Advertisement

Obesity, Persistent Organic Pollutants and Related Health Problems

  • Loukia Vassilopoulou
  • Christos Psycharakis
  • Demetrios Petrakis
  • John Tsiaoussis
  • Aristides M. TsatsakisEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 960)

Abstract

The present review aims to delve into persistent organic pollutants (POPs), as xenobiotics, in correlation to human health. POPs exhibit a group of common characteristics, including lipophilicity, persistence to decomposition and bioaccumulation in tissues. POPs have been thoroughly studied by former researchers, as they offer a particular interest in the elucidation of metabolic, endocrine and immune perturbation caused by their synergy with intracellular mechanisms. Herein particular focus is attributed to the relationship of POPs with obesity provocation. Obesity nowadays receives epidemic dimensions, as its prevalence elevates in an exponential degree. POPs-induced obesity rotates around interfering in metabolic and endocrinal procedures and interacting with peroxisome-proliferator and retinoic receptors. Moreover, polymorphisms in CYP gene families exert a negative result, as they incapacitate detoxification of POPs. Obesity could be deemed as a multidimensional condition, as various factors interact to lead to an obesogenic result. Therefore, concomitant disorders may occur, from mild to lethal, and get intensified due to POPs exposure. POPs exact function mechanisms remain rather enigmatic, thus further investigation should be prospectively performed, for a more lucid picture of this issue, and, consequently for the establishment of alternative solutions.

Keywords

Persistent organic pollutants Xenobiotics Bioaccumulation Toxicokinetics Obesity Diabetes Metabolism Endocrine signaling CYP polymorphism 

References

  1. Agudo, A., F. Goñi, A. Etxeandia, A. Vives, E. Millán, R. López, P. Amiano, E. Ardanaz, A. Barricarte, M.D. Chirlaque, M. Dorronsoro, P. Jakszyn, N. Larrañaga, C. Martínez, C. Navarro, L. Rodríguez, M.J. Sánchez, M.J. Tormo, and C.A. González. 2009. Polychlorinated biphenyls in Spanish adults: Determinants of serum concentrations. Environmental Research 109(5): 620–628. doi: 10.1016/j.envres.2009.03.009.PubMedCrossRefGoogle Scholar
  2. Airaksinen, R., P. Rantakokko, J.G. Eriksson, P. Blomstedt, E. Kajantie, and H. Kiviranta. 2011. Association between type 2 diabetes and exposure to persistent organic pollutants. Diabetes Care 34(9): 1972–1979. doi: 10.2337/dc10-2303.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Almeida-González, M., L.D. Boada, M. Zumbado, L.A. Henríquez-Hernández, P.F. Valeron, and O.P. Luzardo. 2011. Dietary intake of environmentally persistent plaguicides in the european population, Pesticides—The impacts of pesticides exposure. pp. 49–66.Google Scholar
  4. Androutsopoulos, V.P., A.F. Hernandez, J. Liesivuori, and A.M. Tsatsakis. 2013. A mechanistic overview of health associated effects of low levels of organochlorine and organophosphorus pesticides. Toxicology 307: 89–94. doi: 10.1016/j.tox.2012.09.011.PubMedCrossRefGoogle Scholar
  5. Anetor, J.I. 2010. Industrialization and the increasing risk of genome instability in developing countries: Nutrigenomics as a promising antidote. The African Journal of Medical Sciences 39: 7–20.Google Scholar
  6. Aprea, M.C. 2012. Environmental and biological monitoring in the estimation of absorbed doses of pesticides. Toxicology Letters 210(2): 110–118. doi: 10.1016/j.toxlet.2011.08.008.PubMedCrossRefGoogle Scholar
  7. Arrebola, J.P., J. Pumarega, M. Gasull, M.F. Fernandez, P. Martin-Olmedo, J.M. Molina-Molina, M. Fernandez-Rodriguez, M. Porta, and N. Olea. 2013. Adipose tissue concentrations of persistent organic pollutants and prevalence of type 2 diabetes in adults from Southern Spain. Environmental Research 122: 31–37. doi: 10.1016/j.envres.2012.12.001.PubMedCrossRefGoogle Scholar
  8. Arsenescu, V., R.I. Arsenescu, V. King, H. Swanson, and L.A. Cassis. 2008. Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environmental Health Perspectives 116(6): 761–768. doi: 10.1289/ehp.10554.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Arsenescu, V., R. Arsenescu, M. Parulkar, M. Karounos, X. Zhang, and L.A. Cassis. 2011. Polychlorinated biphenyl 77 augments angiotensin II-induced atherosclerosis and abdominal aortic aneurysms in male apolipoprotein E deficient mice. Toxicology and Applied Pharmacology 257(1): 148–154. doi: 10.1016/j.taap.2011.08.028.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Artacho-Cordón, F., M. Fernández-Rodríguez, C. Garde, E. Salamanca, L.M. Iribarne-Durán, P. Torné, J. Expósito, L. Papay-Ramírez, M.F. Fernández, N. Olea, and J.P. Arrebola. 2015. Serum and adipose tissue as matrices for assessment of exposure to persistent organic pollutants in breast cancer patients. Environmental Research 142: 633–643. doi: 10.1016/j.envres.2015.08.020.PubMedCrossRefGoogle Scholar
  11. Baillie-Hamilton, P.F. 2002. Chemical toxins: A hypothesis to explain the global obesity epidemic. Journal of Alternative and Complementary Medicine 8: 185–192.PubMedCrossRefGoogle Scholar
  12. Benedetti, D, F.R. da Silva, K. Kvitko, S.P. Fernandes, and J. da Silva. 2014. Genotoxicity induced by occupational exposure to pesticides, pesticides-toxic aspects. INTECH. doi: 10.5772/57319.
