Exposure to organochlorine pollutants and type 2 diabetes: a systematic review and meta-analysis

Mengling Tang, Kun Chen, Fangxing Yang, Weiping Liu, Mengling Tang, Kun Chen, Fangxing Yang, Weiping Liu

Abstract

Objective: Though exposure to organochlorine pollutants (OCPs) is considered a risk factor for type 2 diabetes (T2DM), epidemiological evidence for the association remains controversial. A systematic review and meta-analysis was applied to quantitatively evaluate the association between exposure to OCPs and incidence of T2DM and pool the inconsistent evidence.

Design and methods: Publications in English were searched in MEDLINE and WEB OF SCIENCE databases and related reference lists up to August 2013. Quantitative estimates and information regarding study characteristics were extracted from 23 original studies. Quality assessments of external validity, bias, exposure measurement and confounding were performed, and subgroup analyses were conducted to examine the heterogeneity sources.

Results: We retrieved 23 eligible articles to conduct this meta-analysis. OR (odds ratio) or RR (risk ratio) estimates in each subgroup were discussed, and the strong associations were observed in PCB-153 (OR, 1.52; 95% CI, 1.19-1.94), PCBs (OR, 2.14; 95% CI, 1.53-2.99), and p,p'-DDE (OR, 1.33; 95% CI, 1.15-1.54) based on a random-effects model.

Conclusions: This meta-analysis provides quantitative evidence supporting the conclusion that exposure to organochlorine pollutants is associated with an increased risk of incidence of T2DM.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. The study search and selection…
Figure 1. The study search and selection process.
Figure 2. Subgroup analysis forest plots of…
Figure 2. Subgroup analysis forest plots of the studies on T2DM risk from exposure to all three biomarkers.
(A) Result of exposure to PCB-153. (B) Result of exposure to PCBs. (C) Result of exposure to p,p′-DDE.
Figure 3. A funnel plot of SE…
Figure 3. A funnel plot of SE versus ln(OR) for the meta-analyses.
(A) Funnel plot for the meta-analysis on T2DM from background exposure to PCB-153. (B) Funnel plot for the subgroup analysis of serum lipid on T2DM from exposure to PCB-153. (C) Funnel plot for the subgroup analysis on T2DM from background exposure to p,p′-DDE. (D) Funnel plot for the subgroup analysis of the cross-sectional study on T2DM from exposure to p,p′-DDE. (E) Funnel plot for the subgroup analysis of the general population on T2DM from exposure to p,p′-DDE. (F) Funnel plot for the subgroup analysis of serum lipid on T2DM from exposure to p,p′-DDE.

