A pharmacokinetic analysis and dietary information are necessary to confirm or reject the hypothesis on persistent organic pollutants causing type 2 diabetes

Toxicology Letters

Volumn 261, Issue , 2016, Pages 41-48

  Tuomisto, Jouko ^a   Airaksinen, Riikka ^a   Kiviranta, Hannu ^a   Tukiainen, Erkki ^b   Pekkanen, Juha ^a,c   Tuomisto, Jouni T ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Diet; Dioxins (PCDD F); Modeling; Persistent organic pollutant (POP); Pharmacokinetics; Type 2 diabetes

Indexed keywords

DIBENZOFURAN DERIVATIVE; DIOXIN; POLYCHLORINATED DIBENZO P DIOXINS DIBENZOFURAN DERIVATIVE; UNCLASSIFIED DRUG; DIBENZOFURAN; POLLUTANT; POLYCHLORINATED DIBENZODIOXIN;

ADULT; ARTICLE; BODY FAT; BODY WEIGHT; CALORIC INTAKE; CAUSALITY; COMPARATIVE STUDY; CONTROLLED STUDY; DAIRY PRODUCT; DIETARY INTAKE; DISEASE ASSOCIATION; ELIMINATION RATE CONSTANT; FISH; FOOD INTAKE; HUMAN; MAJOR CLINICAL STUDY; MASS FRAGMENTOGRAPHY; MEAT; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PERSISTENT ORGANIC POLLUTANT; PRIORITY JOURNAL; SOFT TISSUE SARCOMA; STEADY STATE; SUBCUTANEOUS FAT; SURGICAL PATIENT; BODY MASS; CHEMICALLY INDUCED; FOOD CONTAMINATION; MEDICAL RECORD; PHARMACOKINETICS; POLLUTANT; RETROSPECTIVE STUDY; TOXICITY;

BODY MASS INDEX; DIABETES MELLITUS, TYPE 2; DIBENZOFURANS; DIET RECORDS; ENVIRONMENTAL POLLUTANTS; FOOD CONTAMINATION; HUMANS; POLYCHLORINATED DIBENZODIOXINS; RETROSPECTIVE STUDIES;

EID: 84988737034     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2016.08.024     Document Type: Article

References (60)