  13. Bengmark, S. 2015. Obesity, the deadly quartet and the contribution of the neglected daily organ rest—A new dimension of un-health and its prevention. Hepatobiliary Surgery and Nutrition 4(4): 278–288. doi: 10.3978/j.issn.2304-3881.2015.07.02.PubMedPubMedCentralGoogle Scholar
  14. Berndt, J., P. Kovacs, K. Ruschke, N. Klöting, M. Fasshauer, M.R. Schön, A. Körner, M. Stumvoll, and M. Blüher. 2007. Fatty acid synthase gene expression in human adipose tissue: Association with obesity and type 2 diabetes. Diabetologia 50(7): 1472–1480.PubMedCrossRefGoogle Scholar
  15. Bonefeld-Jorgensen, E.C. 2010. Biomonitoring in Greenland: human biomarkers of exposure and effects—A short review. Rural and Remote Health 10(2): 1362.PubMedGoogle Scholar
  16. Bonefeld-Jorgensen, E.C., M. Long, R. Bossi, P. Ayotte, G. Asmund, T. Kruger, M. Ghisari, G. Mulvad, P. Kern, P. Nzulumiki, and E. Dewailly. 2011. Perfluorinated compounds are related to breast cancer risk in Greenlandic Inuit: A case control study. Environmental Health 10: 88. doi: 10.1186/1476-069X-10-88.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bourdon, J.A., T.M. Bazinet, T.T. Arnason, L.E. Kimpe, J.M. Blais, and P.A. White. 2010. Polychlorinated biphenyls (PCBs) contamination and aryl hydrocarbon receptor (AhR) agonist activity of Omega-3 polyunsaturated fatty acid supplements: Implications for daily intake of dioxins and PCBs. Food and Chemical Toxicology 48(11): 3093–3097. doi: 10.1016/j.fct.2010.07.051.PubMedCrossRefGoogle Scholar
  18. Bourez, S., S. Le Lay, C. Van den Daelen, C. Louis, Y. Larondelle, J.P. Thome, Y.J. Schneider, I. Dugail, and C. Debier. 2012. Accumulation of polychlorinated biphenyls in adipocytes: Selective targeting to lipid droplets and role of caveolin-1. PLoS One 7(2): e31834. doi: 10.1371/journal.pone.0031834.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Caballero, B. 2007. The global epidemic of obesity: An overview. Epidemiologic Reviews 29: 1–5. doi: 10.1093/epirev/mxm012.PubMedCrossRefGoogle Scholar
  20. Caprio, S., S.R. Daniels, A. Drewnowski, F.R. Kaufman, L.A. Palinkas, A.L. Rosenbloom, and J.B. Schwimmer. 2008. Influence of race, ethnicity, and culture on childhood obesity: implications for prevention and treatment: A consensus statement of Shaping America's Health and the Obesity Society. Diabetes Care 31(11): 2211–2221. doi: 10.2337/dc08-9024.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Carpenter, D.O., K. Arcaro, and D.C. Spink. 2002. Understanding the human health effects of chemical mixtures. Environmental Health Perspectives 110(1): 25–42.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Casals-Casas, C., J.N. Feige, and B. Desvergne. 2008. Interference of pollutants with PPARs: Endocrine disruption meets metabolism. International Journal of Obesity 32(6): S53–S61. doi: 10.1038/ijo.2008.207.PubMedCrossRefGoogle Scholar
  23. Chapados, N.A., C. Casimiro, M.A. Robidoux, F. Haman, M. Batal, J.M. Blais, and P. Imbeault. 2012. Increased proliferative effect of organochlorine compounds on human preadipocytes. Molecular and Cellular Biochemistry 365(1–2): 275–278. doi: 10.1007/s11010-012-1268-0.PubMedCrossRefGoogle Scholar
  24. Chen, S.H., F. He, H.L. Zhou, H.R. Wu, C. Xia, and Y.M. Li. 2011. Relationship between non-alcoholic fatty liver disease and metabolic syndrome. Journal of Digestive Diseases 12(2): 125–130. doi: 10.1111/j.1751-2980.2011.00487.x.PubMedCrossRefGoogle Scholar
  25. Colosio, C., A. Alegakis, and A.M. Tsatsakis. 2013. Emerging health issues from chronic pesticide exposure: Innovative methodologies and effects on molecular cell and tissue level. Toxicology 307: 1–2. doi: 10.1016/j.tox.2013.04.006.PubMedCrossRefGoogle Scholar
  26. Consales, C., G. Toft, G. Leter, J.P. Bonde, R. Uccelli, F. Pacchierotti, P. Eleuteri, B.A. Jönsson, A. Giwercman, H.S. Pedersen, P. Struciński, K. Góralczyk, V. Zviezdai, and M. Spanò. 2016. Exposure to persistent organic pollutants and sperm DNA methylation changes in Arctic and European populations. Environmental and Molecular Mutagenesis 57(3): 200–209. doi: 10.1002/em.21994.PubMedCrossRefGoogle Scholar
  27. Corsini, E., R. Luebke, D.R. Germolec, and J.C. DeWitt. 2014. Perfluorinated compounds: Emerging POPs with potential immunotoxicity. Toxicology Letters 230(2): 263–270. doi: 10.1016/j.toxlet.2014.01.038.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cristancho, A.G., and M.A. Lazar. 2011. Forming functional fat: A growing understanding of adipocyte differentiation. Nature Reviews. Molecular Cell Biology 12: 722–724. doi: 10.1038/nrm3198.PubMedCrossRefGoogle Scholar
  29. Daisouke, I., S. Kazunari, and I. Michihico. 2010. Disruption of retinoic acid receptor signaling by environmental pollutants. Journal of Health Science 56(3): 221–230.CrossRefGoogle Scholar
  30. Decherf, S., and B.A. Demeneix. 2011. The obesogen hypothesis: A shift of focus from the periphery to the hypothalamus. Journal of Toxicology and Environmental Health. Part B, Critical Reviews 14(5-7): 423–448. doi: 10.1080/10937404.2011.578561.PubMedCrossRefGoogle Scholar
  31. Dirinck E, Jorens PG, Covaci A, Geens T, Roosens L, Neels H, Mertens I, Van Gaal L (2011), Obesity and persistent organic pollutants: possible obespgenic effect of organochlorine pesticides and polychlorinated biphenyls, Obesity (Silver Spring) 19(4):709–14 doi: 10.1038/oby.2010.133.
