Advertisement

Association between prenatal exposure to perfluoroalkyl substances and asthma-related diseases in preschool children

  • Xinxin Zeng
  • Qian Chen
  • Xi Zhang
  • Huajun Li
  • Quanhua Liu
  • Chunxiao Li
  • Ming Ma
  • Jianhua Zhang
  • Weixi ZhangEmail author
  • Jun ZhangEmail author
  • Lisu HuangEmail author
Research Article
  • 53 Downloads

Abstract

Thus far, the few studies on the associations between perfluoroalkyl substances (PFASs) and asthma in children have yielded inconsistent results. In this study, we aimed to evaluate whether and to what extent prenatal PFASs exposure is associated with childhood asthmatic diseases. Eight PFASs were measured in cord blood drawn from 358 children in the Shanghai Allergy Birth Cohort, and a 5-year follow-up plan was completed. Asthma was diagnosed and reported by pediatric respiratory physicians via repeated symptoms (wheezing and coughing) and laboratory examination (Immunoglobulin E level test and skin prick test). A total of 26.6% and 17.4% subjects were diagnosed with wheezing and asthma, respectively. Multivariable logistic regression and piecewise linear regression were applied, and no association was found between PFASs and asthma or wheezing. However, cord serum PFOA, PFOS, and PFDA were positively correlated with serum total IgE in 5-year-old children as the level of the former beyond the turning point (4.37 ng/mL, 2.95 ng/mL, and 0.42 ng/mL, respectively), but negatively with IgE before it reach turnning point.

Keywords

Perfluoroalkyl substances Prenatal exposure Asthma Immunoglobulin E Birth cohort study 

Notes

Acknowledgments

We thank all officers and staff of the birth cohort study and the physicians at the Xinhua Hospital Affiliated to the Shanghai Jiao Tong University School of Medicine.

Ethics approval and consent to participate

The ethics approval was obtained from the Xinhua Hospital and International Peace Maternity and Infant Health Hospital affiliated to the Shanghai Jiao Tong University School of Medicine. This study was conducted in accordance with the principles of the Helsinki Declaration.

Conflict of Interest

The authors declare that they have no conflicts of interest.

Funding information

This investigation was supported by National Natural Science Foundation of China (No. 81530086), Shanghai Municipal Health Commission (No. 2017YQ033), Zhejiang Provincial Program for the Cultivation of High-level Innovative Health talents, Provincial Natural Science Foundation of Zhejiang (No. LY15H010006), and Zhejiang Provincial Department of Science and Technology Project (No. 2016C33182).

Supplementary material

11356_2019_5864_MOESM1_ESM.docx (75 kb)
ESM 1 (DOCX 74 kb)

