Skip to main content
SpringerLink
Log in

Metabolomics of childhood exposure to perfluoroalkyl substances: a cross-sectional study

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Introduction

Exposure to perfluoroalkyl substances (PFAS), synthetic and persistent chemicals used in commercial and industrial processes, are associated with cardiometabolic dysfunction and related risk factors including reduced birth weight, excess adiposity, and dyslipidemia. Identifying the metabolic changes induced by PFAS exposure could enhance our understanding of biological pathways underlying PFAS toxicity.

Objective

To identify metabolic alterations associated with serum concentrations of four PFAS in children using a metabolome-wide association study.

Methods

We performed untargeted metabolomic profiling by liquid chromatography with ultra-high-resolution mass spectrometry, and separately quantified serum concentrations of perfluorooctanoic acid, perfluorooctanesulfonic acid, perfluorononanoic acid, and perfluorohexanesulfonic acid (PFHxS) for 114 8-year old children from Cincinnati, OH. We evaluated associations between each serum PFAS concentration and 16,097 metabolic features using linear regression adjusted for child age, sex, and race with a false discovery rate < 20%. We annotated PFAS-associated metabolites and conducted pathway enrichment analyses.

Results

Serum PFAS concentrations were associated with metabolic features annotated primarily as lipids and dietary factors. Biological pathways associated with all four PFAS included arginine, proline, aspartate, asparagine, and butanoate metabolism.

Conclusions

In this cross-sectional study, childhood serum PFAS concentrations were correlated with metabolic pathways related to energy production and catabolism. Future studies should determine whether these pathways mediate associations between PFAS exposure and childhood cardiometabolic health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agency for Toxic Substances and Disease Registry. (2015). Draft Toxicological Profile for Perfluoroalkyls. Atlanta: Agency for Toxic Substances and Disease Registry.

    Google Scholar 

  • Alderete, T. L., Jin, R., Walker, D. I., Valvi, D., Chen, Z., Jones, D. P., et al. (2019). Perfluoroalkyl substances, metabolomic profiling, and alterations in glucose homeostasis among overweight and obese Hispanic children: A proof-of-concept analysis. Environment International, 126, 445–453.

    Article  CAS  Google Scholar 

  • Andersen, C. S., Fei, C., Gamborg, M., Nohr, E. A., Sorensen, T. I., & Olsen, J. (2013). Prenatal exposures to perfluorinated chemicals and anthropometry at 7 years of age. American Journal of Epidemiology, 178, 921–927.

    Article  Google Scholar 

  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57, 289–300.

    Google Scholar 

  • Bowman, L. (2015). FluoroCouncil Companies to Phase out Long-Chain Chemicals by Year’s End. Washington, DC: American Chemistry.

    Google Scholar 

  • Braun, J. M. (2016). Early-life exposure to EDCs: Role in childhood obesity and neurodevelopment. Nature Reviews Endocrinology, 13, 161.

    Article  Google Scholar 

  • Braun, J. M., Chen, A., Romano, M. E., Calafat, A. M., Webster, G. M., Yolton, K., et al. (2016a). Prenatal perfluoroalkyl substance exposure and child adiposity at 8 years of age: The HOME study. Obesity (Silver Spring), 24, 231–237.

    Article  CAS  Google Scholar 

  • Braun, J. M., Gennings, C., Hauser, R., & Webster, T. F. (2016b). What can epidemiological studies tell us about the Impact of chemical mixtures on human health? Environmental Health Perspectives, 124, A6–A9.

    Article  Google Scholar 

  • Braun, J. M., Kalloo, G., Chen, A., Dietrich, K. N., Liddy-Hicks, S., Morgan, S., et al. (2017). Cohort profile: The health outcomes and measures of the environment (HOME) study. International Journal of Epidemiology, 46, 24.

    PubMed  Google Scholar 

  • Buck, R. C., Franklin, J., Berger, U., Conder, J. M., Cousins, I. T., de Voogt, P., et al. (2011). Perfluoroalkyl and polyfluoroalkyl substances in the environment: Terminology, classification, and origins. Integrated Environmental Assessment Management, 7, 513–541.

