Time- and dose-dependent biological effects of a sub-chronic exposure to realistic doses of salicylic acid in the gills of mussel Mytilus galloprovincialis.


Journal

Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769

Informations de publication

Date de publication:
Dec 2022
Historique:
received: 25 01 2022
accepted: 01 07 2022
pubmed: 14 7 2022
medline: 22 11 2022
entrez: 13 7 2022
Statut: ppublish

Résumé

Among nonsteroidal anti-inflammatory drugs (NSAIDs) commonly found in seawater and wastewater, salicylic acid (SA) represents one of the most persistent and hazardous compounds for aquatic organisms. This study was therefore designed to elucidate the biological effects of SA in mussel Mytilus galloprovincialis. During a sub-chronic exposure (12 days), mussels were exposed to five realistic concentrations of SA (C1: 0.05 μg/L; C2: 0.5 μg/L; C3: 5 μg/L; C4: 50 μg/L; C5: 100 μg/L) and gills, selected as the target organ, were collected at different time points (T3: 3 days; T5: 5 days; T12: 12 days). Exposure to SA induced no histological alterations in mussel gills, despite a relevant hemocyte infiltration was observed throughout the exposure as a defensive response to SA. Temporal modulation of glutathione S-transferase (GST), catalase (CAT), and superoxide dismutase (SOD) activities suggested the occurrence of antioxidant and detoxifying responses against SA exposure, while lipid peroxidation (LPO), except for a partial increase at T3, was prevented. Inhibition of the cholinergic system was also reported by reduced acetylcholinesterase (AChE) activity, mainly at T12. Overall, findings from this study contribute to enlarge the current knowledge on the cytotoxicity of SA, on non-target aquatic organisms, and might for the enhancement of new ecopharmacovigilance programs and optimization of the efficacy of wastewater treatment plants for mitigation of pharmaceutical pollution in coastal areas.

Identifiants

pubmed: 35829880
doi: 10.1007/s11356-022-21866-8
pii: 10.1007/s11356-022-21866-8
doi:

Substances chimiques

Salicylic Acid O414PZ4LPZ
Acetylcholinesterase EC 3.1.1.7
Water Pollutants, Chemical 0
Catalase EC 1.11.1.6
Glutathione Transferase EC 2.5.1.18
Biomarkers 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

88161-88171

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Afsa S, Hamden K, Lara Martin P, Ben Mansour H (2020) Occurrence of 40 pharmaceutically active compounds in hospital and urban wastewaters and their contribution to Mahdia coastal seawater contamination. Environ Sci Pollut Res 27:1941–1955. https://doi.org/10.1007/s11356-019-06866-5
doi: 10.1007/s11356-019-06866-5
Afsa S, De Marco G, Giannetto A, Parrino V, Cappello T, Ben Mansour H, Maisano M (2022) Histological endpoints and oxidative stress transcriptional responses in the Mediterranean mussel Mytilus galloprovincialis exposed to realistic doses of salicylic acid. Environ Toxicol Pharmacol 92:103855. https://doi.org/10.1016/j.etap.2022.103855
doi: 10.1016/j.etap.2022.103855
Aguirre-Martínez GV, Del Valls TA, Martín-Díaz ML (2013) Identification of biomarkers responsive to chronic exposure to pharmaceuticals in target tissues of Carcinus maenas. Mar Environ Res 87–88:1–11. https://doi.org/10.1016/j.marenvres.2013.02.011
doi: 10.1016/j.marenvres.2013.02.011
