Uptake study in Juncus sp. and Salicornia europaea of six pharmaceuticals by liquid chromatography quadrupole time-of-flight mass spectrometry
Graphical abstract
Introduction
Scientific researchers and government regulators are focusing attention on trace quantities of emerging pollutants in wastewater effluents and surface waters (Wilkinson et al., 2017), the major emerging contaminants are new pesticides, pharmaceuticals, personal care products, surfactants, phthalates (Gorito et al., 2017), and perfluorinated alkylated substances (PAFS) (Mengmeng et al., 2019), resulting in an increased level of concern regarding the potential environmental impact of these compounds (Wilkinson et al., 2017).
The use of treated wastewater for irrigation in many areas has become a common practice and since 1991, European Union regulations established that all its member states must treat urban wastewater before it is discharged into the environment, lakes, rivers and seas (EC Council Directive, 1991) in order to avoid the increasing rates of pollutants in ecosystems.
The increase in the consumption of pharmaceutical products has become an environmental pollution problem, since most wastewater treatment plants lack methods for the adequate pharmaceutical products elimination from wastewaters. These substances still remain present and are discharged into environmental surface waters, where the active components of the pharmaceuticals undergo biodegradation processes at different rates (Szymonik et al., 2012). The processes used in wastewater treatment plants (WWTPs) do not efficiently remove many substances, including those considered emerging contaminants like pharmaceuticals (Tauxe-Wuersch et al., 2005; Hijosa-Valesco et al., 2011; Li, 2014; Rahdar et al., 2019). The pharmaceuticals that are less susceptible to biodegradation in water can be stored in aquatic ecosystems and have been shown to exhibit toxic effects on fish and several aquatic micro-organisms (Huerta et al., 2018). Authors (Fernández-Torres et al., 2011) have found several antibiotics in marine fish samples from southern Spain. Another problem is that pharmaceuticals might infiltrate into groundwater causing contamination of drinking water, which presents a problem for human health (Szymonik et al., 2012). Plants are capable of incorporating, mainly through their roots, the compounds dissolved in the water that irrigates them such as the long-studied for years heavy metals (Arasimowicz et al., 2013; Martínez-Alcalá et al., 2017). However, less attention was paid to the accumulation of pharmaceuticals in plants until the first decade of 2000s, and the majority of studies have been mainly focused in vegetables intended for human consumption while very little work has been done on this topic with wild plant species (Eggen et al., 2011; Wu et al., 2013, 2014; Marsoni et al., 2014; Hurtado et al., 2016; Riemenschneider et al., 2017a, 2017b; Di Baccio et al., 2017; Montemurro et al., 2017; Martínez-Piernas et al., 2018; Picó et al., 2019).
Most common pharmaceuticals detected in surface waters include compounds such as non-steroidal anti-inflammatory drugs (NSAIDs) like diclofenac (DCL) or ibuprofen (IBU), which are persistent in the environment and have been found in water streams (Qureshi et al., 2019); anti-epileptic drugs such as carbamazepine (CBZ) (Szymonik et al., 2012) and antibiotics from several families with, in general, long-term effects on all ecosystems (Liu et al., 2018).
The presence of ciprofloxacin (CPR) in the environment has shown adverse effects on fish (Ziarrusta et al., 2018). For enrofloxacin (ENR), the studies carried out by Wang et al. (2019) revealed non acceptable levels of this substance in an aquatic environment. The toxicity of ENR on agricultural crops has also been evaluated by finding levels of ENR in water between 50 and 5000 μg L−1 producing toxic effects on both plants and animals that are able to metabolize ENR to CPR. (Migliore et al., 2003). The use of pharmaceuticals and their occurrence in the environment have received significant attention owing to antibiotic-resistant bacteria, but their presence in environmental samples near protected areas, livestock farming areas or crops should be monitored to establish effective strategies for reducing their use and evaluate their effects on the surrounding ecosystems. (Chansik et al., 2018).
The high consumption of ibuprofen increases its presence in soils and waters, and it is considered one important emerging pharmaceutical pollutant due to its generalized presence in the natural environment (Di Baccio et al., 2017; Huang et al., 2020).