    Article  CAS  Google Scholar 

  • Cardenas, A., Gold, D. R., Hauser, R., Kleinman, K. P., Hivert, M. F., Calafat, A. M., et al. (2017). Plasma concentrations of per- and polyfluoroalkyl substances at baseline and associations with glycemic indicators and diabetes incidence among high-risk adults in the diabetes prevention program trial. Environmental Health Perspectives, 125, 107001.

    Article  Google Scholar 

  • DeWitt, J. C. (2015). Toxicological effects of perfluoroalkyl and polyfluoroalkyl substances. Switzerland: Humana Press.

    Book  Google Scholar 

  • Environmental Protection Agency. (2000). EPA and 3 M Announce Phase out of PFOS. Washington, DC: Environmental Protection Agency.

    Google Scholar 

  • Eriksen, K. T., Raaschou-Nielsen, O., McLaughlin, J. K., Lipworth, L., Tjønneland, A., Overvad, K., et al. (2013). Association between Plasma PFOA and PFOS levels and total cholesterol in a middle-aged danish population. PLoS ONE, 8, e56969.

    Article  CAS  Google Scholar 

  • European Food Safety Authority. (2008). Perfluoroctane sulfonate, perfluorooctanoic acid and their salts: Scientific opinion of the panel on contaminants in the food chain. European Food Safety Authority Journal, 653, 1–131.

    Google Scholar 

  • Fahy, E., Sud, M., Cotter, D., & Subramaniam, S. (2007). LIPID MAPS online tools for lipid research. Nucleic Acids Research, 35, W606–W612.

    Article  Google Scholar 

  • Fleisch, A. F., Rifas-Shiman, S. L., Mora, A. M., Calafat, A. M., Ye, X., Luttmann-Gibson, H., et al. (2017). Early-life exposure to perfluoroalkyl substances and childhood metabolic function. Environmental Health Perspectives, 125, 481–487.

    Article  CAS  Google Scholar 

  • Fletcher, T., Galloway, T. S., Melzer, D., Holcroft, P., Cipelli, R., Pilling, L. C., et al. (2013). Associations between PFOA, PFOS and changes in the expression of genes involved in cholesterol metabolism in humans. Environment International, 57–58, 2–10.

    Article  Google Scholar 

  • Frisbee, S. J., Shankar, A., Knox, S. S., et al. (2010). Perfluorooctanoic acid, perfluorooctanesulfonate, and serum lipids in children and adolescents: Results from the c8 health project. Archives of Pediatrics and Adolescent Medicine, 164, 860–869.

    Article  Google Scholar 

  • Fromme, H., Tittlemier, S. A., Volkel, W., Wilhelm, M., & Twardella, D. (2009). Perfluorinated compounds–exposure assessment for the general population in Western countries. International Journal of Hygiene and Environmental Health, 212, 239–270.

    Article  CAS  Google Scholar 

  • Guasch-Ferre, M., Hruby, A., Toledo, E., Clish, C. B., Martinez-Gonzalez, M. A., Salas-Salvado, J., et al. (2016). Metabolomics in prediabetes and diabetes: A systematic review and meta-analysis. Diabetes Care, 39, 833–846.

    Article  CAS  Google Scholar 

  • Jain, R. B. (2013). 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. Journal of Toxicology and Environmental Health Part A, 76, 409–421.

    Article  CAS  Google Scholar 

  • Johnson, W. E., Li, C., & Rabinovic, A. (2007). Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics, 8, 118–127.

    Article  Google Scholar 

  • Johnson, P. I., Sutton, P., Atchley, D. S., Koustas, E., Lam, J., Sen, S., et al. (2014). The Navigation Guide—Evidence-based medicine meets environmental health: Systematic review of human evidence for PFOA effects on fetal growth. Environmental Health Perspectives, 122, 1028–1039.

    Article  Google Scholar 

  • Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y., & Morishima, K. (2017). KEGG: New perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Research, 45, D353–D361.