Aguirre-Martínez GV, DelValls AT, Martín-Díaz ML (2015) Yes, caffeine, ibuprofen, carbamazepine, novobiocin and tamoxifen have an effect on Corbicula fluminea (Müller, 1774). Ecotoxicol Environ Saf 120:142–154. https://doi.org/10.1016/j.ecoenv.2015.05.036
doi: 10.1016/j.ecoenv.2015.05.036
Aguirre-Martínez GV, DelValls TA, Martín-Díaz ML (2016) General stress, detoxification pathways, neurotoxicity and genotoxicity evaluated in Ruditapes philippinarum exposed to human pharmaceuticals. Ecotoxicol Environ Saf 124:18–31. https://doi.org/10.1016/j.ecoenv.2015.09.031
doi: 10.1016/j.ecoenv.2015.09.031
Aguirre-Martínez GV, André C, Gagné F, Martín-Díaz LM (2018) The effects of human drugs in Corbicula fluminea. Assessment of neurotoxicity, inflammation, gametogenic activity, and energy status. Ecotoxicol Environ Saf 148:652–663. https://doi.org/10.1016/j.ecoenv.2017.09.042
doi: 10.1016/j.ecoenv.2017.09.042
Akaishi FM, St-Jean SD, Bishay F, Clarke J, da Rabitto IS, de Oliveira Ribeiro CA (2007) Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquat Toxicol 82:1–14. https://doi.org/10.1016/j.aquatox.2007.01.008
doi: 10.1016/j.aquatox.2007.01.008
Alkimin GD, Daniel D, Dionísio R, Soares AMVM, Barata C, Nunes B (2019) Effects of diclofenac and salicylic acid exposure on Lemna minor: is time a factor? Environ Res 177:108609. https://doi.org/10.1016/j.envres.2019.108609
doi: 10.1016/j.envres.2019.108609
Aus der Beek T, Weberv F-A, Bergmann A, Hickmann S, Ebert I, Hein A, Küster A (2016) Pharmaceuticals in the environment-global occurrences and perspectives. Environ Toxicol Chem 35:823–835. https://doi.org/10.1002/etc.3339
doi: 10.1002/etc.3339
Biel-Maeso M, Baena-Nogueras RM, Corada-Fernández C, Lara-Martín PA (2018) Occurrence, distribution and environmental risk of pharmaceutically active compounds (PhACs) in coastal and ocean waters from the Gulf of Cadiz (SW Spain). Sci Total Environ 612:649–659. https://doi.org/10.1016/j.scitotenv.2017.08.279
doi: 10.1016/j.scitotenv.2017.08.279
Botsoglou NA, Fletouris DJ, Papageorgiou GE, Vassilopoulos VN, Mantis AJ, Trakatellis AG (1994) Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food, and feedstuff samples. J Agric Food Chem 42:1931–1937. https://doi.org/10.1021/jf00045a019
doi: 10.1021/jf00045a019
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
doi: 10.1006/abio.1976.9999
Caliani I, De Marco G, Cappello T, Giannetto A, Mancini G, Ancora S, Maisano M, Parrino V, Cappello S, Bianchi N, Oliva S, Luciano A, Mauceri A, Leonzio C, Fasulo S (2022) Assessment of the effectiveness of a novel BioFilm-Membrane BioReactor oil-polluted wastewater treatment technology by applying biomarkers in the mussel Mytilus galloprovincialis. Aquat Toxicol 243:106059. https://doi.org/10.1016/j.aquatox.2021.106059
doi: 10.1016/j.aquatox.2021.106059
Cappello T, Mauceri A, Corsaro C, Maisano M, Parrino V, Lo Paro G, Messina G, Fasulo S (2013) Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics. Mar Pollut Bull 77:132–139. https://doi.org/10.1016/j.marpolbul.2013.10.019
doi: 10.1016/j.marpolbul.2013.10.019
Cappello T, Maisano M, Giannetto A, Parrino V, Mauceri A, Fasulo S (2015) Neurotoxicological effects on marine mussel Mytilus galloprovincialis caged at petrochemical contaminated areas (eastern Sicily, Italy):
doi: 10.1016/j.cbpc.2014.12.006
Cappello T, Vitale V, Oliva S, Villari V, Mauceri A, Fasulo S, Maisano M (2017) Alteration of neurotransmission and skeletogenesis in sea urchin Arbacia lixula embryos exposed to copper oxide nanoparticles. Comp Biochem Physiol C 199:20–27. https://doi.org/10.1016/j.cbpc.2017.02.002
