Prenatal exposure to persistent organic pollutants and markers of obesity and cardiometabolic risk in Spanish adolescents

Nuria Güil-Oumrait, Damaskini Valvi, Raquel Garcia-Esteban, Monica Guxens, Jordi Sunyer, Maties Torrent, Maribel Casas, Martine Vrijheid, Nuria Güil-Oumrait, Damaskini Valvi, Raquel Garcia-Esteban, Monica Guxens, Jordi Sunyer, Maties Torrent, Maribel Casas, Martine Vrijheid

Abstract

Background: Prenatal exposure to persistent organic pollutants (POPs) has been linked to cardiometabolic (CM) risk factors in childhood, but there are no studies evaluating the persistence of these associations into adolescence, a period of relevant changes in endocrine-dependent organ systems and rapid increases in lean and fat mass. We examined the associations of prenatal POP exposures with body mass index (BMI) from age 4 to 18 years, and with other CM risk markers in adolescence.

Methods: We analysed 379 children from the Spanish INMA-Menorca birth cohort study with measured cord blood POP concentrations. We calculated BMI z-scores at ages 4, 6, 11, 14 and 18 years using the WHO growth reference. Body fat % was measured at 11 and 18 years and waist-to-height ratio (WHtR) and blood pressure (BP) at 11, 14 and 18 years. We measured CM biomarkers in fasting blood collected at age 14 years and calculated a CM-risk score as the sum of the sex-, and age-specific z-scores for waist circumference, mean arterial BP, homeostatic model assessment of insulin resistance, fasting blood triglycerides, and high-density lipoprotein cholesterol (HDL-C) (n = 217). Generalised estimating equations and multivariate linear regression models assessed the associations with repeated and single time-point measures, respectively.

Results: Hexachlorobenzene (HCB) exposure in the third tertile, compared to the first tertile, was associated with higher BMI (β = 0.24; 95% CI: 0.01, 0.47) and WHtR z-score (β = 0.27; 95% CI: 0.04, 0.51). A continuous increase in HCB was associated with an elevated body fat % (β per 10-fold increase = 4.21; 95% CI: 0.51, 7.92), systolic BP (β = 0.32; 95% CI: 0.02, 0.64) and diastolic BP z-score (β = 0.32; 95% CI: 0.02, 0.62) across all ages, and with higher CM-risk score (β = 1.59; 95% CI: 0.02, 3.18) and lipid biomarkers (total cholesterol, triglycerides and low-density lipoprotein cholesterol (LDL-C)) at 14 years. Dichlorodiphenyltrichloroethane (p,p'-DDT) exposure was non-monotonically associated with BMI and systolic BP. p,p'-DDE and Σ-polychlorinated biphenyls (PCBs) (sum of congeners 118, 138, 153, 180) were not associated with adiposity or BP. p,p'-DDT exposure was associated with an increased CM-risk score, and ΣPCBs concentrations with LDL-C in all adolescents and with total cholesterol only in girls (p-sex interaction = 0.05).

Conclusion: This first longitudinal study from 4 to 18 years suggests that the previously reported POP associations with child BMI persist later in adolescence and that prenatal POP exposures are associated with major risk factors for adult CM syndrome.

Keywords: Cardiometabolic syndrome; Dichlorodiphenyltrichloroethane (p,p’-DDT); Endocrine disruptors; Hexachlorobenzene (HCB); Persistent organic pollutants (POPs); Polychlorinated biphenyls (PCBs).

Conflict of interest statement

The authors declared that there is no conflict of interest.

Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.

