Human adipose tissue levels of persistent organic pollutants and metabolic syndrome components: Combining a cross-sectional with a 10-year longitudinal study using a multi-pollutant approach

Environment International

Volumn 104, Issue , 2017, Pages 48-57

  Mustieles, Vicente ^a,b   Fernández, Mariana F ^a,b,c   Martin Olmedo, Piedad ^a,d   González Alzaga, Beatriz ^a,d   Fontalba Navas, Andrés ^e   Hauser, Russ ^f,g   Olea, Nicolás ^a,b,c   Arrebola, Juan P ^a,b,c,h  

^a Instituto de Investigación Biosanitaria de Granada ibs GRANADA Granada Health Research Institute ibs GRANADA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^d ANDALUSIAN SCHOOL OF PUBLIC HEALTH   (Spain)

^e Andalusian Health Service   (Spain)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

^h HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

Author keywords

Metabolic disruption; Metabolic syndrome; Organochlorine pesticides; Persistent organic pollutants; Polychlorinated biphenyls

Indexed keywords

DIAGNOSIS; LOGISTIC REGRESSION; METABOLISM; POLYCHLORINATED BIPHENYLS; RISK ASSESSMENT; TISSUE;

COX REGRESSION ANALYSIS; CROSS SECTIONAL ANALYSIS; HEXACHLOROCYCLOHEXANES; INDEPENDENT VARIABLES; METABOLIC DISRUPTION; METABOLIC SYNDROMES; ORGANOCHLORINE PESTICIDES; PERSISTENT ORGANIC POLLUTANT (POP);

ORGANIC POLLUTANTS;

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; BETA HEXACHLOROCYCLOHEXANE; HEXACHLOROBENZENE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; POLYCHLORINATED BIPHENYL; CHLORINATED HYDROCARBON;

HEALTH RISK; METABOLISM; ORGANOCHLORINE PESTICIDE; PCB; PERSISTENT ORGANIC POLLUTANT; REGRESSION ANALYSIS;

ADIPOSE TISSUE; ADULT; AGE; AGED; ALCOHOL CONSUMPTION; ARTICLE; BODY MASS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DEMOGRAPHY; EDUCATION; ENVIRONMENTAL EXPOSURE; FEMALE; FOLLOW UP; HUMAN; HUMAN TISSUE; HYPERTENSION; HYPERTRIGLYCERIDEMIA; LONG TERM EXPOSURE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; MIDDLE AGED; MORBIDITY; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PERSISTENT ORGANIC POLLUTANT; PREVALENCE; PRIORITY JOURNAL; RESIDUE ANALYSIS; RISK ASSESSMENT; SEX DIFFERENCE; SMOKING; SPAIN; ANALYSIS; CHEMISTRY; DYSLIPIDEMIA; POLLUTANT; YOUNG ADULT;

GRANADA [NICARAGUA]; NICARAGUA;

ADIPOSE TISSUE; ADULT; AGED; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; DYSLIPIDEMIAS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; FEMALE; HUMANS; HYDROCARBONS, CHLORINATED; HYPERTENSION; LONGITUDINAL STUDIES; MALE; METABOLIC SYNDROME; MIDDLE AGED; SPAIN; YOUNG ADULT;

EID: 85017567600     PISSN: 01604120     EISSN: 18736750     Source Type: Journal    
DOI: 10.1016/j.envint.2017.04.002     Document Type: Article

References (66)