doi: 10.1016/j.cbpc.2017.02.002
Cappello T, De Marco G, Oliveri G, Giannetto A, Ferrante M, Mauceri A, Maisano M (2021) Time-dependent metabolic disorders induced by short-term exposure to polystyrene microplastics in the Mediterranean mussel Mytilus galloprovincialis. Ecotoxicol Environ Saf 209:111780. https://doi.org/10.1016/j.ecoenv.2020.111780
doi: 10.1016/j.ecoenv.2020.111780
Carraro E, Bonetta S, Bertino C, Lorenzi E, Bonetta S, Gilli G (2016) Hospital effluents management: chemical, physical, microbiological risks and legislation in different countries. J Environ Manag 168:185–199. https://doi.org/10.1016/j.jenvman.2015.11.021
doi: 10.1016/j.jenvman.2015.11.021
Chavoshani A, Hashemi M, Amin MM, Ameta SC (2020) Pharmaceuticals as emerging micropollutants. Micropollut Challenges Emerg Aquat Environ Treat Process:35
Cleuvers M (2004) Mixture toxicity of the anti-inflammatory drugs diclofenac, ibuprofen, naproxen, and acetylsalicylic acid. Ecotoxicol Environ Saf 59:309–315. https://doi.org/10.1016/S0147-6513(03)00141-6
doi: 10.1016/S0147-6513(03)00141-6
De Marco G, Brandão F, Pereira P, Pacheco M, Cappello T (2022a) Organ-specific metabolome deciphering cell pathways to cope with mercury in wild fish (golden grey mullet Chelon auratus). Animals 12:79. https://doi.org/10.3390/ani12010079
doi: 10.3390/ani12010079
De Marco G, Conti GO, Giannetto A, Cappello T, Galati M, Iaria C, Pulvirenti E, Capparucci F, Mauceri A, Ferrante M, Maisano M (2022b) Embryotoxicity of polystyrene microplastics in zebrafish Danio rerio. Environ Res 112552. https://doi.org/10.1016/j.envres.2021.112552
De Marco G, Afsa S, Galati M, Billè B, Parrino V, Ben Mansour H, Cappello T (2022c) Comparison of cellular mechanisms induced by pharmaceutical exposure to caffeine and its combination with salicylic acid in mussel Mytilus galloprovincialis. Environ Toxicol Pharmacol 93:103888. https://doi.org/10.1016/j.etap.2022.103888
doi: 10.1016/j.etap.2022.103888
de Oliveira David JA, Salaroli RB, Fontanetti CS (2008) Fine structure of Mytella falcata (Bivalvia) gill filaments. Micron 39:329–336. https://doi.org/10.1016/j.micron.2007.06.002
doi: 10.1016/j.micron.2007.06.002
Delwing-de Lima D, Wollinger LF, Casagrande ACM, Delwing F, da Cruz JGP, Wyse ATS, Delwing-Dal Magro D (2010) Guanidino compounds inhibit acetylcholinesterase and butyrylcholinesterase activities: effect neuroprotector of vitamins E plus C. Int J Dev Neurosci 28:465–473. https://doi.org/10.1016/j.ijdevneu.2010.06.008
doi: 10.1016/j.ijdevneu.2010.06.008
Doi H, Horie T (2010) Salicylic acid-induced hepatotoxicity triggered by oxidative stress. Chem Biol Interact 183:363–368. https://doi.org/10.1016/j.cbi.2009.11.024
doi: 10.1016/j.cbi.2009.11.024
Ebele AJ, Abou-Elwafa Abdallah M, Harrad S (2017) Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg Contam 3:1–16. https://doi.org/10.1016/j.emcon.2016.12.004
doi: 10.1016/j.emcon.2016.12.004
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
doi: 10.1016/0006-2952(61)90145-9
Fekadu S, Alemayehu E, Dewil R, Van der Bruggen B (2019) Pharmaceuticals in freshwater aquatic environments: a comparison of the African and European challenge. Sci Total Environ 654:324–337. https://doi.org/10.1016/j.scitotenv.2018.11.072
doi: 10.1016/j.scitotenv.2018.11.072
