Strong associations between the pesticide hexachlorocyclohexane and type 2 diabetes in Saudi adults

International Journal of Environmental Research and Public Health

Volumn 11, Issue 9, 2014, Pages 8984-8995

  Al Othman, Abdulaziz ^a,b   Yakout, Sobhy ^b   Abd Alrahman, Sherif H ^b   Al Daghri, Nasser M ^b  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Metabolic syndrome; Organochlorine pesticides; Type 2 diabetes mellitus

Indexed keywords

ADIPONECTIN; ALPHA HEXACHLOROCYCLOHEXANE; BETA HEXACHLOROCYCLOHEXANE; GLUCOSE; HEMOGLOBIN A1C; HEXACHLOROCYCLOHEXANE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LEPTIN; LINDANE; PESTICIDE; RESISTIN; TRIACYLGLYCEROL; INSECTICIDE; POLLUTANT;

DIABETES; DIET; ENVIRONMENTAL RISK; HCH; HEALTH STATUS; LIFESTYLE; ORGANOCHLORINE; PESTICIDE RESIDUE; RISK FACTOR;

ADULT; AGED; ARTICLE; BLOOD LEVEL; BODY BURDEN; BODY MASS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; ENVIRONMENTAL EXPOSURE; FEMALE; HOMEOSTATIC MODEL ASSESSMENT OF INSULIN RESISTANCE; HUMAN; HYPERTENSION; MAJOR CLINICAL STUDY; MALE; MASS FRAGMENTOGRAPHY; METABOLIC PARAMETERS; NON INSULIN DEPENDENT DIABETES MELLITUS; RISK ASSESSMENT; RISK FACTOR; SAUDI ARABIA; ADOLESCENT; BLOOD; BLOOD ANALYSIS; CHEMICALLY INDUCED; DIABETES MELLITUS, TYPE 2; ENVIRONMENTAL MONITORING; METABOLIC SYNDROME X; MIDDLE AGED; POLLUTANT; STATISTICAL MODEL;

SAUDI ARABIA;

ADOLESCENT; ADULT; AGED; BLOOD CHEMICAL ANALYSIS; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; FEMALE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HUMANS; INSECTICIDES; LINDANE; LOGISTIC MODELS; MALE; METABOLIC SYNDROME X; MIDDLE AGED; RISK FACTORS; SAUDI ARABIA;

EID: 84906830398     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph110908984     Document Type: Article

References (47)

