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Prenatal phthalate exposure and 8-isoprostane among Mexican-American children with high prevalence of obesity

Published online by Cambridge University Press:  29 December 2016

V. Tran ,
G. Tindula ,
K. Huen ,
A. Bradman ,
K. Harley ,
K. Kogut ,
A. M. Calafat ,
B. Nguyen ,
K. Parra  and
X. Ye
...Show all authors
V. Tran
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
G. Tindula
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
K. Huen
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
A. Bradman
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
K. Harley
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
K. Kogut
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
A. M. Calafat
Affiliation:
Centers for Disease Control and Prevention, Atlanta, GA, USA
B. Nguyen
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
K. Parra
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
X. Ye
Affiliation:
Centers for Disease Control and Prevention, Atlanta, GA, USA
B. Eskenazi
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
N. Holland*
Affiliation:
School of Public Health, Center for Environmental Research and Children’s Health (CERCH), University of California, Berkeley, CA, USA
*
*Address for correspondence: N. Holland, PhD, 733 University Hall, School of Public Health, UC Berkeley, CA 94720-7360, USA.(Email ninah@berkeley.edu)
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Abstract

Oxidative stress has been linked to many obesity-related conditions among children including cardiovascular disease, diabetes mellitus and hypertension. Exposure to environmental chemicals such as phthalates, ubiquitously found in humans, may also generate reactive oxygen species and subsequent oxidative stress. We examined longitudinal changes of 8-isoprostane urinary concentrations, a validated biomarker of oxidative stress, and associations with maternal prenatal urinary concentrations of phthalate metabolites for 258 children at 5, 9 and 14 years of age participating in a birth cohort residing in an agricultural area in California. Phthalates are endocrine disruptors, and in utero exposure has been also linked to altered lipid metabolism, as well as adverse birth and neurodevelopmental outcomes. We found that median creatinine-corrected 8-isoprostane concentrations remained constant across all age groups and did not differ by sex. Total cholesterol, systolic and diastolic blood pressure were positively associated with 8-isoprostane in 14-year-old children. No associations were observed between 8-isoprostane and body mass index (BMI), BMI Z-score or waist circumference at any age. Concentrations of three metabolites of high molecular weight phthalates measured at 13 weeks of gestation (monobenzyl, monocarboxyoctyl and monocarboxynonyl phthalates) were negatively associated with 8-isoprostane concentrations among 9-year olds. However, at 14 years of age, isoprostane concentrations were positively associated with two other metabolites (mono(2-ethylhexyl) and mono(2-ethyl-5-carboxypentyl) phthalates) measured in early pregnancy. Longitudinal data on 8-isoprostane in this pediatric population with a high prevalence of obesity provides new insight on certain potential cardiometabolic risks of prenatal exposure to phthalates.

Keywords

8-isoprostaneobesityoxidative stressphthalatespregnancy
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 2 , April 2017 , pp. 196 - 205
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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References

1. Montuschi, P, Barnes, PJ, Roberts, LJ II. Isoprostanes: markers and mediators of oxidative stress. FASEB J. 2004; 18, 1791–1800.Google Scholar
2. Holland, N, Huen, K, Tran, V, et al. Urinary phthalate metabolites and biomarkers of oxidative stress in a Mexican-American cohort: variability in early and late pregnancy. Toxics. 2016; 4, 7.Google Scholar
3. Ferguson, KK, McElrath, TF, Mukherjee, B, Loch-Caruso, R, Meeker, JD. Associations between maternal biomarkers of phthalate exposure and inflammation using repeated measurements across pregnancy. PLoS One. 2015; 10, e0135601.CrossRefGoogle ScholarPubMed
