Global climate changes cause water scarcity in many regions, and the sustainable use of recycled water appears crucial, especially in agriculture. However, potentially hazardous compounds such as pharmaceuticals can enter the food chain and pose severe risks. This paper aims to study the presence of selected pharmaceutical active compounds (PhACs) and their metabolites in crops grown in aeroponic conditions and evaluate the potential of PhAC plant uptake. A solvent extraction with an acidified mixture of acetonitrile and water followed by LC-HRMS was developed and validated for quantifying nine pharmaceuticals and their nine metabolites in three plants. We aimed for a robust method with a wide linear range because an extensive concentration range in different matrices was expected. The developed method proved rapid and reliable determination of selected pharmaceuticals in plants in the wide concentration range of 10 to 20,000 ng g-1 and limit of detection range 0.4 to 9.0 ng g-1. The developed method was used to study the uptake and translocation of pharmaceuticals and their metabolites in plant tissues from an aeroponic experiment at three different pH levels. Carbamazepine accumulated more in the leaves of spinach than in arugula. On the other hand, sulfamethoxazole and clindamycin evinced higher accumulation in roots than in leaves, comparable in both plants. The expected effect of pH on plants' uptake was not significant.

Faculty of Agrobiology Food and Natural Resources Department of Soil Science and Soil Protection Czech University of Life Sciences Prague Kamýcká 129 CZ 165 00 Prague Suchdol Czech Republic

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses University of South Bohemia in České Budějovice Zátiší 728 2 CZ 389 25 Vodňany Czech Republic

Faculty of Natural Sciences Department of Analytical Chemistry Comenius University in Bratislava Ilkovičova 6 SK 842 15 Bratislava Slovak Republic

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Al-Farsi RS, Ahmed M, Al-Busaidi A, Choudri BS. Translocation of pharmaceuticals and personal care products (PPCPs) into plant tissues: a review. Emerg Contam. 2017;3:132–137. doi: 10.1016/j.emcon.2018.02.001. DOI

Alvarez-Rivera G, Ballesteros-Vivas D, Parada-Alfonso F, Ibañez E, Cifuentes A. Recent applications of high resolution mass spectrometry for the characterization of plant natural products. TrAC Trends Anal Chem. 2019;112:87–101. doi: 10.1016/j.trac.2019.01.002. DOI

Bartha B, Huber C, Schröder P. Uptake and metabolism of diclofenac in Typha latifolia — how plants cope with human pharmaceutical pollution. Plant Sci. 2014;227:12–20. doi: 10.1016/j.plantsci.2014.06.001. PubMed DOI

Ben Mordechay E, Tarchitzky J, Chen Y, Shenker M, Chefetz B. Composted biosolids and treated wastewater as sources of pharmaceuticals and personal care products for plant uptake: a case study with carbamazepine. Environ Pollut. 2018;232:164–172. doi: 10.1016/j.envpol.2017.09.029. PubMed DOI

Bigott Y, Khalaf DM, Schröder P, Schröder PM, Cruzeiro C. Uptake and translocation of pharmaceuticals in plants: principles and data analysis. In: Pérez Solsona S, Montemurro N, Chiron S, Barceló D, editors. Interaction and Fate of Pharmaceuticals in Soil-Crop Systems: The Impact of Reclaimed Wastewater. Cham: Springer International Publishing; 2021. pp. 103–140.

Boretti A, Rosa L. Reassessing the projections of the World Water Development Report. npj Clean Water. 2019;2:15. doi: 10.1038/s41545-019-0039-9. DOI

Borik A, Staňová AV, Brooks BW, Grabicová K, Randák T, Grabic R. Determination of citalopram in fish brain tissue: benefits of coupling laser diode thermal desorption with low- and high-resolution mass spectrometry. Anal Bioanal Chem. 2020;412:4353–4361. doi: 10.1007/s00216-020-02672-y. PubMed DOI

Borik A, Stanova AV, Kodesova R, Brooks BW, Grabicova K, Novakova P, Grabic R. Ultrafast laser diode thermal desorption method for analysis of representative pharmaceuticals in soil leachate samples. Talanta. 2020;208:120382. doi: 10.1016/j.talanta.2019.120382. PubMed DOI

Brunetti G, Kodešová R, Šimůnek J. Modeling the translocation and transformation of chemicals in the soil-plant continuum: a dynamic plant uptake module for the HYDRUS model. Water Resour Res. 2019;55:8967–8989. doi: 10.1029/2019WR025432. DOI