Freitas R, Silvestro S, Coppola F, Meucci V, Battaglia F, Intorre L, Soares AMVM, Pretti C, Faggio C (2019) Biochemical and physiological responses induced in Mytilus galloprovincialis after a chronic exposure to salicylic acid. Aquat Toxicol 214:105258. https://doi.org/10.1016/j.aquatox.2019.105258
doi: 10.1016/j.aquatox.2019.105258
Freitas R, Silvestro S, Coppola F, Meucci V, Battaglia F, Intorre L, Soares AMVM, Pretti C, Faggio C (2020a) Combined effects of salinity changes and salicylic acid exposure in Mytilus galloprovincialis. Sci Total Environ 715:136804. https://doi.org/10.1016/j.scitotenv.2020.136804
doi: 10.1016/j.scitotenv.2020.136804
Freitas R, Silvestro S, Pagano M, Coppola F, Meucci V, Battaglia F, Intorre L, Soares AMVM, Pretti C, Faggio C (2020b) Impacts of salicylic acid in Mytilus galloprovincialis exposed to warming conditions. Environ Toxicol Pharmacol 80:103448. https://doi.org/10.1016/j.etap.2020.103448
doi: 10.1016/j.etap.2020.103448
Giménez V, Nunes B (2019) Effects of commonly used therapeutic drugs, paracetamol, and acetylsalicylic acid, on key physiological traits of the sea snail Gibbula umbilicalis. Environ Sci Pollut Res Int 26:21858–21870. https://doi.org/10.1007/s11356-019-04653-w
doi: 10.1007/s11356-019-04653-w
Gómez-Oliván LM, Galar-Martínez M, Islas-Flores H, García-Medina S, SanJuan-Reyes N (2014) DNA damage and oxidative stress induced by acetylsalicylic acid in Daphnia magna. Comp Biochem Physiol C 164:21–26. https://doi.org/10.1016/j.cbpc.2014.04.004
doi: 10.1016/j.cbpc.2014.04.004
Gonzalez-Rey M, Bebianno MJ (2011) Non-steroidal anti-inflammatory drug (NSAID) ibuprofen distresses antioxidant defense system in mussel Mytilus galloprovincialis gills. Aquat Toxicol 105:264–269. https://doi.org/10.1016/j.aquatox.2011.06.015
doi: 10.1016/j.aquatox.2011.06.015
Gonzalez-Rey M, Bebianno MJ (2012) Does non-steroidal anti-inflammatory (NSAID) ibuprofen induce antioxidant stress and endocrine disruption in mussel Mytilus galloprovincialis? Environ Toxicol Pharmacol 33:361–371. https://doi.org/10.1016/j.etap.2011.12.017
doi: 10.1016/j.etap.2011.12.017
Gonzalez-Rey M, Bebianno MJ (2014) Effects of non-steroidal anti-inflammatory drug (NSAID) diclofenac exposure in mussel Mytilus galloprovincialis. Aquat Toxicol 148:221–230. https://doi.org/10.1016/j.aquatox.2014.01.011
doi: 10.1016/j.aquatox.2014.01.011
Gornati R, Longo A, Rossi F, Maisano M, Sabatino G, Mauceri A, Bernardini G, Fasulo S (2016) Effects of titanium dioxide nanoparticle exposure in Mytilus galloprovincialis gills and digestive gland. Nanotoxicology 10:807–817. https://doi.org/10.3109/17435390.2015.1132348
doi: 10.3109/17435390.2015.1132348
Gupta V, Liu S, Ando H, Ishii R, Tateno S, Kaneko Y, Yugami M, Sakamoto S, Yamaguchi Y, Nureki O, Handa H (2013) Salicylic acid induces mitochondrial injury by inhibiting ferrochelatase heme biosynthesis activity. Mol Pharmacol 84:824–833. https://doi.org/10.1124/mol.113.087940
doi: 10.1124/mol.113.087940
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
doi: 10.1016/S0021-9258(19)42083-8
Kuznetsov AV, Kehrer I, Kozlov AV, Haller M, Redl H, Hermann M, Grimm M, Troppmair J (2011) Mitochondrial ROS production under cellular stress: comparison of different detection methods. Anal Bioanal Chem 400:2383–2390. https://doi.org/10.1007/s00216-011-4764-2
doi: 10.1007/s00216-011-4764-2
Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666. https://doi.org/10.1016/s0025-326x(01)00060-1
doi: 10.1016/s0025-326x(01)00060-1