Figures

Fig. 1
Fig. 1
Flow chart of sample populations in our study. Note: POPs, persistent organic pollutants.
Fig. 2
Fig. 2
Adjusted associations between prenatal cord blood concentrations of POPs and BMI z-score (A), WHtR z-score (B), Body Fat % (C), Systolic BP z-score (D), and Diastolic BP z-score (E) at each age of follow-up from 4 years until age 18 years. Generalized estimating equation models were adjusted for maternal characteristics (i.e. parity history, pre-pregnancy BMI, education, socioeconomic status, smoking, and age at pregnancy), and child’s follow up visit. Body fat % model was additionally adjusted by sex. Upper values represent the p-values of the age at follow-up interaction term.
Fig. 2
Fig. 2
Adjusted associations between prenatal cord blood concentrations of POPs and BMI z-score (A), WHtR z-score (B), Body Fat % (C), Systolic BP z-score (D), and Diastolic BP z-score (E) at each age of follow-up from 4 years until age 18 years. Generalized estimating equation models were adjusted for maternal characteristics (i.e. parity history, pre-pregnancy BMI, education, socioeconomic status, smoking, and age at pregnancy), and child’s follow up visit. Body fat % model was additionally adjusted by sex. Upper values represent the p-values of the age at follow-up interaction term.