  32. Dirinck, E.L., A.C. Dirtu, M. Govindan, A. Covaci, L.F. van Gaal, and P.G. Jorens. 2014. Exposure to persistent organic pollutants: Relationship with abnormal glucose metabolism and visceral adiposity. Diabetes Care 37(7): 1951–1958. doi: 10.2337/dc13-2329.PubMedCrossRefGoogle Scholar
  33. Eljarrat, E., and D. Barcelo. 2003. Priority lists for persistent organic pollutants and emerging contaminants based on their relative toxic potency in environmental samples. Trends in Analytical Chemistry 22(10): 655–665.CrossRefGoogle Scholar
  34. Feinendegen, L.E., V.P. Bond, C.A. Sondhaus, and K.I. Altman. 1999. Cellular signal adaptation with damage control at low doses vs. the predominance of DNA damage at high doses. Comptes Rendus de l'Académie des Sciences. Série III 322: 245–251.CrossRefGoogle Scholar
  35. Filatov, B.N., T.N. Kolodij, V.M. Kononov, and M.V. Kononov. 2015. Zagrjaznenie hlororganiceskimi pesticidami selskohozjajstvennyh ugodij i risk dlja zdorova naselenija volgogradskoj oblasti. Volgograd.Google Scholar
  36. Fredslund, S.O., and E.C. Bonefeld-Jørgensen. 2012. Breast cancer in the Arctic—Changes over the past decades. International Journal of Circumpolar Health 71: 19155. doi: 10.3402/ijch.v71i0.19155.CrossRefGoogle Scholar
  37. Freire, C., E. Amaya, M.F. Fernandez, M.C. Gonzalez-Galarzo, R. Ramos, J.M. Molina-Molina, J.P. Arrebola, and N. Olea. 2011. Relationship between occupational social class and exposure to organochlorine pesticides during pregnancy. Chemosphere 83(6): 831–838. doi: 10.1016/j.chemosphere.2011.02.076.PubMedCrossRefGoogle Scholar
  38. Gadupudi, G., F.A. Gourronc, G. Ludewig, L.W. Robertson, and A.J. Klingelhutz. 2015. PCB126 inhibits adipogenesis of human preadipocytes. Toxicology In Vitro 29(1): 132–141. doi: 10.1016/j.tiv.2014.09.015.PubMedCrossRefGoogle Scholar
  39. García-García, C.R., T. Parrón, M. Requena, R. Alarcón, A.M. Tsatsakis, and A.F. Hernández. 2016. Occupational pesticide exposure and adverse health effects at the clinical, hematological and biochemical level. Life Sciences 145: 274–283. doi: 10.1016/j.lfs.2015.10.013.PubMedCrossRefGoogle Scholar
  40. Gascon M, Sunyer J, Martinez D, Guerra S, Lavi I, Torrent M, Vrijheid M (2014), Persistent organic pollutants and children’s respiratory health: the role of cytokines and inflammatory biomarkers, Environ Int 69:133–40 doi: 10.1016/j.envint.2014.04.021.
  41. Gasull, M., J. Pumarega, G. Rovira, T. Lopez, J. Alguacil, and M. Porta. 2013. Relative effects of educational level and occupational social class on body concentrations of persistent organic pollutants in a representative sample of the general population of Catalonia, Spain. Environment International 60: 190–201. doi: 10.1016/j.envint.2013.08.001.PubMedCrossRefGoogle Scholar
  42. Giralt, M., and F. Villarroya. 2013. White, brown, beige/brite: Different adipose cells for different functions? Endocrinology 154(9): 2992–3000. doi: 10.1210/en.2013-1403.PubMedCrossRefGoogle Scholar
  43. Goncharov, A., M. Pavuk, H.R. Foushee, D.O. Carpenter, for the Anniston Environmental Health Research Consortium. 2011. Blood pressure in relation to concentrations of PCB congeners and chlorinated pesticides. Environmental Health Perspectives 119(3): 319–325. doi: 10.1289/ehp.1002830.Google Scholar
  44. Gregoraszczuk, E.L., and A. Ptak. 2013. Endocrine-disrupting chemicals: Some actions of POPs on female reproduction. International Journal of Endocrinology 2013: 828532. doi: 10.1155/2013/828532.PubMedPubMedCentralGoogle Scholar
  45. Hennig B, Reiterer G, Majkova Z, Oesterling E, Meerarani P, Toborek M (2005), Modofication of environmental toxicity by nutrients: omplications in atherosclerosis, Cardiovasc Toxicol 5(2):153–60.Google Scholar
  46. Hennig, B., L. Ormsbee, C.J. McClain, B.A. Watkins, B. Blumberg, L.G. Bachas, W. Sanderson, C. Thompson, and W.A. Suk. 2012. Nutrition can modulate the toxicity of environmental pollutants: Implications in risk assessment and human health. Environmental Health Perspectives 120(6): 771–774. doi: 10.1289/ehp.1104712.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Henríquez-Hernández, L.A., O.P. Luzardo, J.L.P. Arellano, C. Carranza, N.J. Sánchez, M. Almeida-González, N. Ruiz-Suárez, P.F. Valerón, M. Camacho, M. Zumbado, and L.D. Boada. 2016. Different pattern of contamination by legacy POPs in two populations from the same geographical area but with completely different lifestyles: Canary Islands (Spain) vs. Morocco. The Science of the Total Environment 541: 51–57. doi: 10.1016/j.scitotenv.2015.09.042.PubMedCrossRefGoogle Scholar
  48. Henríquez-Hernández, L.A., O.P. Luzardo, M. Zumbado, M. Camacho, L. Serra-Majem, E.E. Álvarez-León, and L.D. Boada. 2014. Blood pressure in relation to contamination by polychlorobiphenyls and organochlorine pesticides: Results from a population-based study in the Canary Islands (Spain). Environmental Research 135: 48–54. doi: 10.1016/j.envres.2014.05.036.PubMedCrossRefGoogle Scholar