Brunetti G, Kodešová R, Švecová H, Fér M, Nikodem A, Klement A, Grabic R, Šimůnek J. On the use of mechanistic soil–plant uptake models: a comprehensive experimental and numerical analysis on the translocation of carbamazepine in green pea plants. Environ Sci Technol. 2021;55(5):2991–3000. doi: 10.1021/acs.est.0c07420. PubMed DOI PMC

Brunetti G, Kodešová R, Švecová H, Fér M, Nikodem A, Klement A, Grabic R, Šimůnek J. A novel multiscale biophysical model to predict the fate of ionizable compounds in the soil-plant continuum. J Hazard Mater. 2022;423:127008. doi: 10.1016/j.jhazmat.2021.127008. PubMed DOI

Calderón-Preciado D, Matamoros V, Bayona JM. Occurrence and potential crop uptake of emerging contaminants and related compounds in an agricultural irrigation network. Sci Total Environ. 2011;412-413:14–19. doi: 10.1007/s00216-009-2669-0. PubMed DOI

Carter LJ, Harris E, Williams M, Ryan JJ, Kookana RS, Boxall ABA. Fate and uptake of pharmaceuticals in soil-plant systems. J Agric Food Chem. 2014;62:816–825. doi: 10.1021/jf404282y. PubMed DOI PMC

Cosenza A, Maida CM, Piscionieri D, Fanara S, Di Gaudio F, Viviani G. Occurrence of illicit drugs in two wastewater treatment plants in the south of Italy. Chemosphere. 2018;198:377–385. doi: 10.1016/j.chemosphere.2018.01.158. PubMed DOI

Couto CF, Lange LC, Amaral MCS. Occurrence, fate and removal of pharmaceutically active compounds (PhACs) in water and wastewater treatment plants—a review. J Water Process Eng. 2019;32:100927. doi: 10.1016/j.jwpe.2019.100927. DOI

Cui H, Schröder P. Uptake, translocation and possible biodegradation of the antidiabetic agent metformin by hydroponically grown Typha latifolia. J Hazard Mater. 2016;308:355–361. doi: 10.1016/j.jhazmat.2016.01.054. PubMed DOI

D'Alessio M, Onanong S, Snow DD, Ray C. Occurrence and removal of pharmaceutical compounds and steroids at four wastewater treatment plants in Hawai’i and their environmental fate. Sci Total Environ. 2018;631-632:1360–1370. doi: 10.1016/j.scitotenv.2018.03.100. PubMed DOI

der Beek TA, Weber FA, Bergmann A, Hickmann S, Ebert I, Hein A, Kuster A. Pharmaceuticals in the environment — global occurrences and perspectives. Environ Toxicol Chem. 2016;35:823–835. doi: 10.1002/etc.3339. PubMed DOI

Dordio AV, Belo M, Martins Teixeira D, Palace Carvalho AJ, Dias CMB, Picó Y, Pinto AP. Evaluation of carbamazepine uptake and metabolization by Typha spp., a plant with potential use in phytotreatment. Bioresour Technol. 2011;102:7827–7834. doi: 10.1016/j.biortech.2011.06.050. PubMed DOI

Eggen T, Asp TN, Grave K, Hormazabal V. Uptake and translocation of metformin, ciprofloxacin and narasin in forage- and crop plants. Chemosphere. 2011;85:26–33. doi: 10.1016/j.chemosphere.2011.06.041. PubMed DOI

Emhofer L, Himmelsbach M, Buchberger W, Klampfl CW. High-performance liquid chromatography–mass spectrometry analysis of the parent drugs and their metabolites in extracts from cress (Lepidium sativum) grown hydroponically in water containing four non-steroidal anti-inflammatory drugs. J Chromatogr A. 2017;1491:137–144. doi: 10.1016/j.chroma.2017.02.057. PubMed DOI

Evgenidou EN, Konstantinou IK, Lambropoulou DA. Occurrence and removal of transformation products of PPCPs and illicit drugs in wastewaters: a review. Sci Total Environ. 2015;505:905–926. doi: 10.1016/j.scitotenv.2014.10.021. PubMed DOI

Ghauch A, Ayoub G, Naim S. Degradation of sulfamethoxazole by persulfate assisted micrometric Fe0 in aqueous solution. Chem Eng J. 2013;228:1168–1181. doi: 10.1016/j.cej.2013.05.045. DOI

