Abstract
Contamination of waters, soils, sediments and other environmental media by steroid estrogens is an emerging health issue because estrogens exhibit toxic effects on fishes and animals. Levels of steroid estrogens vary widely, ranging from below the detection limit to hundreds of nanograms per liter. Estrogens alter hormone levels and the homeostasis system of living organisms, they increase the risk of cardiovascular diseases, prostate cancer and breast cancer in humans and they may induce reproductive disorders, fetal malformations and feminization of males. Here, we review detection methods of steroid estrogens in water samples. Methods mainly include chemical analysis, immunoassays and bioassays. Advanced sensors increase the selectivity and sensitivity of electrochemical assays. For instance, graphene-based sensors can decrease the detection limit to 50 fM, though estrogen analogues may interfere. Immunoassays such as ELISA have the advantages of high sensitivity, fast analysis speed and wide applicability from 2 to 4000 ng/L, though it is susceptible to cross-reactivity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adeel M, Song X, Wang Y, Francis D, Yang Y (2017) Environmental impact of estrogens on human, animal and plant life: a critical review. Environ Int 99:107–119. https://doi.org/10.1016/j.envint.2016.12.010
Aichner B, Bussian B, Lehnik-Habrink P, Hein S (2013) Levels and spatial distribution of persistent organic pollutants in the environment: a case study of German forest soils. Environ Sci Technol 47(22):12703–12714. https://doi.org/10.1021/es4019833
Alam AU, Qin Y, Catalano M, Wang L, Kim MJ, Howlader MMR, Hu NX, Deen MJ (2018) Tailoring MWCNTs and beta-cyclodextrin for sensitive detection of acetaminophen and estrogen. ACS Appl Mater Interfaces 10(25):21411–21427. https://doi.org/10.1021/acsami.8b04639
Andaluri G, Suri RP, Kumar K (2012) Occurrence of estrogen hormones in biosolids, animal manure and mushroom compost. Environ Monit Assess 184(2):1197–1205. https://doi.org/10.1007/s10661-011-2032-8
Arnold KE, Brown AR, Ankley GT, Sumpter JP (2014) Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2013.0569
Arnon S, Dahan O, Elhanany S, Cohen K, Pankratov I, Gross A, Ronen Z, Baram S, Shore LS (2008) Transport of testosterone and estrogen from dairy-farm waste lagoons to groundwater. Environ Sci Technol 42(15):5521–5526
Avbersek M, Zegura B, Filipic M, Heath E (2011) Integration of GC-MSD and ER-Calux(R) assay into a single protocol for determining steroid estrogens in environmental samples. Sci Total Environ 409(23):5069–5075. https://doi.org/10.1016/j.scitotenv.2011.08.020
Avbersek M, Zegura B, Filipic M, Uranjek-Zevart N, Heath E (2013) Determination of estrogenic potential in waste water without sample extraction. J Hazard Mater 260:527–533. https://doi.org/10.1016/j.jhazmat.2013.06.009
Backe WJ (2015) An ultrasensitive (parts-per-quadrillion) and SPE-free method for the quantitative analysis of estrogens in surface water. Environ Sci Technol 49(24):14311–14318. https://doi.org/10.1021/acs.est.5b04949
Bakos K, Kovacs R, Balogh E, Sipos DK, Reining M, Gyomorei-Neuberger O, Balazs A, Kriszt B, Bencsik D, Csepeli A, Gazsi G, Hadzhiev Y, Urbanyi B, Mueller F, Kovacs B, Csenki Z (2019) Estrogen sensitive liver transgenic zebrafish (Danio rerio) line (Tg(vtg1:mCherry)) suitable for the direct detection of estrogenicity in environmental samples. Aquat Toxicol 208:157–167. https://doi.org/10.1016/j.aquatox.2019.01.008
Bannan CC, Calabro G, Kyu DY, Mobley DL (2016) Calculating partition coefficients of small molecules in octanol/water and cyclohexane/water. J Chem Theory Comput 12(8):4015–4024. https://doi.org/10.1021/acs.jctc.6b00449
Barton H, Berbel-Filho WM, Consuegra S, Francis L, Tizaoui C, Conlan RS, Teixeira SR (2018) Ultrasensitive environmental assessment of xeno-estrogens in water samples using label-free graphene immunosensors. Anal Biochem 548:102–108. https://doi.org/10.1016/j.ab.2018.02.027
Beck IC, Bruhn R, Gandrass J (2006) Analysis of estrogenic activity in coastal surface waters of the Baltic Sea using the yeast estrogen screen. Chemosphere 63(11):1870–1878. https://doi.org/10.1016/j.chemosphere.2005.10.022
Bekic SS, Marinovic MA, Petri ET, Sakac MN, Nikolic AR, Kojic VV, Celic AS (2018) Identification of d-seco modified steroid derivatives with affinity for estrogen receptor alpha and beta isoforms using a non-transcriptional fluorescent cell assay in yeast. Steroids 130:22–30. https://doi.org/10.1016/j.steroids.2017.12.002
Bilal M, Kazi TG, Afridi HI, Ali J, Baig JA, Arain MB, Khan M (2017) A new tunable dispersive liquid-liquid micro extraction method developed for the simultaneous preconcentration of lead and cadmium from lakes water: a multivariate study. Spectrochim Acta A Mol Biomol Spectrosc 183:417–424. https://doi.org/10.1016/j.saa.2017.04.037
Botelho JC, Ribera A, Cooper HC, Vesper HW (2016) Evaluation of an isotope dilution HPLC tandem mass spectrometry candidate reference measurement procedure for total 17-beta estradiol in human serum. Anal Chem 88(22):11123–11129. https://doi.org/10.1021/acs.analchem.6b03220
Bowerman WW, Best DA, Grubb TG, Sikarskie JG, Giesy JP (2000) Assessment of environmental endocrine disruptors in bald eagles of the Great Lakes. Chemosphere 41(10):1569–1574. https://doi.org/10.1016/s0045-6535(00)00014-x