References

  1. Ashley-Martin J, Dodds L, Levy AR, Platt RW, Marshall JS, Arbuckle TE (2015) Prenatal exposure to phthalates, bisphenol A and perfluoroalkyl substances and cord blood levels of IgE, TSLP and IL-33. Environ Res 140:360–368.  https://doi.org/10.1016/j.envres.2015.04.010 CrossRefGoogle Scholar
  2. Averina M, Brox J, Huber S, Furberg AS, Sorensen M (2018) Serum perfluoroalkyl substances (PFAS) and risk of asthma and various allergies in adolescents. The Tromso study Fit Futures in Northern Norway. Environ Res 169:114–121.  https://doi.org/10.1016/j.envres.2018.11.005 CrossRefGoogle Scholar
  3. Cariou R, Veyrand B, Yamada A, Berrebi A, Zalko D, Durand S, Pollono C, Marchand P, Leblanc JC, Antignac JP, le Bizec B (2015) Perfluoroalkyl acid (PFAA) levels and profiles in breast milk, maternal and cord serum of French women and their newborns. Environ Int 84:71–81.  https://doi.org/10.1016/j.envint.2015.07.014 CrossRefGoogle Scholar
  4. Chang ET, Adami HO, Boffetta P, Wedner HJ, Mandel JS (2016) A critical review of perfluorooctanoate and perfluorooctanesulfonate exposure and immunological health conditions in humans. Crit Rev Toxicol 46:279–331.  https://doi.org/10.3109/10408444.2015.1122573 CrossRefGoogle Scholar
  5. Chen F, Yin S, Kelly BC, Liu W (2017) Isomer-specific transplacental transfer of perfluoroalkyl acids: results from a survey of paired maternal, cord sera, and placentas. Environ Sci Technol 51:5756–5763.  https://doi.org/10.1021/acs.est.7b00268 CrossRefGoogle Scholar
  6. DeWitt JC, Peden-Adams MM, Keller JM, Germolec DR (2012) Immunotoxicity of perfluorinated compounds: recent developments. Toxicol Pathol 40:300–311.  https://doi.org/10.1177/0192623311428473 CrossRefGoogle Scholar
  7. Dong GH, Liu MM, Wang D, Zheng L, Liang ZF, Jin YH (2011) Sub-chronic effect of perfluorooctanesulfonate (PFOS) on the balance of type 1 and type 2 cytokine in adult C57BL6 mice. Arch Toxicol 85:1235–1244.  https://doi.org/10.1007/s00204-011-0661-x CrossRefGoogle Scholar
  8. Dong G-H, Tung KY, Tsai CH, Liu MM, Wang D, Liu W, Jin YH, Hsieh WS, Lee YL, Chen PC (2013) Serum polyfluoroalkyl concentrations, asthma outcomes, and immunological markers in a case-control study of Taiwanese children. Environ Health Perspect 121:507–513.  https://doi.org/10.1289/ehp.1205351 CrossRefGoogle Scholar
  9. Fang X, Zhang L, Feng Y, Zhao Y, Dai J (2008) Immunotoxic effects of perfluorononanoic acid on BALB/c mice. Toxicol Sci 105:312–321.  https://doi.org/10.1093/toxsci/kfn127 CrossRefGoogle Scholar
  10. Fang X, Feng Y, Shi Z, Dai J (2009) Alterations of cytokines and MAPK signaling pathways are related to the immunotoxic effect of perfluorononanoic acid. Toxicol Sci 108:367–376.  https://doi.org/10.1093/toxsci/kfp019 CrossRefGoogle Scholar
  11. Fromme H, Tittlemier SA, Völkel W, Wilhelm M, Twardella D (2009) Perfluorinated compounds – exposure assessment for the general population in western countries. Int J Hyg Environ Health 212:239–270.  https://doi.org/10.1016/j.ijheh.2008.04.007 CrossRefGoogle Scholar
  12. Goudarzi H, Miyashita C, Okada E, Kashino I, Kobayashi S, Chen CJ, Ito S, Araki A, Matsuura H, Ito YM, Kishi R (2016) Effects of prenatal exposure to perfluoroalkyl acids on prevalence ofallergic diseases among 4-year-old children. Environ Int 94:124–132.  https://doi.org/10.1016/j.envint.2016.05.020 CrossRefGoogle Scholar
  13. Granum B, Haug LS, Namork E, Stølevik SB, Thomsen C, Aaberge IS, van Loveren H, Løvik M, Nygaard UC (2013) Pre-natal exposure to perfluoroalkyl substances may be associated with altered vaccine antibody levels and immune-related health outcomes in early childhood. J Immunotoxicol 10:373–379.  https://doi.org/10.3109/1547691X.2012.755580 CrossRefGoogle Scholar