Ghauch A, Baydoun H, Dermesropian P. Degradation of aqueous carbamazepine in ultrasonic/Fe0/H2O2 systems. Chem Eng J. 2011;172(1):18–27. doi: 10.1016/j.cej.2011.04.002. DOI

Girotto F, Alibardi L, Cossu R. Food waste generation and industrial uses: a review. Waste Manag. 2015;45:32–41. doi: 10.1016/j.wasman.2015.06.008. PubMed DOI

Goldstein M, Shenker M, Chefetz B. Insights into the uptake processes of wastewater-borne pharmaceuticals by vegetables. Environ Sci Technol. 2014;48:5593–5600. doi: 10.1021/es5008615. PubMed DOI

Golovko O, Kumar V, Fedorova G, Randak T, Grabic R. Removal and seasonal variability of selected analgesics/anti-inflammatory, anti-hypertensive/cardiovascular pharmaceuticals and UV filters in wastewater treatment plant. Environ Sci Pollut Res. 2014;21:7578–7585. doi: 10.1007/s11356-014-2654-9. PubMed DOI

Golovko O, Kumar V, Fedorova G, Randak T, Grabic R. Seasonal changes in antibiotics, antidepressants/psychiatric drugs, antihistamines and lipid regulators in a wastewater treatment plant. Chemosphere. 2014;111:418–426. doi: 10.1016/j.chemosphere.2014.03.132. PubMed DOI

González García M, Fernández-López C, Pedrero-Salcedo F, Alarcón JJ. Absorption of carbamazepine and diclofenac in hydroponically cultivated lettuces and human health risk assessment. Agric Water Manag. 2018;206:42–47. doi: 10.1016/j.agwat.2018.04.018. DOI

Grabicova K, Stanova AV, Ucun OK, Borik A, Randak T, Grabic R. Development of a robust extraction procedure for the HPLC-ESI-HRPS determination of multi-residual pharmaceuticals in biota samples. Anal Chim Acta. 2018;1022:53–60. doi: 10.1016/j.aca.2018.04.011. PubMed DOI

Herklotz PA, Gurung P, Vanden Heuvel B, Kinney CA. Uptake of human pharmaceuticals by plants grown under hydroponic conditions. Chemosphere. 2010;78:1416–1421. doi: 10.1016/j.chemosphere.2009.12.048. PubMed DOI

Hurtado C, Domínguez C, Pérez-Babace L, Cañameras N, Comas J, Bayona JM. Estimate of uptake and translocation of emerging organic contaminants from irrigation water concentration in lettuce grown under controlled conditions. J Hazard Mater. 2016;305:139–148. doi: 10.1016/j.jhazmat.2015.11.039. PubMed DOI

Ivanová L, Mackuľak T, Grabic R, Golovko O, Koba O, Staňová AV, Szabová P, Grenčíková A, Bodík I. Pharmaceuticals and illicit drugs — a new threat to the application of sewage sludge in agriculture. Sci Total Environ. 2018;634:606–615. doi: 10.1016/j.scitotenv.2018.04.001. PubMed DOI

Klement A, Kodesova R, Golovko O, Fer M, Nikodem A, Kocarek M, Grabic R. Uptake, translocation and transformation of three pharmaceuticals in green pea plants. J Hydrol Hydromech. 2020;68:1–11. doi: 10.2478/johh-2020-0001. DOI

Kodešová R, Klement A, Golovko O, Fer M, Kocarek M, Nikodem A, Grabic R. Soil influences on uptake and transfer of pharmaceuticals from sewage sludge amended soils to spinach. J Environ Manag. 2019;250:109407. doi: 10.1016/j.jenvman.2019.109407. PubMed DOI

Kodešová R, Klement A, Golovko O, Fér M, Nikodem A, Kočárek M, Grabic R. Root uptake of atenolol, sulfamethoxazole and carbamazepine, and their transformation in three soils and four plants. Environ Sci Pollut Res. 2019;26:9876–9891. doi: 10.1007/s11356-019-04333-9. PubMed DOI

Kookana RS, Drechsel P, Jamwal P, Vanderzalm J. Urbanisation and emerging economies: issues and potential solutions for water and food security. Sci Total Environ. 2020;732:139057. doi: 10.1016/j.scitotenv.2020.139057. PubMed DOI

