Abstract
Organophosphate esters (OPEs), as a class of emerging flame retardant and plasticizers, have attracted particular attention due to their ubiquitous existence in the environment and potential effects on human health. Here, we investigated the levels of OPEs in human serum and examined the role of demographic variables on the body burden of such compounds. Of 11 OPEs screened, 8 were detected in human serum samples collected from a population (n = 89) in Bohai Bay, North China. The ∑OPE concentrations ranged from 4.7 to 948 ng/g lipid weight (lw), with a median concentration of 243 ng/g lw. Tris(2-chloroethyl)phosphate (TCEP) was identified as the most abundant OPEs with a median concentration of 214 ng/g lw. The concentrations of the triphenyl phosphate (TPhP) in older adults were higher than those in young adults (p < 0.05), and lower concentrations of tri-iso-butyl phosphate (TIBP) were observed in female samples compared to males. Furthermore, significant differences were observed in tri-n-propyl phosphate (TPrP) concentrations between urban and rural residence groups (p < 0.05). This study provides important information on the accumulation potential of OPEs in human bodies and suggests the need for further investigation to understand the potential human health risk.
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References
Abbasi G, Saini A, Goosey E, Diamond ML (2016) Product screening for sources of halogenated flame retardants in Canadian house and office dust. Sci Total Environ 545–546:299–307. https://doi.org/10.1016/j.scitotenv.2015.12.028
Bekele TG, Zhao H, Wang Q, Chen J (2019) Bioaccumulation and trophic transfer of emerging organophosphate flame retardants in the marine food webs of Laizhou Bay, North China. Environ Sci Technol. https://doi.org/10.1021/acs.est.9b03687
Bentayeb M, Simoni M, Norback D, Baldacci S, Maio S, Viegi G, Annesi-Maesano I (2013) Indoor air pollution and respiratory health in the elderly. J Environ Sci Heal - Part A Toxic/Hazardous Subst Environ Eng 48:1783–1789. https://doi.org/10.1080/10934529.2013.826052
Butt CM, Congleton J, Hoffman K, Fang M, Stapleton HM (2014) Metabolites of organophosphate flame retardants and 2-ethylhexyl tetrabromobenzoate in urine from paired mothers and toddlers. Environ. Sci. Technol. 48:10432–10438. https://doi.org/10.1021/es5025299
Cao Z, Xu F, Covaci A, Wu M, Yu G, Wang B, Deng S, Huang J (2014) Differences in the seasonal variation of brominated and phosphorus flame retardants in office dust. Environ Int 65:100–106. https://doi.org/10.1016/j.envint.2013.12.011
Cequier E, Marcé RM, Becher G, Thomsen C (2014) A high-throughput method for determination of metabolites of organophosphate flame retardants in urine by ultra performance liquid chromatography-high resolution mass spectrometry. Anal Chim Acta 845:98–104. https://doi.org/10.1016/j.aca.2014.06.026
Chung H-W, Ding W-H (2009) Determination of organophosphate flame retardants in sediments by microwave-assisted extraction and gas chromatography-mass spectrometry with electron impact and chemical ionization. Anal Bioanal Chem 395:2325–2334. https://doi.org/10.1007/s00216-009-3139-4
Ding J, Xu Z, Huang W, Feng L, Yang F (2016) Organophosphate ester flame retardants and plasticizers in human placenta in Eastern China. Sci Total Environ 554–555:211–217. https://doi.org/10.1016/j.scitotenv.2016.02.171
Ding J, Deng T, Xu M, Wang S, Yang F (2018) Residuals of organophosphate esters in foodstuffs and implication for. Environ Pollut 233:986–991. https://doi.org/10.1016/j.envpol.2017.09.092
Dishaw LV, Powers CM, Ryde IT, Roberts SC, Seidler FJ, Slotkin TA, Stapleton HM (2011) Is the PentaBDE replacement, tris (1,3-dichloro-2-propyl) phosphate (TDCPP), a developmental neurotoxicant? Studies in PC12 cells. Toxicol Appl Pharmacol 256:281–289. https://doi.org/10.1016/j.taap.2011.01.005
Dishaw LV, Macaulay LJ, Roberts SC, Stapleton HM (2014) Exposures, mechanisms, and impacts of endocrine-active flame retardants. Curr Opin Pharmacol 19:125–133. https://doi.org/10.1016/j.coph.2014.09.018
Egloff C, Crump D, Porter E, Williams KL, Letcher RJ, Gauthier LT, Kennedy SW (2014) Tris(2-butoxyethyl)phosphate and triethyl phosphate alter embryonic development, hepatic mRNA expression, thyroid hormone levels, and circulating bile acid concentrations in chicken embryos. Toxicol Appl Pharmacol 279:303–310. https://doi.org/10.1016/j.taap.2014.06.024