Brennan JC, Bassal A, He G, Denison MS (2016) Development of a recombinant human ovarian (BG1) cell line containing estrogen receptor alpha and beta for improved detection of estrogenic/antiestrogenic chemicals. Environ Toxicol Chem 35(1):91–100. https://doi.org/10.1002/etc.3146
Briciu RD, Kot-Wasik A, Namiesnik J (2009) Analytical challenges and recent advances in the determination of estrogens in water environments. J Chromatogr Sci 47(2):127–139. https://doi.org/10.1093/chromsci/47.2.127
Campbell CG, Borglin SE, Green FB, Grayson A, Wozei E, Stringfellow WT (2006) Biologically directed environmental monitoring, fate, and transport of estrogenic endocrine disrupting compounds in water: a review. Chemosphere 65(8):1265–1280. https://doi.org/10.1016/j.chemosphere.2006.08.003
Cargouet M, Perdiz D, Mouatassim-Souali A, Tamisier-Karolak S, Levi Y (2004) Assessment of river contamination by estrogenic compounds in Paris area (France). Sci Total Environ 324(1–3):55–66. https://doi.org/10.1016/j.scitotenv.2003.10.035
Celic M, Insa S, Skrbic B, Petrovic M (2017) Development of a sensitive and robust online dual column liquid chromatography-tandem mass spectrometry method for the analysis of natural and synthetic estrogens and their conjugates in river water and wastewater. Anal Bioanal Chem 409(23):5427–5440. https://doi.org/10.1007/s00216-017-0408-5
Chen CY, Wen TY, Wang GS, Cheng HW, Lin YH, Lien GW (2007) Determining estrogenic steroids in Taipei waters and removal in drinking water treatment using high-flow solid-phase extraction and liquid chromatography/tandem mass spectrometry. Sci Total Environ 378(3):352–365. https://doi.org/10.1016/j.scitotenv.2007.02.038
Chen B, Huang Y, He M, Hu B (2013) Hollow fiber liquid-liquid-liquid microextraction combined with high performance liquid chromatography-ultraviolet detection for the determination of various environmental estrogens in environmental and biological samples. J Chromatogr A 1305:17–26. https://doi.org/10.1016/j.chroma.2013.06.029
Chen XH, Pan SD, Ye MJ, Li XP, Zhao YG, Jin MC (2016) Magnetic solid-phase extraction based on a triethylenetetramine-functionalized magnetic graphene oxide composite for the detection of ten trace phenolic environmental estrogens in environmental water. J Sep Sci 39(4):762–768. https://doi.org/10.1002/jssc.201501069
Chu WL, Shiizaki K, Kawanishi M, Kondo M, Yagi T (2009) Validation of a new yeast-based reporter assay consisting of human estrogen receptors alpha/beta and coactivator SRC-1: application for detection of estrogenic activity in environmental samples. Environ Toxicol 24(5):513–521. https://doi.org/10.1002/tox.20473
Cocci P, Palermo FA, Quassinti L, Bramucci M, Miano A, Mosconi G (2016) Determination of estrogenic activity in the river Chienti (Marche Region, Italy) by using in vivo and in vitro bioassays. J Environ Sci (China) 43:48–53. https://doi.org/10.1016/j.jes.2015.07.018
Cunha SC, Oliveira C, Fernandes JO (2017) Development of QuEChERS-based extraction and liquid chromatography-tandem mass spectrometry method for simultaneous quantification of bisphenol A and tetrabromobisphenol A in seafood: fish, bivalves, and seaweeds. Anal Bioanal Chem 409(1):151–160. https://doi.org/10.1007/s00216-016-9980-3
Dewalque L, Charlier C (2012) Masculine fertility threatened by the presence of endocrine disruptors in environment? Rev Med Liege 67(5–6):243–249
do Nascimento MTL, Santos ADO, Felix LC, Gomes G, de Oliveira ESM, da Cunha DL, Vieira N, Hauser-Davis RA, Baptista Neto JA, Bila DM (2018) Determination of water quality, toxicity and estrogenic activity in a nearshore marine environment in Rio de Janeiro, Southeastern Brazil. Ecotoxicol Environ Safy 149:197–202. https://doi.org/10.1016/j.ecoenv.2017.11.045
Drzymala SS, Weiz S, Heinze J, Marten S, Prinz C, Zimathies A, Garbe LA, Koch M (2015) Automated solid-phase extraction coupled online with HPLC-FLD for the quantification of zearalenone in edible oil. Anal Bioanal Chem 407(12):3489–3497. https://doi.org/10.1007/s00216-015-8541-5
Dsikowitzky L, Schäfer L, Ariyani F, Irianto HE, Schwarzbauer J (2017) Evidence of massive river pollution in the tropical megacity Jakarta as indicated by faecal steroid occurrence and the seasonal flushing out into the coastal ecosystem. Environ Chem Lett 15(4):703–708. https://doi.org/10.1007/s10311-017-0641-3
Dubey DK, Pardasani D, Gupta AK, Palit M, Kanaujia PK, Tak V (2006) Hollow fiber-mediated liquid-phase microextraction of chemical warfare agents from water. J Chromatogr A 1107(1–2):29–35. https://doi.org/10.1016/j.chroma.2005.12.095
Escher BI, Berg M, Muhlemann J, Schwarz MA, Hermens JL, Vaes WH, Schwarzenbach RP (2002) Determination of liposome/water partition coefficients of organic acids and bases by solid-phase microextraction. Analyst 127(1):42–48
Fan L, Zhao G, Shi H, Liu M, Wang Y, Ke H (2014) A femtomolar level and highly selective 17beta-estradiol photoelectrochemical aptasensor applied in environmental water samples analysis. Environ Sci Technol 48(10):5754–5761. https://doi.org/10.1021/es405685y
Fang TY, Praveena SM, deBurbure C, Aris AZ, Ismail SNS, Rasdi I (2016) Analytical techniques for steroid estrogens in water samples—a review. Chemosphere 165:358–368. https://doi.org/10.1016/j.chemosphere.2016.09.051