    Article  CAS  Google Scholar 

  • Kanehisa, M., & Goto, S. (2000). KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research, 28, 27–30.

    Article  CAS  Google Scholar 

  • Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., & Tanabe, M. (2016). KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research, 44, D457–D462.

    Article  CAS  Google Scholar 

  • Kato, K., Basden, B. J., Needham, L. L., & Calafat, A. M. (2011). Improved selectivity for the analysis of maternal serum and cord serum for polyfluoroalkyl chemicals. Journal of Chromatography A, 1218, 2133–2137.

    Article  CAS  Google Scholar 

  • Kato, K., Wong, L. Y., Chen, A., Dunbar, C., Webster, G. M., Lanphear, B. P., 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. Environmental Science and Technology, 48, 9600–9608.

    Article  CAS  Google Scholar 

  • Kennedy, D. O. (2016). B Vitamins and the Brain: Mechanisms, Dose and Efficacy–A Review. Nutrients, 8, 68.

    Article  Google Scholar 

  • Kingsley, S. L., Eliot, M. N., Kelsey, K. T., Calafat, A. M., Ehrlich, S., Lanphear, B. P., et al. (2018). Variability and predictors of serum perfluoroalkyl substance concentrations during pregnancy and early childhood. Environmental Research, 165, 247–257.

    Article  CAS  Google Scholar 

  • Kuklenyik, Z., Needham, L. L., & Calafat, A. M. (2005). Measurement of 18 Perfluorinated Organic Acids and Amides in Human Serum Using On-Line Solid-Phase Extraction. Analytical Chemistry, 77, 6085–6091.

    Article  CAS  Google Scholar 

  • Lankadurai, B. P., Nagato, E. G., & Simpson, M. J. (2013). Environmental metabolomics: An emerging approach to study organism responses to environmental stressors. Environmental Reviews, 21, 180–205.

    Article  CAS  Google Scholar 

  • Lee, Y. J., Kim, M. K., Bae, J., & Yang, J. H. (2013). Concentrations of perfluoroalkyl compounds in maternal and umbilical cord sera and birth outcomes in Korea. Chemosphere, 90, 1603–1609.

    Article  CAS  Google Scholar 

  • Lee, J. W., Lee, J. W., Kim, K., Shin, Y. J., Kim, J., Kim, S., et al. (2017). PFOA-induced metabolism disturbance and multi-generational reproductive toxicity in Oryzias latipes. Journal of Hazardous Materials, 340, 231–240.

    Article  CAS  Google Scholar 

  • Li, S., Park, Y., Duraisingham, S., Strobel, F. H., Khan, N., Soltow, Q. A., et al. (2013). Predicting network activity from high throughput metabolomics. PLoS Computational Biology, 9, e1003123.

    Article  CAS  Google Scholar 

  • Li, S., Pozhitkov, A., Ryan, R. A., Manning, C. S., Brown-Peterson, N., & Brouwer, M. (2010). Constructing a fish metabolic network model. Genome Biology, 11, R115.

    Article  CAS  Google Scholar 

  • Liu, K. H., Walker, D. I., Uppal, K., Tran, V., Rohrbeck, P., Mallon, T. M., et al. (2016). High-resolution metabolomics assessment of military personnel: Evaluating analytical strategies for chemical detection. Journal of Occupational and Environmental Medicine, 58, S53–S61.

    Article  CAS  Google Scholar 

  • Liu, H. S., Wen, L. L., Chu, P. L., & Lin, C. Y. (2018). Association among total serum isomers of perfluorinated chemicals, glucose homeostasis, lipid profiles, serum protein and metabolic syndrome in adults: NHANES, 2013–2014. Environmental Pollution, 232, 73–79.

    Article  CAS  Google Scholar 

  • Llewellyn, A., Simmonds, M., Owen, C. G., & Woolacott, N. (2015). Childhood obesity as a predictor of morbidity in adulthood: A systematic review and meta-analysis. Obes Rev., 17(1), 56–67.