1. Guariguata L. By the numbers: New estimates from the IDF diabetes atlas update for 2012. Diabetes Res. Clin. Pract. 2012, 98, 524-525.
2. Alzaid, A.A. Time to declare war on diabetes. Ann. Saudi. Med. 1997, 17, 154-155.
3. Fatani, H.H.; Mira, S.A.; el-Zubier, A.G. Prevalence of diabetes mellitus in rural Saudi Arabia. Diabetes Care 1987, 10, 180-183.
4. El-Hazmi, M.; Warsy, A.; Al-Swailem, A.; Sulaimani, R. Diabetes mellitus as a health problem in Saudi Arabia. East Mediterr. Health J. 1998, 4, 58-67.
5. Gillies, C.L.; Abrams, K.R.; Lambert, P.C.; Cooper, N.J.; Sutton, A.J.; Hsu, R.T.; Khunti, K. Pharmacological and lifestyle interventions to prevent or delay type 2 diabetes in people with impaired glucose tolerance: systematic review and meta-analysis. BMJ 2007, 334, doi:10.1136/ bmj.39063.689375.55.
6. Wilson, A.; Gyi, A.A. The status and perspective of diabetes health education in China: Inspiration from Australia. Int. J. Nurs. Pract. 2010, 16, 92-98.
7. Das, U.N. Obesity: genes, brain, gut, and environment. Nutrition 2010, 26, 459-473.
8. Tuomi, T. Type 1 and type 2 diabetes: What do they have in common? Diabetes 2005, 54, S40-S45.
9. Eichler, E.E.; Flint, J.; Gibson, G.; Kong, A.; Leal, S.M.; Moore, J.H.; Nadeau, J.H. Missing heritability and strategies for finding the underlying causes of complex disease. Nat. Rev. Genet. 2010, 11, 446-450.
10. Patel, C.J.; Bhattacharya, J.; Butte, A.J. An Environment-Wide Association Study (EWAS) on type 2 diabetes mellitus. PLoS One 2010, 5, doi:10.1371/journal.pone.0010746.
11. Li, Q.Q.; Loganath, A.; Chong, Y.S.; Tan, J.; Obbard, J.P. Persistent organic pollutants and adverse health effects in humans. J. Toxicol. Environ. Health A. 2006, 69, 1987-2005.
12. Everett, C.J.; Frithsen, I.L.; Diaz, V.A.; Koopman, R.J.; Simpson, W.M., Jr.; Mainous, A.G. 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.
13. Lee, D.H.; Lee, I.K.; Song, K.; Steffes, M.; Toscano, W.; Baker, B.A.; Jacobs, D.R., Jr. 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.
14. 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.
15. Persky, V.; Piorkowski, J.; Turyk, M.; Freels, S.; Chatterton, R., Jr.; Dimos, J.; Bradlow, H.L.; Chary, L.K.; Burse, V.; Unterman, T. 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.
16. Kutz, F.W.; Wood, P.H.; Bottimore, D.P. Organochlorine pesticides and polychlorinated biphenyls in human adipose tissue. Rev. Environ. Contam. Toxicol. 1991, 120, 1-82.
17. Lucena, R.A.; Allam, M.F.; Jimenez, S.S.; Villarejo, M.L. A review of environmental exposure to persistent organochlorine residuals during the last fifty years. Curr. Drug. Saf. 2007, 2, 163-172.
18. Breivik, K.; Pacyna, J.M.; Munch, J. Use of alpha-, beta- and gamma-hexachlorocyclohexane in Europe, 1970-1996. Sci. Total. Environ. 1999, 239, 151-163.
19. Vijgen, J.; Abhilash, P.C.; Li, Y.F.; Lal, R.; Forter, M.; Torres, J.; Singh, N.; Yunus, M.; Tian, C.; Schaffer, A.; Weber, R. Hexachlorocyclohexane (HCH) as new Stockholm Convention POPs-A global perspective on the management of Lindane and its waste isomers. Environ. Sci. Pollut. Res. Int. 2011, 18, 152-162.
20. Al-Othman, A; Abd-Alrahman, S.H.; Al-Daghri, N.M. DDT and its metabolites are linked to increased risk of type 2 diabetes among Saudi adults: a cross-sectional study. Environ. Sci. Pollut. R. 2014, 2014, doi:10.1007/s11356-014-3371-0.
21. Airaksinen, R.; Rantakokko, P.; Eriksson, J.G.; Blomstedt, P.; Kajantie, E.; Kiviranta, H. Association between type 2 diabetes and exposure to persistent organic pollutants. Diabetes Care 2011, 34, 1972-1979.
22. Gasull, M.; Pumarega, J.; Tellez-Plaza, M.; Castell, C.; Tresserras, R.; Lee, D.H.; Porta, M. Blood concentrations of persistent organic pollutants and prediabetes and diabetes in the general population of Catalonia. Environ. Sci. Technol. 2012, 46, 7799-7810.
23. Lee, D.H.; Lind, P.M.; Jacobs, D.R., 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.
24. Wu, H.; Bertrand, K.A.; Choi, A.L.; Hu, F.B.; Laden, F.; Grandjean, P.; Sun, Q. 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.
25. Cox, S.; Niskar, A.S.; Narayan, K.M.; 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.
26. Everett, C.J.; Matheson, E.M. Biomarkers of pesticide exposure and diabetes in the 1999-2004 national health and nutrition examination survey. Environ. Int. 2010, 36, 398-401.