Fayad PB, Prevost M, Sauve S (2013) On-line solid-phase extraction coupled to liquid chromatography tandem mass spectrometry optimized for the analysis of steroid hormones in urban wastewaters. Talanta 115:349–360. https://doi.org/10.1016/j.talanta.2013.05.038
Ferguson EM, Allinson M, Allinson G, Swearer SE, Hassell KL (2013) Fluctuations in natural and synthetic estrogen concentrations in a tidal estuary in south-eastern Australia. Water Res 47(4):1604–1615. https://doi.org/10.1016/j.watres.2012.12.020
Findlay JW, Smith WC, Lee JW, Nordblom GD, Das I, DeSilva BS, Khan MN, Bowsher RR (2000) Validation of immunoassays for bioanalysis: a pharmaceutical industry perspective. J Pharm Biomed Anal 21(6):1249–1273
Friesen CN, Ramsey ME, Cummings ME (2017) Differential sensitivity to estrogen-induced opsin expression in two poeciliid freshwater fish species. Gen Comp Endocrinol 246:200–210. https://doi.org/10.1016/j.ygcen.2016.12.009
Gan SD, Patel KR (2013) Enzyme immunoassay and enzyme-linked immunosorbent assay. J Investig Dermatol 133(9):e12. https://doi.org/10.1038/jid.2013.287
Gao D, Li Z, Wen Z, Ren N (2014) Occurrence and fate of phthalate esters in full-scale domestic wastewater treatment plants and their impact on receiving waters along the Songhua River in China. Chemosphere 95:24–32. https://doi.org/10.1016/j.chemosphere.2013.08.009
Garcia-Corcoles MT, Cipa M, Rodriguez-Gomez R, Rivas A, Olea-Serrano F, Vilchez JL, Zafra-Gomez A (2018) Determination of bisphenols with estrogenic activity in plastic packaged baby food samples using solid-liquid extraction and clean-up with dispersive sorbents followed by gas chromatography tandem mass spectrometry analysis. Talanta 178:441–448. https://doi.org/10.1016/j.talanta.2017.09.067
Gier K, Preininger C, Sauer U (2017) A chip for estrogen receptor action: detection of biomarkers released by MCF-7 cells through Estrogenic and anti-estrogenic effects. Sensors (Basel). https://doi.org/10.3390/s17081760
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
Goh SX, Lee HK (2017) An alternative perspective of hollow fiber-mediated extraction: bundled hollow fiber array-liquid-phase microextraction with sonication-assisted desorption and liquid chromatography-tandem mass spectrometry for determination of estrogens in aqueous matrices. J Chromatogr A 1488:26–36. https://doi.org/10.1016/j.chroma.2017.01.081
Gonzalez A, Avivar J, Cerda V (2015) Estrogens determination in wastewater samples by automatic in-syringe dispersive liquid-liquid microextraction prior silylation and gas chromatography. J Chromatogr A 1413:1–8. https://doi.org/10.1016/j.chroma.2015.08.031
Grange RD, Thompson JP, Lambert DG (2014) Radioimmunoassay, enzyme and non-enzyme-based immunoassays. Br J Anaesth 112(2):213–216. https://doi.org/10.1093/bja/aet293
Grover DP, Zhang ZL, Readman JW, Zhou JL (2009) A comparison of three analytical techniques for the measurement of steroidal estrogens in environmental water samples. Talanta 78(3):1204–1210. https://doi.org/10.1016/j.talanta.2008.12.049
Guo W, Van Langenhove K, Denison MS, Baeyens W, Elskens M, Gao Y (2017) Estrogenic activity measurements in water using diffusive gradients in thin-film coupled with an estrogen bioassay. Anal Chem 89(24):13357–13364. https://doi.org/10.1021/acs.analchem.7b03537
Habauzit D, Boudot A, Kerdivel G, Flouriot G, Pakdel F (2010) Development and validation of a test for environmental estrogens: checking xeno-estrogen activity by CXCL12 secretion in BREAST CANCER CELL LINES (CXCL-test). Environ Toxicol 25(5):495–503. https://doi.org/10.1002/tox.20594
Habauzit D, Martin C, Kerdivel G, Pakdel F (2017) Rapid assessment of estrogenic compounds by CXCL-test illustrated by the screening of the UV-filter derivative benzophenones. Chemosphere 173:253–260. https://doi.org/10.1016/j.chemosphere.2017.01.037
Hallgren P, Nicolle A, Hansson LA, Bronmark C, Nikoleris L, Hyder M, Persson A (2014) Synthetic estrogen directly affects fish biomass and may indirectly disrupt aquatic food webs. Environ Toxicol Chem 33(4):930–936. https://doi.org/10.1002/etc.2528
Hettwer K, Jahne M, Frost K, Giersberg M, Kunze G, Trimborn M, Reif M, Turk J, Gehrmann L, Dardenne F, De Croock F, Abraham M, Schoop A, Waniek JJ, Bucher T, Simon E, Vermeirssen E, Werner A, Hellauer K, Wallentits U, Drewes JE, Dietzmann D, Routledge E, Beresford N, Zietek T, Siebler M, Simon A, Bielak H, Hollert H, Muller Y, Harff M, Schiwy S, Simon K, Uhlig S (2018) Validation of Arxula Yeast Estrogen Screen assay for detection of estrogenic activity in water samples: results of an international interlaboratory study. Sci Total Environ 621:612–625. https://doi.org/10.1016/j.scitotenv.2017.11.211
Ho PW, Tse ZH, Liu HF, Lu S, Ho JW, Kung MH, Ramsden DB, Ho SL (2013) Assessment of cellular estrogenic activity based on estrogen receptor-mediated reduction of soluble-form catechol-O-methyltransferase (COMT) expression in an ELISA-based system. PLoS ONE 8(9):e74065. https://doi.org/10.1371/journal.pone.0074065
Honda L, Becerra-Herrera M, Richter P (2018) Liquid chromatography-time-of-flight high-resolution mass spectrometry study and determination of the dansylated products of estrogens and their hydroxylated metabolites in water and wastewater. Anal Bioanal Chem 410(30):7909–7919. https://doi.org/10.1007/s00216-018-1412-0
Hou C, Lu G, Zhao L, Yin P, Zhu L (2017) Estrogenicity assessment of membrane concentrates from landfill leachate treated by the UV-Fenton process using a human breast carcinoma cell line. Chemosphere 180:192–200. https://doi.org/10.1016/j.chemosphere.2017.04.033