  49. Hernández, A.F., F. Gil, M. Lacasaña, M. Rodríguez-Barranco, A.M. Tsatsakis, M. Requena, T. Parrón, and R. Alarcón. 2013a. Pesticide exposure and genetic variation in xenobiotic-metabolizing enzymes interact to induce biochemical liver damage. Food and Chemical Toxicology 61: 144–151. doi: 10.1016/j.fct.2013.05.012.PubMedCrossRefGoogle Scholar
  50. Hernández, A.F., T. Parrón, A.M. Tsatsakis, M. Requena, R. Alarcón, and O. López-Guarnidoa. 2013b. Toxic effects of pesticide mixtures at a molecular level: Their relevance to human health. Toxicology 307: 136–145. doi: 10.1016/j.tox.2012.06.009.PubMedCrossRefGoogle Scholar
  51. Hopperton, K.E., R.E. Duncan, R.P. Bazinet, and M.C. Archer. 2014. Fatty acid synthase plays a role in cancer metabolism beyond providing fatty acids for phospholipid synthesis or sustaining elevations in glycolytic activity. Experimental Cell Research 320(2): 302–310. doi: 10.1016/j.yexcr.2013.10.016.PubMedCrossRefGoogle Scholar
  52. Ibrahim, M.M., E. Fjære, E.J. Lock, D. Naville, G. Amlund, E. Meugnier, Battistoni B. Le Magueresse, L. Frøyland, L. Madsen, N. Jessen, S. Lund, H. Vidal, and J. Ruzzin. 2011. Chronic consumption of farmed salmon containing persistent organic pollutants causes insulin resistance and obesity in mice. PLoS One 6(9): e25170. doi: 10.1371/journal.pone.0025170.PubMedPubMedCentralCrossRefGoogle Scholar
  53. IGHRC (2009) Chemical Mixtures: A Framework for Assessing Risk to Human Health (CR14). Institute of Environment and Health, Cranfield University, UK.Google Scholar
  54. Jones, P.D., W. Hu, W. De Coen, J.L. Newsted, and J.P. Giesy. 2003. Binding of perfluorinated fatty acids to serum proteins. Environmental Toxicology and Chemistry 22: 2639–2649.PubMedCrossRefGoogle Scholar
  55. Kahleova, H., S. Tonstad, J. Rosmus, P. Fisar, A. Mari, M. Hill, and T. Pelikanova. 2016. The effect of a vegetarian versus conventional hypocaloric diet on serum concentrations of persistent organic pollutants in patients with type 2 diabetes. Nutrition, Metabolism, and Cardiovascular Diseases 26(5): 430–438. doi: 10.1016/j.numecd.2016.01.008.PubMedCrossRefGoogle Scholar
  56. Kang, S.C., B.R. Kim, S.Y. Lee, and T.S. Park. 2013. Sphingolipid metabolism and obesity-induced inflammation. Frontiers in Endocrinology 4: 67. doi: 10.3389/fendo.2013.00067.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Karastergiou, K., S.R. Smith, A.S. Greenberg, and S.K. Fried. 2012. Sex differences in human adipose tissues—The biology of pear shape. Biology of Sex Differences 3(1): 13. doi: 10.1186/2042-6410-3-13.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kasturi, S.S., J. Tannir, and R.E. Brannigan. 2008. The metabolic syndrome and male infertility. Journal of Andrology 29(3): 251–259. doi: 10.2164/jandrol.107.003731.PubMedCrossRefGoogle Scholar
  59. Kim, J.T., and H.K. Lee. 2014. Metabolic syndrome and the environmental pollutants from mitochondrial perspectives. Reviews in Endocrine & Metabolic Disorders 15(4): 253–262. doi: 10.1007/s11154-014-9297-5.CrossRefGoogle Scholar
  60. Kim, K.Y., D.S. Kim, S.K. Lee, I.K. Lee, J.H. Kang, Y.S. Chang, D.R. Jacobs, M. Steffes, and D.H. Lee. 2010. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environmental Health Perspectives 118(3): 370–374. doi: 10.1289/ehp.0901131.PubMedCrossRefGoogle Scholar
  61. Kim, M.J., P. Marchand, C. Henegar, J.P. Antignac, R. Alili, C. Poitou, J.L. Bouillot, A. Basdevant, B. Le Bizec, R. Barouki, and K. Clément. 2011. Fate and complex pathogenic effects of dioxins and polychlorinated biphenyls in obese subjects before and after drastic weight loss. Environmental Health Perspectives 119(3): 377–383. doi: 10.1289/ehp.1002848.PubMedCrossRefGoogle Scholar
  62. Kim, M.J., V. Pelloux, E. Guyot, J. Tordjmann, L.C. Bui, A. Chevallier, C. Forest, C. Benelli, K. Clément, and R. Barouki. 2012. Inflammatory pathway genes belong to major targets of persistent organic pollutants in adipose cells. Environmental Health Perspectives 120(4): 508–514. doi: 10.1289/ehp.1104282.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kim, S.A., K.S. Kim, Y.M. Lee, D.R. Jacobs, and D.H. Lee. 2015. Associations of organochlorine pesticides and polychlorinated biphenyls with total, cardiovascular, and cancer mortality in elders with differing fat mass. Environmental Research 138: 1–7. doi: 10.1016/j.envres.2015.01.021.PubMedCrossRefGoogle Scholar
  64. Koureas, M., F. Karagkouni, V. Rakitskii, C. Hadjichristodoulou, A.M. Tsatsakis, and A. Tsakalof. 2016. Serum levels of organochlorine pesticides in the general population of Thessaly, Greece, determined by HS-SPMEGC–MS method. Environmental Research 148: 318–321. doi: 10.1016/j.envres.2016.04.015.PubMedCrossRefGoogle Scholar