References

    1. Govarts E, Nieuwenhuijsen M, Schoeters G, Ballester F, Bloemen K, et al. (2012) Birth Weight and Prenatal Exposure to Polychlorinated Biphenyls (PCBs) and Dichlorodiphenyldichloroethylene (DDE): A Meta-analysis within 12 European Birth Cohorts. Environ Health Perspect 120: 162–170.
    1. Lopez-Cervantes M, Torres-Sanchez L, Tobias A, Lopez-Carrillo L (2004) Dichlorodiphenyldichloroethane burden and breast cancer risk: A meta-analysis of the epidemiologic evidence. Environ Health Perspect 112: 207–214.
    1. Ntow WJ, Tagoe LM, Drechsel P, Kelderman P, Gijzen HJ, et al. (2008) Accumulation of persistent organochlorine contaminants in milk and serum of farmers from Ghana. Environ Res 106: 17–26.
    1. Ren AG, Qiu XH, Jin L, Ma J, Li ZW, et al. (2011) Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects. Proc Natl Acad Sci U S A 108: 12770–12775.
    1. Navas-Acien A, Silbergeld EK, Streeter RA, Clark JM, Burke TA, et al. (2006) Arsenic exposure and type 2 diabetes: A systematic review of the experimental and epidemiologic evidence. Environ Health Perspect 114: 641–648.
    1. Chiasson JL, Josse RG, Gomis R, Hanefeld M, Karasik A, et al. (2002) Acarbose for prevention of type 2 diabetes mellitus: the STOP-NIDDM randomised trial. Lancet 359: 2072–2077.
    1. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, et al. (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881–885.
    1. Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840–846.
    1. Gress TW, Nieto FJ, Shahar E, Wofford MR, Brancati FL (2000) Hypertension and antihypertensive therapy as risk factors for type 2 diabetes mellitus. Atherosclerosis risk in communities study. N Engl J Med 342: 905–912.
    1. Patel CJ, Bhattacharya J, Butte AJ (2010) An environment-wide association study (EWAS) on type 2 diabetes mellitus. PLoS One 5: e10746.
    1. Everett CJ, Frithsen IL, Diaz VA, Koopman RJ, Simpson WM, et al. (2007) 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 103: 413–418.
    1. Turyk M, Anderson H, Knobeloch L, Imm P, Persky V (2009) Organochlorine exposure and incidence of diabetes in a cohort of Great Lakes sport fish consumers. Environ Health Perspect 117: 1076–1082.
    1. Thayer KA, Heindel JJ, Bucher JR, Gallo MA (2012) Role of environmental chemicals in diabetes and obesity: a national toxicology program workshop review. Environ Health Perspect 120: 779–789.
    1. Remillard RB, Bunce NJ (2002) Linking dioxins to diabetes: epidemiology and biologic plausibility. Environ Health Perspect 110: 853–858.
    1. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39: 359–407.
    1. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, et al. (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6 (7) e1000100.
    1. Downs SH, Black N (1998) The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health 52: 377–384.
    1. Wigle DT, Turner MC, Krewski D (2009) A systematic review and meta-analysis of childhood leukemia and parental occupational pesticide exposure. Environ Health Perspect 117: 1505–1513.
    1. Hardy RJ, Thompson SG (1998) Detecting and describing heterogeneity in meta-analysis. Stat Med 17: 841–856.
    1. Higgins J, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. Br Med J 327: 557–560.
    1. Vrijheid M, Martinez D, Manzanares S, Dadvand P, Schembari A, et al. (2011) Ambient air pollution and risk of congenital anomalies: a systematic review and meta-analysis. Environ Health Perspect 119: 598–606.
    1. Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22: 719–748.
    1. Dersimonian R, Laird N (1986) Meta-analysis in clinical-trials. Controlled Clin Trials 7: 177–188.
    1. Gasull M, Pumarega J, Tellez-Plaza M, Castell C, Tresserras R, et al. (2012) Blood concentrations of persistent organic pollutants and prediabetes and diabetes in the general population of catalonia. Environ Sci Technol 46: 7799–7810.
    1. Silverstone AE, Rosenbaum PF, Weinstock RS, Bartell SM, Foushee HR, et al. (2012) Polychlorinated biphenyl (PCB) exposure and diabetes: results from the Anniston Community Health Survey. Environ Health Perspect 120: 727–732.
    1. Persky V, Piorkowski J, Turyk M, Freels S, Chatterton RJ, et al. (2012) Polychlorinated biphenyl exposure, diabetes and endogenous hormones: a cross-sectional study in men previously employed at a capacitor manufacturing plant. Environ Health 11: 57.
    1. Tanaka T, Morita A, Kato M, Hirai T, Mizoue T, et al. (2011) Congener-specific polychlorinated biphenyls and the prevalence of diabetes in the Saku Control Obesity Program. Endocr J 58: 589–596.
    1. Grandjean P, Henriksen JE, Choi AL, Petersen MS, Dalgard C, et al. (2011) Marine food pollutants as a risk factor for hypoinsulinemia and type 2 diabetes. Epidemiology 22: 410–417.
    1. Airaksinen R, Rantakokko P, Eriksson JG, Blomstedt P, Kajantie E, et al. (2011) Association between type 2 diabetes and exposure to persistent organic pollutants. Diabetes Care 34: 1972–1979.
    1. Lee DH, Lind PM, Jacobs DJ, Salihovic S, van Bavel B, et al. (2011) 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 34: 1778–1784.
    1. Son HK, Kim SA, Kang JH, Chang YS, Park SK, et al. (2010) Strong associations between low-dose organochlorine pesticides and type 2 diabetes in Korea. Environ Int 36: 410–414.
    1. Everett CJ, Matheson EM (2010) Biomarkers of pesticide exposure and diabetes in the 1999–2004 national health and nutrition examination survey. Environ Int 36: 398–401.
