Abstract
The purpose of this study was to investigate the longitudinal effects of perinatal exposure to dioxin on physical growth in a 3-year follow-up study. In 2015, 27 mother–infant pairs living in an electronic waste (e-waste) dismantling region and 35 pairs living in a control region were enrolled in the present study. Breast milk samples were collected at 4 weeks after birth. Physical growth, including weight, height, and head and chest circumferences, was measured at 6 months and 3 years of age. Dioxin levels in the breast milk were measured by gas chromatography/high-resolution mass spectrometry. Levels of 2,3,7,8-tetrachlorodibenzo-p-dioxin and toxic equivalency values in maternal breast milk of polychlorinated dibenzodioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and PCDDs/PCDFs were significantly higher in women residing in the e-waste dismantling region. In 3-year-old boys, inverse associations were found between height and PCDDs-TEQ. In girls, positive associations were found between height and 2,3,7,8-TetraCDD, PCDDs-TEQ, and PCDDs/PCDFs-TEQ, and for weight and PCDDs-TEQ and PCDDs/PCDFs-TEQ at 3 years of age. In this study, sex-specific differences were observed in children, in whom dioxin exposure decreased growth in boys but increased growth in girls during the first 3 years of life.
Similar content being viewed by others
Abbreviations
- E-waste:
-
Electronic waste
- PCDDs:
-
Polychlorinated dibenzo-p-dioxins
- PCDFs:
-
Polychlorinated dibenzofurans
- PBDEs:
-
Polybrominated diphenyl ethers
- PCBs:
-
Polychlorinated biphenyls
- 2,3,7,8-TetraCDD:
-
2,3,7,8-Tetrachlorodibenzo-p-dioxin
- BMI:
-
Body mass index
- TEQ:
-
Toxic equivalency
- LOD:
-
Limit of detection
References
Burns JS, Williams PL, Sergeyev O, Korrick S, Lee MM, Revich B, Altshul L, del Prato JT, Humblet O, Patterson DG, Turner WE, Needham LL, Starovoytov M, Hauser R (2011) Serum dioxins and polychlorinated biphenyls are associated with growth among Russian boys. Pediatrics 127:e59–e68. https://doi.org/10.1542/peds.2009-3556
Chan JKY, Wong MH (2013) A review of environmental fate, body burdens, and human health risk assessment of PCDD/Fs at two typical electronic waste recycling sites in China. Sci Total Environ 463-464:1111–1123
Chao HR, Wang SL, Lee CC, Yu HY, Lu YK, Päpke O (2004) Level of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs) in human milk and the input to infant body burden. Food Chem Toxicol 42:1299–1308
Chen A, Dietrich KN, Xia H, Ho SM (2011) Developmental neurotoxicants in e-waste: an emerging health concern. Environ Health Perspect 119:431–438
Eskenazi B, Mocarelli P, Warner M, Chee WY, Gerthoux PM, Samuels S, Needham LL, Patterson DG Jr (2003) Maternal serum dioxin levels and birth outcomes in women of Seveso, Italy. Environ Health Perspect 111:947–953
Gladen BC, Ragan NB, Rogan WJ (2000) Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. J Pediatr 136:490–496
Grandjean P, Bjerve KS, Weihe P, Steuerwald U (2001) Birth weight in a fishing community: significance of essential fatty acids and marine food contaminants. Int J Epidemiol 30:1272–1278
Hertz-Picciotto I, Charles MJ, James RA, Keller JA, Willman E, Teplin S (2005) In utero polychlorinated biphenyls exposures in relation to fetal and early childhood growth. Epidemiology 16:648–656
Iszatt N, Stigum H, Govarts E, Murinova LP, Schoeters G, Trnovec T, Legler J, Thomsen C, Koppen G, Eggesbø M (2016) Perinatal exposure to dioxins and dioxin-like compounds and infant growth and body mass index at seven years: a pooled analysis of three European birth cohorts. Environ Int 94:399–407
Karmaus W, Zhu X (2004) Maternal concentration of polychlorinated biphenyls and dichlorodiphenyl dichloethylene and birth weight in Michigan fish eaters: a cohort study. Environ Health 3(1). https://doi.org/10.1186/1476-o69X-3-1
