Abstract
Evidence concerning associations between exposure to per- and polyfluoroalkyl substances (PFASs) and preterm birth is limited. We evaluated the associations of preterm birth with gestational exposures to PFAS isomers, PFAS alternatives, and legacy PFASs using a nested case–control study (384 preterm vs. 384 term births) in a northwestern China Uyghur population. Levels of 23 PFASs were determined in cord serum samples. We estimated odds ratios (ORs) and mean differences (βs) for associations between preterm birth and gestational age with an interquartile range increase in each PFAS. Stratified analyses by maternal and infant characteristics were also performed. Although PFAS concentrations were low (median, < 0.455 ng/mL), several were significantly associated with preterm birth [OR for total perfluorooctane sulfonic acid (PFOS), linear PFOS, and branched PFOS were 1.44 (95% CI 1.18, 1.79), 1.41 (95% CI 1.19, 1.73), and 1.11 (95% CI 1.01, 1.29), respectively] and gestational age at delivery [β for perfluoro-n-dodecanoic acid, total PFOS, linear PFOS, ∑2 m-PFOS, and sodium perfluoro-1-heptanesulfonate were − 3.43 (95% CI − 5.55, − 1.32), − 1.26 (95% CI − 2.46, − 0.05), − 1.80 (95% CI − 3.24, − 0.37), − 3.03 (95% CI − 4.45, − 1.60), and − 3.02 (95% CI − 4.93, − 1.11), respectively]. Additionally, the associations between several PFASs and gestational age were stronger among newborn girls, those born to mothers being older, of “other” ethnicity, having higher income, and without periconceptional folic acid intake, compared to their counterparts. In summary, our results suggest that gestational exposure to low-level PFASs, PFOS in particular, was associated with higher odds of preterm birth in a Uyghur population.
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The raw data supporting the conclusions will be made available by the corresponding author (Guang-Hui Dong) on reasonable request.
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References
Beesoon S, Webster GM, Shoeib M et al (2011) Isomer profiles of perfluorochemicals in matched maternal, cord, and house dust samples: manufacturing sources and transplacental transfer. Environ Health Perspect 119:1659–1664
Bell M, Yeung EH, Ma W et al (2018) Concentrations of endocrine disrupting chemicals in newborn blood spots and infant outcomes in the upstate KIDS study. Environ Int 121:232–239
Benskin JP, Bataineh M, Martin JW et al (2007) Simultaneous characterization of perfluoroalkyl carboxylate, sulfonate, and sulfonamide isomers by liquid chromatography-tandem mass spectrometry. Anal Chem 79:6455–6464
Blencowe H, Cousens S, Oestergaard MZ et al (2012) National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379:2162–2172
Blum A, Balan SA, Scheringer M et al (2015) The madrid statement on poly- and perfluoroalkyl substances (PFASs). Environ Health Perspect 123:A107–A111
Boas M, Feldt-Rasmussen U, Main KM et al (2012) Thyroid effects of endocrine disrupting chemicals. Mol Cell Endocrinol 355:240–248
Cai D, Li QQ, Chu C et al (2020) High trans-placental transfer of perfluoroalkyl substances alternatives in the matched maternal-cord blood serum: Evidence from a birth cohort study. Sci Total Environ 705:135885
Chu C, Zhou Y, Li QQ et al (2020) Are perfuorooctane sulfonate alternatives safer? New insights from a birth cohort study. Environ Int 135:105365
Coperchini F, Croce L, Ricci G et al (2020) Thyroid disrupting effects of old and new generation PFAS. Front Endocrinol (lausanne) 11:612320
Darrow LA, Stein CR, Steenland K et al (2013) Serum perfluorooctanoic acid and perfluorooctane sulfonate concentrations in relation to birth outcomes in the Mid-Ohio Valley, 2005–2010. Environ Health Perspect 121:1207–1213