References

    1. Agay-Shay K., Martinez D., Valvi D., Garcia-Esteban R., Basagaña X., Robinson O., Casas M., Sunyer J., Vrijheid M. Exposure to Endocrine-Disrupting Chemicals during Pregnancy and Weight at 7 Years of Age: A Multi-pollutant Approach. Environ. Health Perspect. 2015;123(10):1030–1037. doi: 10.1289/ehp.1409049.
    1. Arrebola J.P., Fernández M.F., Martin-Olmedo P., Bonde J.P., Martín-Rodriguez J.L., Expósito J., Rubio-Domínguez A., Olea N. Historical exposure to persistent organic pollutants and risk of incident hypertension. Environ. Res. 2015;138:217–223. doi: 10.1016/j.envres.2015.02.018.
    1. Ashwell, M., Gunn, P., Gibson, S., 2012. Waist-to-height ratio is a better screening tool than waist circumference and BMI for adult cardiometabolic risk factors: systematic review and meta-analysis: Waist-to-height ratio as a screening tool. Obes. Rev. 13, 275–286. .
    1. Atabek, M.E., Pirgon, O., 2007. Assessment of Insulin Sensitivity from Measurements in Fasting State and During an Oral Glucose Tolerance Test in Obese Children. J. Pediatr. Endocrinol. Metab. 20. .
    1. Baccarelli A., Pfeiffer R., Consonni D., Pesatori A.C., Bonzini M., Patterson D.G., Jr., Bertazzi P.A., Landi M.T. Handling of dioxin measurement data in the presence of non-detectable values: Overview of available methods and their application in the Seveso chloracne study. Chemosphere. 2005;60(7):898–906. doi: 10.1016/j.chemosphere.2005.01.055.
    1. Boll* M., Weber L.W.D., Messner B., Stampfl A. Polychlorinated biphenyls affect the activities of gluconeogenic and lipogenic enzymes in rat liver: is there an interference with regulatory hormone actions? Xenobiotica. 1998;28(5):479–492. doi: 10.1080/004982598239407.
    1. Bozkurt L., Göbl C.S., Hörmayer A.-T., Luger A., Pacini G., Kautzky-Willer A. The impact of preconceptional obesity on trajectories of maternal lipids during gestation. Sci. Rep. 2016;6(1) doi: 10.1038/srep29971.
    1. Cano-Sancho G., Salmon A.G., La Merrill M.A. Association between Exposure to p,p ′-DDT and Its Metabolite p,p ′-DDE with Obesity: Integrated Systematic Review and Meta-Analysis. Environ. Health Perspect. 2017;125(9):096002. doi: 10.1289/EHP527.
    1. Carrizo D., Grimalt J.O., Ribas-Fito N., Sunyer J., Torrent M. Physical-chemical and Maternal Determinants of the Accumulation of Organochlorine Compounds in Four-Year-Old Children. Environ. Sci. Technol. 2006;40(5):1420–1426. doi: 10.1021/es0518427.
    1. Carrizo D., Grimalt J.O., Ribas-Fito N., Torrent M., Sunyer J. In utero and post-natal accumulation of organochlorine compounds in children under different environmental conditions. J. Environ. Monit. 2007;9(6):523. doi: 10.1039/b700247e.
    1. Casas M., Nieuwenhuijsen M., Martínez D., Ballester F., Basagaña X., Basterrechea M., Chatzi L., Chevrier C., Eggesbø M., Fernandez M.F., Govarts E., Guxens M., Grimalt J.O., Hertz-Picciotto I., Iszatt N., Kasper-Sonnenberg M., Kiviranta H., Kogevinas M., Palkovicova L., Ranft U., Schoeters G., Patelarou E., Petersen M.S., Torrent M., Trnovec T., Valvi D., Toft G.V., Weihe P., Weisglas-Kuperus N., Wilhelm M., Wittsiepe J., Vrijheid M., Bonde J.P. Prenatal exposure to PCB-153, p,p′-DDE and birth outcomes in 9000 mother–child pairs: Exposure–response relationship and effect modifiers. Environ. Int. 2015;74:23–31. doi: 10.1016/j.envint.2014.09.013.
    1. Castilla R., Asuaje A., Rivière S., Romero C.G., Martín P., Cao G., Kleiman de Pisarev D., Milesi V., Alvarez L. Environmental pollutant hexachlorobenzene induces hypertension in a rat model. Chemosphere. 2018;195:576–584. doi: 10.1016/j.chemosphere.2017.11.117.
