Environmental Science and Pollution Research

, Volume 22, Issue 1, pp 379–386 | Cite as

DDT and its metabolites are linked to increased risk of type 2 diabetes among Saudi adults: a cross-sectional study

  • AbdulAziz A. Al-Othman
  • Sherif H. Abd-Alrahman
  • Nasser M. Al-Daghri
Research Article


Organochlorine (OC) pesticides have recently been associated with type 2 diabetes in several non-Asian general populations. As there is currently an epidemic of type 2 diabetes mellitus in Asia. The prevalence and incidence of diabetes is increasing rapidly worldwide including many Arab Gulf countries. According to a community-based national epidemiological health survey, the overall prevalence of diabetes mellitus in Saudi adults (age group of 30–50 years) is 23.7 %. A recent study by Al-Daghri et al. (BMC Med 9:76, 2011) reported that the prevalence of diabetes mellitus in the Kingdom of Saudi Arabia (KSA) is 31.6 %. We investigated the associations between OC pesticides and type 2 diabetes in Saudi Arabia using a simple, sensitive, rapid, and selective gas chromatography coupled with mass spectrometry (GC-MS) method that has been recently developed. A total of 280 Saudi adults (136 diabetes mellitus (DM) patients and 144 non-DM controls) were randomly selected from the Riyadh Cohort Study for inclusion. The diagnosis of diabetes was based on established diagnosis and medications taken. Blood dichlorodiphenyltrichloroethane (DDT) and its derivatives were quantified using GC-MS. Residues of DDT and its derivatives were analyzed in serum by means of gas chromatography with a mass spectrometry detector. Associations between DDT exposure and T2DM were analyzed by logistic regression. DDT and its derivatives and serum concentrations of DDT and its derivative DDE showed the strongest and most significant association to type 2 diabetes in both cross-sectional and prospective studies. Associations of DDT and its derivatives varied across different diabetes-related components of the metabolic syndrome. It positively and significantly associated with four of the five of these components especially elevated triacylglycerol, high fasting glucose, high blood pressure, and HOMA-IR but negatively and significantly with HDL. Possible biological mechanisms are discussed. This study confirms previous reports relating organochlorine pesticide (OCP) exposure to diabetes and suggests possible hormonal pathways deserving further exploration. The study will be one of the first to shed light on the associations of serum levels of total DDTs and DDT derivatives among the Saudi Arab ethnicity, and diabetes type 2 chronic noncommunicable diseases are highly prevalent.


OCPs Environmental pollution Diabetes Biomarkers 



Body mass index








Odds ratio


Persistent organochlorine pollutants


Organochlorine pesticides


Diabetes mellitus type 2



The authors gratefully acknowledge the National Plan for Sciences and Technology (NPST) for the financial support (10-ENE995-02). The authors thank Benjamin Vinodson for the statistical analysis of data.

Conflict of interest

The authors have no competing interests to declare.

Authors’ contributions

Dr. Al-Daghri and Dr. Abd-Alrahman designed and initiated the current study and were responsible for collecting the samples and the interview data. Dr. Abd-Alrahman coordinated the current study and was responsible for the OCP analysis using GC-MS and for writing the draft version of the manuscript. Dr. Al-Daghri and Dr. Al-Othman were responsible for reviewing the draft version of the manuscript. All authors commented on and approved the final manuscript.


