Abstract
Steroid estrogens have received worldwide attention and given rise to great challenges of aquatic ecosystems security, posing potential adverse effects on aquatic organisms and human health even at low levels (ng/L). The present study focused on understanding the mobility and abiotic transformation of estrone (E1) and estrone-3-sulfate (E1-3S) over spatial and time scales during soil transport. Column transport experiments showed that the migration capacity of E1-3S was far stronger than E1 in soil. The calculated groundwater ubiquity score and leachability index values also indicated the high leaching mobility of E1-3S. The hydrolysis of E1-3S and abiotic transformation into estradiol and estriol was observed in the sterilized soil. Furthermore, possible transformation products (e.g., SE239, E2378, E1 dimer538, E1-E2 dimer541) of E1 and E1-3S in soil were analyzed and identified after the column transport experiments. The estrogenic activity was estimated by 17β-estradiol equivalency values during the transport process in aqueous and soil phases. Additionally, the potential leaching transport to groundwater of E1-3S requires further critical concern.
Similar content being viewed by others
Data availability
Detailed data are available from the corresponding author.
Abbreviations
- SEs:
-
Steroid estrogens
- FEs:
-
Free estrogens
- CEs:
-
Conjugated estrogens
- E1:
-
Estrone
- 17β-E2:
-
17β-Estradiol
- CSEs:
-
Conjugated sulfate estrogens
- CGEs:
-
Conjugated glucuronide estrogens
- CS-GEs:
-
Conjugated sulfate-glucuronide estrogens
- ArySTS:
-
Arylsulfatase
- GUSB:
-
β-Glucuronidase
- WWTPs:
-
Wastewater treatment plants
- CAFOs:
-
Concentrated animal feeding operations
- E1-3S:
-
Estrone-3-sulfate
- EEQ:
-
17β-Estradiol equivalency
- 17α-E2:
-
17α-Estradiol
- E3:
-
Estriol
- HPLC:
-
High-performance liquid chromatography
- ACN:
-
Acetonitrile
- DCM:
-
Dichloromethane
- EtOAc:
-
Ethyl acetate
- MeOH:
-
Methanol
- PVs:
-
Pore volumes
- CK:
-
Control check
- LC–MS/MS:
-
Liquid chromatography coupled with tandem mass spectrometry
- SPE:
-
Solid-phase extraction
- MRM:
-
Multiple reaction monitoring
- ESI:
-
Electron spray ionization
- m/z :
-
Mass/charge ratio
- LOD:
-
Limit of detection
- LOQ:
-
Limit of quantitation
- GUS:
-
Groundwater ubiquity score
- LIX:
-
Leachability index
- K oc :
-
Organic carbon distribution coefficient
- 16α-OH-E1:
-
16α-Hydroxy-estrone
- DOM:
-
Dissolved organic matter
- EEF:
-
17β-Estradiol equivalent factor
- YES:
-
Yeast estrogen screen
- EC50:
-
Half maximal effective concentration
References:
Arlos, M. J., Parker, W. J., Bicudo, J. R., Law, P., Hicks, K. A., Fuzzen, M. L. M., Andrews, S. A., & Servos, M. R. (2018). Modeling the exposure of wild fish to endocrine active chemicals: Potential linkages of total estrogenicity to field-observed intersex. Water Research, 139, 187–197. https://doi.org/10.1016/j.watres.2018.04.005
Bai, X., Casey, F. X. M., Hakk, H., DeSutter, T. M., Oduor, P. G., & Khan, E. (2015). Sorption and degradation of 17β-estradiol-17-sulfate in sterilized soil–water systems. Chemosphere, 119, 1322–1328. https://doi.org/10.1016/j.chemosphere.2014.02.016
Ben, W., Zhu, B., Yuan, X., Zhang, Y., Yang, M., & Qiang, Z. (2017). Transformation and fate of natural estrogens and their conjugates in wastewater treatment plants: Influence of operational parameters and removal pathways. Water Research, 124, 244–250. https://doi.org/10.1016/j.watres.2017.07.065
Bexfield, L. M., Toccalino, P. L., Belitz, K., Foreman, W. T., & Furlong, E. T. (2019). Hormones and pharmaceuticals in groundwater used as a source of drinking water across the united states. Environmental Science and Technology, 53, 2950–2960. https://doi.org/10.1021/acs.est.8b05592