1. Alberti, K.G., Eckel, R.H., Grundy, S.M., Zimmet, P.Z., Cleeman, J.I., Donato, K.A. et al., Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:16 (2009), 1640–1645.
2. Al-Othman, A., Yakout, S., Abd-Alrahman, S.H., Al-Daghri, N.M., Strong associations between the pesticide hexachlorocyclohexane and type 2 diabetes in Saudi adults. Int. J. Environ. Res. Public Health 11:9 (2014), 8984–8995.
3. Archibeque-Engle, S.L., Tessari, J.D., Winn, D.T., Keefe, T.J., Nett, T.M., Zheng, T., Comparison of organochlorine pesticide and polychlorinated biphenyl residues in human breast adipose tissue and serum. J. Toxicol. Environ. Health 52:4 (1997), 285–293.
4. Arrebola, J.P., Martin-Olmedo, P., Fernandez, M.F., Sanchez-Cantalejo, E., Jimenez-Rios, J.A., Torne, P. et al., Predictors of concentrations of hexachlorobenzene in human adipose tissue: a multivariate analysis by gender in Southern Spain. Environ. Int. 35:1 (2009), 27–32.
5. Arrebola, J.P., Fernandez, M.F., Porta, M., Rosell, J., de la Ossa, R.M., Olea, N. et al., Multivariate models to predict human adipose tissue PCB concentrations in Southern Spain. Environ. Int. 36:7 (2010), 705–713.
6. Arrebola, J.P., Mutch, E., Cuellar, M., Quevedo, M., Claure, E., Mejía, L.M. et al., Factors influencing combined exposure to three indicator polychlorinated biphenyls in an adult cohort from Bolivia. Environ. Res. 116 (2012), 17–25.
7. Arrebola, J.P., Fernández, M.F., Olea, N., Ramos, R., Martin-Olmedo, P., Human exposure to p,p′-dichlorodiphenyldichloroethylene (p,p′-DDE) in urban and semi-rural areas in southeast Spain: a gender perspective. Sci. Total Environ. 458-460 (2013), 209–216.
8. Arrebola, J.P., Ocaña-Riola, R., Arrebola-Moreno, A.L., Fernández-Rodríguez, M., Martin-Olmedo, P., Fernández, M.F. et al., Associations of accumulated exposure to persistent organic pollutants with serum lipids and obesity in an adult cohort from Southern Spain. Environ. Pollut. 195 (2014), 9–15.
9. Arrebola, J.P., Fernández, M.F., Martin-Olmedo, P., Bonde, J.P., Martín-Rodriguez, J.L., Expósito, J. et al., Historical exposure to persistent organic pollutants and risk of incident hypertension. Environ. Res. 138 (2015), 217–223.
10. Arrebola, J.P., González-Jiménez, A., Fornieles-González, C., Artacho-Cordón, F., Olea, N., Escobar-Jiménez, F. et al., Relationship between serum concentrations of persistent organic pollutants and markers of insulin resistance in a cohort of women with a history of gestational diabetes mellitus. Environ. Res. 136 (2015), 435–440.
11. Biemann, R., Fischer, B., Navarrete, Santos A., Adipogenic effects of a combination of the endocrine-disrupting compounds bisphenol A, diethylhexylphthalate, and tributyltin. Obes. Facts 7:1 (2014), 48–56.
12. Bourez, S., Van den Daelen, C., Le Lay, S., Poupaert, J., Larondelle, Y., Thomé, J.P. et al., The dynamics of accumulation of PCBs in cultured adipocytes vary with the cell lipid content and the lipophilicity of the congener. Toxicol. Lett. 216:1 (2013), 40–46.
13. Braun, J.M., Kalkbrenner, A.E., Just, A.C., Yolton, K., Calafat, A.M., Sjödin, A. et al., Gestational exposure to endocrine-disrupting chemicals and reciprocal social, repetitive, and stereotypic behaviors in 4- and 5-year-old children: the HOME study. Environ. Health Perspect. 122:5 (2014), 513–520.
14. Braun, J.M., Gennings, C., Hauser, R., Webster, T.F., What can epidemiological studies tell us about the impact of chemical mixtures on human health?. Environ. Health Perspect. 124:1 (2016), A6–A9.
15. Bräuner, E.V., Andersen, Z.J., Frederiksen, M., Specht, I.O., Hougaard, K.S., Ebbehøj, N. et al., Health effects of PCBs in residences and schools (HESPERUS): PCB - health cohort profile. Sci. Rep., 6, 2016, 24571.