    1. Ukropec J, Radikova Z, Huckova M, Koska J, Kocan A, et al. (2010) High prevalence of prediabetes and diabetes in a population exposed to high levels of an organochlorine cocktail. Diabetologia 53: 899–906.
    1. Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, et al. (2010) Low dose of some persistent organic pollutants predicts type 2 diabetes: a nested case-control study. Environ Health Perspect 118: 1235–1242.
    1. Philibert A, Schwartz H, Mergler D (2009) 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 6: 3179–3189.
    1. Rignell-Hydbom A, Lidfeldt J, Kiviranta H, Rantakokko P, Samsioe G, et al. (2009) Exposure to p,p′-DDE: a risk factor for type 2 diabetes. PLoS One 4: e7503.
    1. Wang SL, Tsai PC, Yang CY, Guo YL (2008) Increased risk of diabetes and polychlorinated biphenyls and dioxins - A 24-year follow-up study of the Yucheng cohort. Diabetes Care 31: 1574–1579.
    1. Codru N, Schymura MJ, Negoita S, Rej R, Carpenter DO (2007) Diabetes in relation to serum levels of polychlorinated biphenyls and chlorinated pesticides in adult Native Americans. Environ Health Perspect 115: 1442–1447.
    1. Rignell-Hydbom A, Rylander L, Hagmar L (2007) Exposure to persistent organochlorine pollutants and type 2 diabetes mellitus. Hum Exp Toxicol 26: 447–452.
    1. Cox S, Niskar AS, Narayan KM, Marcus M (2007) Prevalence of self-reported diabetes and exposure to organochlorine pesticides among Mexican Americans: Hispanic health and nutrition examination survey, 1982–1984. Environ Health Perspect 115: 1747–1752.
    1. Lee DH, Lee IK, Song K, Steffes M, Toscano W, et al. (2006) 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 29: 1638–1644.
    1. Rylander L, Rignell-Hydbom A, Hagmar L (2005) A cross-sectional study of the association between persistent organochlorine pollutants and diabetes. Environ Health 4: 28.
    1. Fierens S, Mairesse H, Heilier JF, De Burbure C, Focant JF, et al. (2003) Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers 8: 529–534.
    1. Arrebola JP, Pumarega J, Gasull M, Fernandez MF, Martin-Olmedo P, et al. (2013) Adipose tissue concentrations of persistent organic pollutants and prevalence of type 2 diabetes in adults from Southern Spain. Environ Res 122: 31–37.
    1. Wu HY, Bertrand KA, Choi AL, Hu FB, Laden F, et al. (2013) Persistent organic pollutants and type 2 diabetes: a prospective analysis in the nurses' health study and meta-analysis. Environ Health Perspect 121: 153–161.
    1. Lee DH, Jacobs DJ, Steffes M (2008) Association of organochlorine pesticides with peripheral neuropathy in patients with diabetes or impaired fasting glucose. Diabetes 57: 3108–3111.
    1. Lee DH, Lee IK, Jin SH, Steffes M, Jacobs DJ (2007) 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 30: 622–628.
    1. Turyk M, Anderson HA, Knobeloch L, Imm P, Persky VW (2009) Prevalence of diabetes and body burdens of polychlorinated biphenyls, polybrominated diphenyl ethers, and p,p′-diphenyldichloroethene in Great Lakes sport fish consumers. Chemosphere 75: 674–679.
    1. Montgomery MP, Kamel F, Saldana TM, Alavanja MC, Sandler DP (2008) Incident diabetes and pesticide exposure among licensed pesticide applicators: Agricultural Health Study, 1993–2003. Am J Epidemiol 167: 1235–1246.
    1. Vasiliu O, Cameron L, Gardiner J, Deguire P, Karmaus W (2006) Polybrominated biphenyls, polychlorinated biphenyls, body weight, and incidence of adult-onset diabetes mellitus. Epidemiology 17: 352–359.
    1. Glynn AW, Granath F, Aune M, Atuma S, Darnerud PO, et al. (2003) Organochlorines in Swedish women: determinants of serum concentrations. Environ Health Perspect 111: 349–355.
    1. Everett CJ, Frithsen IL, Diaz VA, Koopman RJ, Simpson WJ, et al. (2007) 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 103: 413–418.
    1. Longnecker MP, Klebanoff MA, Brock JW, Zhou H (2001) Polychlorinated biphenyl serum levels in pregnant subjects with diabetes. Diabetes Care 24: 1099–1101.
    1. Fierens S, Mairesse H, Heilier JF, De Burbure C, Focant JF, et al. (2003) Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers 8: 529–534.
    1. Bernert JT, Turner WE, Patterson DG, Needham LL (2007) Calculation of serum “total lipid” concentrations for the adjustment of persistent organohalogen toxicant measurements in human samples. Chemosphere 68: 824–831.
    1. Turner MC, Wigle DT, Krewski D (2010) Residential pesticides and childhood leukemia: a systematic review and meta-analysis. Environ Health Perspect 118: 33–41.
    1. Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9: 1–30.
    1. Henley P, Hill J, Moretti ME, Jahedmotlagh Z, Schoeman K, et al. (2012) Relationships between exposure to polyhalogenated aromatic hydrocarbons and organochlorine pesticides and the risk for developing type 2 diabetes: a systematic review and a meta-analysis of exposures to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Environ Chem 94: 814–845.
    1. Everett CJ, Frithsen I, Player M (2011) Relationship of polychlorinated biphenyls with type 2 diabetes and hypertension. J Environ Monit 13: 241–251.
    1. Langer P (2010) The impacts of organochlorines and other persistent pollutants on thyroid and metabolic health. Fron Neuroendocrinol 31: 497–518.
    1. Jorgensen ME, Borch-Johnsen K, Bjerregaard P (2008) A cross-sectional study of the association between persistent organic pollutants and glucose intolerance among Greenland Inuit. Diabetologia 51: 1416–1422.

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