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

Kayoko Kato, Lee-Yang Wong, Aimin Chen, Carmen Dunbar, Glenys M Webster, Bruce P Lanphear, Antonia M Calafat, Kayoko Kato, Lee-Yang Wong, Aimin Chen, Carmen Dunbar, Glenys M Webster, Bruce P Lanphear, Antonia M Calafat

Abstract

Data on predictors of gestational exposure to poly- and perfluoroalkyl substances (PFASs) in the United States are limited. To fill in this gap, in a multiethnic cohort of Ohio pregnant women recruited in 2003-2006, we measured perfluorooctanesulfonate (PFOS), perfluorooctanoate (PFOA), and six additional PFASs in maternal serum at ∼16 weeks gestation (N = 182) and delivery (N = 78), and in umbilical cord serum (N = 202). We used linear regression to examine associations between maternal serum PFASs concentrations and demographic, perinatal, and lifestyle factors. PFASs concentrations in maternal sera and in their infants' cord sera were highly correlated (Spearman rank correlation coefficients = 0.73-0.95). In 71 maternal-infant dyads, unadjusted geometric mean (GM) concentrations (95% confidence interval) (in μg/L) in maternal serum at delivery of PFOS [8.50 (7.01-9.58)] and PFOA [3.43 (3.01-3.90)] were significantly lower than at 16 weeks gestation [11.57 (9.90-13.53], 4.91 (4.32-5.59), respectively], but higher than in infants' cord serum [3.32 (2.84-3.89), 2.85 (2.51-3.24), respectively] (P < 0.001). Women who were parous, with a history of previous breastfeeding, black, or in the lowest income category had significantly lower PFOS and PFOA GM concentrations than other women. These data suggest transplacental transfer of PFASs during pregnancy and nursing for the first time in a U.S. birth cohort.

Figures

Figure 1
Figure 1
Concentrations (in μg/L) for select PFASs in maternal serum at 16 weeks gestation and delivery, and in cord serum (n = 71 paired samples). Whiskers represent the 5th and 95th percentiles. The top and bottom edges of each box represent the 75th and 25th percentiles, respectively. The horizontal line in each box represents the median. Circles represent observations outside the 10th and 90th percentiles.

References

    1. Lau C.; Anitole K.; Hodes C.; Lai D.; Pfahles-Hutchens A.; Seed J. Perfluoroalkyl acids: A review of monitoring and toxicological findings. Toxicol. Sci. 2007, 992366–394.
    1. Lau C. Perfluoroalkyl acids: Recent activities and research progress. Reprod. Toxicol. 2009, 273–4209–211.
    1. Health Canada. Report on Human Biomonitoring of Environmental Chemicals in Canada. Results of the Canadian Health Measures Survey Cycle 1 (2007–2009). []. 2010. Ottawa, Ontario. 3–19–2014.
    1. Health Canada. Canadian Health Measures Survey: Cycle 2 Data Tables. 2009 to 2011. Catalogue no. 82–626-X[]. 2012. Ottawa, Canada, Statistics Canada. 3–17–2014.
    1. CDC. Fourth National Report on Human Exposure to Environmental Chemicals. Updated Tables, July 2014. []. 2013. Atlanta, GA, Centers for Disease Control and Prevention; National Center for Environmental Health; Division of Laboratory Sciences. 7–22–2014.
    1. Yamaguchi M.; Arisawa K.; Uemura H.; Katsuura-Kamano S.; Takami H.; Sawachika F.; Nakamoto M.; Juta T.; Toda E.; Mori K.; Hasegawa M.; Tanto M.; Shima M.; Sumiyoshi Y.; Morinaga K.; Kodama K.; Suzuki T.; Nagai M.; Satoh H. Consumption of seafood, serum liver enzymes, and blood levels of PFOS and PFOA in the Japanese population. J. Occup. Health. 2013, 553184–194.