  1. Airaksinen R, Rantakokko P, Eriksson JG, Blomstedt P, Kajantie E, Kiviranta H (2011) Association between type 2 diabetes and exposure to persistent organic pollutants. Diabetes Care 34:1972–1979CrossRefGoogle Scholar
  2. Al-Daghri NM (2008) Serum polycyclic aromatic hydrocarbons among children with and without asthma: correlation to environmental and dietary factors. Int J Occup Med Environ Health 21:211–217CrossRefGoogle Scholar
  3. Al-Daghri NM, Al-Attas OS, Alokail MS, Alkharfy KM, Yousef M, Sabico SL, Chrousos GP (2011) Diabetes mellitus type 2 and other chronic non-communicable diseases in the central region, Saudi Arabia (Riyadh cohort 2): a decade of an epidemic. BMC Med 9:76CrossRefGoogle Scholar
  4. Al-Nozha MM, Al-Maatouq MA, Al-Mazrou YY, Al-Harthi SS, Arafah MR, Khalil MZ, Khan NB, Al-Khadra A, Al-Marzouki K, Nouh MS, Abdullah M, Attas O, Al-Shahid MS, Al-Mobeireek A (2004) Diabetes mellitus in Saudi Arabia. Saudi Med J 25:1603–1610Google Scholar
  5. Biswas G, Srinivasan S, Anandatheerthavarada HK, Avadhani NG (2008) Dioxin-mediated tumor progression through activation of mitochondria-to-nucleus stress signaling. Proc Natl Acad Sci U S A 105:186–191CrossRefGoogle Scholar
  6. Chadwick RW, Cooper RL, Chang J, Rehnberg GL, McElroy WK (1988) Possible antiestrogenic activity of lindane in female rats. J Biochem Toxicol 3:147–158CrossRefGoogle Scholar
  7. Channa K, Rollin HB, Nost TH, Odland JO, Sandanger TM (2012) Prenatal exposure to DDT in malaria endemic region following indoor residual spraying and in non-malaria coastal regions of South Africa. Sci Total Environ 429:183–190CrossRefGoogle Scholar
  8. Cocco P, Blair A, Congia P, Saba G, Ecca AR, Palmas C (1997) Long-term health effects of the occupational exposure to DDT. A preliminary report. Ann N Y Acad Sci 837:246–256CrossRefGoogle Scholar
  9. Codru N, Schymura MJ, Negoita S, Akwesasne Task Force on E, Rej R, Carpenter DO (2007) Diabetes in relation to serum levels of polychlorinated biphenyls and chlorinated pesticides in adult Native Americans. Environ Health Perspect 115:1442–1447Google Scholar
  10. 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 115:1747–1752CrossRefGoogle Scholar
  11. Dorigo UB, Bourrain X, Berard A, Leboulanger C (2003) Seasonal changes in river microalgae sensitivity to atrazine and isoproturon, along a contamination gradient. Sci Total Environ 318:101–114CrossRefGoogle Scholar
  12. Dugravot S, Grolleau F, Macherel D, Rochetaing A, Hue B, Stankiewicz M, Huignard J, Lapied B (2003) Dimethyl disulfide exerts insecticidal neurotoxicity through mitochondrial dysfunction and activation of insect K(ATP) channels. J Neurophysiol 90:259–270CrossRefGoogle Scholar
  13. Everett CJ, Frithsen IL, Diaz VA, Koopman RJ, Simpson WM Jr, Mainous AG 3rd (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 103:413–418CrossRefGoogle Scholar
  14. Fischer LJ, Wagner MA, Madhukar BV (1999) Potential involvement of calcium, CaM kinase II, and MAP kinases in PCB-stimulated insulin release from RINm5F cells. Toxicol Appl Pharmacol 159:194–203CrossRefGoogle Scholar
  15. Gasull M, Pumarega J, Tellez-Plaza M, Castell C, Tresserras R, Lee DH, Porta M (2012) Blood concentrations of persistent organic pollutants and prediabetes and diabetes in the general population of Catalonia. Environ Sci Technol 46:7799–7810CrossRefGoogle Scholar
  16. Grundy S (1999) Hypertriglyceridemia, insulin resistance, and the metabolic syndrome. Am J Cardiol 83:25F–29FCrossRefGoogle Scholar
  17. Guilherme A, Virbasius JV, Puri V, Czech MP (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nature reviews. Mol Cell Biol 9:367–377Google Scholar
  18. Ibrahim NA, El-Gamal BA (2003) Effect of diazinon, an organophosphate insecticide, on plasma lipid constituents in experimental animals. J Biochem Mol Biol 36:499–504CrossRefGoogle Scholar
  19. 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 51:1416–1422CrossRefGoogle Scholar
  20. Kang JH, Park H, Chang YS, Choi JW (2008) Distribution of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) in human serum from urban areas in Korea. Chemosphere 73:1625–1631CrossRefGoogle Scholar
  21. Kutz FW, Wood PH, Bottimore DP (1991) Organochlorine pesticides and polychlorinated biphenyls in human adipose tissue. Rev Environ Contam Toxicol 120:1–82Google Scholar
  22. Lee DH, Lee IK, Song K, Steffes M, Toscano W, Baker BA, Jacobs DR Jr (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 29:1638–1644CrossRefGoogle Scholar