Kruve A, Rebane R, Kipper K, Oldekop ML, Evard H, Herodes K, Ravio P, Leito I. Tutorial review on validation of liquid chromatography-mass spectrometry methods: Part II. Anal Chim Acta. 2015;870:8–28. doi: 10.1016/j.aca.2015.02.016. PubMed DOI

Kümmerer K. Pharmaceuticals in the environment. Annu Rev Environ Resour. 2010;35:57–75. doi: 10.1146/annurev-environ-052809-161223. DOI

Kunene P, Mahlambi P. Assessment of antiretroviral drugs in vegetables: evaluation of microwave-assisted extraction performance with and without solid-phase extraction cleanup. Sep Sci Plus. 2023;6:2200059. doi: 10.1002/sscp.202200059. DOI

Lindberg RH, Östman M, Olofsson U, Grabic R, Fick J. Occurrence and behaviour of 105 active pharmaceutical ingredients in sewage waters of a municipal sewer collection system. Water Res. 2014;58:221–229. doi: 10.1016/j.watres.2014.03.076. PubMed DOI

Mackuľak T, Mosný M, Škubák J, Grabic R, Birošová L. Fate of psychoactive compounds in wastewater treatment plant and the possibility of their degradation using aquatic plants. Environ Toxicol Pharmacol. 2015;39:969–973. doi: 10.1016/j.etap.2015.02.018. PubMed DOI

Madikizela LM, Ncube S, Chimuka L. Uptake of pharmaceuticals by plants grown under hydroponic conditions and natural occurring plant species: a review. Sci Total Environ. 2018;636:477–486. doi: 10.1016/j.scitotenv.2018.04.297. PubMed DOI

Magwaza ST, Magwaza LS, Odindo AO, Mditshwa A. Hydroponic technology as decentralised system for domestic wastewater treatment and vegetable production in urban agriculture: a review. Sci Total Environ. 2020;698:134154. doi: 10.1016/j.scitotenv.2019.134154. PubMed DOI

Majumder A, Gupta B, Gupta AK. Pharmaceutically active compounds in aqueous environment: a status, toxicity and insights of remediation. Environ Res. 2019;176:108542. doi: 10.1016/j.envres.2019.108542. PubMed DOI

Malchi T, Maor Y, Tadmor G, Shenker M, Chefetz B. Irrigation of root vegetables with treated wastewater: evaluating uptake of pharmaceuticals and the associated human health risks. Environ Sci Technol. 2014;48:9325–9333. doi: 10.1021/es5017894. PubMed DOI

Martínez-Piernas AB, Polo-López MI, Fernández-Ibáñez P, Agüera A. Validation and application of a multiresidue method based on liquid chromatography-tandem mass spectrometry for evaluating the plant uptake of 74 microcontaminants in crops irrigated with treated municipal wastewater. J Chromatogr A. 2018;1534:10–21. doi: 10.1016/j.chroma.2017.12.037. PubMed DOI

Matamoros V, Calderón-Preciado D, Domínguez C, Bayona JM. Analytical procedures for the determination of emerging organic contaminants in plant material: a review. Anal Chim Acta. 2012;722:8–20. doi: 10.1016/j.aca.2012.02.004. PubMed DOI

Miller EL, Nason SL, Karthikeyan KG, Pedersen JA. Root uptake of pharmaceuticals and personal care product ingredients. Environ Sci Technol. 2016;50:525–541. doi: 10.1021/acs.est.5b01546. PubMed DOI

Montemurro N, Postigo C, Lonigro A, Perez S, Barceló D. Development and validation of an analytical method based on liquid chromatography–tandem mass spectrometry detection for the simultaneous determination of 13 relevant wastewater-derived contaminants in lettuce. Anal Bioanal Chem. 2017;409:5375–5387. doi: 10.1007/s00216-017-0363-1. PubMed DOI

Nowak PM, Wietecha-Posłuszny R, Pawliszyn J. White Analytical Chemistry: an approach to reconcile the principles of Green Analytical Chemistry and functionality. TrAC Trends Anal Chem. 2021;138:116223. doi: 10.1016/j.trac.2021.116223. DOI

OECD (2022) Elderly population (indicator). 10.1787/8d805ea1-en

Pal R, Megharaj M, Kirkbride KP, Naidu R. Illicit drugs and the environment—a review. Sci Total Environ. 2013;463-464:1079–1092. doi: 10.1016/j.scitotenv.2012.05.086. PubMed DOI