    1. Ji K.; Kim S.; Kho Y.; Paek D.; Sakong J.; Ha J.; Kim S.; Choi K. Serum concentrations of major perfluorinated compounds among the general population in Korea: Dietary sources and potential impact on thyroid hormones. Env. Int. 2012, 45, 78–85.
    1. Zhang T.; Wu Q.; Sun H. W.; Zhang X. Z.; Yun S. H.; Kannan K. Perfluorinated compounds in whole blood samples from infants, children, and adults in China. Environ. Sci. Technol. 2010, 44114341–4347.
    1. Wilhelm M.; Angerer J.; Fromme H.; Holzer J. Contribution to the evaluation of reference values for PFOA and PFOS in plasma of children and adults from Germany. Int. J. Hyg. Environ. Health. 2009, 212156–60.
    1. Jiang W. W.; Zhang Y. F.; Zhu L. Y.; Deng J. M. Serum levels of perfluoroalkyl acids (PFAAs) with isomer analysis and their associations with medical parameters in Chinese pregnant women. Env. Int. 2014, 64, 40–47.
    1. Lyngso J.; Ramlau-Hansen C. H.; Hoyer B. B.; Stovring H.; Bonde J. P.; Jonsson B. A. G.; Lindh C. H.; Pedersen H. S.; Ludwicki J. K.; Zviezdai V.; Toft G. Menstrual cycle characteristics in fertile women from Greenland, Poland and Ukraine exposed to perfluorinated chemicals: a cross-sectional study. Hum. Reprod. 2014, 292359–367.
    1. Brantsaeter A. L.; Whitworth K. W.; Ydersbond T. A.; Haug L. S.; Haugen M.; Knutsen H. K.; Thomsen C.; Meltzer H. M.; Becher G.; Sabaredzovic A.; Hoppin J. A.; Eggesbo M.; Longnecker M. P. Determinants of plasma concentrations of perfluoroalkyl substances in pregnant Norwegian women. Env. Int. 2013, 54, 74–84.
    1. Hanssen L.; Dudarev A. A.; Huber S.; Odland J. O.; Nieboer E.; Sandanger T. M. Partition of perfluoroalkyl substances (PFASs) in whole blood and plasma, assessed in maternal and umbilical cord samples from inhabitants of arctic Russia and Uzbekistan. Sci. Total Environ. 2013, 447, 430–437.
    1. Jain R. B. Effect of pregnancy on the levels of selected perfluoroalkyl compounds for females aged 17–39 years: Data from National Health and Nutrition Examination Survey 2003–2008. J. Toxicol. Environ. Health Part A 2013, 767409–421.
    1. Javins B.; Hobbs G.; Ducatman A. M.; Pilkerton C.; Tacker D.; Knox S. S. Circulating maternal perfluoroalkyl substances during pregnancy in the C8 Health Study. Environ. Sci. Technol. 2013, 4731606–1613.
    1. Okada E.; Kashino I.; Matsuura H.; Sasaki S.; Miyashita C.; Yamamoto J.; Ikeno T.; Ito Y. M.; Matsumura T.; Tamakoshi A.; Kishi R. Temporal trends of perfluoroalkyl acids in plasma samples of pregnant women in Hokkaido, Japan, 2003–2011. Env. Int. 2013, 60, 89–96.
    1. Porpora M. G.; Lucchini R.; Abballe A.; Ingelido A. M.; Valentini S.; Fuggetta E.; Cardi V.; Ticino A.; Marra V.; Fulgenzi A. R.; De Felip E. Placental transfer of persistent organic pollutants: A preliminary study on mother–newborn pairs. Int. J. Environ. Res. Public Health. 2013, 102699–711.
    1. Glynn A.; Berger U.; Bignert A.; Ullah S.; Aune M.; Lignell S.; Darnerud P. O. Perfluorinated alkyl acids in blood serum from primiparous women in Sweden: Serial sampling during pregnancy and nursing, and temporal trends 1996–2010. Environ. Sci. Technol. 2012, 46169071–9079.