    1. Chen X., Wang Y. Tracking of Blood Pressure From Childhood to Adulthood: A Systematic Review and Meta–Regression Analysis. Circulation. 2008;117(25):3171–3180.
    1. Coker E., Chevrier J., Rauch S., Bradman A., Obida M., Crause M., Bornman R., Eskenazi B. Association between prenatal exposure to multiple insecticides and child body weight and body composition in the VHEMBE South African birth cohort. Environ. Int. 2018;113:122–132. doi: 10.1016/j.envint.2018.01.016.
    1. Cupul-Uicab L.A., Klebanoff M.A., Brock J.W., Longnecker M.P. Prenatal Exposure to Persistent Organochlorines and Childhood Obesity in the U.S. Collaborative Perinatal Project. Environ. Health Perspect. 2013;121(9):1103–1109.
    1. de Onis M., Garza C., Onyango A.W., Rolland-Cachera M.-F. Les standards de croissance de l’Organisation mondiale de la santé pour les nourrissons et les jeunes enfants. Archives de Pédiatrie. 2009;16(1):47–53. doi: 10.1016/j.arcped.2008.10.010.
    1. de Onis M., Onyango A.W., Borghi E., Siyam A., Nishida C., Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull. World Health Organ. 2007;85:660–667. doi: 10.2471/blt.07.043497.
    1. Delvaux I., Van Cauwenberghe J., Den Hond E., Schoeters G., Govarts E., Nelen V., Baeyens W., Van Larebeke N., Sioen I. Prenatal exposure to environmental contaminants and body composition at age 7–9 years. Environ. Res. 2014;132:24–32. doi: 10.1016/j.envres.2014.03.019.
    1. Donat-Vargas C., Åkesson A., Tornevi A., Wennberg M., Sommar J., Kiviranta H., Rantakokko P., Bergdahl I.A. Persistent Organochlorine Pollutants in Plasma, Blood Pressure, and Hypertension in a Longitudinal Study. Hypertension. 2018;71(6):1258–1268. doi: 10.1161/HYPERTENSIONAHA.117.10691.
    1. Eisenmann J.C. On the use of a continuous metabolic syndrome score in pediatric research. Cardiovasc Diabetol. 2008;7(1):17. doi: 10.1186/1475-2840-7-17.
    1. Franks P.W., Hanson R.L., Knowler W.C., Sievers M.L., Bennett P.H., Looker H.C. Childhood Obesity, Other Cardiovascular Risk Factors, and Premature Death. N. Engl. J. Med. 2010;362(6):485–493. doi: 10.1056/NEJMoa0904130.
    1. Gaillard R., Steegers E.A.P., Duijts L., Felix J.F., Hofman A., Franco O.H., Jaddoe V.W.V. Childhood Cardiometabolic Outcomes of Maternal Obesity During Pregnancy: The Generation R Study. Hypertension. 2014;63(4):683–691. doi: 10.1161/HYPERTENSIONAHA.113.02671.
    1. Garced S., Torres-Sánchez L., Cebrián M.E., Claudio L., López-Carrillo L. Prenatal dichlorodiphenyldichloroethylene (DDE) exposure and child growth during the first year of life. Environ. Res. 2012;113:58–62. doi: 10.1016/j.envres.2011.12.002.
    1. Goncharov A., Pavuk M., Foushee H.R., Carpenter D.O. Blood Pressure in Relation to Concentrations of PCB Congeners and Chlorinated Pesticides. Environ. Health Perspect. 2011;119(3):319–325.
    1. Grimalt J.O., Carrizo D., Garí M., Font-Ribera L., Ribas-Fito N., Torrent M., Sunyer J. An evaluation of the sexual differences in the accumulation of organochlorine compounds in children at birth and at the age of 4 years. Environ. Res. 2010;110(3):244–250. doi: 10.1016/j.envres.2010.01.005.
    1. Grün, F., Blumberg, B., 2006. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 147, S50-55. .
    1. Guxens, M., Ballester, F., Espada, M., Fernández, M.F., Grimalt, J.O., Ibarluzea, J., Olea, N., Rebagliato, M., Tardón, A., Torrent, M., Vioque, J., Vrijheid, M., Sunyer, J., 2012. Cohort Profile: The INMA—INfancia y Medio Ambiente—(Environment and Childhood) Project. Int. J. Epidemiol. 41, 930–940. .