Fromme H, Lahrz T, Kraft M, Fembacher L, Mach C, Dietrich S, Burkardt R, Völkel W, Göen T (2014) Organophosphate flame retardants and plasticizers in the air and dust in German daycare centers and human biomonitoring in visiting children (LUPE 3). Environ Int 71:158–163. https://doi.org/10.1016/j.envint.2014.06.016
Gao Z, Deng Y, Yuan W, He H, Yang S, Sun C (2014) Determination of organophosphorus flame retardants in fish by pressurized liquid extraction using aqueous solutions and solid-phase microextraction coupled with gas chromatography-flame photometric detector. J Chromatogr A 1366:31–37. https://doi.org/10.1016/j.chroma.2014.09.028
Geller AM, Zenick H (2005) Aging and the environment: a research framework. Environ Health Perspect 113:1257–1262. https://doi.org/10.1289/ehp.7569
Green, N., Schlabach, M., Bakke, T., Brevik, E.M., Dye, C., Herzke, D., Huber, S., 2007. Screening of selected metals and new organic contaminants 2007. Norway
He CT, Zheng J, Qiao L, Chen SJ, Yang JZ, Yuan JG, Yang ZY, Mai BX (2015) Occurrence of organophosphorus flame retardants in indoor dust in multiple microenvironments of southern China and implications for human exposure. Chemosphere 133:47–52. https://doi.org/10.1016/j.chemosphere.2015.03.043
He MJ, Lu JF, Ma JY, Wang H, Du XF (2018a) Organophosphate esters and phthalate esters in human hair from rural and urban areas, Chongqing, China: concentrations, composition profiles and sources in comparison to street dust. Environ Pollut 237:143–153. https://doi.org/10.1016/j.envpol.2018.02.040
He C, Toms LML, Thai P, Van den Eede N, Wang X, Li Y, Baduel C, Harden FA, Heffernan AL, Hobson P, Covaci A, Mueller JF (2018b) Urinary metabolites of organophosphate esters: concentrations and age trends in Australian children. Environ Int 111:124–130. https://doi.org/10.1016/j.envint.2017.11.019
Hong Y-C (2013) Aging society and environmental health challenges. Environ Health Perspect 121:2000–2001. https://doi.org/10.1289/ehp.1206334
Kang, H., Lee, J., Pyo, J., Choi, K., 2019. Urinary metabolites of organophosphate esters (OPEs) are associated with chronic kidney disease in the general US population, NHANES 2013–2014. Environ Int 131, 105034. https://doi.org/10.1016/j.envint.2019.105034
Kim JW, Isobe T, Chang KH, Amano A, Maneja RH, Zamora PB, Siringan FP, Tanabe S (2011) Levels and distribution of organophosphorus flame retardants and plasticizers in fishes from Manila Bay, the Philippines. Environ Pollut 159:3653–3659. https://doi.org/10.1016/j.envpol.2011.07.020
Kim JW, Isobe T, Muto M, Tue NM, Katsura K, Malarvannan G, Sudaryanto A, Chang KH, Prudente M, Viet PH, Takahashi S, Tanabe S (2014) Organophosphorus flame retardants (PFRs) in human breast milk from several Asian countries. Chemosphere 116:91–97. https://doi.org/10.1016/j.chemosphere.2014.02.033
Kuczmarski MF, Kuczmarski RJ, Najjar M (2001) Effects of age on validity of self reported height, weight, and body mass index: findings from the Third National Health and Nutrition Examination Survey, 1988–1994. Am Diet Assoc 101(1):28–34
Li J, Yu N, Zhang B, Jin L, Li M, Hu M, Zhang X, Wei S, Yu H (2014) Occurrence of organophosphate flame retardants in drinking water from China. Water Res 54:53–61. https://doi.org/10.1016/j.watres.2014.01.031
Li P, Li QX, Ma YL, Jin J, Wang Y, Tian Y (2015) Determination of organophosphate esters in human serum using gel permeation chromatograph and solid phase extraction coupled with gas chromatography-mass spectrometry. Chinese J Anal Chem 43:1033–1039. https://doi.org/10.1016/S1872-2040(15)60840-4
Li P, Jin J, Wang Y, Hu J, Xu M, Sun Y, Ma Y (2017) Concentrations of organophosphorus, polybromobenzene, and polybrominated diphenyl ether flame retardants in human serum, and relationships between concentrations and donor ages. Chemosphere 171:654–660. https://doi.org/10.1016/j.chemosphere.2016.12.126
Li J, Zhao L, Letcher RJ, Zhang Y, Jian K, Zhang J, Su G (2019) A review on organophosphate Ester (OPE) flame retardants and plasticizers in foodstuffs: levels, distribution, human dietary exposure, and future directions. Environ Int 127:35–51. https://doi.org/10.1016/j.envint.2019.03.009