1. 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 34 (2011), 1972–1979.
2. Airaksinen, R., Hallikainen, A., Rantakokko, P., Ruokojärvi, P., Vuorinen, P.J., Parmanne, R., Verta, M., Mannio, J., Kiviranta, H., Time trends and congener profiles of PCDD/Fs, PCBs, and PBDEs in Baltic herring off the coast of Finland during 1978–2009. Chemosphere 114 (2014), 165–171.
3. Deurenberg, P., Weststrate, J.A., Seidell, J.C., Body mass index as a measure of body fatness: age- and sex-specific prediction formulas. Br. J. Nutr. 65 (1991), 105–114.
4. Dirinck, E., Jorens, P.G., Covaci, A., Geens, T., Roosens, L., Neels, H., Mertens, I., van Gaal, L., Obesity and persistent organic pollutants: possible obesogenic effect of organochlorine pesticides and polychlorinated biphenyls. Obesity 19 (2011), 709–714.
5. Elobeid, M.A., Brock, D.W., Allison, D.B., Padilla, M.A., Ruden, D.M., Endocrine disruptors and obesity: an examination of selected persistent organic pollutants in the NHANES 1999–2002 data. Int. J. Environ. Res. Public Health 7 (2010), 2988–3005.
6. Fogelholm, M., Anderssen, S., Gunnarsdottir, I., Lahti-Koski, M., Dietary macronutrients and food consumption as determinants of long-term weight change in adult populations: a systematic literature review. Food Nutr. Res., 56(19103), 2012, 10.3402/fnr.v56i0.19103.
7. Goldstein, A., Aronow, L., Kalman, S.M., The time course of drug action. Principles of Drug Action: The Basis of Pharmacology, 2 ed., 1974, John Wiley & Sons, New York, 301–338.
8. Goodman, M., Narayan, K.M.V., Flanders, D., Chang, E.T., Adami, H.O., Boffetta, P., Mandel, J.S., Dose-response relationship between serum 2,3,7,8-tetrachlorodibenzo-p-dioxin and diabetes mellitus: a meta-analysis. Am. J. Epidemiol. 181 (2015), 374–384.
9. Hallikainen, A., Vartiainen, T., Food control surveys of polychlorinated dibenzo-p-dioxins and dibenzofurans and intake estimates. Food Addit Contam 14 (1997), 355–366.
10. Hill, A.B., The environment and disease: association or causation?. Proc. R. Soc. Med., 1965, 295–300.
11. Hofe, C.R., Feng, L., Zephyr, D., Stromberg, A.J., Hennig, B., Gaetke, L.M., Fruit and vegetable intake, as reflected by serum carotenoid concentrations, predicts reduced probability of polychlorinated biphenyl-associated risk for type 2 diabetes: national health and nutrition examination survey 2003–2004. Nutr. Res. 34 (2014), 285–293.
12. Huang, C.Y., Wu, C.L., Yang, Y.C., Jung-Wei Chang, J.W., Kuo, Y.C., Cheng, Y.Y., Wu, J.S., Lee, C.C., Guo, H.R., Association between dioxin and diabetes mellitus in an endemic area of exposure in Taiwan. A population-based study. Medicine, 94(42), 2015, e1730.
13. Hue, O., Marcotte, J., Berrigan, F., Simoneau, M., Doré, J., Marceau, P., Marceau, S., Tremblay, A., Teasdale, N., Plasma concentration of organochlorine compounds is associated with age and not obesity. Chemosphere 67 (2007), 1463–1467.
14. Ibrahim, M.M., Fjære, E., Lock, E.J., Naville, D., Amlund, H., Meugnier, E., Battistoni, B.L.M., Frøyland, L., Madsen, L., Jessen, N., Lund, S., Vidal, H., Ruzzin, J., Chronic consumption of farmed Salmon containing persistent organic pollutants causes insulin resistance and obesity in mice. PLoS One, 6(9), 2011, e25170.
15. Jaacks, L.M., Staimez, L.R., Association of persistent organic pollutants and non-persistent pesticides with diabetes and diabetes-related health outcomes in Asia: a systematic review. Environ. Int. 76 (2015), 57–70.
16. Kerger, B.D., Scott, P.K., Pavuk, M., Gough, M., Paustenbach, D.J., Re-analysis of Ranch Hand study supports reverse causation hypothesis between dioxin and diabetes. Crit. Rev. Toxicol. 42 (2012), 669–687.
17. Keski-Rahkonen, A., Bulik, C.M., Pietiläinen, K.H., Rose, R.J., Kaprio, J., Rissanen, A., Eating styles, overweight and obesity in young adult twins. Eur. J. Clin. Nutr. 61 (2007), 822–829.
18. Kiviranta, H., Purkunen, R., Vartiainen, T., Levels and trends of PCDD/Fs and PCBs in human milk in Finland. Chemosphere 38 (1999), 311–323.
19. Kiviranta, H., Hallikainen, A., Ovaskainen, M.L., Kumpulainen, J., Vartiainen, T., Dietary intakes of polychlorinated dibenzo-p-dioxins, dibenzofurans and polychlorinated biphenyls in Finland. Food Addit. Contam. 18 (2001), 945–953.
20. Kiviranta, H., Ovaskainen, M.L., Vartiainen, T., Market basket study on dietary intake of PCDD/Fs, PCBs, and PBDEs in Finland. Environ. Int. 30 (2004), 923–932.