  14. Heinzerling L, Mari A, Bergmann KC, Bresciani M, Burbach G, Darsow U, Durham S, Fokkens W, Gjomarkaj M, Haahtela T, Bom AT, Wöhrl S, Maibach H, Lockey R (2013) The skin prick test - European standards. Clin Transl Allergy 3:3.  https://doi.org/10.1186/2045-7022-3-3 CrossRefGoogle Scholar
  15. Humblet O, Diaz-Ramirez LG, Balmes JR, Pinney SM, Hiatt RA (2014) Perfluoroalkyl chemicals and asthma among children 12–19 years of age: NHANES (1999-2008). Environ Health Perspect 122:1129–1133.  https://doi.org/10.1289/ehp.1306606 CrossRefGoogle Scholar
  16. Impinen A, Nygaard UC, Lodrup Carlsen KC, Mowinckel P, Carlsen KH, Haug LS, Granum B (2018) Prenatal exposure to perfluoralkyl substances (PFASs) associated with respiratory tract infections but not allergy- and asthma-related health outcomes in childhood. Environ Res 160:518–523.  https://doi.org/10.1016/j.envres.2017.10.012 CrossRefGoogle Scholar
  17. Impinen A, Longnecker MP, Nygaard UC, London SJ, Ferguson KK, Haug LS, Granum B (2019) Maternal levels of perfluoroalkyl substances (PFASs) during pregnancy and childhood allergy and asthma related outcomes and infections in the Norwegian Mother and Child (MoBa) cohort. Environ Int 124:462–472.  https://doi.org/10.1016/j.envint.2018.12.041 CrossRefGoogle Scholar
  18. Johnson JR, Harker JA (2017) Allergic airway disease: more than meets the IgE. 57:631–632.  https://doi.org/10.1165/rcmb.2017-0271ED
  19. Kim HY, DeKruyff RH, Umetsu DT (2010) The many paths to asthma: phenotype shaped by innate and adaptive immunity. Nat Immunol 11:577–584.  https://doi.org/10.1038/ni.1892 CrossRefGoogle Scholar
  20. Lien GW, Wen TW, Hsieh WS, Wu KY, Chen CY, Chen PC (2011) Analysis of perfluorinated chemicals in umbilical cord blood by ultra-high performance liquid chromatography/tandem mass spectrometry. J Chromatogr B Anal Technol Biomed Life Sci 879:641–646.  https://doi.org/10.1016/j.jchromb.2011.01.037 CrossRefGoogle Scholar
  21. Liu S, Wang X, Lu Y, Li T, Gong Z, Sheng T, Hu B, Peng Z, Sun X (2013) The effects of intraoperative cryoprecipitate transfusion on acute renal failure following orthotropic liver transplantation. Hepatol Int 7:901–909.  https://doi.org/10.1007/s12072-013-9457-9 CrossRefGoogle Scholar
  22. Lovett-Racke AE, Hussain RZ, Northrop S, Choy J, Rocchini A, Matthes L, Chavis JA, Diab A, Drew PD, Racke MK (2004) Peroxisome proliferator-activated receptor alpha agonists as therapy for autoimmune disease. J Immunol (Baltimore, Md : 1950) 172:5790–5798.  https://doi.org/10.4049/jimmunol.172.9.5790 CrossRefGoogle Scholar
  23. Ng CW, How CH (2014) Recurrent wheeze and cough in young children: is it asthma? Singap Med J 55:236–241.  https://doi.org/10.11622/smedj.2014064 CrossRefGoogle Scholar
  24. Okada E, Sasaki S, Saijo Y, Washino N, Miyashita C, Kobayashi S, Konishi K, Ito YM, Ito R, Nakata A, Iwasaki Y, Saito K, Nakazawa H, Kishi R (2012) Prenatal exposure to perfluorinated chemicals and relationship with allergies and infectious diseases in infants. Environ Res 112:118–125.  https://doi.org/10.1016/j.envres.2011.10.003 CrossRefGoogle Scholar
  25. Okada E, Sasaki S, Kashino I, Matsuura H, Miyashita C, Kobayashi S, Itoh K, Ikeno T, Tamakoshi A, Kishi R (2014) Prenatal exposure to perfluoroalkyl acids and allergic diseases in early childhood. Environ Int 65:127–134.  https://doi.org/10.1016/j.envint.2014.01.007 CrossRefGoogle Scholar