Jackson LM, Felgenhauer BE, Klerks PL (2019) Feminization, altered gonadal development, and liver damage in least killifish (Heterandria formosa) exposed to sublethal concentrations of 17alpha-ethinylestradiol. Ecotoxicol Environ Safty 170:331–337. https://doi.org/10.1016/j.ecoenv.2018.11.094
Janex-Habibi ML, Huyard A, Esperanza M, Bruchet A (2009) Reduction of endocrine disruptor emissions in the environment: the benefit of wastewater treatment. Water Res 43(6):1565–1576. https://doi.org/10.1016/j.watres.2008.12.051
Janssens G, Mangelinckx S, Courtheyn D, De Kimpe N, Matthijs B, Le Bizec B (2015) Simultaneous detection of androgen and estrogen abuse in breeding animals by gas chromatography-mass spectrometry/combustion/isotope ratio mass spectrometry (GC-MS/C/IRMS) evaluated against alternative methods. J Agric Food Chem 63(34):7574–7581. https://doi.org/10.1021/acs.jafc.5b02746
Ji L, Wang Y, Wu K, Zhang W (2016) Simultaneous determination of environmental estrogens: diethylstilbestrol and estradiol using Cu-BTC frameworks-sensitized electrode. Talanta 159:215–221. https://doi.org/10.1016/j.talanta.2016.06.030
Ji X, Sun M, Li C, Han S, Wang X, Tian Y, Feng J (2019) Bare polyprolylene hollow fiber as extractive phase for in-tube solid-phase microextraction to determine estrogens in water samples. J Sep Sci. https://doi.org/10.1002/jssc.201900010
Jilani A, Othman MHD, Ansari MO, Hussain SZ, Ismail AF, Khan IU (2018) Graphene and its derivatives: synthesis, modifications, and applications in wastewater treatment. Environ Chem Lett 16(4):1301–1323. https://doi.org/10.1007/s10311-018-0755-2
Jones-Lepp TL, Stevens R (2007) Pharmaceuticals and personal care products in biosolids/sewage sludge: the interface between analytical chemistry and regulation. Anal Bioanal Chem 387(4):1173–1183. https://doi.org/10.1007/s00216-006-0942-z
Jonker W, Ballesteros-Gomez A, Hamers T, Somsen GW, Lamoree MH, Kool J (2016) Highly selective screening of estrogenic compounds in consumer-electronics plastics by liquid chromatography in parallel combined with nanofractionation-bioactivity detection and mass spectrometry. Environ Sci Technol 50(22):12385–12393. https://doi.org/10.1021/acs.est.6b03762
Kabir ER, Rahman MS, Rahman I (2015) A review on endocrine disruptors and their possible impacts on human health. Environ Toxicol Pharmacol 40(1):241–258. https://doi.org/10.1016/j.etap.2015.06.009
Kataoka H, Saito K (2011) Recent advances in SPME techniques in biomedical analysis. J Pharm Biomed Anal 54(5):926–950. https://doi.org/10.1016/j.jpba.2010.12.010
Ke Y, Bertin J, Gonthier R, Simard JN, Labrie F (2014) A sensitive, simple and robust LC-MS/MS method for the simultaneous quantification of seven androgen- and estrogen-related steroids in postmenopausal serum. J Steroid Biochem Mol Biol 144 Pt B:523–534. https://doi.org/10.1016/j.jsbmb.2014.08.015
Keski-Rahkonen P, Desai R, Jimenez M, Harwood DT, Handelsman DJ (2015) Measurement of estradiol in human serum by LC-MS/MS using a novel estrogen-specific derivatization reagent. Anal Chem 87(14):7180–7186. https://doi.org/10.1021/acs.analchem.5b01042
Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci U S A 104(21):8897–8901. https://doi.org/10.1073/pnas.0609568104
Klein KO (2015) Is there a role for estrogen activity assays? Recombinant cell bioassay for estrogen: development and applications. Steroids 99(Pt A):108–112. https://doi.org/10.1016/j.steroids.2014.08.004
Korner W, Hanf V, Schuller W, Kempter C, Metzger J, Hagenmaier H (1999) Development of a sensitive E-screen assay for quantitative analysis of estrogenic activity in municipal sewage plant effluents. Sci Total Environ 225(1–2):33–48. https://doi.org/10.1016/s0048-9697(99)80015-1
Kupcova E, Reiffova K (2017) Dispersive liquid–liquid microextraction as an effective preanalytical step for the determination of estradiol in human urine. J Sep Sci 40(12):2620–2628. https://doi.org/10.1002/jssc.201700123
Kurauchi K, Nakaguchi Y, Tsutsumi M, Hori H, Kurihara R, Hashimoto S, Ohnuma R, Yamamoto Y, Matsuoka S, Kawai S, Hirata T, Kinoshita M (2005) In vivo visual reporter system for detection of estrogen-like substances by transgenic medaka. Environ Sci Technol 39(8):2762–2768. https://doi.org/10.1021/es0486465
Kuswandi B (2019) Nanobiosensor approaches for pollutant monitoring. Environ Chem Lett 17(2):975–990. https://doi.org/10.1007/s10311-018-00853-x
Kwon J, Oh KS, Cho SY, Bang MA, Kim HS, Vaidya B, Kim D (2016) Estrogenic activity of hyperforin in MCF-7 human breast cancer cells transfected with estrogen receptor. Planta Med 82(16):1425–1430. https://doi.org/10.1055/s-0042-112594
Lang L, Meng Z, Sun L, Xiao W, Zhao L, Xiong Z (2018) Intergrated metabonomic study of the effects of Guizhi Fuling capsule intervention on primary dysmenorrheal using RP-UPLC-MS complementary with HILIC-UPLC-MS technique. Biomed Chromatogr. https://doi.org/10.1002/bmc.4093
Lee O, Takesono A, Tada M, Tyler CR, Kudoh T (2012) Biosensor zebrafish provide new insights into potential health effects of environmental estrogens. Environ Health Perspect 120(7):990–996. https://doi.org/10.1289/ehp.1104433
Legler J, van den Brink CE, Brouwer A, Murk AJ, van der Saag PT, Vethaak AD, van der Burg B (1999) Development of a stably transfected estrogen receptor-mediated luciferase reporter gene assay in the human T47D breast cancer cell line. Toxicol Sci 48(1):55–66. https://doi.org/10.1093/toxsci/48.1.55