4. Ferguson, KK, Loch-Caruso, R, Meeker, JD. Urinary phthalate metabolites in relation to biomarkers of inflammation and oxidative stress: NHANES 1999–2006. Environ Res. 2011; 111, 718–726.CrossRefGoogle Scholar
5. Hong, YC, Park, EY, Park, MS, et al. Community level exposure to chemicals and oxidative stress in adult population. Toxicol Lett. 2009; 184, 139–144.CrossRefGoogle ScholarPubMed
6. Kaviarasan, S, Muniandy, S, Qvist, R, Ismail, IS. F(2)-isoprostanes as novel biomarkers for type 2 diabetes: a review. J Clin Biochem Nutr. 2009; 45, 1–8.Google Scholar
7. Basu, S. Metabolism of 8-iso-prostaglandin F2alpha. FEBS Lett. 1998; 428, 32–36.Google Scholar
8. Wu, X, Cai, H, Xiang, YB, et al. Intra-person variation of urinary biomarkers of oxidative stress and inflammation. Cancer Epidemiol Biomarkers Prev. 2010; 19, 947–952.Google Scholar
9. Morrow, JD, Roberts, LJ. The isoprostanes: unique bioactive products of lipid peroxidation. Prog Lipid Res. 1997; 36, 1–21.CrossRefGoogle ScholarPubMed
10. Milne, GL, Dai, Q, Roberts, LJ 2nd. The isoprostanes – 25 years later. Biochim Biophys Acta. 2015; 1851, 433–445.Google Scholar
11. Block, G, Jensen, CD, Dalvi, TB, et al. Vitamin C treatment reduces elevated C-reactive protein. Free Radic Biol Med. 2009; 46, 70–77.CrossRefGoogle ScholarPubMed
12. Rossner, P Jr, Rossnerova, A, Spatova, M, et al. Analysis of biomarkers in a Czech population exposed to heavy air pollution. Part II: chromosomal aberrations and oxidative stress. Mutagenesis. 2013; 28, 97–106.CrossRefGoogle Scholar
13. Morrow, JD. Quantification of isoprostanes as indices of oxidant stress and the risk of atherosclerosis in humans. Arterioscler Thromb Vasc Biol. 2005; 25, 279–286.CrossRefGoogle ScholarPubMed
14. Montuschi, P, Barnes, P, Roberts, LJ II. Insights into oxidative stress: the isoprostanes. Curr Med Chem. 2007; 14, 703–717.Google Scholar
15. Bloomer, RJ, Fisher-Wellman, KH. Systemic oxidative stress is increased to a greater degree in young, obese women following consumption of a high fat meal. Oxid Med Cell Longev. 2009; 2, 19–25.Google Scholar
16. Furukawa, S, Fujita, T, Shimabukuro, M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004; 114, 1752–1761.Google Scholar
17. Aroor, AR, DeMarco, VG. Oxidative stress and obesity: the chicken or the egg? Diabetes. 2014; 63, 2216–2218.Google Scholar
18. Warolin, J, Coenen, KR, Kantor, JL, et al. The relationship of oxidative stress, adiposity and metabolic risk factors in healthy Black and White American youth. Pediatr Obes. 2014; 9, 43–52.Google Scholar
19. Khadir, A, Tiss, A, Kavalakatt, S, et al. Gender-specific association of oxidative stress and inflammation with cardiovascular risk factors in Arab population. Mediators Inflamm. 2015; 2015, 512603.CrossRefGoogle ScholarPubMed
20. Il’yasova, D, Morrow, JD, Wagenknecht, LE. Urinary F2-isoprostanes are not associated with increased risk of type 2 diabetes. Obes Res. 2005; 13, 1638–1644.Google Scholar
21. Ostrow, V, Wu, S, Aguilar, A, et al. Association between oxidative stress and masked hypertension in a multi-ethnic population of obese children and adolescents. J Pediatr. 2011; 158, 628–633 e621.CrossRefGoogle Scholar
22. Araki, S, Dobashi, K, Yamamoto, Y, Asayama, K, Kusuhara, K. Increased plasma isoprostane is associated with visceral fat, high molecular weight adiponectin, and metabolic complications in obese children. Eur J Pediatr. 2010; 169, 965–970.Google Scholar
23. CDC. Fourth National Report on Human Exposure to Environmental Chemicals (ed. Centers for Disease Control and Prevention NCfEH), 2009; pp. 258–294. CDC: Atlanta, GA.Google Scholar
24. Guo, Y, Kannan, K. A survey of phthalates and parabens in personal care products from the United States and its implications for human exposure. Environ Sci Technol. 2013; 47, 14442–14449.Google Scholar
25. Braun, JM, Sathyanarayana, S, Hauser, R. Phthalate exposure and children’s health. Curr Opin Pediatr. 2013; 25, 247–254.CrossRefGoogle ScholarPubMed
26. Ferguson, KK, McElrath, TF, Ko, YA, Mukherjee, B, Meeker, JD. Variability in urinary phthalate metabolite levels across pregnancy and sensitive windows of exposure for the risk of preterm birth. Environ Int. 2014; 70, 118–124.CrossRefGoogle ScholarPubMed
