Elsevier

Environmental Pollution

Volume 232, January 2018, Pages 274-283
Environmental Pollution

Environmental risk assessment of triclosan and ibuprofen in marine sediments using individual and sub-individual endpoints

https://doi.org/10.1016/j.envpol.2017.09.046Get rights and content

Highlights

  • Triclosan and ibuprofen were quantified in order of ng.g-1 in marine sediment.

  • Adverse effects were found in environmentally relevant concentrations.

  • Mytella charruana is an alternative species for monitoring marine and estuarine sediments.

  • Significant environmental risk for triclosan and ibuprofen in a tropical coastal zone.

Abstract

The guidelines for the Environmental Risk Assessment (ERA) of pharmaceuticals and personal care products (PPCP) recommend the use of standard ecotoxicity assays and the assessment of endpoints at the individual level to evaluate potential effects of PPCP on biota. However, effects at the sub-individual level can also affect the ecological fitness of marine organisms chronically exposed to PPCP. The aim of the current study was to evaluate the environmental risk of two PPCP in marine sediments: triclosan (TCS) and ibuprofen (IBU), using sub-individual and developmental endpoints. The environmental levels of TCS and IBU were quantified in marine sediments from the vicinities of the Santos submarine sewage outfall (Santos Bay, São Paulo, Brazil) at 15.14 and 49.0 ng g−1, respectively. A battery (n = 3) of chronic bioassays (embryo-larval development) with a sea urchin (Lytechinus variegatus) and a bivalve (Perna perna) were performed using two exposure conditions: sediment-water interface and elutriates. Moreover, physiological stress through the Neutral Red Retention Time Assay (NRRT) was assessed in the estuarine bivalve Mytella charruana exposed to TCS and IBU spiked sediments. These compounds affected the development of L. variegatus and P. perna (75 ng g−1 for TCS and 15 ng g−1 for IBU), and caused a significant decrease in M. charruana lysosomal membrane stability at environmentally relevant concentrations (0.08 ng g−1 for TCS and 0.15 ng g−1 for IBU). Chemical and ecotoxicological data were integrated and the risk quotient estimated for TCS and IBU were higher than 1.0, indicating a high environmental risk of these compounds in sediments. These are the first data of sediment risk assessment of pharmaceuticals and personal care products of Latin America. In addition, the results suggest that the ERA based only on individual-level and standard toxicity tests may overlook other biological effects that can affect the health of marine organisms exposed to PPCP.

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

References (68)

  • P.C. Francis et al.

    Effects of cadmium-enriched sediment on fiff and amphibian embryo–larval stages

    Ecotoxicol. Environ. Saf.

    (1984)
  • J.E. Hinck et al.

    Widespread occurrence of intersex in black basses (Micropterus spp.) from US rivers, 1995–2004

    Aquat. Toxicol.

    (2009)
  • M.D. Hernando et al.

    Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments

    Talanta

    (2006)
  • X. Huang et al.

    Sorption and degradation of triclosan in sediments and its effect on microbes

    Ecotoxicol. Environ. Saf.

    (2015)
  • S. Huber et al.

    A first screening and risk assessment of pharmaceuticals and additives in personal care products in waste water, sludge, recipient water and sediment from Faroe Islands, Iceland and Greenland

    Sci. Total Environ.

    (2016)
  • D.M. Lowe et al.

    Lysosomal membrane responses in the blood and digestive cells of mussels experimentally exposed to fluoranthene

    Aquat. Toxicol.

    (1995)
  • L.A. Maranho et al.

    Bioavailability, oxidative stress, neurotoxicity and genotoxicity of pharmaceuticals bound to marine sediments. The use of the polychaete Hediste diversicolor as bioindicator species

    Environ. Res.

    (2014)
  • L.A. Maranho et al.

    Toxicological evaluation of sediment samples spiked with human pharmaceutical products: energy status and neuroendocrine effects in marine polychaetes Hediste diversicolor

    Ecotoxicol. Environ. Saf.

    (2015)
  • L.A. Maranho et al.

    Assessing potential risks of wastewater discharges to benthic biota: an integrated approach to biomarker responses in clams (Ruditapes philippinarum) exposed under controlled conditions

    Mar. Pollut. Bull.

    (2015)
  • L. Martin-Diaz et al.

    Effects of environmental concentrations of the antiepilectic drug carbamazepine on biomarkers and cAMP-mediated cell signaling in the mussel Mytilus galloprovincialis

    Aquat. Toxicol.

    (2009)
  • M. Milan et al.

    Gene transcription and biomarker responses in the clam Ruditapes philippinarum after exposure to ibuprofen

    Aquat. Toxicol.

    (2013)
  • M. Nie et al.

    Occurrence, distribution and risk assessment of estrogens in surface water, suspended particulate matter, and sediments of the Yangtze Estuary

    Chemosphere

    (2015)
  • M.G. Pintado-Herrera et al.

    Determining the distribution of triclosan and methyl triclosan in estuarine settings

    Chemosphere

    (2014)
  • A.H. Ringwood et al.

    Linkages between cellular biomarker responses and reproductive success in oysters – Crassostrea virginica

    Mar. Environ. Res.

    (2004)
  • R.J. Smith et al.

    Effect of anti-inflammatory drugs on lysosomes and lysosomal enzymes from rat liver

    Biochem. Pharmacol.

    (1976)
  • J. Villalaín et al.

    Membranotropic effects of the antibacterial agent Triclosan

    Arch. Biochem. Biophys.

    (2001)
  • S. Weigel et al.

    Determination of selected pharmaceuticals and caffeine in sewage and seawater from Tromso/Norway with emphasis on ibuprofen and its metabolites

    Chemosphere

    (2004)
  • B. Wilson et al.

    The partitioning of Triclosan between aqueous and particulate bound phases in the Hudson River Estuary

    Mar. Pollut. Bull.

    (2009)
  • Z. Xie et al.

    Occurrence and distribution of triclosan in the German Bight (North sea)

    Environ. Pollut.

    (2008)
  • J.-L. Zhao et al.

    Occurrence and risks of triclosan and triclocarban in the Pearl River system, South China: from source to the receiving environment

    J. Hazard Mater.

    (2010)
  • ABNT – Associação Brasileira de Normas Técnicas

    NBR 15350: ecotoxicologia aquática: toxicidade crônica de curta duração – método de ensaio com ouriço-do-mar (Echinodermata: Echinoidea). Rio de Janeiro

    (2012)
  • G.V. Aguirre-Martínez et al.

    Stability of lysosomal membrane in Carcinus maenas acts as a biomarker of exposure to pharmaceuticals

    Environ. Monit. Assess.

    (2013)
  • K.E. Arnold et al.

    Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems

    Philos. Trans. R. Soc. B B

    (2014)
  • R. Atkinson et al.

    Atmospheric degradation of volatile organic compounds

    Chem. Rev.

    (2003)
  • Cited by (55)

    View all citing articles on Scopus

    This paper has been recommended for acceptance by Maria Cristina Fossi.

    View full text