Legler J, Zeinstra LM, Schuitemaker F, Lanser PH, Bogerd J, Brouwer A, Vethaak AD, De Voogt P, Murk AJ, Van der Burg B (2002) Comparison of in vivo and in vitro reporter gene assays for short-term screening of estrogenic activity. Environ Sci Technol 36(20):4410–4415. https://doi.org/10.1021/es010323a
Letinski DJ, Parkerton TF, Redman AD, Connelly MJ, Peterson B (2016) Water solubility of selected C9-C18 alkanes using a slow-stir technique: comparison to structure—property models. Chemosphere 150:416–423. https://doi.org/10.1016/j.chemosphere.2015.12.038
Leusch FD, de Jager C, Levi Y, Lim R, Puijker L, Sacher F, Tremblay LA, Wilson VS, Chapman HF (2010) Comparison of five in vitro bioassays to measure estrogenic activity in environmental waters. Environ Sci Technol 44(10):3853–3860. https://doi.org/10.1021/es903899d
Li J, Song J, Bi S, Zhou S, Cui J, Liu J, Wu D (2016) Electrochemical estrogen screen method based on the electrochemical behavior of MCF-7 cells. J Hazard Mater 313:238–243. https://doi.org/10.1016/j.jhazmat.2015.09.031
Li W, Hong B, Li Z, Li Q, Bi K (2018a) GC-MS method for determination and pharmacokinetic study of seven volatile constituents in rat plasma after oral administration of the essential oil of Rhizoma Curcumae. J Pharm Biomed Anal 149:577–585. https://doi.org/10.1016/j.jpba.2017.11.058
Li XS, Li S, Kellermann G (2018b) Simultaneous determination of three estrogens in human saliva without derivatization or liquid-liquid extraction for routine testing via miniaturized solid phase extraction with LC-MS/MS detection. Talanta 178:464–472. https://doi.org/10.1016/j.talanta.2017.09.062
Li Y, Wang J, Zheng M, Zhang Y, Ru S (2018c) Development of ELISAs for the detection of vitellogenin in three marine fish from coastal areas of China. Mar Pollut Bull 133:415–422. https://doi.org/10.1016/j.marpolbul.2018.06.001
Liu M, Qiu B, Jin X, Zhang L, Chen X, Chen G (2008) Determination of estrogens in wastewater using three-phase hollow fiber-mediated liquid-phase microextraction followed by HPLC. J Sep Sci 31(4):622–628. https://doi.org/10.1002/jssc.200700497
Liu X, Zhou S, Zhu Q, Ye Y, Chen H (2014) Ultra preconcentration of polycyclic aromatic hydrocarbons in smoked bacon by a combination of SPE and DLLME. J Chromatogr Sci 52(8):932–937. https://doi.org/10.1093/chromsci/bmt119
Liu Y, Chen Y, Zhang Y, Kou Q, Zhang Y, Wang Y, Chen L, Sun Y, Zhang H, MeeJung Y (2018a) Detection and identification of estrogen based on surface-enhanced resonance Raman scattering (SERRS). Molecules. https://doi.org/10.3390/molecules23061330
Liu YY, Lin YS, Yen CH, Miaw CL, Chen TC, Wu MC, Hsieh CY (2018b) Identification, contribution, and estrogenic activity of potential EDCs in a river receiving concentrated livestock effluent in Southern Taiwan. Sci Total Environ 636:464–476. https://doi.org/10.1016/j.scitotenv.2018.04.031
Liu S, Cheng R, Chen Y, Shi H, Zhao GA (2018c) Simple one-step pretreatment, highly sensitive and selective sensing of 17β-Estradiol in environmental water samples using surface-enhanced raman spectroscopy. Sens Actuators B Chem 254:1157–1164
Liu M, Ke H, Sun C, Wang G, Wang Y, Zhao G (2019a) A simple and highly selective electrochemical label-free aptasensor of 17beta-estradiol based on signal amplification of bi-functional graphene. Talanta 194:266–272. https://doi.org/10.1016/j.talanta.2018.10.035
Liu S, Chen Y, Wang Y, Zhao G (2019b) Group-targeting detection of total steroid estrogen using surface-enhanced raman spectroscopy. Anal Chem 91(12):7639–7647. https://doi.org/10.1021/acs.analchem.9b00534
Locatelli MA, Sodre FF, Jardim WF (2011) Determination of antibiotics in Brazilian surface waters using liquid chromatography-electrospray tandem mass spectrometry. Arch Environ Contam Toxicol 60(3):385–393. https://doi.org/10.1007/s00244-010-9550-1
Lozan E, Shinkaruk S, Al Abed SA, Lamothe V, Potier M, Marighetto A, Schmitter JM, Bennetau-Pelissero C, Bure C (2017) Derivatization-free LC-MS/MS method for estrogen quantification in mouse brain highlights a local metabolic regulation after oral versus subcutaneous administration. Anal Bioanal Chem 409(22):5279–5289. https://doi.org/10.1007/s00216-017-0473-9
Ma L, Yates SR (2018) Dissolved organic matter and estrogen interactions regulate estrogen removal in the aqueous environment: a review. Sci Total Environ 640–641:529–542. https://doi.org/10.1016/j.scitotenv.2018.05.301
Ma M, Zhe T, Song W, Guo P, Wang J, Wang J (2017) A comparative study on the glucose sensors modified by two different β-cyclodextrin functionalized reduced graphene oxide based Au nanocomposites synthesized through developed post immobilization and in situ growth technologies. Sens Actuators B Chem 253:818–829. https://doi.org/10.1016/j.snb.2017.07.003
Manickum T, John W (2015) The current preference for the immuno-analytical ELISA method for quantitation of steroid hormones (endocrine disruptor compounds) in wastewater in South Africa. Anal Bioanal Chem 407(17):4949–4970. https://doi.org/10.1007/s00216-015-8546-0
Martins AF, Dos Santos JB, Todeschini BH, Saldanha LF, da Silva DS, Reichert JF, Souza DM (2017) Occurrence of cocaine and metabolites in hospital effluent—a risk evaluation and development of a HPLC method using DLLME. Chemosphere 170:176–182. https://doi.org/10.1016/j.chemosphere.2016.12.019
