Environmental risk assessment of triclosan and ibuprofen in marine sediments using individual and sub-individual endpoints☆
Graphical abstract
Introduction
Until recently pharmaceuticals and personal care products (PPCP) were not included in environmental monitoring programs mainly because of their low environmental concentrations and the absence of analytical methodologies to detect them. The concern about the environmental contamination by PPCP began to be part of the agenda of governments after the publication of studies showing fish feminization due to exposure to estrogenic substances (Harries et al., 1997, Jobling et al., 1998, Hinck et al., 2009) and the massive death of vultures caused by the ingestion of diclofenac (Green et al., 2004). These studies were important to trigger concern on the environmental risks of PPCP, which include antimicrobial, anti-inflammatory, contraceptives drugs, antidepressants and antiepileptic (USEPA, 2015). The preoccupation has involved especially - although not exclusively - the aquatic biota, since the water bodies are the final destination of many of these substances (Arnold et al., 2014).
The knowledge about the effects of PPCP on freshwater organisms has evolved significantly (e.g. Fent et al., 2006, Arnold et al., 2014), but there are few empirical data about the ecotoxicity of such compounds to marine organisms nowadays (Gaw et al., 2014). This information gap is especially important regarding contaminated sediments and marine or estuarine benthic biota (Brausch and Rand, 2011). Previous studies focusing on marine sediments showed that carbamazepine, ibuprofen, fluoxetine, 17α-ethynylestradiol and propranolol inhibit Vibrio fischeri bioluminescence at concentrations ranging from 36.1 to 163.9 ng g−1, and affect the embryo-larval development of sea urchin and the growth rate of marine algae (Maranho et al., 2014, Maranho et al., 2015a). Maranho et al. (2015b) also observed lethal and sublethal effects (alterations in cellular energy status, metabolism of monoamines, and inflammation properties) in polychaetes exposed to environmental concentrations of human pharmaceuticals in marine spiked sediments.
Currently, triclosan (TCS) and ibuprofen (IBU) belong to classes of emerging compounds of greatest concern to environmental protection agencies, such as the USEPA (2015) and Environment Canada (2011). Triclosan and ibuprofen have been commonly found in environmental matrices such as surface waters and sediments in concentrations ranging from pg L−1 to μg L−1 and pg g−1 to μg g−1, respectively (Kolpin et al., 2002, Lindström et al., 2002, Agüera et al., 2003, Weigel et al., 2004, Xie et al., 2008, Zhao et al., 2010, Pintado-Herrera et al., 2013).
Given the considerable lack of information about the effects of human PPCP in sediments on marine organisms and considering that standard toxicity tests may not be sensitive enough to see the effects of human PPCP in aquatic biota (Aguirre-Martínez et al., 2015), it is important not only to increase the availability of ecotoxicological data but also to adopt new approaches to assess the environmental risks associated with PPCP in coastal areas (Fabbri and Franzellitti, 2016).
The procedure to conduct an environmental risk assessment (ERA) of PPCP within the regulatory scope by the European Medicine Agency (EMEA, 2006) is based on different types of evaluation. The first level of evaluation demands (i) the estimate of the biota exposure to the studied substance, either by direct measurements from environmental samples (Measured Environmental Concentrations - MEC), or indirectly through a prediction of its environmental concentrations (Predicted Environmental Concentrations - PEC). If environmental risks are expected, then the ERA framework leads to the second level of evaluation: (ii) identification of the final destination of the substance (based on its physical-chemical characteristics) and its ecotoxicological effects. From these data, the Predicted No Effect Concentrations (PNEC) can be estimated and at last (iii) the risk quotient (RQ) is calculated from the ratio between PEC (or MEC) and PNEC. If RQ < 1, further evaluations are not required; if RQ > 1, more refined evaluations are needed, including the evaluation of more sensitive endpoints and the performance of sediment bioassays.
