Skip to main content
Log in

Evaluation of the photosynthetic parameters, emission of volatile organic compounds and ultrastructure of common green leafy vegetables after exposure to non-steroidal anti-inflammatory drugs (NSAIDs)

  • Original Research Article
  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Understanding the effects of many essential non-steroidal anti-inflammatory drugs (NSAIDs) on plants is still limited, especially at environmentally realistic concentrations. This paper presents the influence of three of the most frequently used NSAIDs (diclofenac, ibuprofen, and naproxen) at environmentally realistic concentrations on the autochthonous green leafy vegetables: orache (Atriplex patula L.), spinach (Spinacia oleracea L.) and lettuce (Lactuca sativa L.). Our research was focused on the determination of the photosynthetic parameters, the emission rate of volatile organic compounds, and the evaluation of the ultrastructure of leaves of studied vegetables after exposure to abiotic stress induced by environmental pollutants, namely NSAIDs. The data obtained indicate a moderate reduction of foliage physiological activity as a response to the stress induced by NSAIDs to the selected green leafy vegetables. The increase of the 3-hexenal and monoterpene emission rates with increasing NSAIDs concentration could be used as a sensitive and a rapid indicator to assess the toxicity of the NSAIDs. Microscopic analysis showed that the green leafy vegetables were affected by the selected NSAIDs. In comparison to the controls, the green leafy vegetables treated with NSAIDs presented irregular growth of glandular trichomes on the surface of the adaxial side of the leaves, less stomata, cells with less cytoplasm, irregular cell walls and randomly distributed chloroplasts. Of the three NSAIDs investigated in this study, ibuprofen presented the highest influence. The results obtained in this study can be used to better estimate the impact of drugs on the environment and to improve awareness on the importance of the responsible use of drugs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aguirre RAG, Pinero JLH, Estrada RA, Pournavab RF, Limon SM(2015) Microanalysis of leaves of Atriplex canescens (Pursh) Nutt. under saline conditions. Int J Farming Allied Sci 4(1):26–31

    Google Scholar 

  • Andreozzi R, Raffaele M, Nicklas P (2003) Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. Chemosphere 50:1319–1330

    Article  CAS  Google Scholar 

  • Aznar RN, Sánchez-Brunete C, Albero B, Rodríguez JA, Tadeo JL (2014) Occurrence and analysis of selected pharmaceutical compounds in soil from Spanish agricultural fields. Environ Sci Pollut Res 21:4772–4782

    Article  CAS  Google Scholar 

  • Bartha B, Huber C, Schröder P (2014) Uptake and metabolism of diclofenac in Typha latifolia—how plants cope with human pharmaceutical pollution. Plant Sci 227:12–20

    Article  CAS  Google Scholar 

  • Bartrons M, Penuelas J (2017) Pharmaceuticals and personal-care products in plants. Trends Plant Sci 22(3):194–203

    Article  CAS  Google Scholar 

  • Blom-Zandstra M, Lampe JEM (1984) The role of nitrate in the osmoregulation of lettuce (Lactuca sativa) grown at different light intensities. J Exp Bot 36(168):1043–1052

    Google Scholar 

  • Boxall AB, Rudd MA, Brooks BW, Caldwell DJ, Choi K, Hickmann S, Innes E, Ostapyk K, Staveley JP, Verslycke T, Ankley GT, Beazley KF, Belanger SE, Berninger JP, Carriquiriborde P, Coors A, DeLeo PC, Dyer SD, Ericson JF, Gagné F, Giesy JP, Gouin T, Hallstrom L, Karlsson MV, Larsson DGJ, Lazorchak JM, Mastrocco F, McLaughlin A, McMaster ME, Meyerhoff RD, Moore R, Parrott JL, Snape JR, Murray-Smith R, Servos MR, Sibley PK, Straub JO, Szabo ND, Topp E, Tetreault GR, Trudeau VL, Van Der Kraak G (2012) Pharmaceuticals and personal care products in the environment: What are the big questions? Environ Health Perspect 120:1221–1229