Biswas, S., Kranz, W. L., Shapiro, C. A., Snow, D. D., Bartelt-Hunt, S. L., Mamo, M., Tarkalson, D. D., Zhang, T. C., Shelton, D. P., van Donk, S. J., & Mader, T. L. (2017). Effect of rainfall timing and tillage on the transport of steroid hormones in runoff from manure amended row crop fields. Journal of Hazardous Materials, 324, 436–447. https://doi.org/10.1016/j.jhazmat.2016.11.009
Casey, F. X. M., Hakk, H., & DeSutter, T. M. (2020). Free and conjugated estrogens detections in drainage tiles and wells beneath fields receiving swine manure slurry. Environmental Pollution. https://doi.org/10.1016/j.envpol.2019.113384
Casey, F. X. M., Selbie, D., Hakk, H., & Richards, K. G. (2019). Leaching of free and conjugate natural estrogens in soil monoliths. Water, Air, and Soil Pollution, 230, 1–12. https://doi.org/10.1007/s11270-019-4079-z
Chen, X., & Hu, J. (2010). Adsorption of natural estrogens and their conjugates by activated sludge. Water Air and Soil Pollution, 206, 251–261. https://doi.org/10.1007/s11270-009-0102-0
Yu-nv, Dai, Dan, A., Yang, Y., Nora Fung-yee, T., Yi-Ping, T., & Xiao-Yan, T. (2016). Factors affecting behavior of phenolic endocrine disruptors, estrone and estradiol, in constructed wetlands for domestic sewage treatment. Environmental Science and Technology, 50(21), 11844–11852. https://doi.org/10.1021/acs.est.6b02026
Delli Compagni, R., Gabrielli, M., Polesel, F., Turolla, A., Trapp, S., Vezzaro, L., & Antonelli, M. (2020). Risk assessment of contaminants of emerging concern in the context of wastewater reuse for irrigation: An integrated modelling approach. Chemosphere. https://doi.org/10.1016/j.chemosphere.2019.125185
Du, B. H., Fan, G. D., Yu, W. W., Yang, S., Zhou, J. J., & Luo, J. (2020). Occurrence and risk assessment of steroid estrogens in environmental water samples: A five-year worldwide perspective. Environmental Pollution. https://doi.org/10.1016/j.envpol.2020.115405
Escher, B. I., Stapleton, H. M., & Schymanski, E. L. (2020). Tracking complex mixtures of chemicals in our changing environment. Science, 367, 388–392. https://doi.org/10.1126/science.aay6636
Gadd, J. B., Tremblay, L. A., & Northcott, G. L. (2010). Steroid estrogens, conjugated estrogens and estrogenic activity in farm dairy shed effluents. Environmental Pollution, 158, 730–736. https://doi.org/10.1016/j.envpol.2009.10.015
Goeppert, N., Dror, I., & Berkowitz, B. (2014). Detection, fate and transport of estrogen family hormones in soil. Chemosphere, 95, 336–345. https://doi.org/10.1016/j.chemosphere.2013.09.039
Goeppert, N., Dror, I., & Berkowitz, B. (2015). Fate and transport of free and conjugated estrogens during soil passage. Environmental Pollution, 206, 80–87. https://doi.org/10.1016/j.envpol.2015.06.024
Goeppert, N., Dror, I., & Berkowitz, B. (2017). Spatial and temporal distribution of free and conjugated estrogens during soil column transport. CLEAN-Soil Air Water, 45, 12. https://doi.org/10.1002/clen.201600048
Guardian, M. G. E., & Aga, D. S. (2019). Mineralization and biotransformation of estrone in simulated poultry litter and cow manure runoff water. Journal of Environmental Quality, 48, 1120–1125. https://doi.org/10.2134/jeq2019.01.0023
Gustafson, D. I. (1989). Groundwater ubiquity score a simple method for assessing pesticide leachability. Environmental Toxicology and Chemistry, 8, 339–357
Hakk, H., Sikora, L., & Casey, F. X. M. (2018). Fate of estrone in laboratory-scale constructed wetlands. Ecological Engineering, 111, 60–68. https://doi.org/10.1016/j.ecoleng.2017.11.005