21. Kiviranta, H., Tuomisto, J.T., Tuomisto, J., Tukiainen, E., Vartiainen, T., Polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in the general population in Finland. Chemosphere 60 (2005), 854–869.
22. Knutsen, H.K., Kvalem, H.E., Haugen, M., Meltzer, H.M., Brantsæter, A.L., Alexander, J., Päpke, O., Liane, V.H., Georg Becher, G., Thomsen, C., Sex, BMI and age in addition to dietary intakes influence blood concentrations and congener profiles of dioxins and PCBs. Mol. Nutr. Food Res. 55 (2011), 772–782.
23. Kuo, C.C., Moon, K., Thayer, K.A., Navas-Acien, A., Environmental chemicals and type 2 diabetes: an updated systematic review of the epidemiologic evidence. Curr. Diabetes Rep. 13 (2013), 831–849.
24. Lee, D.H., Jacobs, D.R. Jr., Hormesis and public health: can glutathione depletion and mitochondrial dysfunction due to very low-dose chronic exposure to persistent organic pollutants be mitigated?. J. Epidemiol. Commun. Health 69 (2015), 294–300.
25. 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. Diabetes Care 29 (2006), 1638–1644.
26. Lee, D.H., Lee, I.K., Steffes, M., Jacobs, D.R. Jr., Extended analyses of the association between serum concentrations of persistent organic pollutants and diabetes. Diabetes Care 30 (2007), 1596–1598.
27. Lee, D.H., Steffes, M.W., Sjödin, A., Jones, R.S., Needham, L.L., Jacobs, D.R. Jr., Low dose of some persistent organic pollutants predicts type 2 diabetes: a nested case—control study. Environ. Health Perspect. 118 (2010), 1235–1242.
28. Lee, D.H., Steffes, M.W., Sjödin, A., Jones, R.S., Needham, L.L., Jacobs, D.R. Jr., Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes. PLoS One, 6(1), 2011, e15977.
29. Ley, S.H., Hamdy, O., Mohan, V., Hu, F.B., Prevention and management of type 2 diabetes: dietary components and nutritional strategies. Lancet 383 (2014), 1999–2007.
30. Liem, A.K.D., Fürst, P., Rappe, C., Exposure of populations to dioxins and related compounds. Food Addit. Contam. 17 (2000), 241–259.
31. Lignell, S., Aune, M., Darnerud, P.O., Cnattingius, S., Glynn, A., Persistent organochlorine and organobromine compounds in mother's milk from Sweden 1996–2006: compound-specific temporal trends. Environ. Res. 109 (2009), 760–767.
32. Lind, L., Lind, P.M., Lejonklou, M.H., Dunder, L., Bergman, Å., Guerrero-Bosagna, C., Lampa, E., Lee, H.K., Legler, J., Nadal, Å., Pak, Y.K., Phipps, R.P., Vandenberg, L.N., Zalko, D., Ågerstrand, M., Öberg, M., Blumberg, B., Heindel, J.J., Birnbaum, L.S., Uppsala consensus statement on environmental contaminants and the global obesity epidemic. Environ. Health Perspect., 2016(May), 2016.
33. Longnecker, M.P., Daniels, J.L., Environmental contaminants as etiologic factors for diabetes. Environ. Health Perspect. 109:Suppl. 6 (2001), 871–876.
34. Männistö, S., Ovaskainen, M.L., Valsta, L. (Eds.) (2003). Finravinto 2002–tutkimus [The National Findiet 2002 Study]. National Public Health Institute, Series B3, 2003. Available at http://urn.fi/URN:NBN:fi-fe2014030615904.
35. Madden, A.M., Mulrooney, H.M., Shah, S., Estimation of energy expenditure using prediction equations in overweight and obese adults: a systematic review. J. Hum. Nutr. Dietetics, 2016 (online early view).
36. Magliano, D.J., Loh, V.H.Y., Harding, J.L., Botton, J., Shaw, J.E., Persistent organic pollutants and diabetes: a review of the epidemiological evidence. Diabetes Metab. 40 (2014), 1–14.
37. Micha, R., Michas, G., Mozaffarian, D., Unprocessed red and processed meats and risk of coronary artery disease and type 2 diabetes—an updated review of the evidence. Curr. Atheroscler Rep. 14 (2012), 515–524.
38. Milbrath, M.O., Wenger, Y., Chang, C.W., Emond, C., Garabrant, D., Gillespie, B.W., Jolliet, O., Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ. Health Perspect. 117 (2009), 417–425.
39. Montonen, J., Knekt, P., Härkänen, T., Järvinen, R., Heliövaara, M., Aromaa, A., Reunanen, A., Dietary patterns and the incidence of type 2 diabetes. Am. J. Epidemiol. 161 (2005), 219–227.
40. Ngwa, E.N., Kengne, A.P., Tiedeu-Atogho, B., Mofo-Mato, E.P., Sobngwi, E., Persistent organic pollutants as risk factors for type 2 diabetes. Diabetol. Metab. Syndrome, 7, 2015, 41.
41. Pajunen, P., Keinänen-Kiukaanniemi, S., Korpi-Hyövälti, E., Männistö, S., Niskanen, L., Oksa, H., Saaristo, T., Saltevo, J., Sundvall, J., Vanhala, M., Uusitupa, M., Eriksson, J., Peltonen, M., Ylipainon ja lihavuuden esiintyvyys tyypin 2 diabetespotilailla [prevalence of overweight and obesity in patients with type 2 diabetes in Finland, with english summary]. Suomen Lääkärilehti 67 (2012), 2621–2626.