Lolić A, Paíga P, Santos LHMLM, Ramos S, Correia M, Delerue-Matos C (2015) Assessment of non-steroidal anti-inflammatory and analgesic pharmaceuticals in seawaters of North of Portugal: occurrence and environmental risk. Sci Total Environ 508:240–250. https://doi.org/10.1016/j.scitotenv.2014.11.097
doi: 10.1016/j.scitotenv.2014.11.097
Madikizela LM, Ncube S, Tutu H, Richards H, Newman B, Ndungu K, Chimuka L (2020) Pharmaceuticals and their metabolites in the marine environment: sources, analytical methods and occurrence. Trends Environ Anal Chem 28:e00104. https://doi.org/10.1016/j.teac.2020.e00104
doi: 10.1016/j.teac.2020.e00104
Magara G, Khan FR, Pinti M, Syberg K, Inzirillo A, Elia AC (2019) Effects of combined exposures of fluoranthene and polyethylene or polyhydroxybutyrate microplastics on oxidative stress biomarkers in the blue mussel (Mytilus edulis). J Toxicol Environ Health Part A 82:616–625. https://doi.org/10.1080/15287394.2019.1633451
doi: 10.1080/15287394.2019.1633451
Maisano M, Trapani MR, Parrino V, Parisi MG, Cappello T, D’Agata A, Benenati G, Natalotto A, Mauceri A, Cammarata M (2013) Haemolytic activity and characterization of nematocyst venom from Pelagia noctiluca (Cnidaria, Scyphozoa). It J Zool 80(2):168–176. https://doi.org/10.1080/11250003.2012.758782
doi: 10.1080/11250003.2012.758782
Maisano M, Natalotto A, Cappello T, Giannetto A, Oliva S, Parrino V, Sanfilippo M, Mauceri A (2016) Influences of environmental variables on neurotransmission, oxidative system, and hypoxia signaling on two clam species from a Mediterranean coastal lagoon. J Shellfish Res 35:41–49. https://doi.org/10.2983/035.035.0106
doi: 10.2983/035.035.0106
Maisano M, Cappello T, Natalotto A, Vitale V, Parrino V, Giannetto A, Oliva S, Mancini G, Cappello S, Mauceri A, Fasulo S (2017) Effects of petrochemical contamination on caged marine mussels using a multi-biomarker approach: histological changes, neurotoxicity and hypoxic stress. Mar Environ Res 128:114–123. https://doi.org/10.1016/j.marenvres.2016.03.008
doi: 10.1016/j.marenvres.2016.03.008
Manduzio H, Monsinjon T, Galap C, Leboulenger F, Rocher B (2004) Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat Toxicol 70:83–93. https://doi.org/10.1016/j.aquatox.2004.07.003
doi: 10.1016/j.aquatox.2004.07.003
McEachran AD, Shea D, Bodnar W, Nichols EG (2016) Pharmaceutical occurrence in groundwater and surface waters in forests land-applied with municipal wastewater. Environ Toxicol Chem 35:898–905. https://doi.org/10.1002/etc.3216
doi: 10.1002/etc.3216
Mezzelani M, Gorbi S, Regoli F (2018) Pharmaceuticals in the aquatic environments: evidence of emerged threat and future challenges for marine organisms. Mar Environ Res 140:41–60. https://doi.org/10.1016/j.marenvres.2018.05.001
doi: 10.1016/j.marenvres.2018.05.001
Milan M, Pauletto M, Patarnello T, Bargelloni L, Marin MG, Matozzo V (2013) Gene transcription and biomarker responses in the clam Ruditapes philippinarum after exposure to ibuprofen. Aquat Toxicol 126:17–29. https://doi.org/10.1016/j.aquatox.2012.10.007
doi: 10.1016/j.aquatox.2012.10.007
Missawi O, Bousserrhine N, Zitouni N, Maisano M, Boughattas I, De Marco G, Cappello T, Belbekhouche S, Guerrouache M, Alphonse V, Banni M (2021) Uptake, accumulation and associated cellular alterations of environmental samples of microplastics in the seaworm Hediste diversicolor. J Hazard Mater 406:124287. https://doi.org/10.1016/j.jhazmat.2020.124287