    1. Hagmar, L., Wallin, E., Vessby, B., Jönsson, B.A., Bergman, A., Rylander, L., 2006. Intra-individual variations and time trends 1991-2001 in human serum levels of PCB, DDE and hexachlorobenzene. Chemosphere 64, 1507–1513. .
    1. Heggeseth, B., Harley, K., Warner, M., Jewell, N., Eskenazi, B., 2015. Detecting Associations between Early-Life DDT Exposures and Childhood Growth Patterns: A Novel Statistical Approach. PLOS ONE 10, e0131443. .
    1. Heindel, J.J., Balbus, J., Birnbaum, L., Brune-Drisse, M.N., Grandjean, P., Gray, K., Landrigan, P.J., Sly, P.D., Suk, W., Slechta, D.C., Thompson, C., Hanson, M., 2015a. Developmental Origins of Health and Disease: Integrating Environmental Influences. Endocrinology 156, 3416–3421. .
    1. Heindel, J.J., Blumberg, B., Cave, M., Machtinger, R., Mantovani, A., Mendez, M.A., Nadal, A., Palanza, P., Panzica, G., Sargis, R., Vandenberg, L.N., vom Saal, F., 2017. Metabolism disrupting chemicals and metabolic disorders. Reprod. Toxicol. 68, 3–33. .
    1. Heindel J.J., vom Saal F.S., Blumberg B., Bovolin P., Calamandrei G., Ceresini G., Cohn B.A., Fabbri E., Gioiosa L., Kassotis C., Legler J., La Merrill M., Rizzir L., Machtinger R., Mantovani A., Mendez M.A., Montanini L., Molteni L., Nagel S.C., Parmigiani S., Panzica G., Paterlini S., Pomatto V., Ruzzin J., Sartor G., Schug T.T., Street M.E., Suvorov A., Volpi R., Zoeller R.T., Palanza P. Parma consensus statement on metabolic disruptors. Environ Health. 2015;14(1) doi: 10.1186/s12940-015-0042-7.
    1. Horlick, M., Arpadi, S.M., Bethel, J., Wang, J., Moye, J., Cuff, P., Pierson, R.N., Kotler, D., 2002. Bioelectrical impedance analysis models for prediction of total body water and fat-free mass in healthy and HIV-infected children and adolescents. Am. J. Clin. Nutr. 76, 991–999. .
    1. Høyer B.B., Ramlau-Hansen C.H., Henriksen T.B., Pedersen H.S., Góralczyk K., Zviezdai V., Jönsson B.A.G., Heederik D., Lenters V., Vermeulen R., Bonde J.P., Toft G. Body mass index in young school-age children in relation to organochlorine compounds in early life: a prospective study. Int. J. Obes. 2014;38(7):919–925. doi: 10.1038/ijo.2014.58.
    1. Ibarluzea J., Alvarez-Pedrerol M., Guxens M., Marina L.S., Basterrechea M., Lertxundi A., Etxeandia A., Goñi F., Vioque J., Ballester F., Sunyer J. Sociodemographic, reproductive and dietary predictors of organochlorine compounds levels in pregnant women in Spain. Chemosphere. 2011;82(1):114–120. doi: 10.1016/j.chemosphere.2010.09.051.
    1. Iszatt N., Stigum H., Verner M.-A., White R.A., Govarts E., Murinova L.P., Schoeters G., Trnovec T., Legler J., Pelé F., Botton J., Chevrier C., Wittsiepe J., Ranft U., Vandentorren S., Kasper-Sonnenberg M., Klümper C., Weisglas-Kuperus N., Polder A., Eggesbø M. Prenatal and Postnatal Exposure to Persistent Organic Pollutants and Infant Growth: A Pooled Analysis of Seven European Birth Cohorts. Environ. Health Perspect. 2015;123(7):730–736. doi: 10.1289/ehp.1308005.
    1. Juhola J., Magnussen C.G., Viikari J.S.A., Kähönen M., Hutri-Kähönen N., Jula A., Lehtimäki T., Åkerblom H.K., Pietikäinen M., Laitinen T., Jokinen E., Taittonen L., Raitakari O.T., Juonala M. Tracking of Serum Lipid Levels, Blood Pressure, and Body Mass Index from Childhood to Adulthood: The Cardiovascular Risk in Young Finns Study. J. Pediatrics. 2011;159(4):584–590. doi: 10.1016/j.jpeds.2011.03.021.