Hom-Diaz, A., Llorca, M., Rodríguez-Mozaz, S., Vicent, T., Barceló, D., & Blánquez, P. (2015). Microalgae cultivation on wastewater digestate: Β-estradiol and 17α-ethynylestradiol degradation and transformation products identification. Journal of Environmental Management, 155, 106–113. https://doi.org/10.1016/j.jenvman.2015.03.003
Hutchins, S. R., White, M. V., Hudson, F. M., & Fine, D. D. (2007). Analysis of lagoon samples from different concentrated animal feeding operations for estrogens and estrogen conjugates. Environmental Science and Technology. https://doi.org/10.1021/es062234
Kumar, V., Johnson, A. C., Nakada, N., Yamashita, N., & Tanaka, H. (2012). De-conjugation behavior of conjugated estrogens in the raw sewage, activated sludge and river water. Journal of Hazardous Materials, 227–228, 49–54. https://doi.org/10.1016/j.jhazmat.2012.04.078
Li, Y., Yang, Y., Shen, F., Tian, D., Zeng, Y., Yang, G., Zhang, Y., & Deng, S. (2019). Partitioning biochar properties to elucidate their contributions to bacterial and fungal community composition of purple soil. Science of the Total Environment, 648, 1333–1341. https://doi.org/10.1016/j.scitotenv.2018.08.222
Liu, X., Shi, J., Bo, T., Meng, Y., Zhan, X., Zhang, M., & Zhang, Y. (2017). Distributions and ecological risk assessment of estrogens and bisphenol a in an arid and semiarid area in northwest China. Environmental Science and Pollution Research, 24, 7216–7225. https://doi.org/10.1007/s11356-017-8434-6
Liu, Z., Lu, G., Yin, H., Dang, Z., & Rittmann, B. (2015). Removal of natural estrogens and their conjugates in municipal wastewater treatment plants: A critical review. Environmental Science and Technology, 49, 5288–5300. https://doi.org/10.1021/acs.est.5b00399
Ma, L., & Yates, S. R. (2018a). Degradation and metabolite formation of 17ß-estradiol-3-glucuronide and 17ß-estradiol-3-sulphate in river water and sediment. Water Research, 139, 1–9. https://doi.org/10.1016/j.watres.2018.03.071
Ma, L., & Yates, S. R. (2018b). Dissolved organic matter and estrogen interactions regulate estrogen removal in the aqueous environment: A review. Science of the Total Environment, 640–641, 529–542. https://doi.org/10.1016/j.scitotenv.2018.05.301
Machalová Šišková, K., Jančula, D., Drahoš, B., Machala, L., Babica, P., Alonso, P. G., Trávníček, Z., Tuček, J., Maršálek, B., Sharma, V. K., & Zbořil, R. (2016). High-valent iron (FeVI, FeV, and FeIV) species in water: Characterization and oxidative transformation of estrogenic hormones. Physical Chemistry Chemical Physics, 18, 18802–18810. https://doi.org/10.1039/C6CP02216B
Marfil-Vega, R., Suidan, M. T., & Mills, M. A. (2012). Assessment of the abiotic transformation of 17β-estradiol in the presence of vegetable matter – II: The role of molecular oxygen. Chemosphere, 87, 521–526. https://doi.org/10.1016/j.chemosphere.2011.12.054
Mina, O., Gall, H. E., Elliott, H. A., Watson, J. E., Mashtare, M. L., Langkilde, T., Harper, J. P., & Boyer, E. W. (2018). Estrogen occurrence and persistence in vernal pools impacted by wastewater irrigation practices. Agriculture, Ecosystems and Environment, 257, 103–112. https://doi.org/10.1016/j.agee.2018.01.022
Neale, P. A., Escher, B. I., & Schäfer, A. I. (2008). Quantification of solute–solute interactions using Negligible-Depletion Solid-Phase microextraction: Measuring the affinity of estradiol to bulk organic matter. Environmental Science and Technology, 42, 2886–2892. https://doi.org/10.1021/es0717313
Nkoom, M., Lu, G., & Liu, J. (2018). Occurrence and ecological risk assessment of pharmaceuticals and personal care products in Taihu Lake, China: A review. Environmental Science: Processes and Impacts, 20, 1640–1648. https://doi.org/10.1039/C8EM00327K