  65. Kouretas, D., A.M. Tsatsakis, J.L. Domingo, and A.W. Hayes. 2013. Mechanisms involved in oxidative stress regulation. Food and Chemical Toxicology 61: 1–2. doi: 10.1016/j.fct.2013.10.016.PubMedCrossRefGoogle Scholar
  66. La Merrill, M., C. Emond, M.J. Kim, J.P. Antignac, B. Le Bizec, K. Clement, L.S. Birnbaum, and R. Barouki. 2013. Toxicological function of adipose tissue: Focus on persistent organic pollutants. Environmental Health Perspectives 121(2): 162–169. doi: 10.1289/ehp.1205485.PubMedGoogle Scholar
  67. Lauenborg, J., E. Mathiesen, T. Hansen, C. Glumer, T. Jorgensen, K. Borch-Johnsen, P. Hornnes, O. Pedersen, and P. Damm. 2005. The prevalence of the metabolic syndrome in a Danish population of women with previous gestational diabetes mellitus is three-fold higher than in the general population. The Journal of Clinical Endocrinology and Metabolism 90: 4004–4010. doi: 10.1210/jc.2004-1713.PubMedCrossRefGoogle Scholar
  68. Lautenbach, A., A. Budde, C.D. Wrann, B. Teichmann, G. Vieten, T. Karl, and H. Nave. 2009. Obesity and the associated mediators leptin, estrogen and IGF-I enhance the cell proliferation and early tumorigenesis of breast cancer cells. Nutrition and Cancer 61(4): 484–491. doi: 10.1080/01635580802610115.PubMedCrossRefGoogle Scholar
  69. Lee, D.H., I.K. Lee, M. Porta, M. Steffes, and D.R. Jacobs Jr. 2007a. 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 50(9): 1841–1851.PubMedCrossRefGoogle Scholar
  70. Lee, D.H. 2012. Persistent organic pollutants and obesity-related metabolic dysfunction: Focusing on type 2 diabetes. Epidemiology and Health 34: e2012002. doi: 10.4178/epih/e2012002.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lee, D.H., I.K. Lee, K. Song, M. Steffes, W. Toscano, B.A. Baker, and D.R. Jacobs 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(7): 1638–44.Google Scholar
  72. Lee, D.H., M.W. Steffes, and D.R. Jacobs. 2008. Can persistent organic pollutants explain the association between serum γ-glutamyltransferase and type 2 diabetes? Diabetologia 51(3): 402–407.PubMedCrossRefGoogle Scholar
  73. ———. 2007b. Positive associations of serum concentration of polychlorinated biphenyls of organochlorine pesticides with self-reported arthritis, especially rheumatoid type in women. Environmental Health Perspectives 115(6): 883–888.Google Scholar
  74. Lee, D.H., M.W. Steffes, A. Sjödin, R.S. Jones, L.L. Needham, and D.R. Jacobs Jr. 2011. Low dose organochlorines and polychlorinated biphenyls predict obesity dyslipidemia and insulin resistance among people free of diabetes. PLoS One 6(1): e15977. doi: 10.1371/journal.pone.0015977.PubMedPubMedCentralCrossRefGoogle Scholar
  75. ———. 2010. Low dose of some persistent organic pollutants predicts type 2 diabetes: A nested case-control study. Environmental Health Perspectives 118(9): 1235–1242. doi: 10.1289/ehp.0901480.
  76. Lee, D.H., M. Porta, D.R. Jacobs Jr, and L.N. Vandenberg. 2014. Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr Rev 35(4):557–601, doi: 10.1210/er.2013-1084.
  77. Lee, H.A., S.H. Park, Y.S. Hong, E.H. Ha, and H. Park. 2016. The effect of exposure to persistent organic pollutants in metabolic health among Korean children at 1-year follow-up. International Journal of Environmental Research and Public Health 13(3): 270. doi: 10.3390/ijerph13030270.PubMedCentralCrossRefGoogle Scholar
  78. Lemaire, G., W. Mnif, P. Mauvais, P. Balaguer, and R. Rahmani. 2006. Activation of alpha- and beta-estrogen receptors by persistent pesticides in reporter cell lines. Life Sciences 79(12): 1160–1169.PubMedCrossRefGoogle Scholar
  79. Letcher, R.J., J.O. Bustnes, R. Dietz, B.M. Jenssen, E.H. Jorgensen, C. Sonne, J. Verreault, M.M. Vijayan, and G.W. Gabrielsen. 2010. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. The Science of the Total Environment 408(15): 2995–3043. doi: 10.1016/j.scitotenv.2009.10.038.PubMedCrossRefGoogle Scholar
  80. Lim, J., and S.H. Jee. 2015. Association between serum levels of adiponectin and polychlorinated biphenyls in Korean men and women. Endocrine 48(1): 211–217. doi: 10.1007/s12020-014-0231-0.PubMedCrossRefGoogle Scholar
  81. Lind, P.M., D.H. Lee, D.R. Jacobs, S. Salihovic, B. van Bavel, M.S. Wolff, and L. Lind. 2013. Circulating levels of persistent organic pollutants are related to retrospective assessment of life-time weight change. Chemosphere 90(3): 998–1004. doi: 10.1016/j.chemosphere.2012.07.051.PubMedCrossRefGoogle Scholar
  82. Ljunggren, S.A., I. Helmfrid, S. Salihovic, B. van Bavel, G. Wingren, M. Lindahl, and H. Karlsson. 2014. Persistent organic pollutants distribution in lipoprotein fractions in relation to cardiovascular disease and cancer. Environment International 65: 93–99. doi: 10.1016/j.envint.2013.12.017.PubMedCrossRefGoogle Scholar
  83. Long, M., A.K. Knudsen, H.S. Pedersen, and E.C. Bonefeld-Jørgensen. 2015. Food intake and serum persistent organic pollutants in the Greenlandic pregnant women: The accept sub-study. The Science of the Total Environment 529: 198–212. doi: 10.1016/j.scitotenv.2015.05.022.PubMedCrossRefGoogle Scholar