    Article  Google Scholar 

  • Choma I (2004) Antibiotics: Analysis by TLC. In: Cazes J, Dekker M (eds) Encyclopedia of chromatography, Update Supplement, USA

  • Christou A, Antoniou C, Christodoulou C, Hapeshi E, Stavrou I, Michael C, Fatta-Cassinos D, Fotopoulos V (2016) Stress-related phenomena and detoxification mechanisms induced by common pharmaceuticals in alfalfa (Medicago sativa L.) plants. Sci Total Environ 557‒558:652–664

    Article  CAS  Google Scholar 

  • Codd GA, Metcalf JS, Beattie KA (1998) Retention of Microcystis aeruginosa and microcystin by salad lettuce (Lactuca sativa) after spray irrigation with water containing cyanobacteria. Toxicon 37:1181–1185

    Article  Google Scholar 

  • Copaciu F, Opriş O, Coman V, Ristoiu D, Niinemets Ü, Copolovici L (2013) Diffuse water pollution by anthraquinone and azo dyes in environment importantly alters foliage volatiles, carotenoids and physiology in wheat (Triticum aestivum). Water Air Soil Pollut 224:1478

    Article  CAS  Google Scholar 

  • Copolovici L, Kännaste A, Pazouki L, Niinemets Ü (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169:664–672

    Article  CAS  Google Scholar 

  • Copolovici L, Niinemets U (2016) Environmental impacts on plant volatile emission. Blande JD and Glinwood R (eds). Springer, New York

  • Copolovici L, Timis D, Taschina M, Copolovici D, Cioca G, Bungau S (2017) Diclofenac influence on photosynthetic parameters and volatile organic compounds emission from Phaseolus vulgaris L. plants. Rev Chim 68(9):2076–2078

    CAS  Google Scholar 

  • Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner J, Amelung W, Grohmann E, Siemens J (2012) Accumulation of pharmaceuticals, Enterococcus, and resistance genes in soils irrigated with wastewater for zero to 100 years in Central Mexico. PLoS ONE 7:e45397

    Article  CAS  Google Scholar 

  • Dodgen LK, Li J, Parker D, Gan JJ (2013) Uptake and accumulation of four PPCP/EDCs in two leaf vegetables. Environ Pollut 182:150–156

    Article  CAS  Google Scholar 

  • Emhofer L, Himmelsbach M, Buchberger W, Klampf CW (2017) 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 1491:137–144

    Article  CAS  Google Scholar 

  • Es’haghi Z (2009) Determination of widely used non-steroidal anti-inflammatory drugs in water samples by in situ derivatization, continuous hollow fiber liquid-phase microextraction and gas chromatography-flame ionization detector. Anal Chim Acta 641:83–88

    Article  CAS  Google Scholar 

  • Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159

    Article  CAS  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  CAS  Google Scholar 

  • Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131:5–17

    Article  CAS  Google Scholar 

  • Huber C, Bartha B, Schröder P (2012) Metabolism of diclofenac in plants—hydroxylation is followed by glucose conjugation. J Hazard Mater 243:250–256

    Article  CAS  Google Scholar 

  • Hurtado C, Cañameras N, Domínguez C, Price GW, Comas J, Bayona JM (2017) Effect of soil biochar concentration on the mitigation of emerging organic contaminant uptake in lettuce. J Hazard Mater 323:386–393

    Article  CAS  Google Scholar 

  • Hurtado C, Trapp S, Bayona JM (2016) Inverse modeling of the biodegradation of emerging organic contaminants in the soil-plant system. Chemosphere 156:236–244

    Article  CAS  Google Scholar 

  • Isidori M, Lavorgna M, Nardelli A, Parrella A, Previtera L, Rubino M (2005) Ecotoxicity of naproxen and its phototransformation products. Sci Total Environ 348:93–101