    Article  Google Scholar 

  • Lopez-Espinosa, M. J., Fletcher, T., Armstrong, B., Genser, B., Dhatariya, K., Mondal, D., et al. (2011). Association of Perfluorooctanoic Acid (PFOA) and Perfluorooctane Sulfonate (PFOS) with age of puberty among children living near a chemical plant. Environmental Science and Technology, 45, 8160–8166.

    Article  CAS  Google Scholar 

  • Maisonet, M., Terrell, M. L., McGeehin, M. A., Christensen, K. Y., Holmes, A., Calafat, A. M., et al. (2012). Maternal concentrations of polyfluoroalkyl compounds during pregnancy and fetal and postnatal growth in British girls. Environmental Health Perspectives, 120, 1432–1437.

    Article  CAS  Google Scholar 

  • Mora, A. M., Oken, E., Rifas-Shiman, S. L., Webster, T. F., Gillman, M. W., Calafat, A. M., et al. (2017). Prenatal Exposure to Perfluoroalkyl Substances and Adiposity in Early and Mid-Childhood. Environmental Health Perspectives, 125, 467–473.

    Article  CAS  Google Scholar 

  • Nelson, J. W., Hatch, E. E., & Webster, T. F. (2009). Exposure to polyfluoroalkyl chemicals and cholesterol, body weight, and insulin resistance in the general US population. Environmental Health Perspectives, 118, 197–202.

    Article  Google Scholar 

  • Olsen, G. W., Burris, J. M., Ehresman, D. J., Froehlich, J. W., Seacat, A. M., Butenhoff, J. L., et al. (2007). Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environmental Health Perspectives, 115, 1298–1305.

    Article  CAS  Google Scholar 

  • Park, M. H., Falconer, C., Viner, R. M., & Kinra, S. (2012). The impact of childhood obesity on morbidity and mortality in adulthood: a systematic review. Obesity Reviews, 13, 985–1000.

    Article  CAS  Google Scholar 

  • Peng, S., Yan, L., Zhang, J., Wang, Z., Tian, M., & Shen, H. (2013). An integrated metabonomics and transcriptomics approach to understanding metabolic pathway disturbance induced by perfluorooctanoic acid. Journal of Pharmaceutical and Biomedical Analysis, 86, 56–64.

    Article  CAS  Google Scholar 

  • Perng, W., Gillman, M. W., Fleisch, A. F., Michalek, R. D., Watkins, S. M., Isganaitis, E., et al. (2014). Metabolomic profiles and childhood obesity. Obesity (Silver Spring), 22, 2570–2578.

    CAS  Google Scholar 

  • Rappazzo, K. M., Coffman, E., & Hines, E. P. (2017). Exposure to Perfluorinated Alkyl Substances and Health Outcomes in Children: A Systematic Review of the Epidemiologic Literature. International Journal of Environmental Research and Public Health, 14(7), 691.

    Article  Google Scholar 

  • Ruiz-Canela, M., Hruby, A., Clish, C. B., Liang, L., Martinez-Gonzalez, M. A., & Hu, F. B. (2017). Comprehensive metabolomic profiling and incident cardiovascular disease: A systematic review. Journal of the American Heart Association, 6, e005705.

    Article  Google Scholar 

  • Salihovic, S., Fall, T., Ganna, A., Broeckling, C. D., Prenni, J. E., Hyotylainen, T., et al. (2018). Identification of metabolic profiles associated with human exposure to perfluoroalkyl substances. Journal of Exposure Science and Environmental Epidemiology, 29(2), 196–205.

    Article  Google Scholar 

  • Soltow, Q. A., Strobel, F. H., Mansfield, K. G., Wachtman, L., Park, Y., & Jones, D. P. (2013). High-performance metabolic profiling with dual chromatography-Fourier-transform mass spectrometry (DC-FTMS) for study of the exposome. Metabolomics, 9, S132–S143.

    Article  Google Scholar 

  • Steenland, K., Tinker, S., Frisbee, S., Ducatman, A., & Vaccarino, V. (2009). Association of perfluorooctanoic acid and perfluorooctane sulfonate with serum lipids among adults living near a chemical plant. American Journal of Epidemiology, 170, 1268–1278.