    1. Juonala M., Magnussen C.G., Berenson G.S., Venn A., Burns T.L., Sabin M.A., Srinivasan S.R., Daniels S.R., Davis P.H., Chen W., Sun C., Cheung M., Viikari J.S.A., Dwyer T., Raitakari O.T. Childhood Adiposity, Adult Adiposity, and Cardiovascular Risk Factors. N. Engl. J. Med. 2011;365(20):1876–1885. doi: 10.1056/NEJMoa1010112.
    1. Karlsen M., Grandjean P., Weihe P., Steuerwald U., Oulhote Y., Valvi D. Early-life exposures to persistent organic pollutants in relation to overweight in preschool children. Reprod. Toxicol. 2017;68:145–153. doi: 10.1016/j.reprotox.2016.08.002.
    1. Keskin M., Kurtoglu S., Kendirci M., Atabek M.E., Yazici C. Homeostasis Model Assessment Is More Reliable Than the Fasting Glucose/Insulin Ratio and Quantitative Insulin Sensitivity Check Index for Assessing Insulin Resistance Among Obese Children and Adolescents. Pediatrics. 2005;115(4):e500–e503.
    1. Kim J.H. Multicollinearity and misleading statistical results. Korean J Anesthesiol. 2019;72(6):558–569.
    1. Kim M.-J., Marchand P., Henegar C., Antignac J.-P., Alili R., Poitou C., Bouillot J.-L., Basdevant A., Le Bizec B., Barouki R., Clément K. Fate and Complex Pathogenic Effects of Dioxins and Polychlorinated Biphenyls in Obese Subjects before and after Drastic Weight Loss. Environ. Health Perspect. 2011;119(3):377–383.
    1. La Merrill, M., Karey, E., Moshier, E., Lindtner, C., La Frano, M.R., Newman, J.W., Buettner, C., 2014. Perinatal Exposure of Mice to the Pesticide DDT Impairs Energy Expenditure and Metabolism in Adult Female Offspring. PLoS ONE 9, e103337. .
    1. La Merrill M.A., Sethi S., Benard L., Moshier E., Haraldsson B., Buettner C. Perinatal DDT Exposure Induces Hypertension and Cardiac Hypertrophy in Adult Mice. Environ. Health Perspect. 2016;124(11):1722–1727.
    1. Lauritzen H.B., Larose T.L., Øien T., Sandanger T.M., Odland J.Ø., van de Bor M., Jacobsen G.W. Prenatal exposure to persistent organic pollutants and child overweight/obesity at 5-year follow-up: a prospective cohort study. Environ Health. 2018;17(1) doi: 10.1186/s12940-017-0338-x.
    1. Lee, H., Park, S., Hong, Y., Ha, E., Park, H., 2016. 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, 270. .
    1. Lee H.K. Mitochondrial Dysfunction and Insulin Resistance: The Contribution of Dioxin-Like Substances. Diabetes Metab. J. 2011;35(3):207. doi: 10.4093/dmj.2011.35.3.207.
    1. Li J., Li N., Ma M., Giesy J., Wang Z. In vitro profiling of the endocrine disrupting potency of organochlorine pesticides. Toxicol. Lett. 2008 doi: 10.1016/j.toxlet.2008.10.002.
    1. Lim J.-E., Lee S., Lee S., Jee S.H. Serum persistent organic pollutants levels and stroke risk. Environ. Pollut. 2018;233:855–861.
    1. Lind P.M., Penell J., Salihovic S., van Bavel B., Lind L. Circulating levels of p,p'-DDE are related to prevalent hypertension in the elderly. Environ. Res. 2014;129:27–31.
    1. Little, R.J.A., Rubin, D.B., 2014. Statistical analysis with missing data.
    1. Ludwig‐Walz, H., Schmidt, M., Günther, A.L.B., Kroke, A., 2018. Maternal prepregnancy BMI or weight and offspring’s blood pressure: Systematic review. Matern. Child. Nutr. 14. .
    1. Mauvais-Jarvis, F., Clegg, D.J., Hevener, A.L., 2013. The Role of Estrogens in Control of Energy Balance and Glucose Homeostasis. Endocr. Rev. 34, 309–338. .
    1. Mendez M.A., Garcia-Esteban R., Guxens M., Vrijheid M., Kogevinas M., Goñi F., Fochs S., Sunyer J. Prenatal Organochlorine Compound Exposure, Rapid Weight Gain, and Overweight in Infancy. Environ. Health Perspect. 2011;119(2):272–278.
