HR, Lee CC. Dioxin exposure and insulin resistance in Taiwanese living near a highly contaminated area. Epidemiology. 2010; 21: 56–61.
20. Everett CJ, Thompson OM. Associations of dioxins, furans and dioxin-like PCBs with diabetes and pre-diabetes: Is the toxic equivalency approach useful? Environ Res. 2012; 118: 107–111.
21. Longnecker MP, Klebanoff MA, Brock JW, Zhou H. Polychlorinated biphenyl serum levels in pregnant subjects with diabetes. Diabetes Care. 2001; 24: 1099–1101.
22. 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.
23. Codru N, Schymura MJ, Negoita S, 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: 1442–1447.
24. Rignell-Hydbom A, Rylander L, Hagmar L. Exposure to persistent organochlorine pollutants and type 2 diabetes mellitus. Hum Exp Toxicol. 2007; 26: 447–452.
25. Jorgensen 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: 1416–1422.
26. Chen JW, Wang SL, Liao PC, Chen HY, Ko YC, Lee CC. Relationship between insulin sensitivity and exposure to dioxins and polychlorinated biphenyls in pregnant women. Environ Res. 2008; 107: 245–253.
27. Philibert A, Schwartz H, Mergler D. An exploratory study of diabetes in a First Nation community with respect to serum concentrations of p,p′-DDE and PCBs and fish consumption. Int J Environ Res Public Health. 2009; 6: 3179–3189.
28. Langer P, Kocan A, Tajtakova M et al. Multiple adverse thyroid and metabolic health signs in the population from the area heavily polluted by organochlorine cocktail (PCB, DDE, HCB, dioxin). Thyroid Res. 2009; 2: 3.
29. Ukropec J, Radikova Z, Huckova M et al. High prevalence of prediabetes and diabetes in a population exposed to high levels of an organochlorine cocktail. Diabetologia. 2010; 53: 899–906.
30. 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: 1972–1979.
31. Dirinck E, Jorens PG, Covaci A et al. Obesity and persistent organic pollutants: Possible obesogenic effect of organochlorine pesticides and polychlorinated biphenyls. Obesity (Silver Spring). 2011; 19: 709–714.
32. Gasull M, Pumarega J, Tellez-Plaza M et al. Blood concentrations of persistent organic pollutants and prediabetes and diabetes in the general population of Catalonia. Environ Sci Technol. 2012; 46: 7799–7810.
33. Lim JS, Lee DH, Jacobs DR Jr. Association of brominated flame retardants with diabetes and metabolic syndrome in the U.S. population, 2003–2004. Diabetes Care. 2008; 31: 1802–1807.
34. 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: 1747–1752.
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. 2007; 30: 622–628.
36. Son HK, Kim SA, Kang JH et al. Strong associations between low-dose organochlorine pesticides and type 2 diabetes in Korea. Environ Int. 2010; 36: 410–414.
37. Park SK, Son HK, Lee SK et al. Relationship between serum concentrations of organochlorine pesticides and metabolic syndrome among non-diabetic adults. J Prev Med Public Health. 2010; 43: 1–8.
38. Arrebola JP, Pumarega J, Gasull M et al. Adipose tissue concentrations of persistent organic pollutants and prevalence of type 2 diabetes in adults from Southern Spain. Environ Res. 2013; 122: 31–37.
39. Lang IA, Galloway TS, Scarlett A et al. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA. 2008; 300: 1303–1310.
40. Ning G, Bi Y, Wang T et al. Relationship of urinary bisphenol A concentration to risk for prevalent type 2 diabetes in Chinese adults: A cross-sectional analysis. Ann Intern Med. 2011; 155: 368–374.
41. Shankar A. Teppala S. Relationship between urinary bisphenol A levels and diabetes mellitus. J Clin Endocrinol Metab. 2011; 96: 3822–3826.
42. Li TT, Xu LZ, Chen YH et al. Effects of eight environmental endocrine disruptors on insulin resistance in patients with polycystic ovary syndrome: A preliminary investigation. Nan Fang Yi Ke Da Xue Xue Bao. 2011; 31: 1753–1756 (in Chinese).
43. Wang T, Li M, Chen B et al. Urinary bisphenol A (BPA) concentration associates with obesity and insulin resistance. J Clin Endocrinol Metab. 2012; 97: e223–227.
44. Kim K, Park H. Association between urinary concentrations of bisphenol A and type 2 diabetes in Korean adults: A population-based cross-sectional study. Int J Hyg Environ Health. 2013; 216: 467–471.
45. Beydoun HA, Khanal S, Zonderman AB, Beydoun MA. Sex differences in the association of urinary bisphenol-A concentration with selected indices of glucose homeostasis among US adults. Ann Epidemiol. 2014; 24: 90–97.
46. Stahlhut RW, van Wijngaarden E, 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: 876–882.
47. Lind PM, Zethelius B, Lind L. Circulating levels of phthalate metabolites are associated with prevalent diabetes in the elderly. Diabetes Care. 2012; 35: 1519–1524.
48. James-Todd T, Stahlhut R, Meeker JD et al. Urinary phthalate metabolite concentrations and diabetes among women in the National Health and Nutrition Examination Survey (NHANES) 2001–2008. Environ Health Perspect. 2012; 120: 1307–1313.
