Abstract
Epidemiological evidence suggests that exposure to per- and polyfluoroalkyl substances (PFAS) is associated with lipid profile levels, but with inconsistent conclusions from different studies. The aim of this study was to conduct a meta-analysis of the relationship between PFAS exposure and lipid profile levels based on population-based epidemiological studies. Embase, PubMed, Ovid database, The Cochrane Library and Web of Science database were used to search appropriate studies (before September 6, 2022) on the correlation between PFAS exposure and lipid profile levels. β value, odd ratio (OR) and 95 % confidence intervals (CIs) were extracted from studies. In this study, we found that higher low-density lipoprotein (LDL) levels were associated with exposure to perfluoroundecanoic acid (PFUnDA) (β value=0.13, 95 % CIs: 0.02, 0.24) and perfluorooctane sulfonic acid (PFOS) (β value=0.13, 95 % CIs: 0.04, 0.21). PFOA, PFOS and PFNA exposure were significantly related to the higher levels of total cholesterol (TC) with the pooled effect estimates of 0.08 (95 % CI: 0.02, 0.14), 0.13 (95 % CI: 0.05, 0.21) and 0.14 (95 % CI: 0.08, 0.20) respectively. In sum, our results identified that PFOA, PFOS, PFNA and PFUnDA were the most important risk factors for abnormal levels of lipid profile, indicating that we should prevent cerebrovascular disease by reducing and controlling PFAS exposure.
Funding source: Outstanding Young Backbone Teachers of Qinglan Project in Jiangsu Province
Funding source: Key R&D Program of Lianyungang
Award Identifier / Grant number: SF2201
Funding source: College Students’ Innovative Entrepreneurial Training Plan Program in Jiangsu Province
Award Identifier / Grant number: 202313980005Y
Funding source: Science Foundation of Kangda College of Nanjing Medical University
Award Identifier / Grant number: KD2021KYRC016
-
Research ethics: Not applicable.
-
Informed consent: Not applicable.
-
Author contributions: Xinru song: Software, Investigation, Writing – original draft preparation; Tingtao Ye: Investigation, Conceptualization, Writing – original draft preparation; Dongmei Jing: Investigation and data check; Kai Wei and Yue Ge: Validation; Xinyue Bei, Yuqian Qi and Huanqiang Wang: data curation; Jun Li: Data curation, writing—review and editing; Yan Zhang: Funding acquisition, Conceptualization and Supervision.
-
Competing interests: The authors declare that they have no competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
-
Research funding: This work was supported by Outstanding Young Backbone Teachers of Qinglan Project in Jiangsu Province, Key R&D Program of Lianyungang (Grant numbers [SF2201]), College Students’ Innovative Entrepreneurial Training Plan Program in Jiangsu Province (Grant numbers [202313980005Y]), Science Foundation of Kangda College of Nanjing Medical University (Grant numbers [KD2021KYRC016]).
-
Data availability: Not applicable.