Pico Y, Alvarez-Ruiz R, Wijaya L, Alfarhan A, Alyemeni M, Barcelo D. Analysis of ibuprofen and its main metabolites in roots, shoots, and seeds of cowpea (Vigna unguiculata L. Walp) using liquid chromatography-quadrupole time-of-flight mass spectrometry: uptake, metabolism, and translocation. Anal Bioanal Chem. 2018;410:1163–1176. doi: 10.1007/s00216-017-0796-6. PubMed DOI

Riemenschneider C, Al-Raggad M, Moeder M, Seiwert B, Salaineh E, Reemtsma T. Pharmaceuticals, their metabolites, and other polar pollutants in field-grown vegetables irrigated with treated municipal wastewater. J Agric Food Chem. 2016;64:5784–5792. doi: 10.1021/acs.jafc.6b01696. PubMed DOI

Roberts PH, Thomas KV. The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci Total Environ. 2006;356:143–153. doi: 10.1016/j.scitotenv.2005.04.031. PubMed DOI

Shahriar A, Hanigan D, Verburg P, Pagilla K, Yang Y. Modeling the fate of ionizable pharmaceutical and personal care products (iPPCPs) in soil-plant systems: pH and speciation. Environ Pollut. 2022;315:120367. doi: 10.1016/j.envpol.2022.120367. PubMed DOI

Sheikh Mohammad Fakhrul I, Zahurul K. World’s demand for food and water: the consequences of climate change. In: Mohammad Hossein DAF, Vahid V, Amir Hooshang T, editors. Desalination. IntechOpen, Rijeka; 2019. p. Ch. 4.

Singh A, Gautam K, Agrawal M. Chapter 7 — sustainable wastewater remediation technologies for agricultural uses. In: Varjani S, Pandey A, Taherzadeh MJ, Ngo HH, Tyagi RD, editors. Biomass, Biofuels, Biochemicals. Elsevier; 2022. pp. 153–179.

Taverniers I, De Loose M, Van Bockstaele E. Trends in quality in the analytical laboratory. II. Analytical method validation and quality assurance. Trac-Trends Anal Chem. 2004;23:535–552. doi: 10.1016/j.trac.2004.04.00. DOI

Thebo AL, Drechsel P, Lambin EF, Nelson KL. A global, spatially-explicit assessment of irrigated croplands influenced by urban wastewater flows. Environ Res Lett. 2017;12:074008. doi: 10.1088/1748-9326/aa75d1. DOI

Verlicchi P, Zambello E. Pharmaceuticals and personal care products in untreated and treated sewage sludge: occurrence and environmental risk in the case of application on soil — a critical review. Sci Total Environ. 2015;538:750–767. doi: 10.1016/j.scitotenv.2015.08.108. PubMed DOI

Wu X, Conkle JL, Ernst F, Gan J. Treated wastewater irrigation: uptake of pharmaceutical and personal care products by common vegetables under field conditions. Environ Sci Technol. 2014;48:11286–11293. doi: 10.1021/es502868k. PubMed DOI

Wu X, Dodgen LK, Conkle JL, Gan J. Plant uptake of pharmaceutical and personal care products from recycled water and biosolids: a review. Sci Total Environ. 2015;536:655–666. doi: 10.1016/j.scitotenv.2015.07.129. PubMed DOI

Yang C, Wang J, Li D. Microextraction techniques for the determination of volatile and semivolatile organic compounds from plants: a review. Anal Chim Acta. 2013;799:8–22. doi: 10.1016/j.aca.2013.07.069. PubMed DOI

Zhang C, Feng Y, Liu Y-W, Chang H-Q, Li Z-J, Xue J-M. Uptake and translocation of organic pollutants in plants: a review. J Integr Agric. 2017;16:1659–1668. doi: 10.1016/S2095-3119(16)61590-3. DOI

Zhang DQ, Hua T, Gersberg RM, Zhu J, Ng WJ, Tan SK. Carbamazepine and naproxen: fate in wetland mesocosms planted with Scirpus validus. Chemosphere. 2013;91:14–21. doi: 10.1016/j.chemosphere.2012.11.018. PubMed DOI

Assessing Lettuce Exposure to a Multipharmaceutical Mixture under Hydroponic Conditions: Findings through LC-ESI-TQ Analysis and Ecotoxicological Assessments