27. Ku, HY, Su, PH, Wen, HJ, et al. Prenatal and postnatal exposure to phthalate esters and asthma: a 9-year follow-up study of a taiwanese birth cohort. PLoS One. 2015; 10, e0123309.Google Scholar
28. Yaghjyan, L, Sites, S, Ruan, Y, Chang, SH. Associations of urinary phthalates with body mass index, waist circumference and serum lipids among females: National Health and Nutrition Examination Survey 1999–2004. Int J Obes (Lond). 2015; 39, 994–1000.Google Scholar
29. Zhang, Y, Meng, X, Chen, L, et al. Age and sex-specific relationships between phthalate exposures and obesity in Chinese children at puberty. PLoS One. 2014; 9, e104852.Google Scholar
30. Buser, MC, Murray, HE, Scinicariello, F. Age and sex differences in childhood and adulthood obesity association with phthalates: analyses of NHANES 2007–2010. Int J Hyg Environ Health. 2014; 217, 687–694.Google Scholar
31. Trasande, L, Attina, TM, Sathyanarayana, S, Spanier, AJ, Blustein, J. Race/ethnicity-specific associations of urinary phthalates with childhood body mass in a nationally representative sample. Environ Health Perspect. 2013; 121, 501–506.Google Scholar
32. Goodman, M, Lakind, JS, Mattison, DR. Do phthalates act as obesogens in humans? A systematic review of the epidemiological literature. Crit Rev Toxicol. 2014; 44, 151–175.Google Scholar
33. Hatch, EE, Nelson, JW, Qureshi, MM, et al. Association of urinary phthalate metabolite concentrations with body mass index and waist circumference: a cross-sectional study of NHANES data, 1999–2002. Environ Health. 2008; 7, 27.CrossRefGoogle ScholarPubMed
34. Buckley, JP, Engel, SM, Braun, JM, et al. Prenatal phthalate exposures and body mass index among 4- to 7-year-old children: a pooled analysis. Epidemiology. 2016; 27, 449–458.Google Scholar
35. Buckley, JP, Engel, SM, Mendez, MA, et al. Prenatal phthalate exposures and childhood fat mass in a New York City cohort. Environ Health Perspect. 2016; 124, 507–513.Google Scholar
36. Valvi, D, Casas, M, Romaguera, D, et al. Prenatal phthalate exposure and childhood growth and blood pressure: evidence from the Spanish INMA-Sabadell birth cohort study. Environ Health Perspect. 2015; 123, 1022–1029.CrossRefGoogle ScholarPubMed
37. Maresca, MM, Hoepner, LA, Hassoun, A, et al. Prenatal exposure to phthalates and childhood body size in an urban cohort. Environ Health Perspect. 2016; 124, 514–520.CrossRefGoogle Scholar
38. Agay-Shay, K, Martinez, D, Valvi, D, et al. Exposure to endocrine-disrupting chemicals during pregnancy and weight at 7 years of age: a multi-pollutant approach. Environ Health Perspect. 2015; 123, 1030–1037.Google Scholar
39. Ferguson, KK, Chen, YH, VanderWeele, TJ, et al. Mediation of the relationship between maternal phthalate exposure and preterm birth by oxidative stress with repeated measurements across pregnancy. Environ Health Perspect. 2016; doi:10.1289/EHP282.Google Scholar
40. Eskenazi, B, Bradman, A, Gladstone, E, et al. CHAMACOS, a longitudinal birth cohort study: lessons from the fields. J Childrens Healt. 2003; 1, 3–27.Google Scholar
41. Huen, K, Calafat, AM, Bradman, A, et al. Maternal phthalate exposure during pregnancy is associated with DNA methylation of LINE-1 and Alu repetitive elements in Mexican-American children. Environ Res. 2016; 148, 55–62.CrossRefGoogle ScholarPubMed
42. Silva, MJ, Samandar, E, Preau, JL, et al. Quantification of 22 phthalate metabolites in human urine. J Chromatogr B Analyt Technol Biomed Life Sci. 2007; 860, 106–112.Google Scholar
43. Lubin, JH, Colt, JS, Camann, D, et al. Epidemiologic evaluation of measurement data in the presence of detection limits. Environ Health Perspect. 2004; 112, 1691–1696.Google Scholar
44. Laird, NM, Ware, JH. Random-effects models for longitudinal data. Biometrics. 1982; 38, 963–974.Google Scholar
45. Ferguson, KK, McElrath, TF, Meeker, JD. Environmental phthalate exposure and preterm birth. JAMA Pediatr. 2014; 168, 61–67.Google Scholar
46. Comporti, M, Signorini, C, Leoncini, S, et al. Plasma F2-isoprostanes are elevated in newborns and inversely correlated to gestational age. Free Radic Biol Med. 2004; 37, 724–732.CrossRefGoogle ScholarPubMed