  84. Lundin, J.I., G. Ylitalo, R.K. Booth, B. Anulacion, J. Hempelmann, K. Parsons, M.B. Hanson, and S.K. Wasser. 2016. Modulation in persistent organic pollutant concentration and profile by prey availability and reproductive status in Southern Resident killer whale scat samples. Environmental Science & Technology 50(12): 6506–6516. doi: 10.1021/acs.est.6b00825.CrossRefGoogle Scholar
  85. Lv, Z., G. Li, Y. Li, C. Ying, J. Chen, T. Chen, J. Wei, Y. Lin, Y. Jiang, Y. Wang, B. Shu, B. Xu, and S. Xu. 2013. Glucose and lipid homeostasis in adult rat is impaired by early-life exposure to perfluorooctane sulfonate. Environmental Toxicology 28(9): 532–542. doi: 10.1002/tox.20747.PubMedCrossRefGoogle Scholar
  86. Lyche, J.L., R. Nourizadeh-Lillabadib, C. Karlsson, B. Stavik, V. Berg, J.U. Skåre, P. Alestrømb, and E. Ropstad. 2011. Natural mixtures of POPs affected body weight gain and induced transcription of genes involved in weight regulation and insulin signaling. Aquatic Toxicology 102(3-4): 197–204. doi: 10.1016/j.aquatox.2011.01.017.PubMedCrossRefGoogle Scholar
  87. Marti, A., M.J. Moreno-Aliaga, A. Zulet, and J.A. Martinez. 2005. Advances in molecular nutrition: Nutrigenomics and/or nutrigenetics. Nutrición Hospitalaria 20(3): 157–164.PubMedGoogle Scholar
  88. Mathew, A.V., S. Okada, and K. Sharma. 2011. Obesity related kidney disease. Current Diabetes Reviews 7(1): 41–49.PubMedCrossRefGoogle Scholar
  89. McKinney JD, Waller CL (1994), Polychlorinated biphenyls as hormonally active structural analogues, Environ Health Perspect 102:290–297.Google Scholar
  90. Meng, G., Z. Nie, Y. Feng, X. Wu, Y. Yin, and Y. Wang. 2016. Typical halogenated persistent organic pollutants in indoor dust and the associations with childhood asthma in Shanghai, China. Environmental Pollution (Barking, Essex: 1987) 211: 389–398. doi: 10.1016/j.envpol.2015.12.006.CrossRefGoogle Scholar
  91. Miller, A.L., M.A. Horodynski, H.E. Brophy Herb, K.E. Peterson, D. Contreras, N. Kaciroti, J. Staples-Watson, and J.C. Lumeng. 2012. Enhancing self-regulation as a strategy for obesity prevention in Head Start preschoolers: The growing healthy study. BMC Public Health 12: 1040. doi: 10.1186/1471-2458-12-1040.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Moreno-Aliaga, M.J., and F. Matsumura. 2002. Effects of 1,1,1-trichloro-2,2-bis(p-chlorophenyl)-ethane (p,p′-DDT) on 3T3-L1 and 3T3-F442A adipocyte differentiation. Biochemical Pharmacology 63(5): 997–1007.PubMedCrossRefGoogle Scholar
  93. Mori, C., K. Kakuta, Y. Matsuno, E. Todaka, M. Watanabe, M. Hanazato, Y. Kawashiro, and H. Fukata. 2014. Polychlorinated biphenyl levels in the blood of Japanese individuals ranging from infants to over 80 years of age. Environmental Science and Pollution Research 21(10): 6434–6439. doi: 10.1007/s11356-013-1965-6.PubMedCrossRefGoogle Scholar
  94. Mrema, E.J., F.M. Rubino, G. Brambilla, A. Moretto, A.M. Tsatsakis, and C. Colosio. 2013. Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicology 307: 74–88. doi: 10.1016/j.tox.2012.11.015.PubMedCrossRefGoogle Scholar
  95. Mumtaz, M.M., D.B. Tully, H.A. El-Masri, and C.T. De Rosa. 2002. Gene induction studies and toxicity of chemical mixtures. Environmental Health Perspectives 110(Suppl 6): 947–956.PubMedPubMedCentralCrossRefGoogle Scholar
  96. Müllerová, D., J. Kopecky, D. Matějková, L. Müller, J. Rosmus, J. Racek, F. Sefrna, S. Opatrna, O. Kuda, and M. Matejovic. 2008. Negative association between plasma levels of adiponectin and polychlorinated biphenyl 153 in obese women under non-energy-restrictive regime. International Journal of Obesity 32(12): 1875–1878. doi: 10.1038/ijo.2008.169.PubMedCrossRefGoogle Scholar
  97. Müllerová, D., and J. Kopecky. 2007. White adipose tissue: storage and effector site for environmental pollutants. Physiological Research 56: 375–381.PubMedGoogle Scholar
  98. Müllerová, D., D. Matějková, J. Dvořáková, L. Müller, J. Rosmus, and K. Kovářová. 2015. Persistent organochlorine pollutants in obese women after diet induced weight loss: Five years follow up study. Central European Journal of Public Health 23(3): 214–217.PubMedCrossRefGoogle Scholar
  99. Myre, M., and P. Imbeault. 2014. Persistent organic pollutants meet adipose tissue hypoxia: Does cross-talk contribute to inflammation during obesity? Obesity Reviews 15(1): 19–28. doi: 10.1111/obr.12086.PubMedCrossRefGoogle Scholar
  100. Myrmel, L.S., E. Fjære, L. Kolden Midtbø, A. Bernhard, R. Koefoed Petersen, S.B. Sonne, A. Mortensen, Q. Hao, T. Brattelid, B. Liaset, K. Kristiansen, and L. Madsen. 2016. Macronutrient composition determines accumulation of persistent organic pollutants from dietary exposure in adipose tissue of mice. Journal of Nutritional Biochemistry 27: 307–316. doi: 10.1016/j.jnutbio.2015.09.019.PubMedCrossRefGoogle Scholar