    1. 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. 2009;117(3):417–425.
    1. NCD Risk Factor Collaboration (NCD-RisC), 2020. Repositioning of the global epicentre of non-optimal cholesterol. Nature 582, 73–77. .
    1. NCD Risk Factor Collaboration (NCD-RisC), 2017a. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet Lond. Engl. 390, 2627–2642. .
    1. NCD Risk Factor Collaboration (NCD-RisC), 2017b. Worldwide trends in blood pressure from 1975 to 2015: a pooled analysis of 1479 population-based measurement studies with 19·1 million participants. Lancet Lond. Engl. 389, 37–55. .
    1. NCD Risk Factor Collaboration (NCD-RisC), 2016. Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4.4 million participants. Lancet Lond. Engl. 387, 1513–1530. .
    1. Ong Ken K.L., Preece Michael A., Emmett Pauline M., Ahmed Marion L., Dunger David B. Size at Birth and Early Childhood Growth in Relation to Maternal Smoking, Parity and Infant Breast-Feeding: Longitudinal Birth Cohort Study and Analysis. Pediatr. Res. 2002;52(6):863–867.
    1. Park Su Hyun, Lim Jung-eun, Park Hyesook, Jee Sun Ha. Body burden of persistent organic pollutants on hypertension: a meta-analysis. Environ. Sci. Pollut. Res. 2016;23(14):14284–14293.
    1. Porta Miquel, Puigdomènech Elisa, Ballester Ferran, Selva Javier, Ribas-Fitó Núria, Llop Sabrina, López Tomàs. Monitoring concentrations of persistent organic pollutants in the general population: The international experience. Environ. Int. 2008;34(4):546–561.
    1. Roland, M.C.P., Lekva, T., Godang, K., Bollerslev, J., Henriksen, T., 2020. Changes in maternal blood glucose and lipid concentrations during pregnancy differ by maternal body mass index and are related to birthweight: A prospective, longitudinal study of healthy pregnancies. PLOS ONE 15, e0232749. .
    1. Royston Patrick. Multiple Imputation of Missing Values: Update of Ice. Stata J. 2005;5(4):527–536.
    1. Ruiz, L.D., Zuelch, M.L., Dimitratos, S.M., Scherr, R.E., 2019. Adolescent Obesity: Diet Quality, Psychosocial Health, and Cardiometabolic Risk Factors. Nutrients 12, 43. .
    1. Ruzzin Jérôme, Petersen Rasmus, Meugnier Emmanuelle, Madsen Lise, Lock Erik-Jan, Lillefosse Haldis, Ma Tao, Pesenti Sandra, Sonne Si Brask, Marstrand Troels Torben, Malde Marian Kjellevold, Du Zhen-Yu, Chavey Carine, Fajas Lluis, Lundebye Anne-Katrine, Brand Christian Lehn, Vidal Hubert, Kristiansen Karsten, Frøyland Livar. Persistent Organic Pollutant Exposure Leads to Insulin Resistance Syndrome. Environ. Health Perspect. 2010;118(4):465–471.
    1. Savitri Ary I, Zuithoff Peter, Browne Joyce L, Amelia Dwirani, Baharuddin Mohammad, Grobbee Diederick E, Uiterwaal Cuno S P M. Does pre-pregnancy BMI determine blood pressure during pregnancy? A prospective cohort study. BMJ Open. 2016;6(8):e011626. doi: 10.1136/bmjopen-2016-011626.
    1. Shrier Ian, Platt Robert W. Reducing bias through directed acyclic graphs. BMC Med. Res. Method. 2008;8(1) doi: 10.1186/1471-2288-8-70.
    1. Sjöberg Lind, Y., Lind, L., Salihovic, S., van Bavel, B., Lind, P.M., 2013. Persistent organic pollutants and abnormal geometry of the left ventricle in the elderly: J. Hypertens. 31, 1547–1553. .
    1. Smink, A., Ribas-Fito, N., Garcia, R., Torrent, M., Mendez, M.A., Grimalt, J.O., Sunyer, J., 2008. Exposure to hexachlorobenzene during pregnancy increases the risk of overweight in children aged 6 years. Acta Paediatr. 97, 1465–1469. .