49. Olsen L, Lind L, Lind PM. Associations between circulating levels of bisphenol A and phthalate metabolites and coronary risk in the elderly. Ecotoxicol Environ Saf. 2012; 80: 179–183.
50. Kim JH, Park HY, Bae S, Lim YH, Hong YC. Diethylhexyl phthalates is associated with insulin resistance via oxidative stress in the elderly: A panel study. PLoS ONE. 2013; 8: e71392.
51. 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: 352–359.
52. 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: 1574–1579.
53. 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. Environ Health Perspect. 2009; 117: 1076–1082.
54. Rignell-Hydbom A, Lidfeldt J, Kiviranta H et al. Exposure to p,p′-DDE: A risk factor for type 2 diabetes. PLoS ONE. 2009; 4: e7503.
55. Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, Jacobs DR Jr. Low dose of some persistent organic pollutants predicts type 2 diabetes: A nested case-control study. Environ Health Perspect. 2010; 118: 1235–1242.
56. Lee DH, Lind PM, Jacobs DR Jr, Salihovic S, van Bavel B, Lind L. Polychlorinated biphenyls and organochlorine pesticides in plasma predict development of type 2 diabetes in the elderly: The prospective investigation of the vasculature in Uppsala Seniors (PIVUS) study. Diabetes Care. 2011; 34: 1778–1784.
57. Sun Q, Cornelis MC, Townsend MK et al. Association of urinary concentrations of bisphenol A and phthalate metabolites with risk of type 2 diabetes: A prospective investigation in the Nurses' Health Study (NHS) and NHSII Cohorts. Environ Health Perspect. 2014; 122: 616–623.
58. Ding EL, Song Y, Malik VS, Liu S. Sex differences of endogenous sex hormones and risk of type 2 diabetes: A systematic review and meta-analysis. JAMA. 2006; 295: 1288–1299.
59. Ding EL, Song Y, Manson JE, Rifai N, Buring JE, Liu S. Plasma sex steroid hormones and risk of developing type 2 diabetes in women: A prospective study. Diabetologia. 2007; 50: 2076–2084.
60. Li C, Ford ES, Li B, Giles WH, Liu S. Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care. 2010; 33: 1618–1624.
61. Grun F, Blumberg B. Perturbed nuclear receptor signaling by environmental obesogens as emerging factors in the obesity crisis. Rev Endocr Metab Disord. 2007; 8: 161–171.
62. Byford JR, Shaw LE, Drew MG, Pope GS, Sauer MJ, Darbre PD. Oestrogenic activity of parabens in MCF7 human breast cancer cells. J Steroid Biochem Mol Biol. 2002; 80: 49–60.
63. Jung EM, An BS, Choi KC, Jeung EB. Potential estrogenic activity of triclosan in the uterus of immature rats and rat pituitary GH3 cells. Toxicol Lett. 2012; 208: 142–148.
64. Janjua NR, Mogensen B, Andersson AM et al. Systemic absorption of the sunscreens benzophenone-3, octyl-methoxycinnamate, and 3-(4-methyl-benzylidene) camphor after whole-body topical application and reproductive hormone levels in humans. J Invest Dermatol. 2004; 123: 57–61.
65. 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. 2007; 50: 1841–1851.
66. Melzer D, Rice NE, Lewis C, Henley WE, Galloway TS. Association of urinary bisphenol a concentration with heart disease: Evidence from NHANES 2003/06. PLoS ONE. 2010; 5: e8673.
67. Silver MK, O'Neill MS, Sowers MR, Park SK. Urinary bisphenol A and type-2 diabetes in US adults: Data from NHANES 2003–2008. PLoS ONE. 2011; 6: e26868.
68. 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: 674–679.
69. Grandjean P, Henriksen JE, Choi AL et al. Marine food pollutants as a risk factor for hypoinsulinemia and type 2 diabetes. Epidemiology. 2011; 22: 410–417.
70. Patel CJ, Bhattacharya J, Butte AJ. An environment-wide association study (EWAS) on type 2 diabetes mellitus. PLoS ONE. 2010; 5: e10746.
71. Persky V, Piorkowski J, Turyk M et al. Associations of polychlorinated biphenyl exposure and endogenous hormones with diabetes in post-menopausal women previously employed at a capacitor manufacturing plant. Environ Res. 2011; 111: 817–824.
72. Persky V, Piorkowski J, Turyk M et al. Polychlorinated biphenyl exposure, diabetes and endogenous hormones: A cross-sectional study in men previously employed at a capacitor manufacturing plant. Environ Health. 2012; 11: 57.
73. Svensson K, Hernandez-Ramirez RU, Burguete-Garcia A et al. Phthalate exposure associated with self-reported diabetes among Mexican women. Environ Res. 2011; 111: 792–796.
74. Montgomery MP, Kamel F, Saldana TM, Alavanja MC, Sandler DP. Incident diabetes and pesticide exposure among licensed pesticide applicators: Agricultural Health Study, 1993–2003. Am J Epidemiol. 2008; 167: 1235–1246.