47. Kauffman, LD, Sokol, RJ, Jones, RH, et al. Urinary F2-isoprostanes in young healthy children at risk for type 1 diabetes mellitus. Free Radic Biol Med. 2003; 35, 551–557.Google Scholar
48. Dennis, BA, Ergul, A, Gower, BA, Allison, JD, Davis, CL. Oxidative stress and cardiovascular risk in overweight children in an exercise intervention program. Child Obes. 2013; 9, 15–21.Google Scholar
49. Weyer, C, Pratley, RE, Salbe, AD, et al. Energy expenditure, fat oxidation, and body weight regulation: a study of metabolic adaptation to long-term weight change. J Clin Endocrinol Metab. 2000; 85, 1087–1094.Google Scholar
50. Schutz, Y, Tremblay, A, Weinsier, RL, Nelson, KM. Role of fat oxidation in the long-term stabilization of body weight in obese women. Am J Clin Nutr. 1992; 55, 670–674.Google Scholar
51. Tremblay, A, Doucet, E. Obesity: a disease or a biological adaptation? Obes Rev. 2000; 1, 27–35.Google Scholar
52. Rosenbaum, M, Leibel, RL, Hirsch, J. Obesity. N Engl J Med. 1997; 337, 396–407.Google Scholar
53. Leibel, RL, Rosenbaum, M, Hirsch, J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995; 332, 621–628.Google Scholar
54. Otani, H. Oxidative stress as pathogenesis of cardiovascular risk associated with metabolic syndrome. Antioxid Redox Sign. 2011; 15, 1911–1926.Google Scholar
55. Touyz, RM. Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance? Hypertension. 2004; 44, 248–252.Google Scholar
56. Atabek, ME, Vatansev, H, Erkul, I. Oxidative stress in childhood obesity. J Pediatr Endocrinol Metab. 2004; 17, 1063–1068.Google Scholar
57. Fisher, MM, Eugster, EA. What is in our environment that effects puberty? Reprod Toxicol. 2014; 44, 7–14.Google Scholar
58. Herman-Giddens, ME. Recent data on pubertal milestones in United States children: the secular trend toward earlier development. Int J Androl. 2006; 29, 241–246, discussion 286–290.Google Scholar
59. Herman-Giddens, ME, Wang, L, Koch, G. Secondary sexual characteristics in boys: estimates from the national health and nutrition examination survey III, 1988–1994. Arch Pediatr Adolesc Med. 2001; 155, 1022–1028.Google Scholar
60. Eskenazi, B, Rauch, SA, Tenerelli, R, et al. In utero and childhood DDT, DDE, PBDE, and PCBs exposure and sex hormones in adolescent boys: the CHAMACOS study. Int J Hyg Environ Health (in press). doi:10.1016/j.ijheh.2016.11.001.Google Scholar
61. Kogawa, T, Nishimura, M, Kurauchi, S, Kashiwakura, I. Characteristics of reactive oxygen metabolites in serum of early teenagers in Japan. Environ Health Prev Med. 2012; 17, 364–370.Google Scholar
62. Desvergne, B, Feige, JN, Casals-Casas, C. PPAR-mediated activity of phthalates: a link to the obesity epidemic? Mol Cell Endocrinol. 2009; 304, 43–48.Google Scholar
63. Block, G, Dietrich, M, Norkus, EP, et al. Factors associated with oxidative stress in human populations. Am J Epidemiol. 2002; 156, 274–285.Google Scholar
64. Lammi, N, Moltchanova, E, Blomstedt, PA, et al. Childhood BMI trajectories and the risk of developing young adult-onset diabetes. Diabetologia. 2009; 52, 408–414.Google Scholar
65. Jepsen, KF, Abildtrup, A, Larsen, ST. Monophthalates promote IL-6 and IL-8 production in the human epithelial cell line A549. Toxicol In Vitro. 2004; 18, 265–269.Google Scholar
66. Ogden, CL, Carroll, MD, Kit, BK, Flegal, KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014; 311, 806–814.Google Scholar
67. Cantonwine, DE, Cordero, JF, Rivera-Gonzalez, LO, et al. Urinary phthalate metabolite concentrations among pregnant women in Northern Puerto Rico: distribution, temporal variability, and predictors. Environ Int. 2014; 62, 1–11.Google Scholar
68. Braun, JM, Smith, KW, Williams, PL, et al. Variability of urinary phthalate metabolite and bisphenol A concentrations before and during pregnancy. Environ Health Perspect. 2012; 120, 739–745.Google Scholar
69. Adibi, JJ, Whyatt, RM, Williams, PL, et al. Characterization of phthalate exposure among pregnant women assessed by repeat air and urine samples. Environ Health Perspect. 2008; 116, 467–473.Google Scholar
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