    Article  Google Scholar 

  • Sumner, L. W., Amberg, A., Barrett, D., Beale, M. H., Beger, R., Daykin, C. A., et al. (2007). Proposed minimum reporting standards for chemical analysis. Metabolomics, 3, 211–221.

    Article  CAS  Google Scholar 

  • Swedish Chemical Agency. (2015). Occurrence and use of highly fluorinated substances and alternatives. Arkitektkopia, Stockholm. https://www.kemi.se/en/global/rapporter/2015/report-7-15-occurrence-and-use-of-highly-fluorinated-substances-and-alternatives.pdf.

  • Tan, X., Xie, G., Sun, X., Li, Q., Zhong, W., Qiao, P., et al. (2013). High fat diet feeding exaggerates perfluorooctanoic acid-induced liver injury in mice via modulating multiple metabolic pathways. PLoS ONE, 8, e61409.

    Article  CAS  Google Scholar 

  • Trier, X., Lunderberg, D., Peaslee, G., & Wang, Z. (2015). PFAS suspect list: Fluorinated substances. Available at https://www.norman-network.com/?q=node/236; https://doi.org/10.5281/zenodo.2621988.

  • Uppal, K., Soltow, Q. A., Promislow, D. E., Wachtman, L. M., Quyyumi, A. A., & Jones, D. P. (2015). MetabNet: An R Package for metabolic association analysis of high-resolution metabolomics data. Front Bioeng Biotechnol, 3, 87.

    Article  Google Scholar 

  • Uppal, K., Soltow, Q. A., Strobel, F. H., Pittard, W. S., Gernert, K. M., Yu, T., et al. (2013). xMSanalyzer: Automated pipeline for improved feature detection and downstream analysis of large-scale, non-targeted metabolomics data. BMC Bioinformatics, 14, 15.

    Article  Google Scholar 

  • Uppal, K., Walker, D. I., & Jones, D. P. (2017). xMSannotator: An R Package for network-based annotation of high-resolution metabolomics data. Analytical Chemistry, 89, 1063–1067.

    Article  CAS  Google Scholar 

  • Uppal, K., Walker, D. I., Liu, K., Li, S., Go, Y.-M., & Jones, D. P. (2016). Computational metabolomics: A framework for the million metabolome. Chemical Research in Toxicology, 29, 1956–1975.

    Article  CAS  Google Scholar 

  • Verner, M. A., Ngueta, G., Jensen, E. T., Fromme, H., Volkel, W., Nygaard, U. C., et al. (2016). A simple pharmacokinetic model of prenatal and postnatal exposure to perfluoroalkyl substances (PFASs). Environmental Science and Technology, 50, 978–986.

    Article  CAS  Google Scholar 

  • Walker, D. I., Lane, K. J., Liu, K., Uppal, K., Patton, A. P., Durant, J. L., et al. (2018). Metabolomic assessment of exposure to near-highway ultrafine particles. Journal of Exposure Science & Environmental Epidemiology, 1, 1. https://doi.org/10.1038/s41370-018-0102-5.

    Article  CAS  Google Scholar 

  • Wang, X., Liu, L., Zhang, W., Zhang, J., Du, X., Huang, Q., et al. (2017). Serum metabolome biomarkers associate low-level environmental perfluorinated compound exposure with oxidative/nitrosative stress in humans. Environmental Pollution, 229, 168–176.

    Article  CAS  Google Scholar 

  • Whitworth, K. W., Haug, L. S., Baird, D. D., Becher, G., Hoppin, J. A., Skjaerven, R., et al. (2012). Perfluorinated compounds in relation to birth weight in the Norwegian Mother and Child Cohort Study. American Journal of Epidemiology, 175, 1209–1216.

    Article  Google Scholar 

  • Wishart, D. S., Feunang, Y. D., Marcu, A., Guo, A. C., Liang, K., Vazquez-Fresno, R., et al. (2018). HMDB 4.0: The human metabolome database for 2018. Nucleic Acids Research, 46, D608–D617.