  101. Ngwa, E.N., A.P. Kengne, B. Tiedeu-Atogho, E.P. Mofo-Mato, and E. Sobngwi. 2015. Persistent organic pollutants as risk factors for type 2 diabetes. Diabetology and Metabolic Syndrome 7: 41. doi: 10.1186/s13098-015-0031-6.PubMedPubMedCentralCrossRefGoogle Scholar
  102. OECD. 2013. Health at a glance 2013: OECD indicators. OECD Publishing. http://dx.doi.org/10.1787/health_glance-2013-en
  103. Park, J., T.S. Morley, M. Kim, D.J. Clegg, and P.E. Scherer. 2014. Obesity and cancer—Mechanisms underlying tumour progression and recurrence. Nature Reviews. Endocrinology 10(8): 455–465. doi: 10.1038/nrendo.2014.94.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Pereira-Fernandes, A., E. Dirinck, A.C. Dirtu, G. Malarvannan, van Gaal L. Covaci, C. Vanparys, P.G. Jorens, and R. Blust. 2014. Expression of obesity markers and persistent organic pollutants levels in adipose tissue of obese patients: Reinforcing the obesogen hypothesis? PLoS One 9(1): e84816. doi: 10.1371/journal.pone.0084816.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Petreas, M., D. Nelson, F.R. Brown, D. Goldberg, S. Hurley, and P. Reynolds. 2011. High concentrations of polybrominated diphenylethers (PBDEs) in breast adipose tissue of California women. Environment International 37(1): 190–197. doi: 10.1016/j.envint.2010.09.001.PubMedCrossRefGoogle Scholar
  106. Pestana, D., G. Faria, C. Sá, V. Fernandes, D. Teixeira, S. Norberto, A. Faria, M. Meireles, C. Marques, L. Correia-Sá, A. Cunha, J. Guimarães, A. Taveira-Gomes, A.C. Santos, V.F. Domingues, C. Delerue-Matos, R. Monteiro, and C. Calhau. 2014. Persistent organic pollutant levels in human visceral and subcutaneous adipose tissue in obese individuals—Depot differences and dysmetabolism implications. Environmental Research 133: 170–177. doi: 10.1016/j.envres.2014.05.026.PubMedCrossRefGoogle Scholar
  107. Rantakokko, P., V. Männistö, R. Airaksinen, J. Koponen, M. Viluksela, H. Kiviranta, and J. Pihlajamäki. 2015. Persistent organic pollutants and non-alcoholic fatty liver disease in morbidly obese patients: A cohort study. Environmental Health 14: 79. doi: 10.1186/s12940-015-0066-z.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Reaves, D.K., E. Ginsburg, J.J. Bang, and J.M. Fleming. 2015. Persistence organic pollutants & obesity: Potential mechanisms for breast cancer promotion? Endocrine-Related Cancer 22(2): R69–R86. doi: 10.1530/ERC-14-0411.PubMedPubMedCentralCrossRefGoogle Scholar
  109. Redinger, R.N. 2007. The pathophysiology of obesity and its clinical manifestations. Gastroenterology & Hepatology 3(11): 856–863.Google Scholar
  110. Roos, V., M. Rönn, S. Salihovic, L. Lind, B. van Bavel, J. Kullberg, L. Johansson, H. Ahlström, and P.M. Lind. 2013. Circulating levels of persistent organic pollutants in relation to visceral and subcutaneous adipose tissue by abdominal MRI. Obesity (Silver Spring) 21(2): 413–418. doi: 10.1002/oby.20267.CrossRefGoogle Scholar
  111. Rönn, M., L. Lind, B. van Bavel, S. Salihovic, K. Michaëlsson, and P.M. Lind. 2011. Circulating levels of persistent organic pollutants associate in divergent ways to fat mass measured by DXA in humans. Chemosphere 85(3): 335–343. doi: 10.1016/j.chemosphere.2011.06.095.PubMedCrossRefGoogle Scholar
  112. Ruzzin, J., R. Petersen, E. Meugnier, L. Madsen, E.J. Lock, H. Lillefosse, T. Ma, S. Pesenti, S.B. Sonne, T.T. Marstrand, M.K. Malde, Z.Y. Du, C. Chavey, L. Fajas, A.K. Lundebye, C.L. Brand, H. Vidal, K. Kristiansen, and L. Frøyland. 2010. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environmental Health Perspectives 118(4): 465–471. doi: 10.1289/ehp.0901321.PubMedCrossRefGoogle Scholar
  113. Ruzzin, J. 2012. Public health concern behind the exposure to persistent organic pollutants and the risk of metabolic diseases. BMC Public Health 12: 298. doi: 10.1186/1471-2458-12-298.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Rylander, L., A. Rignell-Hydbom, and L. Hagmar. 2005. A cross-sectional study of the association between persistent organochlorine pollutants and diabetes. Environmental Health 4: 28.PubMedPubMedCentralCrossRefGoogle Scholar
  115. Sjöberg Lind, Y., P.M. Lind, S. Salihovic, B. van Bavel, and L. Lind. 2013a. Circulating levels of persistent organic pollutants (POPs) are associated with left ventricular systolic and diastolic dysfunction in the elderly. Environmental Research 123: 39–45. doi: 10.1016/j.envres.2013.02.007.PubMedCrossRefGoogle Scholar
  116. Sjöberg Lind, Y., P.M. Lind, S. Salihovic, B. van Bavel, and P.M. Lind. 2013b. Persistent organic pollutants and abnormal geometry of the left ventricle in the elderly. Journal of Hypertension 31(8): 1547–1553. doi: 10.1097/HJH.0b013e32836221b3.PubMedCrossRefGoogle Scholar
  117. Skinner, M.K., M. Manikkam, R. Tracey, C. Guerrero-Bosagna, M. Haque, and E.E. Nilsson. 2013. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Medicine 11: 128. doi: 10.1186/1741-7015-11-228.CrossRefGoogle Scholar