Falandysz J, Taniyasu S, Gulkowska A et al (2006) Is fish a major source of fluorinated surfactants and repellents in humans living on the Baltic Coast? Environ Sci Technol 40:748–751
Fei C, MaLaughlin JK, Tarone RE et al (2007) Perfluorinated chemicals and fetal growth: a study within the Danish National Birth Cohort. Environ Health Perspect 115:1677–1682
Fisher M, Arbuckle TE, Wade M et al (2013) Do perfluoroalkyl substances affect metabolic function and plasma lipids? Analysis of the 2007–2009, Canadian Health Measures Survey (CHMS) Cycle 1. Environ Res 121:95–103
Forsthuber M, Kaiser AM, Granitzer S et al (2019) Albumin is the major carrier protein for PFOS, PFOA, PFHxS, PFNA and PFDA in human plasma. Environ Int 137:105324
Gardener H, Sun Q, Grandjean P (2021) PFAS concentration during pregnancy in relation to cardiometabolic health and birth outcomes. Environ Res 192:110287
GBD (2017) DALYs and HALE Collaborators (2018). Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392:1859–1922
Gockener B, Weber T, Rudel H et al (2021b) Human biomonitoring of per-polyfluoroalkyl substances in German blood plasma samples from 1982 to 2019. Environ Int 145:106123
Guo J, Zhang J, Zeng L et al (2021c) Umbilical cord serum perfluoroalkyl substance mixtures in relation to thyroid function of newborns: Findings from Sheyang Mini Birth Cohort Study. Chemosphere 273:129664
Hamm MP, Cherry NM, Chan E et al (2010) Maternal exposure to perfluorinated acids and fetal growth. J Expo Sci Environ Epidemiol 20:589–597
Hjermitslev MH, Long M, Wielsoe M et al (2020) Persistent organic pollutants in Greenlandic pregnant women and indices of foetal growth: The ACCEPT study. Sci Total Environ 698:134118
Hong J, Park KA, Kim YJ et al (2008) Association of antioxidant vitamins and oxidative stress levels in pregnancy with infant growth during the first year of life. Public Health Nutr 11:998–1005
Hornung RW, Reed LD (1990) Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 1:46–51
ITRC (Interstate Technology and Regulatory Council) (2020a) Naming conventions and physical and chemical properties of per- and polyfluoroalkyl substances (PFAS). [Fact sheet.] https://pfas-1.itrcweb.org/fact_sheets_page/PFAS_Fact_Sheet_Naming_Conventions_April2020.pdf Accessed 27 October 2021
ITRC (Interstate Technology and Regulatory Council) (2020b) History and use of per- and polyfluoroalkyl substances (PFAS). [Fact sheet.] https://pfas-1.itrcweb.org/fact_sheets_page/PFAS_Fact_Sheet_History_and_Use_April2020.pdf Accessed 27 September 2021
Jensen AA, Leffers H (2008) Emerging endocrine disrupters: perfluoroalkylated substances. Int J Androl 31:161–169
Jian JM, Chen D, Han FJ et al (2018) A short review on human exposure to and tissue distribution of per- and polyfluoroalkyl substances (PFASs). Sci Total Environ 636:1058–1069
Jian JM, Guo Y, Zeng L et al (2017) Global distribution of perfluorochemicals (PFCs) in potential human exposure source: a review. Environ Int 108:51–62
Jin Q, Ma J, Shi Y et al (2020) Biomonitoring of chlorinated polyfluoroalkyl ether sulfonic acid in the general population in central and eastern China: occurrence and associations with age/sex. Environ Int 144:106043
Kato K, Wong LY, Chen A et al (2014) Changes in serum concentrations of maternal poly- and perfluoroalkyl substances over the course of pregnancy and predictors of exposure in a multiethnic cohort of Cincinnati, Ohio pregnant women during 2003–2006. Environ Sci Technol 48:9600–9608