    Article  CAS  Google Scholar 

  • Kannaste A, Copolovici L, Niinemets Ü (2014) Gas chromatography-mass spectrometry method for determination of biogenic volatile organic compounds emitted by plants. Methods Mol Biol 1153:161–169

    Article  CAS  Google Scholar 

  • Kosjek T, Heath E, Krbavčič A (2005) Determination of non-steroidal anti-inflammatory drug (NSAIDs) residues in water samples. Environ Int 31:679–685

    Article  CAS  Google Scholar 

  • Kümmerer K (2010) Pharmaceuticals in the environment. Annu Rev Environ Resour 35:57–75

    Article  Google Scholar 

  • Kummerova M, Zezulka S, Babula P, Triska J (2016) Possible ecological risk of two pharmaceuticals diclofenac and paracetamol demonstrated on a model plant Lemna minor. J Hazard Mater 302:351–361

    Article  CAS  Google Scholar 

  • Lange OL, Nobel P,Osmond C, Ziegler H (1981) Physiological plant Ecology I. Response to different quantum flux densities. Springer, Germany

    Book  Google Scholar 

  • Law MY, Charle SA, Halliwell B (1982) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. Biochem J 210:899–903

    Article  Google Scholar 

  • Liavonchanka A, Feussner N (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163:348–357

    Article  CAS  Google Scholar 

  • Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166

    Article  CAS  Google Scholar 

  • Madikizela LM, Ncube S, Chimuka L (2018) Uptake of pharmaceuticals by plants grown under hydroponic conditions and natural occurring plant species: a review. Sci Total Environ 636:477–486

    Article  CAS  Google Scholar 

  • Madikizela LM, Chimuka L (2017) Occurrence of naproxen, ibuprofen, and diclofenac residues in wastewater and river water of KwaZulu-Natal province in South Africa. Environ Monit Assess 189:348

    Article  CAS  Google Scholar 

  • Manzo V, Honda L, Navarro O, Ascar L, Richter P (2014) Microextraction of non-steroidal anti-inflammatory drugs from wastewater samples by rotating-disk sorptive extraction. Talanta 128:486–492

    Article  CAS  Google Scholar 

  • Mezzelani M, Gorbi S, Da Ros Z, Fattorini D, d’Errico G, Milan M, Bargelloni L, Regoli F (2016) Ecotoxicological potential of non-steroidal anti-inflammatory drugs (NSAIDs) in marine organisms: bioavailability, biomarkers and natural occurrence in Mytilus galloprovincialis. Mar Environ Res 121:31–39

    Article  CAS  Google Scholar 

  • Niinemets Ü (2010) Mild versus severe stress and BVOCs: thresholds, priming and consequences. Trends Plant Sci 15:145–153

    Article  CAS  Google Scholar 

  • Opriş O, Copaciu F, Soran ML, Ristoiu D, Niinemets Ü, Copolovici L (2013) Influence of nine antibiotics on key secondary metabolites and physiological characteristics in Triticum aestivum: leaf volatiles as a promising new tool to assess toxicity. Ecotoxicol Environ Safe 87:70–79

    Article  CAS  Google Scholar 

  • Quintana JB, Weiss S, Reemtsma T (2005) Pathways and metabolites of microbial degradation of selected acidic pharmaceutical and their occurrence in municipal wastewater treated by a membrane bioreactor. Water Res 39:2654–2664

    Article  CAS  Google Scholar 

  • Rajapaksha AU, Vithanage M, Lim JE, Ahmed MBM, Zhang M, Lee SS, Ok YS (2014) Invasive plant-derived biochar inhibits sulfamethazine uptake by lettuce in soil. Chemosphere 111:500–504

    Article  CAS  Google Scholar 

  • Rede D, Santos LHMLM, Ramos S, Oliva-Teles F, Antao C, Sousa SR, Delerue-Matos C (2016) Ecotoxicological impact of two soil remediation treatments in Lactuca sativa seeds. Chemosphere 159:193–198

