Environmentally relevant concentrations of galaxolide (HHCB) and tonalide (AHTN) induced oxidative and genetic damage in Dreissena polymorpha.

Synthetic musk compounds (SMCs) are extensively used as fragrances in several personal care products and have been recognized as emerging aquatic pollutants. Among SMCs, galaxolide (HHCB) and tonalide (AHTN) are extensively used and have been measured in aquatic ecosystems worldwide. However, their potential risk to organisms remains largely unknown. The aim of this study was to investigate whether 21-day exposures to HHCB and AHTN concentrations frequently measured in aquatic ecosystems can induce oxidative and genetic damage in Dreissena polymorpha. The lipid peroxidation (LPO) and protein carbonyl content (PCC) were measured as oxidative stress indexes, while the DNA precipitation assay and the micronucleus test (MN test) were applied to investigate genetic injuries. HHCB induced significant increases in LPO and PCC levels, while AHTN enhanced only protein carbonylation. Moreover, significant increases in DNA strand breaks were caused by exposure to the highest concentrations of HHCB and AHTN tested in the present study, but no fixed genetic damage was observed.

[1]  D. Dietrich,et al.  Bioaccumulation and Ecotoxicity of Synthetic Musks in the Aquatic Environment , 2004 .

[2]  B. Shao,et al.  The occurrence of synthetic musks in human breast milk in Sichuan, China. , 2012, Chemosphere.

[3]  Hyo-Bang Moon,et al.  Occurrence and accumulation features of polycyclic aromatic hydrocarbons and synthetic musk compounds in finless porpoises (Neophocaena phocaenoides) from Korean coastal waters. , 2011, Marine pollution bulletin.

[4]  M Babut,et al.  Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. , 2000, Ecotoxicology and environmental safety.

[5]  B. van der Burg,et al.  In vitro and in vivo antiestrogenic effects of polycyclic musks in zebrafish. , 2004, Environmental science & technology.

[6]  Malcolm B. Jones,et al.  Linking genotoxic responses with cytotoxic and behavioural or physiological consequences: differential sensitivity of echinoderms (Asterias rubens) and marine molluscs (Mytilus edulis). , 2009, Aquatic toxicology.

[7]  Adverse effects induced by ecgonine methyl ester to the zebra mussel: a comparison with the benzoylecgonine. , 2013, Environmental pollution.

[8]  M. Valko,et al.  Free radicals, metals and antioxidants in oxidative stress-induced cancer. , 2006, Chemico-biological interactions.

[9]  I. Corsi,et al.  Fatal attraction: synthetic musk fragrances compromise multixenobiotic defense systems in mussels. , 2004, Marine Environmental Research.

[10]  D. Giustarini,et al.  Biomarkers of oxidative damage in human disease. , 2006, Clinical chemistry.

[11]  R A Ford,et al.  Environmental risk assessment for the polycyclic musks AHTN and HHCB in the EU. I. Fate and exposure assessment. , 1999, Toxicology letters.

[12]  V. Forbes,et al.  Individual‐ and population‐level effects of the synthetic musk, hhcb, on the deposit‐feeding polychaete, Capitella sp. I , 2009, Environmental toxicology and chemistry.

[13]  Qixing Zhou,et al.  Antioxidant enzyme activities and lipid peroxidation in earthworm Eisenia fetida exposed to 1,3,4,6,7,8‐hexahydro‐4,6,6,7,8,8‐hexamethyl‐cyclopenta‐γ‐2‐benzopyran , 2012, Environmental toxicology.

[14]  M. Parolini,et al.  Variation of Antioxidant Activity in Dreissena polymorpha Specimens Exposed to 2,2′,4,4′,5,6′-Hexa BDE (BDE-154) , 2012, Water, Air, & Soil Pollution.

[15]  L. Marnett,et al.  Determination of malondialdehyde-induced DNA damage in human tissues using an immunoslot blot assay. , 1998, Carcinogenesis.

[16]  J. Catalán,et al.  Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro river (NE Spain). , 2010, Chemosphere.