Qin, C., Troya, D., Shang, C., Hildreth, S., Helm, R., & Xia, K. (2015). Surface catalyzed oxidative oligomerization of 17β-Estradiol by fe3+ -Saturated montmorillonite. Environmental Science and Technology, 49, 956–964. https://doi.org/10.1021/es504815t
Qu, S., Kolodziej, E. P., & Cwiertny, D. M. (2014). Sorption and Mineral-Promoted transformation of synthetic hormone growth promoters in soil systems. Journal of Agricultural and Food Chemistry, 62, 12277–12286. https://doi.org/10.1021/jf5035527
Scherr, F. F., & Sarmah, A. K. (2011). Simultaneous analysis of free and sulfo-conjugated steroid estrogens in artificial urine solution and agricultural soils by high-performance liquid chromatography. Journal of Environmental Science and Health, Part B, 46, 763–772. https://doi.org/10.1080/03601234.2012.597702
Scherr, F. F., Sarmah, A. K., Di, H. J., & Cameron, K. C. (2009). Sorption of estrone and estrone-3-sulfate from CaCl2 solution and artificial urine in pastoral soils of New Zealand. Environmental Toxicology and Chemistry, 28, 2564–2571. https://doi.org/10.1897/08-534.1
Sheng, D. G., Xu, C., Xu, L., Qiu, Y., & Zhou, H. (2009). Abiotic oxidation of 17β-estradiol by soil manganese oxides. Environmental Pollution, 157, 2710–2715. https://doi.org/10.1016/j.envpol.2009.04.030
Shrestha, S. L., Casey, F. X. M., Hakk, H., Smith, D. J., & Padmanabhan, G. (2012). Fate and transformation of an estrogen conjugate and its metabolites in agricultural soils. Environmental Science and Technology, 46, 11047–11053. https://doi.org/10.1021/es3021765
Spadotto, C.A. (2002). Screening method for assessing pesticide leaching potential. Pesticidas: ecotoxicol. e Meio Ambiente, 12:69–78.
Stanford, B. D., Amoozegar, A., & Weinberg, H. S. (2010). The impact of co-contaminants and septic system effluent quality on the transport of estrogens and nonylphenols through soil. Water Research, 44, 1598–1606. https://doi.org/10.1016/j.watres.2009.11.011
Sun, Y., Huang, H., Sun, Y., Wang, C., Shi, X. L., Hu, H. Y., Kameya, T., & Fujie, K. (2013). Ecological risk of estrogenic endocrine disrupting chemicals in sewage plant effluent and reclaimed water. Environmental Pollution, 180, 339–344. https://doi.org/10.1016/j.envpol.2013.05.006
Välitalo, P., Perkola, N., Seiler, T., Sillanpää, M., Kuckelkorn, J., Mikola, A., Hollert, H., & Schultz, E. (2016). Estrogenic activity in Finnish municipal wastewater effluents. Water Research, 88, 740–749. https://doi.org/10.1016/j.watres.2015.10.056
Wang, X., Yao, J., Wang, S., Pan, X., Xiao, R., Huang, Q., Wang, Z., & Qu, R. (2018). Phototransformation of estrogens mediated by Mn(III), not by reactive oxygen species, in the presence of humic acids. Chemosphere, 201, 224–233. https://doi.org/10.1016/j.chemosphere.2018.03.003
Yang, L., Cheng, Q., Tam, N. F., Lin, L., Su, W., & Luan, T. (2016). Contributions of abiotic and biotic processes to the aerobic removal of phenolic Endocrine-Disrupting chemicals in a simulated estuarine aquatic environment. Environmental Science and Technology, 50, 4324–4334. https://doi.org/10.1021/acs.est.5b06196
Yang, S., Yu, W. W., Yang, L., Du, B. H., Chen, S. L., Sun, W. Z., Jiang, H., Xie, M. Y., & Tang, J. J. (2021). Occurrence and fate of steroid estrogens in a Chinese typical concentrated dairy farm and slurry irrigated soil. Journal of Agricultural and Food Chemistry, 69, 67–77. https://doi.org/10.1021/acs.jafc.0c05068
Yao, B., Li, R., Yan, S., Chan, S., & Song, W. (2018). Occurrence and estrogenic activity of steroid hormones in Chinese streams: A nationwide study based on a combination of chemical and biological tools. Environment International, 118, 1–8. https://doi.org/10.1016/j.envint.2018.05.026