    1. Christensen K. Y.; Maisonet M.; Rubin C.; Holmes A.; Calafat A. M.; Kato K.; Flanders W. D.; Heron J.; McGeehin M. A.; Marcus M. Exposure to polyfluoroalkyl chemicals during pregnancy is not associated with offspring age at menarche in a contemporary British cohort. Env. Int. 2011, 371129–135.
    1. Kim S.; Choi K.; Ji K.; Seo J.; Kho Y.; Park J.; Kim S.; Park S.; Hwang I.; Jeon J.; Yang H.; Giesy J. P. Trans-placental transfer of thirteen perfluorinated compounds and relations with fetal thyroid hormones. Environ. Sci. Technol. 2011, 45177465–7472.
    1. Fromme H.; Mosch C.; Morovitz M.; ba-Alejandre I.; Boehmer S.; Kiranoglu M.; Faber F.; Hannibal I.; Genzel-Boroviczeny O.; Koletzko B.; Volkel W. Pre- and postnatal exposure to perfluorinated compounds (PFCs). Environ. Sci. Technol. 2010, 44187123–7129.
    1. Hamm M. P.; Cherry N.; Chan E.; Martin J. W.; Burstyn I. Maternal exposure to perfluorinated acids and fetal growth. J. Expo. Sci. Environ. Epidemiol. 2010, 207589–597.
    1. Halldorsson T. I.; Fei C. Y.; Olsen J.; Lipworth L.; McLaughlin J. K.; Olsen S. F. Dietary predictors of perfluorinated chemicals: A study from the Danish National Birth Cohort. Environ. Sci. Technol. 2008, 42238971–8977.
    1. Monroy R.; Morrison K.; Teo K.; Atkinson S.; Kubwabo C.; Stewart B.; Foster W. G. Serum levels of perfluoroalkyl compounds in human maternal and umbilical cord blood samples. Environ. Res. 2008, 108156–62.
    1. Woodruff T. J.; Zota A. R.; Schwartz J. M. Environmental chemicals in pregnant women in the United States: NHANES 2003–2004. Environ. Health Perspect. 2011, 1196878–885.
    1. Ode A.; Rylander L.; Lindh C. H.; Kallen K.; Jonsson B. A. G.; Gustafsson P.; Olofsson P.; Ivarsson S. A.; Rignell-Hydbom A. Determinants of maternal and fetal exposure and temporal trends of perfluorinated compounds. Environ. Sci. Pollut. Res. Int. 2013, 20117970–7978.
    1. Arbuckle T. E.; Kubwabo C.; Walker M.; Davis K.; Lalonde K.; Kosarac I.; Wen S. W.; Arnold D. L. Umbilical cord blood levels of perfluoroalkyl acids and polybrominated flame retardants. Int. J. Hyg. Environ. Health. 2013, 2162184–194.
    1. Lee Y. J.; Kim M. K.; Bae J.; Yang J. H. Concentrations of perfluoroalkyl compounds in maternal and umbilical cord sera and birth outcomes in Korea. Chemosphere 2013, 9051603–1609.
    1. Lien G. W.; Huang C. C.; Wu K. Y.; Chen M. H.; Lin C. Y.; Chen C. Y.; Hsieh W. S.; Chen P. C. Neonatal-maternal factors and perfluoroalkyl substances in cord blood. Chemosphere. 2013, 927843–850.
    1. Zhang T.; Sun H. W.; Lin Y.; Qin X. L.; Zhang Y. F.; Geng X.; Kannan K. Distribution of poly- and perfluoroalkyl substances in matched samples from pregnant women and carbon chain length related maternal transfer. Environ. Sci. Technol. 2013, 47147974–7981.
    1. Chen M. H.; Ha E. H.; Wen T. W.; Su Y. N.; Lien G. W.; Chen C. Y.; Chen P. C.; Hsieh W. S. Perfluorinated compounds in umbilical cord blood and adverse birth outcomes. Plos One. 2012, 78e42474.