Kemse N, Sundrani D, Kale A et al (2017) Maternal micronutrients, omega-3 fatty acids and gene expression of angiogenic and inflammatory markers in pregnancy induced hypertension rats. Arch Med Res 48:414–422
Kurwadkar S, Dane J, Kanel SR, Nadagouda MN et al (2021d) Per- and polyfluoroalkyl substances in water and wastewater: A critical review of their global occurrence and distribution. Sci Total Environ 10:151003
Leader J, Bajwa A, Lanes A et al (2018) The effect of very advanced maternal age on maternal and neonatal outcomes: a systematic review. J Obstet Gynaecol Can 40:1208–1218
Li K, Gao P, Xiang P et al (2017a) Molecular mechanisms of PFOA-induced toxicity in animals and humans: Implications for health risks. Environ Int 99:43–54
Li L, Zhai Z, Liu J, Hu J (2015) Estimating industrial and domestic environment releases of perfluorooctanoic acid and its salts in China from 2004 to 2012. Chemosphere 129:100–109
Li M, Zeng XW, Qian ZM et al (2017b) Isomers of perfluorooctanesulfonate (PFOS) in cord serum and birth outcomes in China: Guangzhou Birth Cohort Study. Environ Int 102:1–8
Li Y, Tony F, Daniel M et al (2018) Half-lives of PFOS, PFHxS and PFOA after end of exposure to contaminated drink water. Occup Environ Med 75:46–51
Lin PD, Cardenas A, Hauser R et al (2019) Per- and polyfluoroalkyl substances and blood lipid levels in pre-diabetic adults-longitudinal analysis of the diabetes prevention program outcomes study. Environ Int 129:343–353
Liu L, Oza S, Hogan D et al (2016) Global, regional, and national causes of under-5 mortality in 2000–15: an updated systematic analysis with implications for the Sustainable Development Goals. Lancet 388:3027–3035
Liu M, Yi S, Chen P et al (2019) Thyroid endocrine disruption effects of perfluoroalkyl phosphinic acids on zebrafish at early development. Sci Total Environ 676:290–297
Liu X, Chen D, Wang B et al (2020) Does low maternal exposure to per- and polyfluoroalkyl substances elevate the risk of spontaneous preterm birth? A Nested Case-Control Study in China. Environ Sci Technol 54:8259–8268
Maisonet M, Nayha S, Lawlor DA, Marcus M (2015) Prenatal exposures to perfluoroalkyl acids and serum lipids at ages 7 and 15 in females. Environ Int 82:49–60
Maisonet M, Terrell ML, McGeehin MA et al (2012) Maternal concentrations of polyfluoroalkyl compounds during pregnancy and fetal and postnatal growth in British girls. Environ Health Perspect 120:1432–1437
Mancini FR, Rajaobelina K, Praud D et al (2018) Nonlinear associations between dietary exposures to perfluorooctanoic acid (PFOA) or perfluorooctane sulfonate (PFOS) and type 2 diabetes risk in women: Findings from the E3N cohort study. Int J Hyg Environ Health 221:1054–1060
Manzano-Salgado CB, Casas M, Lopez-Espinosa MJ et al (2017) Prenatal exposure to perfluoroalkyl substances and birth outcomes in a Spanish birth cohort. Environ Int 108:278–284
Meng Q, Inoue K, Ritz B et al (2018) Prenatal exposure to perfluoroalkyl substances and birth outcomes; an updated analysis from the Danish National Birth Cohort. Int J Environ Res Public Health 15:1832
O’Brien JM, Austin AJ, Williams A et al (2011) Technical-grade perfluorooctane sulfonate alters the expression of more transcripts in cultured chicken embryonic hepatocytes than linear perfluorooctane sulfonate. Environ Toxicol Chem 30:2846–2859
Pan Y, Zhu Y, Zheng T et al (2017) Novel chlorinated polyfluorinated ether sulfonates and legacy per-/polyfluoroalkyl substances: placental transfer and relationship with serum albumin and glomerular filtration rate. Environ Sci Technol 51(1):634–644
Perkins RG, Butenhoff JL, Kennedy GLJr, et al (2004) 13-week dietary toxicity study of ammonium perfluorooctanoate (APFO) in male rats. Drug Chem Toxicol 27:361–378