Yu, W. W., Du, B. H., Fan, G. D., Yang, S., Yang, L., & Zhang, M. N. (2020a). Spatio-temporal distribution and transformation of 17α- and 17β-estradiol in sterilized soil: A column experiment. Journal of Hazardous Materials. https://doi.org/10.1016/j.jhazmat.2020.122092
Yu, W. W., Du, B. H., Yang, L., Zhang, Z., Yang, C., Yuan, S. C., & Zhang, M. N. (2019). Occurrence, sorption, and transformation of free and conjugated natural steroid estrogens in the environment. Environmental Science and Pollution Research, 26, 9443–9468. https://doi.org/10.1007/s11356-019-04402-z
Yu, W. W., Yang, S., Du, B. H., Zhang, Z., Xie, M. Y., Chen, Y., Zhao, C. J., Chen, X. Y., & Li, Q. (2020b). Feasibility and mechanism of enhanced 17β-estradiol degradation by the nano Zero Valent Iron-citrate system. Journal of Hazardous Materials. https://doi.org/10.1016/j.jhazmat.2020.122657
Zhang, F., Xie, Y., Li, X., Wang, D., Yang, L., & Nie, Z. (2015). Accumulation of steroid hormones in soil and its adjacent aquatic environment from a typical intensive vegetable cultivation of North China. Science of the Total Environment, 538, 423–430. https://doi.org/10.1016/j.scitotenv.2015.08.067
Zhang, H., Shi, J., Liu, X., Zhan, X., & Chen, Q. (2014a). Occurrence and removal of free estrogens, conjugated estrogens, and bisphenol a in manure treatment facilities in East China. Water Research, 58, 248–257. https://doi.org/10.1016/j.watres.2014.03.074
Zhang, Q. Q., Zhao, J., Ying, G., Liu, Y., & Pan, C. (2014b). Emission estimation and multimedia fate modeling of seven steroids at the river basin scale in china. Environmental Science and Technology, 48, 7982–7992. https://doi.org/10.1021/es501226h
Zheng, W., Zou, Y., Li, X., & Machesky, M. L. (2013). Fate of estrogen conjugate 17α-estradiol-3-sulfate in dairy wastewater: Comparison of aerobic and anaerobic degradation and metabolite formation. Journal of Hazardous Materials, 258–259, 109–115. https://doi.org/10.1016/j.jhazmat.2013.04.038
Zhong, C., Zhao, H., Cao, H., & Huang, Q. (2019). Polymerization of micropollutants in natural aquatic environments: A review. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2019.133751
Funding
The research was funded by the National Natural Science Foundation of China (51608079), National Engineering Technology Research Center for Inland Waterway Regulation and Key Laboratory of Hydraulic & Waterway Engineering of the Ministry of Education Open Funding (SLK2018A04), Basic and Frontier Research Program of Chongqing Municipality (cstc2017jcyjAX0104), and Graduate Education Innovation Funding of School of River and Ocean Engineering, Chongqing Jiaotong University (YC2019004; YC2019008).
Author information
Authors and Affiliations
Contributions
Weiwei Yu conceived and designed the experiments; Banghao Du and Weiwei Yu analyzed the data and wrote the paper; Banghao Du, Lun Yang, and Shuo Yang performed the experiments; Gongduan Fan, Hui Jiang, Shenglan Bi, and Cheng Yu reviewed and edited the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests.
Consent for publication
Informed consent was obtained from all individual participants included in the study.
Human or animal rights
This study contains no animal research.
Informed consent
Informed consent was obtained from all individual participants in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Du, B., Yu, W., Yang, L. et al. Migration and abiotic transformation of estrone (E1) and estrone-3-sulfate (E1-3S) during soil column transport. Environ Geochem Health 44, 911–924 (2022). https://doi.org/10.1007/s10653-021-00968-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-021-00968-1