References
1. Collaborators GBDCoD, Abate, D, Abate, KH, Abay, SM, Abbafati, C, Abbasi, N, et al.. Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 2018;392:1736–88. https://doi.org/10.1016/s0140-6736(18)32203-7.Search in Google Scholar
2. de Bont, J, Jaganathan, S, Dahlquist, M, Persson, A, Stafoggia, M, Ljungman, P. Ambient air pollution and cardiovascular diseases: an umbrella review of systematic reviews and meta-analyses. J Intern Med 2022;291:779–800. https://doi.org/10.1111/joim.13467.Search in Google Scholar PubMed PubMed Central
3. Yilmaz, B, Terekeci, H, Sandal, S, Kelestimur, F. Endocrine disrupting chemicals: exposure, effects on human health, mechanism of action, models for testing and strategies for prevention. Rev Endocr Metab Disord 2020;21:127–47. https://doi.org/10.1007/s11154-019-09521-z.Search in Google Scholar PubMed
4. Abrantes-Soares, F, Lorigo, M, Cairrao, E. Effects of BPA substitutes on the prenatal and cardiovascular systems. Crit Rev Toxicol 2022;52:469–98. https://doi.org/10.1080/10408444.2022.2142514.Search in Google Scholar PubMed
5. Liberda, EN, Zuk, AM, Tsuji, LJS. Complex contaminant mixtures and their associations with intima-media thickness. BMC Cardiovasc Disord 2019;19:289. https://doi.org/10.1186/s12872-019-1246-5.Search in Google Scholar PubMed PubMed Central
6. Zhu, X, Yin, T, Yue, X, Liao, S, Cheang, I, Zhu, Q, et al.. Association of urinary phthalate metabolites with cardiovascular disease among the general adult population. Environ Res 2021;202:111764. https://doi.org/10.1016/j.envres.2021.111764.Search in Google Scholar PubMed
7. Rasdi, Z, Kamaludin, R, Ab Rahim, S, Syed Ahmad Fuad, SB, Othman, MHD, Siran, R, et al.. The impacts of intrauterine Bisphenol A exposure on pregnancy and expression of miRNAs related to heart development and diseases in animal model. Sci Rep 2020;10:5882. https://doi.org/10.1038/s41598-020-62420-1.Search in Google Scholar PubMed PubMed Central
8. Curtzwiler, GW, Silva, P, Hall, A, Ivey, A, Vorst, K. Significance of perfluoroalkyl substances (PFAS) in food packaging. Integr Environ Assess Manage 2021;17:7–12. https://doi.org/10.1002/ieam.4346.Search in Google Scholar PubMed
9. Blake, BE, Fenton, SE. Early life exposure to per- and polyfluoroalkyl substances (PFAS) and latent health outcomes: a review including the placenta as a target tissue and possible driver of peri- and postnatal effects. Toxicology 2020;443:152565. https://doi.org/10.1016/j.tox.2020.152565.Search in Google Scholar PubMed PubMed Central
10. Roth, K, Yang, Z, Agarwal, M, Liu, W, Peng, Z, Long, Z, et al.. Exposure to a mixture of legacy, alternative, and replacement per- and polyfluoroalkyl substances (PFAS) results in sex-dependent modulation of cholesterol metabolism and liver injury. Environ Int 2021;157:106843. https://doi.org/10.1016/j.envint.2021.106843.Search in Google Scholar PubMed PubMed Central
11. Li, D, Jiang, L, Hong, Y, Cai, Z. Multilayered glycoproteomic analysis reveals the hepatotoxic mechanism in perfluorooctane sulfonate (PFOS) exposure mice. Environ Pollut 2021;268:115774. https://doi.org/10.1016/j.envpol.2020.115774.Search in Google Scholar PubMed
12. Feingold, KR. Lipid and lipoprotein metabolism. Endocrinol Metab Clin North Am 2022;51:437–58. https://doi.org/10.1016/j.ecl.2022.02.008.Search in Google Scholar PubMed
13. Geiger, SD, Xiao, J, Ducatman, A, Frisbee, S, Innes, K, Shankar, A. The association between PFOA, PFOS and serum lipid levels in adolescents. Chemosphere 2014;98:78–83. https://doi.org/10.1016/j.chemosphere.2013.10.005.Search in Google Scholar PubMed