  26. Pedersen SE, Hurd SS, Lemanske RF Jr, Becker A, Zar HJ, Sly PD, Soto-Quiroz M, Wong G, Bateman ED, Global Initiative for Asthma (2011) Global strategy for the diagnosis and management of asthma in children 5 years and younger. Pediatr Pulmonol 46:1–17.  https://doi.org/10.1002/ppul.21321 CrossRefGoogle Scholar
  27. Pennings JL, Jennen DG, Nygaard UC, Namork E, Haug LS, van Loveren H, Granum B (2016) Cord blood gene expression supports that prenatal exposure to perfluoroalkyl substances causes depressed immune functionality in early childhood. J Immunotoxicol 13:173–180.  https://doi.org/10.3109/1547691x.2015.1029147 CrossRefGoogle Scholar
  28. Pinart M, Benet M, Annesi-Maesano I, von Berg A, Berdel D, Carlsen KCL, Carlsen KH, Bindslev-Jensen C, Eller E, Fantini MP, Lenzi J, Gehring U, Heinrich J, Hohmann C, Just J, Keil T, Kerkhof M, Kogevinas M, Koletzko S, Koppelman GH, Kull I, Lau S, Melén E, Momas I, Porta D, Postma DS, Rancière F, Smit HA, Stein RT, Tischer CG, Torrent M, Wickman M, Wijga AH, Bousquet J, Sunyer J, Basagaña X, Guerra S, Garcia-Aymerich J, Antó JM (2014) Comorbidity of eczema, rhinitis, and asthma in IgE-sensitised and non-IgE-sensitised children in MeDALL: a population-based cohort study. Lancet Respir Med 2:131–140.  https://doi.org/10.1016/s2213-2600(13)70277-7 CrossRefGoogle Scholar
  29. Smit LA et al (2015) Prenatal exposure to environmental chemical contaminants and asthma and eczema in school-age children. Allergy 70:653–660.  https://doi.org/10.1111/all.12605 CrossRefGoogle Scholar
  30. Stein CR, McGovern KJ, Pajak AM, Maglione PJ (2016) Perfluoroalkyl and polyfluoroalkyl substances and indicators of immune function in children aged 12-19 y: National Health and Nutrition Examination Survey 79:348-357  https://doi.org/10.1038/pr.2015.213
  31. Timmermann CAG, Budtz-Jørgensen E, Jensen TK, Osuna CE, Petersen MS, Steuerwald U, Nielsen F, Poulsen LK, Weihe P, Grandjean P (2017) Association between perfluoroalkyl substance exposure and asthma and allergic disease in children as modified by MMR vaccination. J Immunotoxicol 14:39–49.  https://doi.org/10.1080/1547691x.2016.1254306 CrossRefGoogle Scholar
  32. Vanden Heuvel JP, Thompson JT, Frame SR, Gillies PJ (2006) Differential activation of nuclear receptors by perfluorinated fatty acid analogs and natural fatty acids: a comparison of human, mouse, and rat peroxisome prolif-erator-activated receptor-α, -β, and -γ, liver X receptor-β, and retinoid X receptor-α. Toxicol Sci 92:476–489CrossRefGoogle Scholar
  33. Wang IJ, Hsieh WS, Chen CY, Fletcher T, Lien GW, Chiang HL, Chiang CF, Wu TN, Chen PC (2011) The effect of prenatal perfluorinated chemicals exposures on pediatric atopy. Environ Res 111:785–791.  https://doi.org/10.1016/j.envres.2011.04.006 CrossRefGoogle Scholar
  34. Wang B, Chen Q, Shen L, Zhao S, Pang W, Zhang J (2016) Perfluoroalkyl and polyfluoroalkyl substances in cord blood of newborns in Shanghai, China: Implications for risk assessment. Environ Int 97:7–14.  https://doi.org/10.1016/j.envint.2016.10.008 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Pediatrics Infectious Diseases, Xinhua HospitalAffiliated to Shanghai Jiao Tong University School of MedicineShanghaiChina
  2. 2.Department of Pediatric Allergy and ImmunologyThe Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical UniversityWenzhouChina
  3. 3.MOE-Shanghai Key Laboratory of Children’s Environmental Health, Xinhua HospitalAffiliated to Shanghai Jiao Tong University School of MedicineShanghaiChina
  4. 4.Clinical Research Center, Xinhua HospitalAffiliated to Shanghai Jiao Tong University School of MedicineShanghaiChina
  5. 5.Department of Dermatological, Xinhua HospitalAffiliated to Shanghai Jiao Tong University School of MedicineShanghaiChina

Personalised recommendations