    1. Spratt M., Carpenter J., Sterne J.A.C., Carlin J.B., Heron J., Henderson J., Tilling K. Strategies for Multiple Imputation in Longitudinal Studies. Am. J. Epidemiol. 2010;172(4):478–487.
    1. Sterne J.A.C., White I.R., Carlin J.B., Spratt M., Royston P., Kenward M.G., Wood A.M., Carpenter J.R. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ. 2009;338 b2393-b2393.
    1. Tang-Péronard, J.L., Heitmann, B.L., Andersen, H.R., Steuerwald, U., Grandjean, P., Weihe, P., Jensen, T.K., 2014. Association between prenatal polychlorinateSd biphenyl exposure and obesity development at ages 5 and 7 y: a prospective cohort study of 656 children from the Faroe Islands. Am. J. Clin. Nutr. 99, 5–13. .
    1. Tang-Péronard Jeanett L., Heitmann Berit L., Jensen Tina K., Vinggaard Anne M., Madsbad Sten, Steuerwald Ulrike, Grandjean Philippe, Weihe Pál, Nielsen Flemming, Andersen Helle R. Prenatal exposure to persistent organochlorine pollutants is associated with high insulin levels in 5-year-old girls. Environ. Res. 2015;142:407–413.
    1. Vafeiadi Marina, Georgiou Vaggelis, Chalkiadaki Georgia, Rantakokko Panu, Kiviranta Hannu, Karachaliou Marianna, Fthenou Eleni, Venihaki Maria, Sarri Katerina, Vassilaki Maria, Kyrtopoulos Soterios A., Oken Emily, Kogevinas Manolis, Chatzi Leda. Association of Prenatal Exposure to Persistent Organic Pollutants with Obesity and Cardiometabolic Traits in Early Childhood: The Rhea Mother–Child Cohort (Crete, Greece) Environ. Health Perspect. 2015;123(10):1015–1021.
    1. Valera Beatriz, Jørgensen Marit E., Jeppesen Charlotte, Bjerregaard Peter. Exposure to persistent organic pollutants and risk of hypertension among Inuit from Greenland. Environ. Res. 2013;122:65–73.
    1. Valvi Damaskini, Mendez Michelle Ann, Garcia-Esteban Raquel, Ballester Ferran, Ibarluzea Jesús, Goñi Fernando, Grimalt Joan O., Llop Sabrina, Marina Loreto Santa, Vizcaino Esther, Sunyer Jordi, Vrijheid Martine. Prenatal exposure to persistent organic pollutants and rapid weight gain and overweight in infancy: Prenatal POPs and Early Postnatal Growth. Obesity. 2014;22(2):488–496.
    1. Valvi Damaskini, Mendez Michelle A., Martinez David, Grimalt Joan O., Torrent Maties, Sunyer Jordi, Vrijheid Martine. Prenatal Concentrations of Polychlorinated Biphenyls, DDE, and DDT and Overweight in Children: A Prospective Birth Cohort Study. Environ. Health Perspect. 2012;120(3):451–457.
    1. VanderWeele, T.J., 2009. On the relative nature of overadjustment and unnecessary adjustment. Epidemiol. Camb. Mass 20, 496–499. .
    1. Verhulst Stijn L., Nelen Vera, Hond Elly Den, Koppen Gudrun, Beunckens Caroline, Vael Carl, Schoeters Greet, Desager Kristine. Intrauterine Exposure to Environmental Pollutants and Body Mass Index during the First 3 Years of Life. Environ. Health Perspect. 2009;117(1):122–126.
    1. Warner, M., Wesselink, A., Harley, K.G., Bradman, A., Kogut, K., Eskenazi, B., 2014. Prenatal Exposure to Dichlorodiphenyltrichloroethane and Obesity at 9 Years of Age in the CHAMACOS Study Cohort. Am. J. Epidemiol. 179, 1312–1322. .
    1. Warner Marcella, Ye Morgan, Harley Kim, Kogut Katherine, Bradman Asa, Eskenazi Brenda. Prenatal DDT exposure and child adiposity at age 12: The CHAMACOS study. Environ. Res. 2017;159:606–612.
    1. Wright, C.M., Emmett, P.M., Ness, A.R., Reilly, J.J., Sherriff, A., 2010. Tracking of obesity and body fatness through mid-childhood. Arch. Dis. Child. 95, 612–617. .

Source: PubMed

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