doi: 10.1016/j.jhazmat.2020.124287
Natalotto A, Sureda A, Maisano M, Spanò N, Mauceri A, Deudero S (2015) Biomarkers of environmental stress in gills of Pinna nobilis (Linnaeus 1758) from Balearic Island. Ecotoxicol Environ Saf 122:9–16. https://doi.org/10.1016/j.ecoenv.2015.06.035
doi: 10.1016/j.ecoenv.2015.06.035
Nunes B (2019) Acute ecotoxicological effects of salicylic acid on the polychaeta species Hediste diversicolor: evidences of low to moderate pro-oxidative effects. Environ Sci Pollut Res Int 26:7873–7882. https://doi.org/10.1007/s11356-018-04085-y
doi: 10.1007/s11356-018-04085-y
Nunes B, Campos JC, Gomes R, Braga MR, Ramos AS, Antunes SC, Correia AT (2015a) Ecotoxicological effects of salicylic acid in the freshwater fish Salmo trutta fario: antioxidant mechanisms and histological alterations. Environ Sci Pollut Res Int 22:667–678. https://doi.org/10.1007/s11356-014-3337-2
doi: 10.1007/s11356-014-3337-2
Nunes B, Verde MF, Soares AMVM (2015b) Biochemical effects of the pharmaceutical drug paracetamol on Anguilla anguilla. Environ Sci Pollut Res 22:11574–11584. https://doi.org/10.1007/s11356-015-4329-6
doi: 10.1007/s11356-015-4329-6
Nunes B, Nunes J, Soares AMVM, Figueira E, Freitas R (2017) Toxicological effects of paracetamol on the clam Ruditapes philippinarum: exposure vs recovery. Aquat Toxicol 192:198–206. https://doi.org/10.1016/j.aquatox.2017.09.015
doi: 10.1016/j.aquatox.2017.09.015
Nyúl E, Kuzma M, Mayer M, Lakatos S, Almási A, Perjési P (2018) HPLC study on Fenton-reaction initiated oxidation of salicylic acid. Biological relevance of the reaction in intestinal biotransformation of salicylic acid. Free Radic Res 52:1040–1051. https://doi.org/10.1080/10715762.2018.1517260
doi: 10.1080/10715762.2018.1517260
Oliveira LLD, Antunes SC, Gonçalves F, Rocha O, Nunes B (2015) Evaluation of ecotoxicological effects of drugs on Daphnia magna using different enzymatic biomarkers. Ecotoxicol Environ Saf 119:123–131. https://doi.org/10.1016/j.ecoenv.2015.04.028
doi: 10.1016/j.ecoenv.2015.04.028
Osorio V, Larrañaga A, Aceña J, Pérez S, Barceló D (2016) Concentration and risk of pharmaceuticals in freshwater systems are related to the population density and the livestock units in Iberian Rivers. Sci Total Environ 540:267–277. https://doi.org/10.1016/j.scitotenv.2015.06.143
doi: 10.1016/j.scitotenv.2015.06.143
Pagano M, Capillo G, Sanfilippo M, Palato S, Trischitta F, Manganaro A, Faggio C (2016) Evaluation of functionality and biological responses of Mytilus galloprovincialis after exposure to quaternium-15 (methenamine 3-chloroallylochloride). Molecules. https://doi.org/10.3390/molecules21020144
Paoletti F, Mocali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol 186:209–220. https://doi.org/10.1016/0076-6879(90)86110-h
doi: 10.1016/0076-6879(90)86110-h
Parolini M, Binelli A, Provini A (2011) Chronic effects induced by ibuprofen on the freshwater bivalve Dreissena polymorpha. Ecotoxicol Environ Saf 74:1586–1594. https://doi.org/10.1016/j.ecoenv.2011.04.025
doi: 10.1016/j.ecoenv.2011.04.025
Parrino V, De Marco G, Minutoli R, Lo Paro G, Giannetto A, Cappello T, De Plano LM, Cecchini S, Fazio F (2021a) Effects of pesticides on Chelon labrosus (Risso, 1827) evaluated by enzymatic activities along the north eastern Sicilian coastlines (Italy). Eur Zool J 88:540–548. https://doi.org/10.1080/24750263.2021.1905090