Konishi K, Sasaki S, Kato S, Ban S, Washino N, Kajiwara J, Todaka T, Hirakawa H, Hori T, Yasutake D, Kishi R (2009) Prenatal exposure to PCDDs/PCDFs and dioxin-like PCBs in relation to birth weight. Environ Res 109:906–913
Longnecker MP, Klebanoff MA, Brock JW, Guo X (2005) Maternal levels of polychlorinated biphenyls in relation to preterm and small-forgestation-age birth. Epidemiology 16:641–647
Manh HD, Kido T, Tai PT, Okamoto R, Honma S, Liang SX, Anh LT, Maruzeni S, Nghi TN, Nishijo M, Nakagawa H, Nhu DD, van Tung D, Hung NN, Son LK (2015) Levels of polychlorinated dibenzodioxins and polychlorinated dibenzofurans in breast milk samples from three dioxin-contaminated hotspots of Vietnam. Sci Total Environ 511:416–422
Nishijo M, Tawara K, Nakagawa H, Honda R, Kido T, Nishijo H, Saito S (2008) 2,3,7,8-Tetrachlorodibenzo-p-dioxin in maternal breast milk and newborn head circumference. J Expo Sci Environ Epidemiol 18:246–251
Nishijo M, Nakagawa H, Maruzeni S et al (2012) Impact of perinatal dioxin exposure on infant growth: a cross-sectional and longitudinal studies in dioxin-contaminated areas in Vietnam. PloS One 7:e40273. https://doi.org/10.1371/journal.pone.0040273
Papadopoulou E, Caspersen IH, Kvalem HE, Knutsen HK, Duarte-Salles T, Alexander J, Meltzer HM, Kogevinas M, Brantsæter AL, Haugen M (2013) Maternal dietary intake of dioxins and polychlorinated biphenyls and birth size in the Norwegian mother and child cohort study (MoBa). Environ Int 60:209–216
Patadin S, Koopman-Esseboom C, de Ridder MA, Weiglas-Kuperus N, Sauer PJ (1998) Effects of environmental exposure to polychlorinated biphenyls and dioxins on birth size and growth in Dutch children. Pediatr Res 44:538–545
Patandin S, Dagnelie PC, Mulder P et al (1999) Dietary exposure to polychlorinated biphenyls and dioxins from infancy until adulthood: a comparison between breast-feeding, toddler, and long-term exposure. Environ Health Perspect 107:45–51
Rashid CS, Carter LG, Hennig B, Pearson KJ (2013) Perinatal polychlorinated biphenyl 126 exposure alters offspring body composition. J Pediatr Biochem 3:47–53
Sagiv SK, Tolbert BE, Altshul LM, Korrick SA (2007) Organochlorine exposures during pregnancy and infant size at birth. Epidemiology 18:120–129
Schecter A, Päpke O, Ball M (1990) Evidence for transplacental transfer of dioxins from mother to fetus: chlorinated dioxin and dibenzofuran levels in the livers of stillborn infants. Chemosphere 21:1017–1022
Shen C, Chen Y, Huang S, Wang ZJ, Yu CN, Qiao M, Xu YP, Setty K, Zhang JY, Zhu YF, Lin Q (2009) Dioxin-like compounds in agricultural soils near e-waste recycling sites from Taizhou area, China: chemical and bioanalytical characterization. Environ Int 35:50–55
Shen H, Guan R, Ding G, Chen Q, Lou X, Chen Z, Zhang L, Xing M, Han J, Wu Y (2017) Polychlorinated dibenzo-p-dioxins/furans (PCDD/Fs) and polychlorinated biphenyls (PCBs) in Zhejiang foods (2006–2015): market basket and polluted areas. Sci Total Environ 574:120–127
Song Q, Li J (2015) A review on human health consequences of metals exposure to e-waste in China. Environ Pollut 196:450–461
Sonneborn D, Park HY, Petrik J, Kocan A, Palkovicova L, Trnovec T, Nguyen D, Hertz-Picciotto I (2008) Prenatal polychlorinated biphenyls exposures in eastern Slovakia modify effects of social factors on birthweight. Paediatr Perinat Epidemiol 22:202–213
Stellman JM, Stellman SD, Christian R, Weber T, Tomasallo C (2003) The extent and patterns of usage of Agent Orange and other herbicides in Vietnam. Nature 422:681–687
Tai PT, Nishijo M, Nghi TN, Nakagawa H, Luong HV, Anh TH, Nishijo H (2016) Effects of perinatal dioxin exposure on development of children during the first 3 years of life. J Pediatr 175:159–166
Tsukimori K, Uchi H, Mitoma C, Yasukawa F, Chiba T, Todaka T, Kajiwara J, Yoshimura T, Hirata T, Fukushima K, Wake N, Furue M (2012) Maternal exposure to high levels of dioxins in relation to birth weight in women affected by Yusho disease. Environ Int 38:79–86