Liu LY, Salamova A, He K, Hites RA (2015) Analysis of polybrominated diphenyl ethers and emerging halogenated and organophosphate flame retardants in human hair and nails. J Chromatogr A 1406:251–257. https://doi.org/10.1016/j.chroma.2015.06.003
Liu LY, He K, Hites RA, Salamova A (2016) Hair and nails as noninvasive biomarkers of human exposure to brominated and organophosphate flame retardants. Environ. Sci. Technol. 50:3065–3073. https://doi.org/10.1021/acs.est.5b05073
Liu Y, Luo X, Zapata P, Zeng Y, Mai B (2019) Organophosphorus fl ame retardants in a typical freshwater food web: bioaccumulation factors, tissue distribution, and trophic transfer*. Environ Pollut 255:113286. https://doi.org/10.1016/j.envpol.2019.113286
Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, Zhang J, Liang S, Wang XC (2014) A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci Total Environ 473–474:619–641. https://doi.org/10.1016/j.scitotenv.2013.12.065
Ma Y, Jin J, Li P, Xu M, Sun Y, Wang Y, Yuan H (2017) Organophosphate ester flame retardant concentrations and distributions in serum from inhabitants of Shandong, China, and changes between 2011 and 2015. Environ Toxicol Chem 36:414–421. https://doi.org/10.1002/etc.3554
Ma J, Zhu H, Kannan K (2019) Organophosphorus flame retardants and plasticizers in breast milk from the United States. Environ Sci Technol Lett 6:525–531. https://doi.org/10.1021/acs.estlett.9b00394
Marklund A, Andersson B, Haglund P (2003) Screening of organophosphorus compounds and their distribution in various indoor environments. Chemosphere 53:1137–1146. https://doi.org/10.1016/S0045-6535(03)00666-0
Marklund A, Andersson B, Haglund P (2005) Organophosphorus flame retardants and plasticizers in Swedish sewage treatment plants. Environ. Sci. Technol. 39:7423–7429. https://doi.org/10.1021/es051013l
Meeker JD, Stapleton HM (2010) House dust concentrations of organophosphate flame retardants in relation to hormone levels and semen quality parameters. Environ Health Perspect 118:318–323. https://doi.org/10.1289/ehp.0901332
Mendelsohn E, Hagopian A, Hoffman K, Butt CM, Lorenzo A, Congleton J, Webster TF, Stapleton HM (2016) Nail polish as a source of exposure to triphenyl phosphate. Environ Int 86:45–51. https://doi.org/10.1016/j.envint.2015.10.005
Milbrath MOG, Wenger Y, Chang CWCW, Emond C, Garabrant D, Gillespie BW, Jolliet O (2009) Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ Health Perspect 117:417–425. https://doi.org/10.1289/ehp.11781
Poma G, Glynn A, Malarvannan G, Covaci A, Darnerud PO (2017) Dietary intake of phosphorus flame retardants (PFRs) using Swedish food market basket estimations. Food Chem Toxicol 100:1–7. https://doi.org/10.1016/j.fct.2016.12.011
Reemtsma T, Lingott J, Roegler S (2011) Determination of 14 monoalkyl phosphates, dialkyl phosphates and dialkyl thiophosphates by LC-MS/MS in human urinary samples. Sci Total Environ 409:1990–1993. https://doi.org/10.1016/j.scitotenv.2011.01.032
Sasaki K, Takeda M, Uchiyama M (1981) Toxicity, absorption and elimination of phosphoric acid triesters by killifish and goldfish. Bull Environ Contam Toxicol 27–27:775–782. https://doi.org/10.1007/bf01611095
Schindler BK, Förster K, Angerer J (2009) Quantification of two urinary metabolites of organophosphorus flame retardants by solid-phase extraction and gas chromatography-tandem mass spectrometry. Anal Bioanal Chem 395:1167–1171. https://doi.org/10.1007/s00216-009-3064-6
St. John LE, Eldefrawi ME, Lisk DJ (1976) Studies of possible absorption of a flame retardant from treated fabrics worn by rats and humans. Bull Environ Contam Toxicol 15:192–197. https://doi.org/10.1007/BF01685160
Staaf T, Östman C (2005) Organophosphate triesters in indoor environments. J Environ Monit 7:883–887. https://doi.org/10.1039/b506631j
Sühring R, Wolschke H, Diamond ML, Jantunen LM, Scheringer M (2016) Distribution of organophosphate esters between the gas and particle phase − model predictions vs measured data. Environ. Sci. Technol. 50:6644–6651. https://doi.org/10.1021/acs.est.6b00199
Sundkvist AM, Olofsson U, Haglund P (2010) Organophosphorus flame retardants and plasticizers in marine and fresh water biota and in human milk. J Environ Monit 12:943. https://doi.org/10.1039/b921910b