Rothman KJ (2014) Six persistent research misconceptions. J Gen Intern Med 29:1060–1064
Sagiv SK, Rifas-Shiman SL, Fleisch AF et al (2018) Early-pregnancy plasma concentrations of perfluoroalkyl substances and birth outcomes in project viva: confounded by pregnancy hemodynamics? Am J Epidemiol 187:793–802
Statistical Communique of Kashgar on the 2018 Economic and Social Development. http://www.kashi.gov.cn/Item/47217.aspx. Accessed on May 24, 2021. (In Chinese)
Steenland K, Tinker S, Frisbee S et al (2009) Association of perfluorooctanoic acid and perfluorooctane sulfonate with serum lipids among adults living near a chemical plant. Am J Epidemiol 170:1268–1278
Strong KL, Pedersen J, Johansson EW et al (2021e) Patterns and trends in causes of child and adolescent mortality 2000–2016: setting the scene for child health redesign. BMJ Glob Health 6:e004760
United States Environmental Protection Agency (2013) The 2010/2015 PFOA Stewardship Program. http://www.epa.gov/oppt.pfoa/pubs/stewardship/. Accessed October 19, 2021
Wacholder S, Silverman DT, McLaughlin JK et al (1992) Selection of controls in case-control studies. III. Design Options. Am J Epidemiol 135:1042–1050
Wu K, Xu X, Peng L et al (2012) Association between maternal exposure to perfluorooctanoic acid (PFOA) from electronic waste recycling and neonatal health outcomes. Environ Int 48:1–8
Yang Q, Xie Y, Alexson SE et al (2002) Involvement of the peroxisome proliferator-activated receptor alpha in the immunomodulation caused by peroxisome proliferators in mice. Biochem Pharmacol 63:1893–1900
Zeng XW, Qian Z, Vaughn M et al (2015) Human serum levels of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) in Uyghurs from Sinkiang-Uighur Autonomous Region, China: background levels study. Environ Sci Pollut Res Int 22:4736–4746
Zhang YZ, Zeng XW, Qian ZM et al (2017) Perfluoroalkyl substances with isomer analysis in umbilical cord serum in China. Environ Sci Pollut Res Int 24:13626–13637
Zhou W, Zhang L, Tong C et al (2017) Plasma perfluoroalkyl and polyfluoroalkyl substances concentration and menstrual cycle characteristics in preconception women. Environ Health Perspect 125:067012
Acknowledgements
The research was supported by the Natural Science Foundation of the Xinjiang Uyghur Autonomous Region, China (No. 2018D01C013; 2018D01C021); the National Key Research and Development Program of China (No. 2018YFC1004300; No. 2018YFC1004302); the Fundamental Research Funds for the Central Universities (No. 20ykzd10). The authors acknowledge the cooperation of participants in this study who have been very generous with their time and assistance.
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BYY, GHD, XZ, TL, and JW contributed to the study conception and design. Material preparation, blood sample collection, and data analysis were performed by XN, CH, MSB, MA (Maihefuzaimu Abudoukade), MA (Mairiyemu Abulizi), AX, BL, XZ, QZW, CC, YNL, XXL, XWZ, and YY. The first draft of the manuscript was written BYY and all authors commented on previous versions of the manuscript. All authors contributed critically to the draft and gave final approval for publication.
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Yang, BY., Wu, J., Niu, X. et al. Low-Level Environmental Per- and Polyfluoroalkyl Substances and Preterm Birth: A Nested Case–Control Study Among a Uyghur Population in Northwestern China. Expo Health 14, 793–805 (2022). https://doi.org/10.1007/s12403-021-00454-0
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DOI: https://doi.org/10.1007/s12403-021-00454-0