Matthews J, Zacharewski T (2000) Differential binding affinities of PCBs, HO-PCBs, and aroclors with recombinant human, rainbow trout (Onchorhynkiss mykiss), and green anole (Anolis carolinensis) estrogen receptors, using a semi-high throughput competitive binding assay. Toxicol Sci 53(2):326–339. https://doi.org/10.1093/toxsci/53.2.326
Mei M, Yu J, Huang X, Li H, Lin L, Yuan D (2015) Monitoring of selected estrogen mimics in complicated samples using polymeric ionic liquid-based multiple monolithic fiber solid-phase microextraction combined with high-performance liquid chromatography. J Chromatogr A 1385:12–19. https://doi.org/10.1016/j.chroma.2015.01.072
Mertl J, Kirchnawy C, Osorio V, Grininger A, Richter A, Bergmair J, Pyerin M, Washuttl M, Tacker M (2014) Characterization of estrogen and androgen activity of food contact materials by different in vitro bioassays (YES, YAS, ERalpha and AR CALUX) and chromatographic analysis (GC-MS, HPLC-MS). PLoS ONE 9(7):e100952. https://doi.org/10.1371/journal.pone.0100952
Mohagheghian A, Nabizadeh R, Mesdghinia A, Rastkari N, Mahvi AH, Alimohammadi M, Yunesian M, Ahmadkhaniha R, Nazmara S (2014) Distribution of estrogenic steroids in municipal wastewater treatment plants in Tehran, Iran. J Environ Health Sci Eng 12:97. https://doi.org/10.1186/2052-336X-12-97
Monneret C (2017) What is an endocrine disruptor? C R Biol 340(9–10):403–405. https://doi.org/10.1016/j.crvi.2017.07.004
Moraes FC, Rossi B, Donatoni MC, de Oliveira KT, Pereira EC (2015) Sensitive determination of 17beta-estradiol in river water using a graphene based electrochemical sensor. Anal Chim Acta 881:37–43. https://doi.org/10.1016/j.aca.2015.04.043
Morimoto M, Takahashi M, Honda J, Yoshida T, Yoshida M, Toba H, Imoto I, Tangoku A, Sasa M (2016) Assay of serum E2 concentration in postmenopausal breast cancer patients using a high-sensitivity RIA method is generally useful. J Med Investig 63(3–4):236–240. https://doi.org/10.2152/jmi.63.236
Muz M, Sonmez MS, Komesli OT, Bakirdere S, Gokcay CF (2012) Determination of selected natural hormones and endocrine disrupting compounds in domestic wastewater treatment plants by liquid chromatography electrospray ionization tandem mass spectrometry after solid phase extraction. Analyst 137(4):884–889. https://doi.org/10.1039/c2an15644j
Naldi AC, Fayad PB, Prevost M, Sauve S (2016) Analysis of steroid hormones and their conjugated forms in water and urine by on-line solid-phase extraction coupled to liquid chromatography tandem mass spectrometry. Chem Cent J 10:30. https://doi.org/10.1186/s13065-016-0174-z
Ni X, Xia B, Wang L, Ye J, Du G, Feng H, Zhou X, Zhang T, Wang W (2017) Fluorescent aptasensor for 17beta-estradiol determination based on gold nanoparticles quenching the fluorescence of Rhodamine B. Anal Biochem 523:17–23. https://doi.org/10.1016/j.ab.2017.01.021
Omi K, Ando T, Sakyu T, Shirakawa T, Uchida Y, Oka A, Ise N, Aoyagi K, Goishi K (2015) Noncompetitive immunoassay detection system for haptens on the basis of antimetatype antibodies. Clin Chem 61(4):627–635. https://doi.org/10.1373/clinchem.2014.232728
On J, Pyo H, Myung SW (2018) Effective and sensitive determination of eleven disinfection byproducts in drinking water by DLLME and GC-MS. Sci Total Environ 639:208–216. https://doi.org/10.1016/j.scitotenv.2018.05.077
Pacakova V, Loukotkova L, Bosakova Z, Stulik K (2009) Analysis for estrogens as environmental pollutants—a review. J Sep Sci 32(5–6):867–882. https://doi.org/10.1002/jssc.200800673
Pessoa GP, de Souza NC, Vidal CB, Alves JA, Firmino PI, Nascimento RF, dos Santos AB (2014) Occurrence and removal of estrogens in Brazilian wastewater treatment plants. Sci Total Environ 490:288–295. https://doi.org/10.1016/j.scitotenv.2014.05.008
Polyakova OV, Mazur DM, Artaev VB, Lebedev AT (2016) Rapid liquid–liquid extraction for the reliable GC/MS analysis of volatile priority pollutants. Environ Chem Lett 14(2):251–257. https://doi.org/10.1007/s10311-015-0544-0
Prochazkova T, Sychrova E, Javurkova B, Vecerkova J, Kohoutek J, Lepsova-Skacelova O, Blaha L, Hilscherova K (2017) Phytoestrogens and sterols in waters with cyanobacterial blooms—analytical methods and estrogenic potencies. Chemosphere 170:104–112. https://doi.org/10.1016/j.chemosphere.2016.12.006
Racz L, Goel RK (2010) Fate and removal of estrogens in municipal wastewater. J Environ Monit 12(1):58–70. https://doi.org/10.1039/b917298j
Rajasarkka J, Koponen J, Airaksinen R, Kiviranta H, Virta M (2014) Monitoring bisphenol A and estrogenic chemicals in thermal paper with yeast-based bioreporter assay. Anal Bioanal Chem 406(23):5695–5702. https://doi.org/10.1007/s00216-014-7812-x
Rather JA, Khudaish EA, Kannan P (2018) Graphene-amplified femtosensitive aptasensing of estradiol, an endocrine disruptor. Analyst 143(8):1835–1845. https://doi.org/10.1039/c7an02092a
Rey F, Ramos JG, Stoker C, Bussmann LE, Luque EH, Munoz-de-Toro M (2006) Vitellogenin detection in Caiman latirostris (Crocodylia: alligatoridae): a tool to assess environmental estrogen exposure in wildlife. J Comp Physiol B 176(3):243–251. https://doi.org/10.1007/s00360-005-0045-8
Romera D, Mateo EM, Mateo-Castro R, Gomez JV, Gimeno-Adelantado JV, Jimenez M (2018) Determination of multiple mycotoxins in feedstuffs by combined use of UPLC-MS/MS and UPLC-QTOF-MS. Food Chem 267:140–148. https://doi.org/10.1016/j.foodchem.2017.11.040