[17]  Kurunthachalam Kannan,et al.  Polycyclic Musks in Water, Sediment, and Fishes from the Upper Hudson River, New York, USA , 2011 .

[18]  Maricar Prudente,et al.  Asia-Pacific mussel watch for emerging pollutants: Distribution of synthetic musks and benzotriazole UV stabilizers in Asian and US coastal waters. , 2012, Marine pollution bulletin.

[19]  P. Olive DNA precipitation assay: A rapid and simple method for detecting DNA damage in mammalian cells , 1988, Environmental and molecular mutagenesis.

[20]  T. Baussant,et al.  The neutral red lysosomal retention assay and Comet assay on haemolymph cells from mussels (Mytilus edulis) and fish (Symphodus melops) exposed to styrene. , 2005, Aquatic toxicology.

[21]  Qixing Zhou,et al.  Acute toxicity, biochemical and gene expression responses of the earthworm Eisenia fetida exposed to polycyclic musks. , 2011, Chemosphere.

[22]  R. Erben,et al.  Detection of micronuclei in haemocytes of zebra mussel and great ramshorn snail exposed to pentachlorophenol. , 2000, Mutation research.

[23]  M. Breitholtz,et al.  Effects of four synthetic musks on the life cycle of the harpacticoid copepod Nitocra spinipes. , 2003, Aquatic toxicology.

[24]  M. Parolini,et al.  Oxidative and genetic responses induced by Δ-9-tetrahydrocannabinol (Δ-9-THC) to Dreissena polymorpha. , 2014, The Science of the total environment.

[25]  T. Poiger,et al.  Behavior of the polycyclic musks HHCB and AHTN in lakes, two potential anthropogenic markers for domestic wastewater in surface waters. , 2003, Environmental science & technology.

[26]  T. Ternes,et al.  Pharmaceuticals and personal care products in the environment: agents of subtle change? , 1999, Environmental health perspectives.

[27]  Michael Scoullos,et al.  Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. , 2006, Ecotoxicology and environmental safety.

[28]  Qixing Zhou,et al.  Toxicity assessment of simulated urban runoff containing polycyclic musks and cadmium in Carassius auratus using oxidative stress biomarkers. , 2012, Environmental pollution.

[29]  Joon-Woo Kim,et al.  Effects of synthetic polycyclic musks on estrogen receptor, vitellogenin, pregnane X receptor, and cytochrome P450 3A gene expression in the livers of male medaka (Oryzias latipes). , 2008, Aquatic toxicology.

[30]  K. Kannan,et al.  Polycyclic musk compounds in higher trophic level aquatic organisms and humans from the United States. , 2005, Chemosphere.

[31]  Hyo-Bang Moon,et al.  Accumulation of PAHs and synthetic musk compound in minke whales (Balanoptera acutorostrata) and long‐beaked common dolphins (Delphinus capensis) from Korean coastal waters , 2012, Environmental toxicology and chemistry.

[32]  P. Mecocci,et al.  Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. , 1999, Free radical biology & medicine.

[33]  D. Wink,et al.  The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations , 2004, Biological chemistry.

[34]  P. K. Lam,et al.  Application of the comet and micronucleus assays to the detection of B[a]P genotoxicity in haemocytes of the green-lipped mussel (Perna viridis). , 2004, Aquatic toxicology.

[35]  M. Fenech,et al.  Report from the In Vitro Micronucleus Assay Working Group , 2003, Mutation research.

[36]  J. da Silva,et al.  DNA damage and repair in haemolymph cells of golden mussel (Limnoperna fortunei) exposed to environmental contaminants. , 2006, Mutation research.

[37]  M. Parolini,et al.  Chemical and biomarker responses for site-specific quality assessment of the Lake Maggiore (Northern Italy) , 2013, Environmental Science and Pollution Research.

[38]  S. Tanabe,et al.  Bioaccumulation, temporal trend, and geographical distribution of synthetic musks in the marine environment. , 2007, Environmental science & technology.