  23. Lee DH, Lee IK, Steffes M, Jacobs DR Jr (2007) Extended analyses of the association between serum concentrations of persistent organic pollutants and diabetes. Diabetes Care 30:1596–1598CrossRefGoogle Scholar
  24. Lee DH, Lind PM, Jacobs DR Jr, Salihovic S, van Bavel B, Lind L (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 34:1778–1784CrossRefGoogle Scholar
  25. Longnecker MP, Rogan WJ, Lucier G (1997) The human health effects of DDT (dichlorodiphenyltrichloroethane) and PCBS (polychlorinated biphenyls) and an overview of organochlorines in public health. Annu Rev Public Health 18:211–244CrossRefGoogle Scholar
  26. Lucena RA, Allam MF, Jimenez SS, Villarejo ML (2007) A review of environmental exposure to persistent organochlorine residuals during the last fifty years. Curr Drug Saf 2:163–172CrossRefGoogle Scholar
  27. Ogunbode AM, Ladipo M, Ajayi IO, Fatiregun AA (2011) Obesity: an emerging disease. Niger J Clin Pract 14:390–394CrossRefGoogle Scholar
  28. Park MJ, Lee SK, Yang JY, Kim KW, Lee SY, Lee WT, Chung KH, Yun YP, Yoo YC (2005) Distribution of organochlorines and PCB congeners in Korean human tissues. Arch Pharm Res 28:829–838CrossRefGoogle Scholar
  29. 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 6:3179–3189CrossRefGoogle Scholar
  30. Remillard RB, Bunce NJ (2002) Linking dioxins to diabetes: epidemiology and biologic plausibility. Environ Health Perspect 110:853–858CrossRefGoogle Scholar
  31. Rezg R, Mornagui B, Benahmed M, Chouchane SG, Belhajhmida N, Abdeladhim M, Kamoun A, El-fazaa S, Gharbi N (2010) Malathion exposure modulates hypothalamic gene expression and induces dyslipedemia in Wistar rats. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc 48:1473–1477CrossRefGoogle Scholar
  32. Rignell-Hydbom A, Elfving M, Ivarsson SA, Lindh C, Jonsson BA, Olofsson P, Rylander L (2010) A nested case-control study of intrauterine exposure to persistent organochlorine pollutants in relation to risk of type 1 diabetes. PLoS One 5:e11281CrossRefGoogle Scholar
  33. Rogan WJ, Chen A (2005) Health risks and benefits of bis(4-chlorophenyl)-1,1,1-trichloroethane (DDT). Lancet 366:763–773CrossRefGoogle Scholar
  34. Stratton IM, Adler AI, Neil HA, Matthews DR, Manley SE, Cull CA, Hadden D, Turner RC, Holman RR (2000) Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 321:405–412CrossRefGoogle Scholar
  35. Turusov V, Rakitsky V, Tomatis L (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110:125–128CrossRefGoogle Scholar
  36. 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 75:674–679CrossRefGoogle Scholar
  37. 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 17:352–359CrossRefGoogle Scholar
  38. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407CrossRefGoogle Scholar
  39. Wang F, Roberts SM, Butfiloski EJ, Morel L, Sobel ES (2007) Acceleration of autoimmunity by organochlorine pesticides: a comparison of splenic B-cell effects of chlordecone and estradiol in (NZBxNZW)F1 mice. Toxicol Sci Off J Soc Toxicol 99:141–152CrossRefGoogle Scholar
  40. WHO (1979) DDT and its derivatives, Environmental Health CriteriaGoogle Scholar
  41. Wild S, Roglic G, Green A, Sicree R, King H (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047–1053CrossRefGoogle Scholar
  42. Wu H, Bertrand KA, Choi AL, Hu FB, Laden F, Grandjean P, Sun Q (2013) Persistent organic pollutants and type 2 diabetes: a prospective analysis in the nurses’ health study and meta-analysis. Environ Health Perspect 121:153–161Google Scholar
  43. Yoon KH, Lee JH, Kim JW, Cho JH, Choi YH, Ko SH, Zimmet P, Son HY (2006) Epidemic obesity and type 2 diabetes in Asia. Lancet 368:1681–1688CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • AbdulAziz A. Al-Othman
    • 1
    • 2
  • Sherif H. Abd-Alrahman
    • 2
    • 3
    • 4
  • Nasser M. Al-Daghri
    • 2
    • 3
  1. 1.College of Applied Medical SciencesKing Saud UniversityRiyadhSaudi Arabia
  2. 2.Prince Mutaib Chair for Biomarkers of Osteoporosis, Biochemistry Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  3. 3.Biomarkers Research Program, Biochemistry Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  4. 4.Pesticides Residues and Environmental Pollution Department, Central Agricultural Pesticide LaboratoryAgricultural Research CenterGizaEgypt

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