    1. Gutzkow K. B.; Haug L. S.; Thomsen C.; Sabaredzovic A.; Becher G.; Brunborg G. Placental transfer of perfluorinated compounds is selective—A Norwegian mother and child sub-cohort study. Int. J. Hyg. Environ. Health. 2012, 2152216–219.
    1. Llorca M.; Perez F.; Farre M.; Agramunt S.; Kogevinas M.; Barcelo D. Analysis of perfluoroalkyl substances in cord blood by turbulent flow chromatography coupled to tandem mass spectrometry. Sci. Total Environ. 2012, 433, 151–160.
    1. Beesoon S.; Webster G. M.; Shoeib M.; Harner T.; Benskin J. P.; Martin J. W. Isomer profiles of perfluorochemicals in matched maternal, cord, and house dust samples: Manufacturing sources and transplacental transfer. Environ. Health Perspect. 2011, 119111659–1664.
    1. Kim S. K.; Lee K. T.; Kang C. S.; Tao L.; Kannan K.; Kim K. R.; Kim C. K.; Lee J. S.; Park P. S.; Yoo Y. W.; Ha J. Y.; Shin Y. S.; Lee J. H. Distribution of perfluorochemicals between sera and milk from the same mothers and implications for prenatal and postnatal exposures. Environ. Pollut. 2011, 1591169–174.
    1. Lien G. W.; Wena T. W.; Hsiehb W. S.; Wua K. Y.; Chenc C. Y.; Chena P. C. Analysis of perfluorinated chemicals in umbilical cord blood by ultra-high performance liquid chromatography/tandem mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2011, 8799–10641–646.
    1. Liu J. Y.; Li J. G.; Liu Y.; Chan H. M.; Zhao Y. F.; Cai Z. W.; Wu Y. N. Comparison on gestation and lactation exposure of perfluorinated compounds for newborns. Env. Int. 2011, 3771206–1212.
    1. Zhang W.; Lin Z. K.; Hu M. Y.; Wang X. D.; Lian Q. Q.; Lin K. F.; Dong Q. X.; Huang C. J. Perfluorinated chemicals in blood of residents in Wenzhou, China. Ecotoxicol. Environ. Saf. 2011, 7461787–1793.
    1. Hanssen L.; Rollin H.; Odland J. O.; Moe M. K.; Sandanger T. M. Perfluorinated compounds in maternal serum and cord blood from selected areas of South Africa: Results of a pilot study. J. Environ. Monit. 2010, 1261355–1361.
    1. Apelberg B. J.; Goldman L. R.; Calafat A. M.; Herbstman J. B.; Kuklenyik Z.; Heidler J.; Needham L. L.; Halden R. U.; Witter F. R. Determinants of fetal exposure to polyfluoroalkyl compounds in Baltimore, Maryland. Environ. Sci. Technol. 2007, 41113891–3897.
    1. Midasch O.; Drexler H.; Hart N.; Beckmann M. W.; Angerer J. Transplacental exposure of neonates to perfluorooctanesulfonate and perfluorooctanoate: A pilot study. Int. Arch. Occup. Environ. Health. 2007, 807643–648.
    1. Inoue K.; Okada F.; Ito R.; Kato S.; Sasaki S.; Nakajima S.; Uno A.; Saijo Y.; Sata F.; Yoshimura Y.; Kishi R.; Nakazawa H. Perfluorooctane sulfonate (PFOS) and related perfluorinated compounds in human maternal and cord blood samples: Assessment of PFOS exposure in a susceptible population during pregnancy. Environ. Health Perspect. 2004, 112111204–1207.
    1. Needham L. L.; Grandjean P.; Heinzow B.; Jorgensen P. J.; Nielsen F.; Patterson D. G.; Sjodin A.; Turner W. E.; Weihe P. Partition of environmental chemicals between maternal and fetal blood and tissues. Environ. Sci. Technol. 2011, 4531121–1126.
    1. Kato K.; Basden B. J.; Needham L. L.; Calafat A. M. Improved selectivity for the analysis of maternal serum and cord serum for polyfluoroalkyl chemicals. J. Chromatogr. A 2011, 1218, 2133–2137.