14. Zeng, XW, Qian, Z, Emo, B, Vaughn, M, Bao, J, Qin, XD, et al.. Association of polyfluoroalkyl chemical exposure with serum lipids in children. Sci Total Environ 2015;512–513:364–70. https://doi.org/10.1016/j.scitotenv.2015.01.042.Search in Google Scholar PubMed
15. Wang, J, Zhang, Y, Zhang, W, Jin, Y, Dai, J. Association of perfluorooctanoic acid with HDL cholesterol and circulating miR-26b and miR-199-3p in workers of a fluorochemical plant and nearby residents. Environ Sci Technol 2012;46:9274–81. https://doi.org/10.1021/es300906q.Search in Google Scholar PubMed
16. Sunderland, EM, Hu, XC, Dassuncao, C, Tokranov, AK, Wagner, CC, Allen, JG. A review of the pathways of human exposure to poly- and perfluoroalkyl substances (PFASs) and present understanding of health effects. J Expo Sci Environ Epidemiol 2019;29:131–47. https://doi.org/10.1038/s41370-018-0094-1.Search in Google Scholar PubMed PubMed Central
17. Battineni, G, Sagaro, GG, Chintalapudi, N, Amenta, F, Tomassoni, D, Tayebati, SK. Impact of obesity-induced inflammation on cardiovascular diseases (CVD). Int J Mol Sci 2021;22:4798. https://doi.org/10.3390/ijms22094798.Search in Google Scholar PubMed PubMed Central
18. Lo, CK, Mertz, D, Loeb, M. Newcastle-Ottawa Scale: comparing reviewers’ to authors’ assessments. BMC Med Res Methodol 2014;14:45. https://doi.org/10.1186/1471-2288-14-45.Search in Google Scholar PubMed PubMed Central
19. Manosroi, W, Phudphong, P, Atthakomol, P, Phimphilai, M. The differences of serum lipid profiles between primary aldosteronism and essential hypertension: a meta-analysis and systematic review. BMC Endocr Disord 2022;22:217. https://doi.org/10.1186/s12902-022-01135-y.Search in Google Scholar PubMed PubMed Central
20. Higgins, JP, Thompson, SG, Deeks, JJ, Altman, DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60. https://doi.org/10.1136/bmj.327.7414.557.Search in Google Scholar PubMed PubMed Central
21. Costa, G, Sartori, S, Consonni, D. Thirty years of medical surveillance in perfluooctanoic acid production workers. J Occup Environ Med 2009;51:364–72. https://doi.org/10.1097/jom.0b013e3181965d80.Search in Google Scholar PubMed
22. Olsen, GW, Ehresman, DJ, Buehrer, BD, Gibson, BA, Butenhoff, JL, Zobel, LR. Longitudinal assessment of lipid and hepatic clinical parameters in workers involved with the demolition of perfluoroalkyl manufacturing facilities. J Occup Environ Med 2012;54:974–83. https://doi.org/10.1097/jom.0b013e31825461d2.Search in Google Scholar PubMed
23. Donat-Vargas, C, Bergdahl, IA, Tornevi, A, Wennberg, M, Sommar, J, Koponen, J, et al.. Associations between repeated measure of plasma perfluoroalkyl substances and cardiometabolic risk factors. Environ Int 2019;124:58–65. https://doi.org/10.1016/j.envint.2019.01.007.Search in Google Scholar PubMed
24. Lin, PD, Cardenas, A, Hauser, R, Gold, DR, Kleinman, KP, Hivert, MF, et al.. Per- and polyfluoroalkyl substances and blood lipid levels in pre-diabetic adults-longitudinal analysis of the diabetes prevention program outcomes study. Environ Int 2019;129:343–53. https://doi.org/10.1016/j.envint.2019.05.027.Search in Google Scholar PubMed PubMed Central
25. Dunder, L, Lind, PM, Salihovic, S, Stubleski, J, Karrman, A, Lind, L. Changes in plasma levels of per- and polyfluoroalkyl substances (PFAS) are associated with changes in plasma lipids – a longitudinal study over 10 years. Environ Res 2022;211:112903. https://doi.org/10.1016/j.envres.2022.112903.Search in Google Scholar PubMed