    Article  CAS  Google Scholar 

  • Yu, T., Park, Y., Li, S., & Jones, D. P. (2013). Hybrid feature detection and information accumulation using high-resolution LC-MS metabolomics data. Journal of Proteome Research, 12, 1419–1427.

    Article  CAS  Google Scholar 

  • Yu, N., Wei, S., Li, M., Yang, J., Li, K., Jin, L., et al. (2016). Effects of perfluorooctanoic acid on metabolic profiles in brain and liver of mouse revealed by a high-throughput targeted metabolomics approach. Sci Rep, 6, 23963.

    Article  CAS  Google Scholar 

  • Zhang, Y., Beesoon, S., Zhu, L., & Martin, J. W. (2013). Biomonitoring of perfluoroalkyl acids in human urine and estimates of biological half-life. Environmental Science and Technology, 47, 10619–10627.

    Article  CAS  Google Scholar 

  • Zheng, F., Sheng, N., Zhang, H., Yan, S., Zhang, J., & Wang, J. (2017). Perfluorooctanoic acid exposure disturbs glucose metabolism in mouse liver. Toxicology and Applied Pharmacology, 335, 41–48.

    Article  CAS  Google Scholar 

Download references

Funding

Support: NIEHS R01 ES025214, R01 ES020349, P01 ES011261, P42 ES013660, U2C ES026561, and P30 ES23515.

Author information

Authors and Affiliations

  1. Department of Epidemiology, School of Public Health, Brown University, Box G-S121-2, Providence, RI, 02912, USA

    Samantha L. Kingsley & Joseph M. Braun

  2. Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Douglas I. Walker

  3. Division of Laboratory Sciences, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA, USA

    Antonia M. Calafat

  4. Department of Environmental Health, University of Cincinnati, Cincinnati, OH, USA

    Aimin Chen

  5. Department of Biostatistics, School of Public Health, Brown University, Providence, RI, USA

    George D. Papandonatos

  6. Division of General and Community Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Yingying Xu

  7. Division of Pulmonary, Allergy, Critical Care and Sleep Medicine, Emory University, Atlanta, GA, USA

    Dean P. Jones

  8. Child and Family Research Institute, BC Children’s and Women’s Hospital, Vancouver, BC, Canada

    Bruce P. Lanphear

  9. Faculty of Health Sciences, Simon Fraser University, Burnaby, Canada

    Bruce P. Lanphear

  10. School of Engineering, Brown University, Providence, RI, USA

    Kurt D. Pennell

Authors
  1. Samantha L. Kingsley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas I. Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonia M. Calafat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aimin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. George D. Papandonatos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yingying Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dean P. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bruce P. Lanphear
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kurt D. Pennell
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Joseph M. Braun
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JMB and KDP conceived the study. AC, JMB, and BPL led the HOME Study and YX supported the HOME Study and provided all HOME Study data. AMC measured serum PFOA and other PFAS concentrations. DIW, DPJ, and KDP provided metabolomics expertise and high-resolution metabolomic profiling of serum samples. SLK performed all statistical analyses with guidance from GDP and DIW. SLK drafted the manuscript, tables, and supplemental material. DIW also contributed to manuscript writing. All authors reviewed, edited, and approved the final manuscript.

Corresponding author

Correspondence to Joseph M. Braun.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest. JMB was financially compensated for serving as an expert witness for plaintiffs in litigation related to tobacco smoke exposures. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the National Institutes of Health or the Centers for Disease Control and Prevention (CDC). Use of trade names is for identification only and does not imply endorsement by the CDC, the Public Health Service, or the US Department of Health and Human Services.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 137 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kingsley, S.L., Walker, D.I., Calafat, A.M. et al. Metabolomics of childhood exposure to perfluoroalkyl substances: a cross-sectional study. Metabolomics 15, 95 (2019). https://doi.org/10.1007/s11306-019-1560-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11306-019-1560-z

Search

Navigation