    1. Hornung R. W.; Reed L. D. Estimation of average concentration in the presence of nondetectable values. Appl. Occup. Environ. Hyg. 1990, 5146–51.
    1. Bernert J. T.; McGuffey J. E.; Morrison M. A.; Pirkle J. L. Comparison of serum and salivary cotinine measurements by a sensitive high-performance liquid chromatography-tandem mass spectrometry method as an indicator of exposure to tobacco smoke among smokers and nonsmokers. J. Anal. Toxicol. 2000, 245333–339.
    1. Hernick A. D.; Brown M. K.; Pinney S. M.; Biro F. M.; Ball K. M.; Bornschein R. L. Sharing unexpected biomarker results with study participants. Environ. Health Perspect. 2011, 11911–5.
    1. Pinney S. M.; Biro F. M.; Windham G. C.; Herrick R. L.; Yaghjyan L.; Calafat A. M.; Succop P.; Sucharew H.; Ball K. M.; Kato K.; Kushi L. H.; Bornschein R. Serum biomarkers of polyfluoroalkyl compound exposure in young girls in Greater Cincinnati and the San Francisco Bay Area, U.S.A. Environ. Pollut. 2014, 184, 327–334.
    1. Frisbee S. J.; Brooks A. P.; Maher A.; Flensborg P.; Arnold S.; Fletcher T.; Steenland K.; Shankar A.; Knox S. S.; Pollard C.; Halverson J. A.; Vieira V. M.; Jin C. F.; Leyden K. M.; Ducatman A. M. The C8 Health Project: Design, methods, and participants. Environ. Health Perspect. 2009, 117121873–1882.
    1. Emmett E. A.; Shofer F. S.; Zhang H.; Freeman D.; Desai C.; Shaw L. M. Community exposure to perfluorooctanoate: Relationships between serum concentrations and exposure sources. J. Occup. Environ. Med. 2006, 488759–770.
    1. Prevedouros K.; Cousins I. T.; Buck R. C.; Korzeniowski S. H. Sources, fate and transport of perfluorocarboxylates. Environ. Sci. Technol. 2006, 40132–44.
    1. Kato K.; Wong L. Y.; Jia L. T.; Kuklenyik Z.; Calafat A. M. Trends in exposure to polyfluoroalkyl chemicals in the U.S. population: 1999–2008. Environ. Sci. Technol. 2011, 45198037–8045.
    1. Uhl S. A.; James-Todd T.; Bell M. L. Association of osteoarthritis with perfluorooctanoate and perfluorooctane sulfonate in NHANES 2003–2008. Environ. Health Perspect. 2013, 1214447–452.
    1. Eriksen K. T.; Sorensen M.; McLaughlin J. K.; Tjonneland A.; Overvad K.; Raaschou-Nielsen O. Determinants of plasma PFOA and PFOS levels among 652 Danish men. Environ. Sci. Technol. 2011, 45198137–8143.
    1. Antignac J. P.; Veyrand B.; Kadar H.; Marchand P.; Oleko A.; Le Bizec B.; Vandentorren S. Occurrence of perfluorinated alkylated substances in breast milk of French women and relation with socio-demographical and clinical parameters: Results of the ELFE pilot study. Chemosphere 2013, 916802–808.
    1. Ji K.; Kim S.; Kho Y.; Sakong J.; Paek D.; Choi K. Major perfluoroalkyl acid (PFAA) concentrations and influence of food consumption among the general population of Daegu, Korea. Sci. Total Environ. 2012, 438, 42–48.
    1. Rylander C.; Duong T. P.; Odland J. O.; Sandanger T. M. Perfluorinated compounds in delivering women from south central Vietnam. J. Environ. Monit. 2009, 11112002–2008.
    1. Rylander C.; Sandanger T. M.; Froyland L.; Lund E. Dietary patterns and plasma concentrations of perfluorinated compounds in 315 Norwegian women: The NOWAC postgenome study. Environ. Sci. Technol. 2010, 44135225–5232.