[39]  P. K. Lam,et al.  Relationships between tissue concentrations of chlorinated hydrocarbons (polychlorinated biphenyls and chlorinated pesticides) and antioxidative responses of marine mussels, Perna viridis. , 2002, Marine pollution bulletin.

[40]  K. Kannan,et al.  Polybrominated diphenyl ethers and synthetic musks in umbilical cord serum, maternal serum, and breast milk from Seoul, South Korea. , 2010, Chemosphere.

[41]  T. Gabryelak,et al.  Response of DNA, proteins and membrane bilayer in the digestive gland cells of freshwater mussel Unio tumidus to tannins exposure. , 2004, Toxicology in vitro : an international journal published in association with BIBRA.

[42]  Kurunthachalam Kannan,et al.  A survey of polycyclic musks in selected household commodities from the United States. , 2006, Chemosphere.

[43]  S. Villa,et al.  First evidences of the occurrence of polycyclic synthetic musk fragrances in surface water systems in Italy: spatial and temporal trends in the Molgora River (Lombardia Region, Northern Italy). , 2012, The Science of the total environment.

[44]  A. Quintanilha,et al.  Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. , 2002, Free radical biology & medicine.

[45]  S. Focardi,et al.  Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. , 2002, Marine environmental research.

[46]  M. Parolini,et al.  Cyto-genotoxic effects induced by three brominated diphenyl ether congeners on the freshwater mussel Dreissena polymorpha. , 2012, Ecotoxicology and environmental safety.

[47]  M. Breitholtz,et al.  Inhibition of larval development of the marine copepod Acartia tonsa by four synthetic musk substances. , 2003, The Science of the total environment.

[48]  Roberto Colombo,et al.  Protein carbonyl groups as biomarkers of oxidative stress. , 2003, Clinica chimica acta; international journal of clinical chemistry.

[49]  M. Parolini,et al.  Chronic effects induced by ibuprofen on the freshwater bivalve Dreissena polymorpha. , 2011, Ecotoxicology and environmental safety.

[50]  M. Parolini,et al.  Assessment of the Potential Cyto–Genotoxicity of the Nonsteroidal Anti-Inflammatory Drug (NSAID) Diclofenac on the Zebra Mussel (Dreissena polymorpha) , 2011 .

[51]  Z. Moldovan Occurrences of pharmaceutical and personal care products as micropollutants in rivers from Romania. , 2006, Chemosphere.

[52]  Yu Fang,et al.  Occurrence of synthetic musk fragrances in effluent and non-effluent impacted environments. , 2012, The Science of the total environment.

[53]  K. Yagi,et al.  Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. , 1979, Analytical biochemistry.

[54]  P. Teichert,et al.  Transformations of polycyclic musks AHTN and HHCB upon disinfection with hypochlorite: two new chlorinated disinfection by-products (CDBP) of AHTN and a possible source for HHCB-lactone , 2011, Analytical and bioanalytical chemistry.

[55]  Andrea Binelli,et al.  Sub-lethal effects caused by the cocaine metabolite benzoylecgonine to the freshwater mussel Dreissena polymorpha. , 2013, The Science of the total environment.

[56]  V. Mersch-Sundermann,et al.  In vitro genotoxicity of polycyclic musk fragrances in the micronucleus test. , 1997, Mutation research.

[57]  M. Parolini,et al.  Multi-biomarker approach for the evaluation of the cyto-genotoxicity of paracetamol on the zebra mussel (Dreissena polymorpha). , 2010, Chemosphere.

[58]  Qixing Zhou,et al.  Ecotoxicological effects of typical personal care products on seed germination and seedling development of wheat (Triticum aestivum L.). , 2009, Chemosphere.

[59]  Adriano Joss,et al.  Scrutinizing pharmaceuticals and personal care products in wastewater treatment. , 2004, Environmental science & technology.

[60]  D. Sheehan,et al.  Oxidative stress and toxicity of gold nanoparticles in Mytilus edulis. , 2010, Aquatic toxicology.

[61]  T. Newton,et al.  Toxicity of Synthetic Musks to Early Life Stages of the Freshwater Mussel Lampsilis cardium , 2006, Archives of environmental contamination and toxicology.