Consequently, the evaluation of the potential effects of PPCP to aquatic organisms plays an important role in the ERA. The use of standardized ecotoxicological assays (e.g. OECD Guidelines for Testing Chemicals) is the most common ecotoxicological approach employed in the scope of the ERA in relation to PPCP (Hernando et al., 2006). Although such assays bring relevant information, they are unable to show a more realistic view of environmental risks of PPCP since the biological responses are quantified only at the individual level. The inclusion of chronic or sub-chronic endpoints, as well as sensitive responses at sub-individual levels are important to evaluate the risks of PPCP, since the most common environmental scenario is a continuous exposure to low concentrations in the marine environment. In addition, the evaluation of effects at lower levels of biological organization (i.e. sub-individual) can predict effects at higher levels (e.g. mortality, population decline, community structure) and may generate information about the mechanisms of action of PPCP in non-target organisms (Villalaín et al., 2001, Martin-Diaz et al., 2009, Pereira et al., 2014).
The current study evaluated the environmental risk of two widely used pharmaceutical substances (TCS and IBU) in three marine invertebrates used in sediment assessments (the mussel Perna perna and the sea urchin Lytechinus variegatus) including a new alternative sediment sentinel species, the mussel Mytella charruana. The biota exposure was firstly estimated by measuring environmental concentration of these substances in sediments from the vicinity of the sewage outfall of Santos Bay, Southeast Brazil. Then the concentration effect of TCS and IBU was established based on chronic and sub-individual endpoints measured in the organisms exposed to spiked sediments. At last, following the environmental risk assessment of EMEA (2006), it was estimated the RQ for each of the substances studied. This study is the first environmental risk assessment for PPCP in marine sediments from an area of the Latin America coast and will contribute to the knowledge of environmental risks associated with these substances in marine tropical ecosystems.
Section snippets
Chemicals
The bactericidal triclosan (CAS number: 3380-34-5) has a molecular weight of 289.5 g mol−1, water solubility of 10 mg L−1, pKa value of 7.9 and log Kow 4.76 with half live of 40 days (Huang et al., 2015, TOXNET – Toxicology Data Network, 2016). The anti-inflammatory ibuprofen (CAS number: 15687-27-1) has a molecular weight of 206.28 g mol−1, water solubility of 21 mg L−1, pKa value of 4.91 and log Kow 3.97 with half live of 19 days (Conkle et al., 2012, TOXNET – Toxicology Data Network, 2016).
Physical and chemical analysis
Sediment grain size and levels of carbonates were quite similar between the reference sediments used in the toxicity assays, and the sediments from the surroundings of the submarine sewage outfall. The level of OM, however, was higher in the sediments affected by sewage. The reference sediment was composed by 7.6% of coarse sand, 27.7% of medium sand, 56.8% of fine sand, 0.7% of very fine sand, 7.2% of silt and clay, 22.1% of carbonates and 0.36% of OM, while the sediment sampled in the study
Discussion
The chemical analysis performed with sediments samples from the vicinity of the submarine sewage outfall at Santos Bay demonstrated the occurrence of TCS (15.14 ng g−1) and IBU (49.0 ng g−1) in the same concentration range as reported by previous studies. Data on sediment concentrations range from 2.0 to 400 ng g−1 for TCS and 12.8–100 ng g−1 for IBU in aquatic environments worldwide (Agüera et al., 2003, Xie et al., 2008, Wilson et al., 2009, Cantwell et al., 2010, Duan et al., 2013,
Conclusion
Considering the growing need for environmental risk assessment to PPCP in marine sediments, this study presents the first data based on both measured environmental concentrations and PPCP spiked sediments in Latin America. Both triclosan and ibuprofen presented a high environmental risk and should be considered in future legislation on environmental management and waste policies as well as in wastewater treatment, in order to minimize possible environmental impacts. The marine benthic bivalve
Acknowledgment
This study was funded by CNPq – Conselho Nacional de Desenvolvimento Científico e Tecnológico (Process no 481553/2012-6 and no 481358/2012-9). Cesar, A. and Pereira, C.D.S., and Choueri, R.B. thanks CNPq fellowships (Process: PQ#305869/2013-2; PQ#307074/2013-7; and PQ#308079/2015-9 respectively). The authors would like to thank Daniel Temponi Lebre from Applied Mass Spectrometry Centre – Nuclear and Energy Research Institute (CEMSA, IPEN, São Paulo Brasil) for technical support in LC-MS/MS
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This paper has been recommended for acceptance by Maria Cristina Fossi.