26. Frisbee, SJ, Shankar, A, Knox, SS, Steenland, K, Savitz, DA, Fletcher, T, et al.. Perfluorooctanoic acid, perfluorooctanesulfonate, and serum lipids in children and adolescents: results from the C8 Health Project. Arch Pediatr Adolesc Med 2010;164:860–9. https://doi.org/10.1001/archpediatrics.2010.163.Search in Google Scholar PubMed PubMed Central
27. Fisher, M, Arbuckle, TE, Wade, M, Haines, DA. Do perfluoroalkyl substances affect metabolic function and plasma lipids? Analysis of the 2007-2009, Canadian Health Measures Survey (CHMS) Cycle 1. Environ Res 2013;121:95–103. https://doi.org/10.1016/j.envres.2012.11.006.Search in Google Scholar PubMed
28. Canova, C, Barbieri, G, Zare Jeddi, M, Gion, M, Fabricio, A, Dapra, F, et al.. Associations between perfluoroalkyl substances and lipid profile in a highly exposed young adult population in the Veneto region. Environ Int 2020;145:106117. https://doi.org/10.1016/j.envint.2020.106117.Search in Google Scholar PubMed
29. Li, Y, Barregard, L, Xu, Y, Scott, K, Pineda, D, Lindh, CH, et al.. Associations between perfluoroalkyl substances and serum lipids in a Swedish adult population with contaminated drinking water. Environ Health 2020;19:33. https://doi.org/10.1186/s12940-020-00588-9.Search in Google Scholar PubMed PubMed Central
30. Cong, J, Chu, C, Li, QQ, Zhou, Y, Min Qian, Z, Dee Geiger, S, et al.. Associations of perfluorooctane sulfonate alternatives and serum lipids in Chinese adults. Environ Int 2021;155:106596. https://doi.org/10.1016/j.envint.2021.106596.Search in Google Scholar PubMed
31. Averina, M, Brox, J, Huber, S, Furberg, AS. Exposure to perfluoroalkyl substances (PFAS) and dyslipidemia, hypertension and obesity in adolescents. The Fit Futures study. Environ Res 2021;195:110740. https://doi.org/10.1016/j.envres.2021.110740.Search in Google Scholar PubMed
32. Zare Jeddi, M, Dalla Zuanna, T, Barbieri, G, Fabricio, ASC, Dapra, F, Fletcher, T, et al.. Associations of perfluoroalkyl substances with prevalence of metabolic syndrome in highly exposed young adult community residents-A cross-sectional study in Veneto region, Italy. Int J Environ Res Public Health 2021;18:1194. https://doi.org/10.3390/ijerph18031194.Search in Google Scholar PubMed PubMed Central
33. Yang, J, Wang, H, Du, H, Fang, H, Han, M, Xu, L, et al.. Serum perfluoroalkyl substances in relation to lipid metabolism in Chinese pregnant women. Chemosphere 2021;273:128566. https://doi.org/10.1016/j.chemosphere.2020.128566.Search in Google Scholar PubMed
34. Starling, AP, Engel, SM, Whitworth, KW, Richardson, DB, Stuebe, AM, Daniels, JL, et al.. Perfluoroalkyl substances and lipid concentrations in plasma during pregnancy among women in the Norwegian mother and child cohort study. Environ Int 2014;62:104–12. https://doi.org/10.1016/j.envint.2013.10.004.Search in Google Scholar PubMed PubMed Central
35. Vuong, AM, Braun, JM, Sjodin, A, Calafat, AM, Yolton, K, Lanphear, BP, et al.. Exposure to endocrine disrupting chemicals (EDCs) and cardiometabolic indices during pregnancy: the HOME study. Environ Int 2021;156:106747. https://doi.org/10.1289/isee.2021.p-700.Search in Google Scholar
36. Schuch, FB, Vancampfort, D, Richards, J, Rosenbaum, S, Ward, PB, Stubbs, B. Exercise as a treatment for depression: a meta-analysis adjusting for publication bias. J Psychiatr Res 2016;77:42–51. https://doi.org/10.1016/j.jpsychires.2016.02.023.Search in Google Scholar PubMed
37. Zhang, Y, Mustieles, V, Sun, Y, Oulhote, Y, Wang, YX, Messerlian, C. Association between serum per- and polyfluoroalkyl substances concentrations and common cold among children and adolescents in the United States. Environ Int 2022;164:107239. https://doi.org/10.1016/j.envint.2022.107239.Search in Google Scholar PubMed PubMed Central