16. Buckland, G., González, C.A., Agudo, A., Vilardell, M., Berenguer, A., Amiano, P. et al., Adherence to the Mediterranean diet and risk of coronary heart disease in the Spanish EPIC cohort study. Am. J. Epidemiol. 170:12 (2009), 1518–1529.
17. Burns, J.S., Williams, P.L., Korrick, S.A., Hauser, R., Sergeyev, O., Revich, B. et al., Association between chlorinated pesticides in the serum of prepubertal Russian boys and longitudinal biomarkers of metabolic function. Am. J. Epidemiol. 180:9 (2014), 909–919.
18. CDC (Centers for Disease Control and Prevention), Fourth National Report on Human Exposure to Environmental Chemicals. 2015 (Accessed on August, 2016: http://www.cdc.gov/biomonitoring/pdf/FourthReport_UpdatedTables_Feb2015.pdf).
19. Dhurandhar, E.J., Keith, S.W., The aetiology of obesity beyond eating more and exercising less. Best Pract. Res. Clin. Gastroenterol. 28:4 (2014), 533–544.
20. Dirinck, E., Jorens, P.G., Covaci, A., Geens, T., Roosens, L., Neels, H. et al., Obesity and persistent organic pollutants: possible obesogenic effect of organochlorine pesticides and polychlorinated biphenyls. Obesity 19:4 (2011), 709–714.
21. Evangelou, E., Ntritsos, G., Chondrogiorgi, M., Kavvoura, F.K., Hernández, A.F., Ntzani, E.E. et al., Exposure to pesticides and diabetes: a systematic review and meta-analysis. Environ. Int. 91 (2016), 60–68.
22. Friedman, J., Hastie, T., Tibshirani, R., Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33:1 (2010), 1–22.
23. Galic, S., Oakhill, J.S., Steinberg, G.R., Adipose tissue as an endocrine organ. Mol. Cell. Endocrinol. 316:2 (2010), 129–139.
24. Gaskins, A.J., Schisterman, E.F., The effect of lipid adjustment on the analysis of environmental contaminants and the outcome of human health risks. Methods Mol. Biol. 580 (2009), 371–381.
25. Gasull, M., Bosch de Basea, M., Puigdomènech, E., Pumarega, J., Porta, M., Empirical analyses of the influence of diet on human concentrations of persistent organic pollutants: a systematic review of all studies conducted in Spain. Environ. Int. 37:7 (2011), 1226–1235.
26. Gauthier, M.S., Rabasa-Lhoret, R., Prud'homme, D., Karelis, A.D., Geng, D., van Bavel, B. et al., The metabolically healthy but obese phenotype is associated with lower plasma levels of persistent organic pollutants as compared to the metabolically abnormal obese phenotype. J. Clin. Endocrinol. Metab. 99:6 (2014), E1061–E1066, 10.1210/jc.2013-3935.
27. Gonzalez, C.A., Riboli, E., Diet and cancer prevention: contributions from the European prospective investigation into cancer and Nutrition (EPIC) study. Eur. J. Cancer 46:14 (2010), 2555–2562.
28. Guh, D.P., Zhang, W., Bansback, N., Amarsi, Z., Birmingham, C.L., Anis, A.H., The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health, 9, 2009, 88.
29. Heindel, J.J., vom Saal FS, Blumberg B, Bovolin P, Calamandrei G, Ceresini G, et al., Parma consensus statement on metabolic disruptors. Environ. Health, 14, 2015, 54.
30. Ibrahim, M.M., Fjære, E., Lock, E.J., Naville, D., Amlund, H., Meugnier, E. et al., Chronic consumption of farmed salmon containing persistent organic pollutants causes insulin resistance and obesity in mice. PLoS One, 6(9), 2011, e25170, 10.1371/journal.pone.0025170.
31. Jakszyn, P., Goñi, F., Etxeandia, A., Vives, A., Millán, E., López, R. et al., Serum levels of organochlorine pesticides in healthy adults from five regions of Spain. Chemosphere 76:11 (2009), 1518–1524.