    Article  CAS  Google Scholar 

  • Pierattini EC, Francini A, Huber C, Sebastiani L, Schröder P (2018) Poplar and diclofenac pollution: a focus on physiology, oxidative stress and uptake in plant organs. Sci Total Environ 636:944–952

    Article  CAS  Google Scholar 

  • Santos LHMLM, Araújo AN, Fachini A, Pena A, Delerue-Matos C, Montenegro MCBSM (2010) Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 175:45–95

    Article  CAS  Google Scholar 

  • Schmidt W, Redshaw CH (2015) Evaluation of biological endpoints in crop plants after exposure to non-steroidal anti-inflammatory drugs (NSAIDs): implications for phytotoxicological assessment of novel contaminants. Ecotoxicol Environ Safe 112:212–222

    Article  CAS  Google Scholar 

  • Tăşchină M, Copolovici DM, Bungău S, Lupitu AI, Copolovici L, Iovan C (2017) The influence of residual acetaminophen on Phaseolus vulgaris L. secondary metabolites. Farmacia 65(5):709–713

    Google Scholar 

  • Ternes TA (1998) Occurrence of drugs in German sewage treatments plants and rivers. Water Res 32(11):3245–3260

    Article  CAS  Google Scholar 

  • Tixier C, Singer HP, Oellers S, Mqller SR (2003) Occurrence and fate of carbamazepine, ibuprofen, ketoprofen and naproxen in surface waters. Environ Sci Technol 37(6):1061–1068

    Article  CAS  Google Scholar 

  • Ungar I (1996) Effect of salinity on seed germination, growth, and ion accumulation of Atriplex patula (Chenopodiaceae). Am J Bot 83(5):604–607

    Article  Google Scholar 

  • Vazquez-Roig P, Segarra R, Blasco C, Andreu V, Picó Y (2010) Determination of pharmaceuticals in soils and sediments by pressurized liquid extraction and liquid chromatography tandem mass spectrometry. J Chromatogr A 1217:2471–2483

    Article  CAS  Google Scholar 

  • Wu X, Conkle JL, Gan J (2012) Multi-residue determination of pharmaceutical and personal care products in vegetables. J Chromatogr A 1254:78–86

    Article  CAS  Google Scholar 

  • Wu X, Ernst F, Conkle JL, Gan J (2013) Comparative uptake and translocation of pharmaceutical and personal care products (PPCPs) by common vegetables. Environ Int 60:15–22

    Article  CAS  Google Scholar 

  • Zorita S, Mårtensson L, Mathiasson L (2009) Occurrence and removal of pharmaceuticals in a municipal sewage treatment system in the South of Sweden Sci Total Environ 407:2760–2770

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant of Romanian Ministry of Research and Innovation, CNCS – UEFISCDI, project number PN-III-P1-1.1-PD-2016-0484 within PNCDI III. We also thank LIME-CETATEA (Integrated Electron Microscopy Laboratory—Center for Research and Advanced Technologies for Alternative Energies) and “Constantin Crăciun” Electron Microscopy Laboratory, “Babeş-Bolyai” University of Cluj-Napoca (Romania) for the access to transmission electron microscopy facilities.

Author contributions

OO, MLS, and LC designed the experiments and supervised the study. OO, AC, IL, DC, and LC carried out the experiments and data collection. OO and AC wrote the paper with input from all authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucian Copolovici.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The present article does not contain studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Opriş, O., Ciorîţă, A., Soran, ML. et al. Evaluation of the photosynthetic parameters, emission of volatile organic compounds and ultrastructure of common green leafy vegetables after exposure to non-steroidal anti-inflammatory drugs (NSAIDs). Ecotoxicology 28, 631–642 (2019). https://doi.org/10.1007/s10646-019-02059-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-019-02059-5

Keywords

Navigation