27. Son, H.K.; Kim, S.A.; Kang, J.H.; Chang, Y.S.; Park, S.K.; Lee, S.K.; Jacobs, D.R., Jr.; Lee, D.H. Strong associations between low-dose organochlorine pesticides and type 2 diabetes in Korea. Environ. Int. 2010, 36, 410-414.
28. Arrebola, J.P.; Pumarega, J.; Gasull, M.; Fernandez, M.F.; Martin-Olmedo, P.; Molina-Molina, J.M.; Fernandez-Rodriguez, M.; Porta, M.; Olea, N. Adipose tissue concentrations of persistent organic pollutants and prevalence of type 2 diabetes in adults from Southern Spain. Environ. Res. 2013, 122, 31-37.
29. Yoon, KH; Lee, JH; Kim, J.W.; Cho, J.H.; Choi, Y.H.; Ko, S.H.; Zimmet, P.; Son, H.Y. Epidemic obesity and type 2 diabetes in Asia. Lancet 2006, 368, 1681-1688
30. Sexton, K.; Salinas, J.J.; McDonald, T.J.; Gowen, R.M.; Miller, R.P.; McCormick, J.B.; Fisher-Hoch, S.P. Biomarkers of maternal and fetal exposure to organochlorine pesticides measured in pregnant Hispanic women from Brownsville, Texas. Int. J. Environ. Res. Public Health 2013, 10, 237-248.
31. Agency for Toxic Substances and Disease Registry (ATSDR). Available online: http://www.atsdr.cdc.gov/ToxProfiles/TP.asp?id=754&tid=138 (accessed on 20 August 2014).
32. Drummond, L.; Gillanders, E.M.; Wilson, H.K. Plasma gamma-hexachlorocyclohexane concentrations in forestry workers exposed to lindane. Br. J. Ind. Med. 1988, 45, 493-497.
33. Jung, D.; Becher, H.; Edler, L.; Flesch-Janys, D.; Gurn, P.; Konietzko, J.; Manz, A.; Papke, O. Elimination of beta-hexachlorocyclohexane in occupationally exposed persons. J. of Toxicol. and Environ. Health 1997, 51, 23-34.
34. Nigam, S.K.; Karnik, A.B.; Majumder, S.K.; Visweswariah, K.; Raju, G.S.; Bai, K.M.; Lakkad, B.C.; Thakore, K.N.; Chatterjee, B.B. Serum hexachlorocyclohexane residues in workers engaged at a HCH manufacturing plant. Int. Arch. Occup. Environ. Health 1986, 57, 315-320.
35. Baumann, K.; Angerer, J.; Heinrich, R.; Lehnert, G. Occupational exposure to hexachlorocyclohexane. I. Body burden of HCH-isomers. Int. Arch. Occup. Environ. Health 1980, 47, 119-127.
36. Al-Saleh, I.; Echeverria-Quevedo, A.; Al-Dgaither, S.; Faris, R. Residue levels of organochlorinated insecticides in breast milk: a preliminary report from Al-Kharj, Saudi Arabia. J. Environ. Pathol. Toxicol. Oncol. 1998, 17, 37-50.
37. Radikova, Z.; Koska, J.; Ksinantova, L.; Imrich, R.; Kocan, A.; Petrik, J. Increased frequency of diabetes and other forms of dysglycemia in the population of specific areas of eastern Slovakia chronically exposed to contamination with polychlorinated biphenyls (PCB). Organohal. Comp. 2004, 66, 3547-3551.
38. 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.
39. Grundy, S. Hypertriglyceridemia, insulin resistance, and the metabolic syndrome. Am. J. of Cardiol. 1999, 83, 25-29.
40. Ibrahim, N.A.; El-Gamal, B.A. Effect of diazinon, an organophosphate insecticide, on plasma lipid constituents in experimental animals. J. Biochem. Mol. Biol. 2003, 36, 499-504.
41. Rezg, R.; Mornagui, B.; Benahmed, M.; Chouchane, S.G.; Belhajhmida, N.; Abdeladhim, M.; Kamoun, A.; El-fazaa, S.; Gharbi, N. Malathion exposure modulates hypothalamic gene expression and induces dyslipedemia in Wistar rats. Food Chem. Toxicol. 2010, 48, 1473-1477.
42. Ogunbode, A.M.; Ladipo, M.; Ajayi, I.O.; Fatiregun, A.A. Obesity: an emerging disease. Niger. J. Clin. Pract. 2011, 14, 390-394.
43. Alokail, S; Al-Daghri, N; Abdulkareem, A; Draz, H.M.; Yakout, S.M.; Alnaami, A.M.; Sabico, S.; Alenad, A.M.; Chrousos, G.P. Metabolic syndrome biomarkers and early breast cancer in Saudi women: evidence for the presence of a systemic stress response and/or pre-existing metabolic syndrome-related neoplasia risk? BMC Cancer 2013, 13, doi:10.1186/1471-2407-13-54.
44. Remillard, R.B.; Bunce, N.J. Linking dioxins to diabetes: epidemiology and biologic plausibility. Environ. Health Perspect. 2002, 110, 853-858.
45. Wallace, D.C. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 2005, 39, 359-407.
46. Fischer, L.J.; Wagner, M.A.; Madhukar, B.V. Potential involvement of calcium, CaM kinase II, and MAP kinases in PCB-stimulated insulin release from RINm5F cells. Toxicol. Appl. Pharmacol. 1999, 159, 194-203.
47. Biswas, G.; Srinivasan, S.; Anandatheerthavarada, H.K.; Avadhani, N.G. Dioxin-mediated tumor progression through activation of mitochondria-to-nucleus stress signaling. Proc. Natl. Acad. Sci. USA 2008, 105, 186-191.