32. Kim, M.J., Pelloux, V., Guyot, E., Tordjman, J., Bui, L.C., Chevallier, A. et al., Inflammatory pathway genes belong to major targets of persistent organic pollutants in adipose cells. Environ. Health Perspect. 120:4 (2012), 508–514.
33. Kohlmeier, L., Kohlmeier, M., Adipose tissue as a medium for epidemiologic exposure assessment. Environ. Health Perspect. 103:Suppl. 3 (1995), 99–106.
34. La Merrill, M., Emond, C., Kim, M.J., Antignac, J.P., Le Bizec, B., Clément, K. et al., Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ. Health Perspect. 121:2 (2013), 162–169.
35. Lee, D.H., Lee, I.K., Jin, S.H., Steffes, M., Jacobs, D.R. Jr., Association between serum concentrations of persistent organic pollutants and insulin resistance among non-diabetic adults: results from the National Health and Nutrition Examination Survey 1999–2002. Diabetes Care 30:3 (2007), 622–628.
36. Lee, D.H., Lee, I.K., Porta, M., Steffes, M., Jacobs, D.R. Jr., 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 (2007), 1841–1851.
37. 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, 10.1371/journal.pone.0015977.
38. Lee, Y.M., Kim, K.S., Kim, S.A., Hong, N.S., Lee, S.J., Lee, D.H., Prospective associations between persistent organic pollutants and metabolic syndrome: a nested case-control study. Sci. Total Environ. 496 (2014), 219–225.
39. Lee, D.H., Porta, M., Jacobs, D.R. Jr., Vandenberg, L.N., Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr. Rev. 4 (2014), 557–601.
40. Lee, H.A., Park, S.H., Hong, Y.S., Ha, E.H., Park, H., The effect of exposure to persistent organic pollutants on metabolic health among Korean children during a 1-year follow-up. Int. J. Environ. Res. Public Health, 13(3), 2016.
41. Lenters, V., Portengen, L., Rignell-Hydbom, A., Jönsson, B.A., Lindh, C.H., Piersma, A.H. et al., Prenatal phthalate, perfluoroalkyl acid, and organochlorine exposures and term birth weight in three birth cohorts: multi-pollutant models based on elastic net regression. Environ. Health Perspect. 124:3 (2016), 365–372.
42. Lim, S., Cho, Y.M., Park, K.S., Lee, H.K., Persistent organic pollutants, mitochondrial dysfunction, and metabolic syndrome. Ann. N. Y. Acad. Sci. 1201 (2010), 166–176.
43. Luo, F., Song, J., Chen, M.F., Wei, J., Pan, Y.Y., Yu, H.B., Risk assessment of manufacturing equipment surfaces contaminated with DDTs and dicofol. Sci. Total Environ. 468-469 (2014), 176–185.
44. Malarvannan, G., Dirinck, E., Dirtu, A.C., Pereira-Fernandes, A., Neels, H., Jorens, P.G. et al., Distribution of persistent organic pollutants in two different fat compartments from obese individuals. Environ. Int. 55 (2013), 33–42.
45. Moreno Frías, M., Jiménez Torres, M., GarridoFrenich, A., Martínez Vidal, J.L., Olea-Serrano, F., Olea, N., Determination of organochlorine compounds in human biological samples by GC-MS/MS. Biomed. Chromatogr. 18:2 (2004), 102–111.
46. Mrema, E.J., Rubino, F.M., Brambilla, G., Moretto, A., Tsatsakis, A.M., Colosio, C., Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicology 307 (2013), 74–88.
47. Muñoz-Garach, A., Cornejo-Pareja, I., Tinahones, F.J., Does metabolically healthy obesity exist?. Nutrients, 8(6), 2016, 10.3390/nu8060320 (pii: E320).
48. Park, S.K., Son, H.K., Lee, S.K., Kang, J.H., Chang, Y.S., Jacobs, D.R. et al., Relationship between serum concentrations of organochlorine pesticides and metabolic syndrome among non-diabetic adults. J. Prev. Med. Public Health 43:1 (2010), 1–8.
49. Pauwels, A., Covaci, A., Weyler, J., Delbeke, L., Dhont, M., De Sutter, P. et al., Comparison of persistent organic pollutant residues in serum and adipose tissue in a female population in Belgium, 1996–1998. Arch. Environ. Contam. Toxicol. 39:2 (2000), 265–270.