Tajima S, Araki A, Kawai T, Tsuboi T, Ait Bamai Y, Yoshioka E, Kanazawa A, Cong S, Kishi R (2014) Detection and intake assessment of organophosphate flame retardants in house dust in Japanese dwellings. Sci Total Environ 478:190–199. https://doi.org/10.1016/j.scitotenv.2013.12.121
Thomas GO, Wilkinson M, Hodson S, Jones KC (2006) Organohalogen chemicals in human blood from the United Kingdom. Environ Pollut 141:30–41. https://doi.org/10.1016/j.envpol.2005.08.027
Van Den Eede N, Maho W, Erratico C, Neels H, Covaci A (2013) First insights in the metabolism of phosphate flame retardants and plasticizers using human liver fractions. Toxicol Lett 223:9–15. https://doi.org/10.1016/j.toxlet.2013.08.012
van der Veen I, de Boer J (2012) Phosphorus flame retardants: properties, production, environmental occurrence, toxicity and analysis. Chemosphere 88:1119–1153. https://doi.org/10.1016/j.chemosphere.2012.03.067
Wang X, He Y, Lin L, Zeng F, Luan T (2014) Application of fully automatic hollow fiber liquid phase microextraction to assess the distribution of organophosphate esters in the Pearl River estuaries. Sci Total Environ 470–471:263–269. https://doi.org/10.1016/j.scitotenv.2013.09.069
Wang R, Tang J, Xie Z, Mi W, Chen Y, Wolschke H, Tian C, Pan X, Luo Y, Ebinghaus R (2015) Occurrence and spatial distribution of organophosphate ester flame retardants and plasticizers in 40 rivers draining into the Bohai Sea, north China. Environ Pollut 198:172–178. https://doi.org/10.1016/j.envpol.2014.12.037
Wang Y, Hou M, Zhang Q, Wu X, Zhao H, Xie Q, Chen J (2017) Organophosphorus flame retardants and plasticizers in building and decoration materials and their potential burdens in newly decorated houses in China. Environ Sci Technol 51:10991–10999. https://doi.org/10.1021/acs.est.7b03367
Wensing M, Uhde E, Salthammer T (2005) Plastics additives in the indoor environment - flame retardants and plasticizers. Sci Total Environ 339:19–40. https://doi.org/10.1016/j.scitotenv.2004.10.028
World Health Organization (1991a) Triphenyl phosphate. In: Environmental Health Criteria 111. Switzerland, World Health Organization, Geneva
World Health Organization (1991b) Tri-n-butyl phosphate. In: Environmental health criteria 112. Switzerland, World Health Organization, Geneva
World Health Organization (1998) Flame retardants: tris-(chloropropyl) phosphate and tris(2-chloroethyl) phosphate. In: Environmental Health Criteria 209. Switzerland, World Health Organization, Geneva
Yang F, Ding J, Huang W, Xie W, Liu W (2014) Particle size-specific distributions and preliminary exposure assessments of organophosphate flame retardants in office air particulate matter. Environ. Sci. Technol. 48:63–70. https://doi.org/10.1021/es403186z
Zhang X, Zou W, Mu L, Chen Y, Ren C, Hu X, Zhou Q (2016) Rice ingestion is a major pathway for human exposure to organophosphate flame retardants ( OPFRs ) in China. J Hazard Mater 318:686–693. https://doi.org/10.1016/j.jhazmat.2016.07.055
Zhao, L., Jian, K., Su, H., Zhang, Y., Li, J., Letcher, R.J., 2019. Organophosphate esters (OPEs) in Chinese foodstuffs: dietary intake estimation via a market basket method, and suspect screening using high-resolution mass spectrometry. Environ Int 128, 343–352. https://doi.org/10.1016/j.envint.2019.04.055
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This work was supported by National Natural Science Foundation of China (81772812, 21677023, and 2018J138N096).
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All participants provided informed consent when they were enrolled and agreed to donate their serum sample for analysis. Ethical approval of this study was given by the Second Affiliated Hospital of Dalian Medical University Ethics Committee.
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Dute Gao and Jun Yang share first authorship of this study.
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Gao, D., Yang, J., Bekele, T.G. et al. Organophosphate esters in human serum in Bohai Bay, North China. Environ Sci Pollut Res 27, 2721–2729 (2020). https://doi.org/10.1007/s11356-019-07204-5
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DOI: https://doi.org/10.1007/s11356-019-07204-5