Rose E, Paczolt KA, Jones AG (2013) The effects of synthetic estrogen exposure on premating and postmating episodes of selection in sex-role-reversed Gulf pipefish. Evol Appl 6(8):1160–1170. https://doi.org/10.1111/eva.12093
Scala-Benuzzi ML, Raba J, Soler-Illia G, Schneider RJ, Messina GA (2018) Novel electrochemical paper-based immunocapture assay for the quantitative determination of ethinylestradiol in water samples. Anal Chem 90(6):4104–4111. https://doi.org/10.1021/acs.analchem.8b00028
Schoenborn A, Schmid P, Bram S, Reifferscheid G, Ohlig M, Buchinger S (2017) Unprecedented sensitivity of the planar yeast estrogen screen by using a spray-on technology. J Chromatogr A 1530:185–191. https://doi.org/10.1016/j.chroma.2017.11.009
Schultis T, Metzger JW (2004) Determination of estrogenic activity by LYES-assay (yeast estrogen screen-assay assisted by enzymatic digestion with lyticase). Chemosphere 57(11):1649–1655. https://doi.org/10.1016/j.chemosphere.2004.06.027
Scrimshaw MD, Lester JN (2004) In-vitro assays for determination of oestrogenic activity. Anal Bioanal Chem 378(3):576–581. https://doi.org/10.1007/s00216-003-2227-0
Serra H, Brion F, Porcher JM, Budzinski H, Ait-Aissa S (2018) Triclosan lacks anti-estrogenic effects in zebrafish cells but modulates estrogen response in zebrafish embryos. Int J Mol Sci. https://doi.org/10.3390/ijms19041175
Shappell NW (2013) Egg wash wastewater: estrogenic risk or environmental asset? Integr Environ Assess Manag 9(3):517–523. https://doi.org/10.1002/ieam.1415
Silva CP, Otero M, Esteves V (2012) Processes for the elimination of estrogenic steroid hormones from water: a review. Environ Pollut 165:38–58. https://doi.org/10.1016/j.envpol.2012.02.002
Singh AC, Asif MH, Bacher G, Danielsson B, Willander M, Bhand S (2019) Nanoimmunosensor based on ZnO nanorods for ultrasensitive detection of 17beta-Estradiol. Biosens Bioelectron 126:15–22. https://doi.org/10.1016/j.bios.2018.10.004
Socas-Rodriguez B, Hernandez-Borges J, Asensio-Ramos M, Herrera-Herrera AV, Palenzuela JA, Rodriguez-Delgado MA (2014) Determination of estrogens in environmental water samples using 1,3-dipentylimidazolium hexafluorophosphate ionic liquid as extraction solvent in dispersive liquid–liquid microextraction. Electrophoresis 35(17):2479–2487. https://doi.org/10.1002/elps.201400024
Stasinakis AS, Mermigka S, Samaras VG, Farmaki E, Thomaidis NS (2012) Occurrence of endocrine disrupters and selected pharmaceuticals in Aisonas River (Greece) and environmental risk assessment using hazard indexes. Environ Sci Pollut Res Int 19(5):1574–1583. https://doi.org/10.1007/s11356-011-0661-7
Surujlal-Naicker S, Bux F (2013) Application of radio-immunoassays to assess the fate of estrogen EDCs in full scale wastewater treatment plants. J Environ Sci Health A Tox Hazard Subst Environ Eng 48(1):37–47. https://doi.org/10.1080/10934529.2012.707832
Tarnow P, Bross S, Wollenberg L, Nakajima Y, Ohmiya Y, Tralau T, Luch A (2017) A novel dual-color luciferase reporter assay for simultaneous detection of estrogen and aryl hydrocarbon receptor activation. Chem Res Toxicol 30(7):1436–1447. https://doi.org/10.1021/acs.chemrestox.7b00076
Tsikas D, Zoerner AA (2014) Analysis of eicosanoids by LC-MS/MS and GC-MS/MS: a historical retrospect and a discussion. J Chromatogr B Analyt Technol Biomed Life Sci 964:79–88. https://doi.org/10.1016/j.jchromb.2014.03.017
Uraipong C, Allan RD, Li C, Kennedy IR, Wong V, Lee NA (2017) A survey of 17alpha-ethinylestradiol and mestranol residues in Hawkesbury River, Australia, using a highly specific enzyme-linked immunosorbent assay (ELISA) demonstrates the levels of potential biological significance. Ecotoxicol Environ Saf 144:585–592. https://doi.org/10.1016/j.ecoenv.2017.06.077
Uraipong C, Allan RD, Li C, Kennedy IR, Wong V, Lee NA (2018) 17beta-Estradiol residues and estrogenic activities in the Hawkesbury River, Australia. Ecotoxicol Environ Saf 164:363–369. https://doi.org/10.1016/j.ecoenv.2018.08.013
Valitalo P, Perkola N, Seiler TB, Sillanpaa M, Kuckelkorn J, Mikola A, Hollert H, Schultz E (2016) Estrogenic activity in Finnish municipal wastewater effluents. Water Res 88:740–749. https://doi.org/10.1016/j.watres.2015.10.056
Van Donk E, Peacor S, Grosser K, De Senerpont Domis LN, Lurling M (2016) Pharmaceuticals may disrupt natural chemical information flows and species interactions in aquatic systems: ideas and perspectives on a hidden global change. Rev Environ Contam Toxicol 238:91–105. https://doi.org/10.1007/398_2015_5002
Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33(3):378–455. https://doi.org/10.1210/er.2011-1050
Vela-Soria F, Jimenez-Diaz I, Diaz C, Perez J, Iribarne-Duran LM, Serrano-Lopez L, Arrebola JP, Fernandez MF, Olea N (2016) Determination of endocrine-disrupting chemicals in human milk by dispersive liquid–liquid microextraction. Bioanalysis 8(17):1777–1791. https://doi.org/10.4155/bio-2016-0073
Vijayan V, Giersberg M, Chamas A, Mehrotra M, Chelikani V, Kunze G, Baronian K (2015) Use of recombinant oestrogen binding protein for the electrochemical detection of oestrogen. Biosens Bioelectron 66:379–384. https://doi.org/10.1016/j.bios.2014.11.043
Walker CW, Watson JE (2010) Adsorption of estrogens on laboratory materials and filters during sample preparation. J Environ Qual 39(2):744–748. https://doi.org/10.2134/jeq2009.0017