50. Porta, M., A Dictionary of Epidemiology. Sixth edition, 2014, Oxford University Press, 78.
51. Quintana, P.J., Delfino, R.J., Korrick, S., Ziogas, A., Kutz, F.W., Jones, E.L. et al., Adipose tissue levels of organochlorine pesticides and polychlorinated biphenyls and risk of non-Hodgkin's lymphoma. Environ. Health Perspect. 112:8 (2004), 854–861.
52. Rajapakse, N., Silva, E., Kortenkamp, A., Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environ. Health Perspect. 110:9 (2002), 917–921.
53. Rivas, A., Fernandez, M.F., Cerrillo, I., Ibarluzea, J., Olea-Serrano, M.F., Pedraza, V. et al., Human exposure to endocrine disrupters: standardization of a marker of estrogenic exposure in adipose tissue. APMIS 109:3 (2001), 185–197.
54. Ruiz, P., Perlina, A., Mumtaz, M., Fowler, B.A., A systems biology approach reveals converging molecular mechanisms that link different POPs to common metabolic diseases. Environ. Health Perspect. 124:7 (2016), 1034–1041.
55. Ruzzin, J., Petersen, R., Meugnier, E., Madsen, L., Lock, E.J., Lillefosse, H. et al., Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ. Health Perspect. 118:4 (2010), 465–471.
56. Shen, H., Main, K.M., Virtanen, H.E., Damggard, I.N., Haavisto, A.M., Kaleva, M. et al., From mother to child: investigation of prenatal and postnatal exposure to persistent bioaccumulating toxicants using breast milk and placenta biomonitoring. Chemosphere 67:9 (2007), S256–S262.
57. Shen, H., Han, J., Tie, X., Xu, W., Ren, Y., Ye, C., Polychlorinated dibenzo-p-dioxins/furans and polychlorinated biphenyls in human adipose tissue from Zhejiang Province, China. Chemosphere 74:3 (2009), 384–388.
58. Simon, N., Friedman, J., Hastie, T., Tibshirani, R., Regularization paths for cox's proportional hazards model via coordinate descent. J. Stat. Softw. 39:5 (2011), 1–13.
59. Tang-Péronard, J.L., Heitmann, B.L., Jensen, T.K., Vinggaard, A.M., Madsbad, S., Steuerwald, U. et al., Prenatal exposure to persistent organochlorine pollutants is associated with high insulin levels in 5-year-old girls. Environ. Res. 142 (2015), 407–413.
60. Tibshirani, R., Bien, J., Friedman, J., Hastie, T., Simon, N., Taylor, J. et al., Strong rules for discarding predictors in lasso-type problems. J. R. Stat. Soc. Ser. B Stat Methodol. 74:2 (2012), 245–266.
61. Tomar, L.R., Agarwal, M.P., Avasthi, R., Tyagi, V., Mustafa, M., Banerjee, B.D., Serum organochlorine pesticide levels in patients with metabolic syndrome. Indian J. Endocrinol. Metab. 17:Suppl. 1 (2013), S342–S344.
62. Tuomisto, J., Airaksinen, R., Kiviranta, H., Tukiainen, E., Pekkanen, J., Tuomisto, J.T., A pharmacokinetic analysis and dietary information are necessary to confirm or reject the hypothesis on persistent organic pollutants causing type 2 diabetes. Toxicol. Lett. 261 (2016), 41–48.
63. Vaclavik, E., Tjonneland, A., Stripp, C., Overvad, K., Philippe Weber, J., Raaschou-Nielsen, O., Organochlorines in Danish women: predictors of adipose tissue concentrations. Environ. Res. 100:3 (2006), 362–370.
64. Valera, B., Ayotte, P., Poirier, P., Dewailly, E., Associations between plasma persistent organic pollutant levels and blood pressure in Inuit adults from Nunavik. Environ. Int. 59 (2013), 282–289.
65. Zhang, L., Nichols, R.G., Correll, J., Murray, I.A., Tanaka, N., Smith, P.B. et al., Persistent organic pollutants modify gut microbiota-host metabolic homeostasis in mice through aryl hydrocarbon receptor activation. Environ. Health Perspect. 123:7 (2015), 679–688.
66. Zou, H., Hastie, T., Regularization and variable selection via the elastic net. J. R. Stat. Soc. 67:2 (2005), 301–320.