42. Quetelet, L.A., Physique Sociale, vol. 2, 1869, C. Muquardt, Brussels, 92.
43. Reaves, D.K., Ginsburg, E., Bang, J.J., Fleming, J.M., Persistent organic pollutants and obesity: are they potential mechanisms for breast cancer promotion?. Endocr. Relat. Cancer 22 (2015), R69–R86.
44. Rignell-Hydbom, A., Rylander, L., Hagmar, L., Exposure to persistent organochlorine pollutants and type 2 diabetes mellitus. Hum. Exp. Toxicol. 26 (2007), 447–452.
45. Ruzzin, J., Petersen, R., Meugnier, E., Madsen, L., Lock, E.J., Lillefosse, H., Ma, T., Pesenti, S., Sonne, S.B., Marstrand, T.T., Malde, M.K., Du, Z.Y., Chavey, C., Fajas, L., Lundebye, A.K., Brand, C.L., Vidal, H., Kristiansen, K., Frøyland, L., Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ. Health Perspect. 118 (2010), 465–471.
46. Sahlstrom, L.M.O., Sellstrom, U., de Wit, C.A., Lignell, S., Darnerud, P.O., Estimated intakes of brominated flame retardants via diet and dust compared to internal concentrations in a Swedish mother-toddler cohort. Int. J. Hyg. Environ. Health 218 (2015), 422–432.
47. Schecter, A., Päpke, O., Harris, T.R., Tung, K.C., Musumba, A., Olson, J., Birnbaum, L., Polybrominated diphenyl ether (PBDE) levels in an expanded market basket survey of U.S. food and estimated PBDE dietary intake by age and sex. Environ. Health Perspect. 114 (2006), 1515–1520.
48. Steenland, K., Calvert, G., Ketchum, N., Michalek, J., Dioxin and diabetes mellitus: an analysis of the combined NIOSH and Ranch Hand data. Occup. Environ. Med. 58 (2001), 641–648.
49. Suarez-Lopez, J.R., Lee, D.H., Porta, M., Steffes, M.W., Jacobs, D.R. Jr., Persistent organic pollutants in young adults and changes in glucose related metabolism over a 23-year follow-up. Environ. Res. 137 (2015), 485–494.
50. Taylor, K.W., Novak, R.F., Anderson, H.A., Birnbaum, L.S., Blystone, C., DeVito, M., Jacobs, D., Köhrle, J., Lee, D.H., Rylander, L., Rignell-Hydbom, A., Tornero-Velez, R., Turyk, M.E., Boyles, A.L., Thayer, K.A., Lind, L., Evaluation of the association between persistent organic pollutants (POPs) and diabetes in epidemiological studies: a national toxicology program workshop review. Environ. Health Perspect. 121 (2013), 774–783.
51. Tuomisto, J.T., Pekkanen, J., Kiviranta, H., Tukiainen, E., Vartiainen, T., Tuomisto, J., Soft-tissue sarcoma and dioxin: a case-control study. Int. J. Cancer 108 (2004), 893–900.
52. Tuomisto, J., Pekkanen, J., Kiviranta, H., Tukiainen, E., Vartiainen, T., Viluksela, M., Tuomisto, J.T., Dioxin cancer risk—example of hormesis?. Dose Response 3 (2005), 332–341.
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. 117 (2009), 1076–1082.
54. Turyk, M., Fantuzzi, G., Persky, V., Freels, S., Lambertino, A., Pini, M., Rhodes, D.H., Anderson, H.A., Persistent organic pollutants and biomarkers of diabetes risk in a cohort of great lakes sport caught fish consumers. Environ. Res. 140 (2015), 335–344.
55. Vartiainen, T., Saarikoski, S., Jaakkola, J., Tuomisto, J., PCDD, PCDF, and PCB concentrations in human milk from two areas in Finland. Chemosphere 34 (1997), 2571–2583.
56. Vasiliu, O., Cameron, L., Gardiner, J., Deguire, P., Karmaus, W., Polybrominated biphenyls, polychlorinated biphenyls, body weight, and incidence of adult-onset diabetes mellitus. Epidemiology 17 (2006), 352–359.
57. Wu, J.H.Y., Micha, R., Imamura, F., Pan, A., Biggs, M.L., Ajaz, O., Djousse, L., Hu, F., Mozaffarian, D., Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Br. J. Nutr. 107 (2012), S214–S227.
58. 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. 121 (2013), 153–161.
59. Zazpe, I., Bes-Rastrollo, M., Ruiz-Canela, M., Sánchez-Villegas, A., Serrano-Martínez, M., Martínez-González, M.A., A brief assessment of eating habits and weight gain in a Mediterranean cohort. Br. J. Nutr. 105 (2011), 765–775.
60. van den Berg, M., Birnbaum, L.S., Michael Denison, M., De Vito, M., Farland, W., Feeley, M., Heidelore Fiedler, H., Hakansson, H., Hanberg, A., Haws, L., Rose, M., Safe, S., Schrenk, D., Tohyama, C., Tritscher, A., Tuomisto, J., Tysklind, M., Walker, N., Peterson, R.E., The 2005 World Health Organization re-evaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 2006 (2006), 223–241.