  118. Smith, A.G. 1991. Chlorinated hydrocarbon insecticides. In Handbook of pesticide toxicology, ed. W.J. Hayes and E.R. Laws. New York: Academic Press Inc. 3(15).Google Scholar
  119. Takada, I., A.P. Kouzmenko, and S. Kato. 2009. Wnt and PPARγ signaling in osteoblastogenesis and adipogenesis. Nature Reviews. Rheumatology 5(8): 442–447. doi: 10.1038/nrrheum.2009.137.PubMedCrossRefGoogle Scholar
  120. Tang-Péronard, J.L., B.L. Heitmann, T.K. Jensen, A.M. Vinggaard, S. Madsbad, U. Steuerwald, P. Grandjean, P. Weihe, F. Nielsen, and H.R. Andersen. 2015. Prenatal exposure to persistent organochlorine pollutants is associated with high insulin levels in 5-year-old girls. Environmental Research 142: 407–413. doi: 10.1016/j.envres.2015.07.009.PubMedPubMedCentralCrossRefGoogle Scholar
  121. Taylor, K.W., R.F. Novak, H.A. Anderson, L.S. Birnbaum, C. Blystone, M. DeVito, D. Jacobs, J. Köhrle, D.H. Lee, L. Rylander, A. Rignell-Hydbom, R. Tornero-Velez, M.E. Turyk, A.L. Boyles, K.A. Thayer, and L. Lind. 2013. Evaluation of the association between persistent organic pollutants and diabetes in epidemiological studies: A national toxicology program workshop review. Environmental Health Perspectives 121(7): 774–783. doi: 10.1289/ehp.1205502.PubMedPubMedCentralCrossRefGoogle Scholar
  122. Tsatsakis, A.M., M. Christakis-Hampsas, and J. Liesivuori. 2012. The increasing significance of biomonitoring for pesticides and organic pollutants. Toxicology Letters 210: 107–109.PubMedCrossRefGoogle Scholar
  123. Tsatsakis, A.M., M.N. Tzatzarakis, M. Tutudaki, A.K. Alegakis, and C. Koutis. 2008. Assessment of levels of organochlorine pesticides and their metabolites in the hair of a Greek rural human population. Human & Experimental Toxicology 27(12): 933–940. doi: 10.1177/0960327108102047.CrossRefGoogle Scholar
  124. Vafeiadi, M., V. Georgiou, G. Chalkiadaki, P. Rantakokko, H. Kiviranta, M. Karachaliou, E. Fthenou, M. Venihaki, K. Sarri, M. Vassilaki, S.A. Kyrtopoulos, E. Oken, M. Kogevinas, and L. Chatzi. 2015. Association of prenatal exposure to persistent organic pollutants with obesity and cardiometabolic traits in early childhood: The Rhea mother-child cohort (Crete, Greece). Environmental Health Perspectives 123(10): 1015–1021. doi: 10.1289/ehp.1409062.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Valera, B., P. Ayotte, P. Poirier, and E. Dewailly. 2013. Associations between plasma persistent organic pollutant levels and blood pressure in Inuit adults from Nunavik. Environment International 59: 282–289. doi: 10.1016/j.envint.2013.06.019.PubMedCrossRefGoogle Scholar
  126. Valvi, D., M.A. Mendez, R. Garcia-Esteban, F. Ballester, J. Ibarluzea, F. Goñi, J.O. Grimalt, S. Llop, L. Santa Marina, E. Vizcaino, J. Sunyer, and M. Vrijheid. 2014. Prenatal exposure to persistent organic pollutants and rapid weight gain and overweight in infancy. Obesity (Silver Spring) 22(2): 488–496. doi: 10.1002/oby.20603.CrossRefGoogle Scholar
  127. van den Dungen, M.W., J.C. Rijk, E. Kampman, W.T. Steegenga, and A.J. Murk. 2015. Steroid hormone related effects of marine persistent organic pollutants in human H295R adrenocortical carcinoma cells. Toxicology In Vitro 29(4): 769–778. doi: 10.1016/j.tiv.2015.03.002.PubMedCrossRefGoogle Scholar
  128. Walker, C.H. 2001. Organic pollutants: An ecotoxicological perspective. 2nd ed. Broken Sound Pkwy NW, Boca Raton, FL: Taylor & Francis Group.CrossRefGoogle Scholar
  129. Walker CH, Sibly RM, Hopkin SP, Peakall DB (2012), Principles of Ecotoxicology, 4th ed. CRC Press Taylor & Francis Group, 141–156.Google Scholar
  130. Wayman, G.A., D. Yang, D.D. Bose, A. Lesiak, V. Ledoux, D. Bruun, I.N. Pessah, and P.J. Lein. 2012. PCB-95 promotes dendritic growth via ryanodine receptor-dependent mechanisms. Environmental Health Perspectives 120(7): 997–1002. doi: 10.1289/ehp.1104832.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Yu, G.W., J. Laseter, and C. Mylander. 2011. Persistent organic pollutants in serum and several different fat compartments in humans. Journal of Environmental and Public Health 2011: 417980. doi: 10.1155/2011/417980.PubMedPubMedCentralCrossRefGoogle Scholar
  132. Zeliger, H.I. 2013. Lipophilic chemical exposure as a cause of cardiovascular disease. Interdisciplinary Toxicology 6(2): 55–62.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Loukia Vassilopoulou
    • 1
  • Christos Psycharakis
    • 1
  • Demetrios Petrakis
    • 1
  • John Tsiaoussis
    • 2
  • Aristides M. Tsatsakis
    • 3
    Email author
  1. 1.Laboratory of Toxicology, Medical SchoolUniversity of CreteHeraklionGreece
  2. 2.Laboratory of Anatomy, Medical SchoolUniversity of CreteHeraklionGreece
  3. 3.Department of Forensic Sciences and Toxicology, Medical SchoolUniversity of CreteHeraklionGreece

Personalised recommendations