Carbamazepine (CBZ) is a frequently detected pharmaceutical compound in aquatic environments, causing chronic toxicity and endocrine disruption in a variety of non-target aquatic organisms (Chen et al., 2019). Several studies have shown its presence in different environmental samples, such as water and sediments due to inefficient disposal from wastewater treatment plants or even through direct dumping of untreated wastewaters (Gros et al., 2010; Camacho-Muñoz et al., 2010, 2012; Verlicchi et al., 2012). Its presence in protected areas such as Doñana National Park, among other protected areas, has aroused great interest (Camacho-Muñoz et al., 2013; Carmona et al., 2014; Rivera-Jaimes et al., 2018) due to its potential risk for surrounding ecosystems.
Therefore, in this work we have studied the accumulation of different active pharmaceutical substances (flumequine (FMQ), cirproloxacin, enrofloxacin, carbamazepine, diclofenac and ibuprofen) on two types of plants that grow mainly in aquatic ecosystems, seeking to assess the incidence, at laboratory scale, that discharge of waters containing pharmaceuticals would have in an aquatic ecosystem. These plants were selected because they are widespread in the ecosystems of the Mediterranean area where several protected areas are located. Juncus sp. grows on the banks of rivers and wetlands and Salicornia europaea, grows in coastal marshes and inland salt habitats, for being a halophilic plant, although it is also found in different nature reserves such as the Yellow River Nature Reserve (China) (Wang et al., 2020) or in the Sierra de Cartagena (Spain) (Ottenhof et al., 2007). Different investigations have shown the capacity of different Salicornia types for phytoremediation, for example the studies of (Kannan et al., 2009) show the capacity of Salicornia brachiata as a phytoremediation agent in the accumulation of NaCl in wastewater (Kannan et al., 2009). Or the use of Salicornia remosissima in the phytoremediation of various metals such as cadmium (Rathore et al., 2016). Also, some studies, have showed the power of Juncus effusus, as well as Juncus inbricatus, to remove metals and other freshwater pollutants from waste or runoff. (Bobadilla et al., 2013; Zhang et al., 2019). This survey was designed to evaluate the presence of the selected analytes in the leaves/stems and roots of these plants, with phytoremediation capability, for two purposes, on one hand, evaluating their possible use in the recovery of contaminated ecosystems and on the other hand, studying their absorption capability versus pharmaceuticals which would have implications on wild ecosystems.
Section snippets
Chemicals and reagents
A Suprapur formic acid (98–100% purity) from Merck Darmstadt (Germany) was used. LC-MS Ultra Chromasolv® acetonitrile and water were supplied from Sigma-Aldrich (Madrid, Spain). Ultrapure water from a Milli-Q Plus (Millipore, Billerica, MA, USA) was used for aqueous solutions and dilutions. Waters (Barcelona, Spain) supplied sodium hydroxide in 2- propanol:water and Leucine Enkephalin.
Pharmaceutical standards (ENR, CPR, FMQ, DCL, CBZ and IBU) were 98% purity or higher and were purchased from
Results and discussion
The uptake study described in section 2.2 was applied to plants of Juncus sp. and Salicornia europaea in order to evaluate somehow, by means of a laboratory experiment, the incidence that the presence of pharmaceuticals in waters that irrigates wetlands and natural areas might have. The assay was carried out using two botanical species usually present in aquatic ecosystems, which are endemic in southern Spain, where some protected nature reserves exist. Thus, the variety Juncus sp. is usually
Conclusions
In the present work, an UPLC-QTOF/MS method was used for the quantitation of six pharmacological active substances in different parts (stem/leaf and roots) of Juncus sp. and Salicornia europaea subjected to an uptake study. The results showed that the accumulation of the active ingredients evaluated depend to a large extent on the type of plant, thus, in Juncus sp. most of the analytes were measured at quantifiable levels at almost all the exposure concentrations and very different behaviors
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors want to thankful Miguel Salazar from Agro-On/Riafresh® Centro Empresarial Gambelas E2. University Algarve. Campus Gambelas. Faro. Portugal for supplying Salicornia europaea for this research.
Authors are grateful to Servicio General de Investigación de Microanálisis, CENTRO DE INVESTIGACIÓN TECNOLÓGICA E INNOVACIÓN (CITIUS). Universidad de Sevilla, for the use of the chromatographic equipment. Authors also want to thanks FEDER Funds Project UNSE10-1E-429.
Authors also are grateful to
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