38. Ding, N, Harlow, SD, Randolph, JFJr., Loch-Caruso, R, Park, SK. Perfluoroalkyl and polyfluoroalkyl substances (PFAS) and their effects on the ovary. Hum Reprod Update 2020;26:724–52. https://doi.org/10.1093/humupd/dmaa018.Search in Google Scholar PubMed PubMed Central
39. Bangma, J, Eaves, LA, Oldenburg, K, Reiner, JL, Manuck, T, Fry, RC. Identifying risk factors for levels of per- and polyfluoroalkyl substances (PFAS) in the placenta in a high-risk pregnancy cohort in North Carolina. Environ Sci Technol 2020;54:8158–66. https://doi.org/10.1021/acs.est.9b07102.Search in Google Scholar PubMed PubMed Central
40. Evich, MG, Davis, MJB, McCord, JP, Acrey, B, Awkerman, JA, Knappe, DRU, et al.. Per- and polyfluoroalkyl substances in the environment. Science 2022;375:eabg9065. https://doi.org/10.1126/science.abg9065.Search in Google Scholar PubMed PubMed Central
41. Wen, ZJ, Wei, YJ, Zhang, YF, Zhang, YF. A review of cardiovascular effects and underlying mechanisms of legacy and emerging per- and polyfluoroalkyl substances (PFAS). Arch Toxicol 2023;97:1195–245. https://doi.org/10.1007/s00204-023-03477-5.Search in Google Scholar PubMed
42. Pirillo, A, Casula, M, Olmastroni, E, Norata, GD, Catapano, AL. Global epidemiology of dyslipidaemias. Nat Rev Cardiol 2021;18:689–700. https://doi.org/10.1038/s41569-021-00541-4.Search in Google Scholar PubMed
43. Schillemans, T, Bergdahl, IA, Hanhineva, K, Shi, L, Donat-Vargas, C, Koponen, J, et al.. Associations of PFAS-related plasma metabolites with cholesterol and triglyceride concentrations. Environ Res 2023;216:114570. https://doi.org/10.1016/j.envres.2022.114570.Search in Google Scholar PubMed
44. Fadini, GP, Ceolotto, G, Pagnin, E, de Kreutzenberg, S, Avogaro, A. At the crossroads of longevity and metabolism: the metabolic syndrome and lifespan determinant pathways. Aging Cell 2011;10:10–7. https://doi.org/10.1111/j.1474-9726.2010.00642.x.Search in Google Scholar PubMed
45. Kinlen, D, Cody, D, O’Shea, D. Complications of obesity. QJM 2018;111:437–43. https://doi.org/10.1093/qjmed/hcx152.Search in Google Scholar PubMed
46. Sun, W, Zhang, X, Qiao, Y, Griffin, N, Zhang, H, Wang, L, et al.. Exposure to PFOA and its novel analogs disrupts lipid metabolism in zebrafish. Ecotoxicol Environ Saf 2023;259:115020. https://doi.org/10.1016/j.ecoenv.2023.115020.Search in Google Scholar PubMed
47. Wu, X, Liang, M, Yang, Z, Su, M, Yang, B. Effect of acute exposure to PFOA on mouse liver cells in vivo and in vitro. Environ Sci Pollut Res Int 2017;24:24201–6. https://doi.org/10.1007/s11356-017-0072-5.Search in Google Scholar PubMed
48. Das, KP, Wood, CR, Lin, MT, Starkov, AA, Lau, C, Wallace, KB, et al.. Perfluoroalkyl acids-induced liver steatosis: effects on genes controlling lipid homeostasis. Toxicology 2017;378:37–52. https://doi.org/10.1016/j.tox.2016.12.007.Search in Google Scholar PubMed PubMed Central
49. Kennedy, GLJr. Increase in mouse liver weight following feeding of ammonium perfluorooctanoate and related fluorochemicals. Toxicol Lett 1987;39:295–300. https://doi.org/10.1016/0378-4274(87)90245-1.Search in Google Scholar PubMed
50. Wan, HT, Zhao, YG, Wei, X, Hui, KY, Giesy, JP, Wong, CK. PFOS-induced hepatic steatosis, the mechanistic actions on beta-oxidation and lipid transport. Biochim Biophys Acta 2012;1820:1092–101. https://doi.org/10.1016/j.bbagen.2012.03.010.Search in Google Scholar PubMed
Supplementary Material
This article contains supplementary material (https://doi.org/10.1515/reveh-2023-0146).
© 2024 Walter de Gruyter GmbH, Berlin/Boston