Tsukimori K, Uchi H, Tokunaga S, Yasukawa F, Chiba T, Kajiwara J, Hirata T, Furue M (2013) Blood levels of PCDDs, PCDFs, and coplanar PCBs in Yusho mothers and their descendants: association with fetal Yusho disease. Chemosphere 90:1581–1588
UNEP (2005) DEWA/GRID-Europe (2005) E-waste, the hidden side of IT equipment’s manufacturing and use. Environment Alert Bulletin 5, UNEP: Nairobi, Kenya. http://www.grid.unep.ch/products/3_Reports/ew_ewaste.en.pdf. Accessed 9 May 2019
Van den Berg M, Birnbaum LS, Denison M et al (2006) The 2005 World Health Organization Reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93:223–241
van Esterik JCJ, Verharen HW, Hodemaekers HM, Gremmer ER, Nagarajah B, Kamstra JH, Dollé MET, Legler J, van der Ven LTM (2015) Compound-and sex-specific effects on programming of energy and immune homeostasis in adult C57BL/6JxFVB mice after perinatal TCDD and PCB 153. Toxicol Appl Pharmacol 289:262–275
Van Tung D, Kido T, Honma S et al (2016) Low birth weight of Vietnamese infants is related to their mother’s dioxin and glucocorticoid levels. Environ Sci Pollut Res Int 23:10922–10929
Verhulst S, Nelen V, Hond E et al (2009) Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life. Environ Health Perspect 117:122–126
Wang SL, Lin CY, Guo YL et al (2004) Infant exposure to polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs)––correlation between prenatal and postnatal exposure. Chemosphere 54:1459–1473
Weisskopf MG, Anderson HA, Hanrahan LP, Kanarek MS, Falk CM, Steenport DM, Draheim LA (2005) Maternal exposure to Great Lakes sport-caught fish and dichlorodiphenyl dichloroethylene, but not polychlorinated biphenyls, is associated with birth weight. Environ Res 97:149–162
WHO (2016) Updated June (2016) Dioxin and their effects on human health. http://www.who.int/mediacentre/factsheets/fs225/en/. Accessed 9 May 2019
Wohlfahrt-Veje C, Audouze K, Brunak S, Antignac JP, le Bizec B, Juul A, Skakkebæk NE, Main KM (2014) Polychlorinated dibenzo-p-dioxins, furans, and biphenyls (PCDDs/PCDFs and PCBs) in breast milk and early childhood growth and IGF1. Reproduction 147:391–399
Xiao X, Hu JF, Peng P, Chen DY, Bi XH (2016) Characterization of polybrominated dibenzo-p-dioxins and dibenzofurans (PBDDs/Fs) in environmental matrices from an intensive electronic waste recycling site, South China. Environ Pollut 212:464–471
Xu PW, Lou XM, Ding GA, Shen HT, Wu LZ, Chen ZJ, Han JL, Han GG, Wang XF (2014) Association of PCB, PBDE and PCDD/F body burdens with hormone levels for children in an e-waste dismantling area of Zhejiang Province, China. Sci Total Environ 499:55–61
Zhang JQ, Jiang YH, Zhou J, Wu B, Liang J, Peng ZQ, Fang DK, Liu B, Huang HY, He C, Wang CL, Lu FN (2010) Elevated body burdens of PBDEs, dioxin, and PCBs on thyroid hormone homeostasis at an electronic waste recycling site in China. Environ Sci Technol 44:3956–3962
Zhu BT, Gallo MA, Burger CW Jr, Meeker RJ, Cai MX, Xu S, Conney AH (2008) Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin administration and high-fat diet on the body weight and hepatic estrogen metabolism in female C3H/HeN mice. Toxicol Appl Pharmacol 226:107–118
Funding
The study was supported by the Zhejiang Province Public Welfare Technology Application Research Project (CN) no. LGF18H260008.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Written informed consent was obtained from all of the mothers. The study design was approved by the institutional ethics board for epidemiologic studies at Jiaxing University.
Competing interests
The authors declare that they have no competing interests.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, Z., Hang, J.G., Feng, H. et al. Effects of perinatal dioxin exposure on development of children: a 3-year follow-up study of China cohort. Environ Sci Pollut Res 26, 20780–20786 (2019). https://doi.org/10.1007/s11356-019-05362-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05362-0