Wang J, Wang W, Zhang X, Tian H, Ru S (2015) Development of a lipovitellin-based goldfish (Carassius auratus) vitellogenin ELISA for detection of environmental estrogens. Chemosphere 132:166–171. https://doi.org/10.1016/j.chemosphere.2015.03.038
Wang G, Lu G, Zhao J, Yin P, Zhao L (2016) Evaluation of toxicity and estrogenicity of the landfill-concentrated leachate during advanced oxidation treatment: chemical analyses and bioanalytical tools. Environ Sci Pollut Res Int 23(16):16015–16024. https://doi.org/10.1007/s11356-016-6669-2
Wang C, Yang L, Li N, Zhang X, Guo Y, Li C (2017) Development of immunoaffinity solid phase microextraction rods for analysis of three estrogens in environmental water samples. J Chromatogr B Anal Technol Biomed Life Sci 1061–1062:41–48. https://doi.org/10.1016/j.jchromb.2017.07.005
Wang A, Ding Y, Li L, Duan D, Mei Q, Zhuang Q, Cui S, He X (2019a) A novel electrochemical enzyme biosensor for detection of 17beta-estradiol by mediated electron-transfer system. Talanta 192:478–485. https://doi.org/10.1016/j.talanta.2018.09.018
Wang W, He C, Gao Y, Zhang Y, Shi Q (2019b) Isolation and characterization of hydrophilic dissolved organic matter in waters by ion exchange solid phase extraction followed by high resolution mass spectrometry. Environ Chem Lett 17(4):1857–1866. https://doi.org/10.1007/s10311-019-00898-6
Woclawek-Potocka I, Mannelli C, Boruszewska D, Kowalczyk-Zieba I, Wasniewski T, Skarzynski DJ (2013) Diverse effects of phytoestrogens on the reproductive performance: cow as a model. Int J Endocrinol 2013:650984. https://doi.org/10.1155/2013/650984
Worawit C, Cocovi-Solberg DJ, Varanusupakul P, Miro M (2018) In-line carbon nanofiber reinforced hollow fiber-mediated liquid phase microextraction using a 3D printed extraction platform as a front end to liquid chromatography for automatic sample preparation and analysis: a proof of concept study. Talanta 185:611–619. https://doi.org/10.1016/j.talanta.2018.04.007
Wu C, Huang X, Lin J, Liu J (2015) Occurrence and fate of selected endocrine-disrupting chemicals in water and sediment from an urban lake. Arch Environ Contam Toxicol 68(2):225–236. https://doi.org/10.1007/s00244-014-0087-6
Xu N, Xu YF, Xu S, Li J, Tao HC (2012) Removal of estrogens in municipal wastewater treatment plants: a Chinese perspective. Environ Pollut 165:215–224. https://doi.org/10.1016/j.envpol.2011.12.025
Yamamoto H, Liljestrand HM, Shimizu Y, Morita M (2003) Effects of physical-chemical characteristics on the sorption of selected endocrine disruptors by dissolved organic matter surrogates. Environ Sci Technol 37(12):2646–2657. https://doi.org/10.1021/es026405w
Yin GG, Kookana RS, Ru YJ (2002) Occurrence and fate of hormone steroids in the environment. Environ Int 28(6):545–551
Yuan SF, Liu ZH, Lian HX, Yang C, Lin Q, Yin H, Dang Z (2016) Simultaneous determination of estrogenic odorant alkylphenols, chlorophenols, and their derivatives in water using online headspace solid phase microextraction coupled with gas chromatography-mass spectrometry. Environ Sci Pollut Res Int 23(19):19116–19125. https://doi.org/10.1007/s11356-016-7107-1
Zacs D, Perkons I, Bartkevics V (2016) Determination of steroidal oestrogens in tap water samples using solid-phase extraction on a molecularly imprinted polymer sorbent and quantification with gas chromatography-mass spectrometry (GC-MS). Environ Monit Assess 188(7):433. https://doi.org/10.1007/s10661-016-5435-8
Zeng Y, Zhang Y, Dong L, Zhang B, Zhao Y (2013) Simultaneous determination of six estrogens in different water bodies by solid phase extraction and ultra performance liquid chromatography coupled with triple quadrupole mass spectrometry. Se Pu 31(12):1176–1181
Zhang Q, Lu M, Wang C, Du J, Zhou P, Zhao M (2014) Characterization of estrogen receptor alpha activities in polychlorinated biphenyls by in vitro dual-luciferase reporter gene assay. Environ Pollut 189:169–175. https://doi.org/10.1016/j.envpol.2014.03.001
Zhang Q, Han L, Wang J, Lin H, Ke P, Zhuang J, Huang X (2017) Simultaneous quantitation of endogenous estrone, 17beta-estradiol, and estriol in human serum by isotope-dilution liquid chromatography-tandem mass spectrometry for clinical laboratory applications. Anal Bioanal Chem 409(10):2627–2638. https://doi.org/10.1007/s00216-017-0207-z
Zheng M, Wang L, Bi Y, Liu F (2011) Improved method for analyzing the degradation of estrogens in water by solid-phase extraction coupled with ultra performance liquid chromatography-ultraviolet detection. J Environ Sci (China) 23(4):693–698
Zhou Y, Zha J, Xu Y, Lei B, Wang Z (2012) Occurrences of six steroid estrogens from different effluents in Beijing. China. Environ Monit Assess 184(3):1719–1729. https://doi.org/10.1007/s10661-011-2073-z
Zorita S, Martensson L, Mathiasson L (2007) Hollow-fibre supported liquid membrane extraction for determination of fluoxetine and norfluoxetine concentration at ultra trace level in sewage samples. J Sep Sci 30(15):2513–2521. https://doi.org/10.1002/jssc.200700165
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Li, C., Wei, Y., Zhang, S. et al. Advanced methods to analyze steroid estrogens in environmental samples. Environ Chem Lett 18, 543–559 (2020). https://doi.org/10.1007/s10311-019-00961-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10311-019-00961-2