    1. Fei C. Y.; McLaughlin J. K.; Tarone R. E.; Olsen J. Perfluorinated chemicals and fetal growth: A study within the Danish National Birth Cohort. Environ. Health Perspect. 2007, 115111677–1682.
    1. Washino N.; Saijo Y.; Sasaki S.; Kato S.; Ban S.; Konishi K.; Ito R.; Nakata A.; Iwasaki Y.; Saito K.; Nakazawa H.; Kishi R. Correlations between prenatal exposure to perfluorinated chemicals and reduced fetal growth. Environ. Health Perspect. 2009, 1174660–667.
    1. Costantine M. M.Front. Pharmacol. 2014, Apr 3;5:65. DOI: 10.3389/fphar.2014.00065. eCollection 2014.
    1. Ouzounian J. G.; Elkayam U. Physiologic changes during normal pregnancy and delivery. Cardiol. Clin. 2012, 303317–329.
    1. Barbarossa A.; Masetti R.; Gazzotti T.; Zama D.; Astolfi A.; Veyrand B.; Pession A.; Pagliuca G. Perfluoroalkyl substances in human milk: A first survey in Italy. Env. Int. 2013, 51, 27–30.
    1. Guerranti C.; Perra G.; Corsolini S.; Focardi S. E. Pilot study on levels of perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) in selected foodstuffs and human milk from Italy. Food Chem. 2013, 1401–2197–203.
    1. Karrman A.; Lindstrom G. Trends, analytical methods and precision in the determination of perfluoroalkyl acids in human milk. TrAC-Trends Anal. Chem. 2013, 46, 118–128.
    1. Kubwabo C.; Kosarac I.; Lalonde K. Determination of selected perfluorinated compounds and polyfluoroalkyl phosphate surfactants in human milk. Chemosphere. 2013, 916771–777.
    1. Croes K.; Colles A.; Koppen G.; Govarts E.; Bruckers L.; Van de Mieroop E.; Nelen V.; Covaci A.; Dirtu A. C.; Thomsen C.; Haug L. S.; Becher G.; Mampaey M.; Schoeters G.; Van Larebeke N.; Baeyens W. Persistent organic pollutants (POPs) in human milk: A biomonitoring study in rural areas of Flanders (Belgium). Chemosphere 2012, 898988–994.
    1. Fujii Y.; Yan J. X.; Harada K. H.; Hitomi T.; Yang H.; Wang P. Y.; Koizumi A. Levels and profiles of long-chain perfluorinated carboxylic acids in human breast milk and infant formulas in East Asia. Chemosphere 2012, 863315–321.
    1. Thomsen C.; Haug L. S.; Stigum H.; Froshaug M.; Broadwell S. L.; Becher G. Changes in concentrations of perfluorinated compounds, polybrominated biphenyl ethers, and polychlorinated biphenyls in Norwegian breast-milk during twelve months of lactation. Environ. Sci. Technol. 2010, 44249550–9556.
    1. Tao L.; Kannan K.; Wong C. M.; Arcaro K. F.; Butenhoff J. L. Perfluorinated compounds in human milk from Massachusetts, U.S.A. Environ. Sci. Technol. 2008, 4283096–3101.
    1. Volkel W.; Genzel-Boroviczeny O.; Demmelmair H.; Gebauer C.; Koletzko B.; Twardella D.; Raab U.; Fromme H. Perfluorooctane sulphonate (PFOS) and perfluorooctanoic acid (PFOA) in human breast milk: Results of a pilot study. Int. J. Hyg. Environ. Health. 2008, 2113–4440–446.
    1. Karrman A.; Ericson I.; van Bavel B.; Darnerud P. O.; Aune M.; Glynn A.; Lignell S.; Lindstrom G. Exposure of perfluorinated chemicals through lactation: Levels of matched human milk and serum and a temporal trend, 1996–2004, in Sweden. Environ. Health Perspect. 2007, 1152226–230.

Source: PubMed

3
Předplatit