doi: 10.1080/24750263.2021.1905090
Parrino V, Costa G, Giannetto A, De Marco G, Cammilleri G, Acar Ü, Piccione G, Fazio F (2021b) Trace elements (Al, Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn) in Mytilus galloprovincialis and Tapes decussatus from Faro and Ganzirri Lakes (Sicily, Italy): flow cytometry applied for hemocytes analysis. J Trace Elem Med Biol 68:126870. https://doi.org/10.1016/j.jtemb.2021.12687
doi: 10.1016/j.jtemb.2021.12687
Piscopo M, Notariale R, Rabbito D, Ausió J, Olanrewaju OS, Guerriero G (2018) Mytilus galloprovincialis (Lamarck, 1819) spermatozoa: hsp70 expression and protamine-like protein property studies. Environ Sci Pollut Res 25:12957–12966
doi: 10.1007/s11356-018-1570-9
Pozdnyakov IP, Plyusnin VF, Grivin VP, Oliveros E (2015) photochemistry of Fe(III) complexes with salicylic acid derivatives in aqueous solutions. J Photochem Photobiol A 307–308:9–15. https://doi.org/10.1016/j.jphotochem.2015.03.018
doi: 10.1016/j.jphotochem.2015.03.018
Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106–117. https://doi.org/10.1016/j.marenvres.2013.07.006
doi: 10.1016/j.marenvres.2013.07.006
Rogowska J, Cieszynska-Semenowicz M, Ratajczyk W, Wolska L (2020) Micropollutants in treated wastewater. Ambio 49:487–503. https://doi.org/10.1007/s13280-019-01219-5
doi: 10.1007/s13280-019-01219-5
Rossi F, Palombella S, Pirrone C, Mancini G, Bernardini G, Gornati R (2016) Evaluation of tissue morphology and gene expression as biomarkers of pollution in mussel Mytilus galloprovincialis caging experiment. Aquat Toxicol 181:57–66. https://doi.org/10.1016/j.aquatox.2016.10.018
doi: 10.1016/j.aquatox.2016.10.018
Sim W-J, Lee J-W, Lee E-S, Shin S-K, Hwang S-R, Oh J-E (2011) Occurrence and distribution of pharmaceuticals in wastewater from households, livestock farms, hospitals and pharmaceutical manufactures. Chemosphere 82:179–186. https://doi.org/10.1016/j.chemosphere.2010.10.026
doi: 10.1016/j.chemosphere.2010.10.026
Stara A, Pagano M, Albano M, Savoca S, Di Bella G, Albergamo A, Koutkova Z, Sandova M, Velisek J, Fabrello J, Matozzo V, Faggio C (2021) Effects of long-term exposure of Mytilus galloprovincialis to thiacloprid: a multibiomarker approach. Environ Pollut 289:117892. https://doi.org/10.1016/j.envpol.2021.117892
doi: 10.1016/j.envpol.2021.117892
Sureda A, Box A, Tejada S, Blanco A, Caixach J, Deudero S (2011) Biochemical responses of Mytilus galloprovincialis as biomarkers of acute environmental pollution caused by the Don Pedro oil spill (Eivissa Island, Spain). Aquat Toxicol 101:540–549. https://doi.org/10.1016/j.aquatox.2010.12.011
doi: 10.1016/j.aquatox.2010.12.011
Świacka K, Maculewicz J, Smolarz K, Szaniawska A, Caban M (2019) Mytilidae as model organisms in the marine ecotoxicology of pharmaceuticals – a review. Environ Pollut 254:113082. https://doi.org/10.1016/j.envpol.2019.113082
doi: 10.1016/j.envpol.2019.113082
Świacka K, Michnowska A, Maculewicz J, Caban M, Smolarz K (2021) Toxic effects of NSAIDs in non-target species: a review from the perspective of the aquatic environment. Environ Pollut 273:115891. https://doi.org/10.1016/j.envpol.2020.115891
doi: 10.1016/j.envpol.2020.115891
Szwajgier D (2013) Anticholinesterase activity of phenolic acids and their derivatives. Z Naturforsch C 68:125–132
doi: 10.1515/znc-2013-3-408
Trombini C, Hampel M, Blasco J (2019) Assessing the effect of human pharmaceuticals (carbamazepine, diclofenac and ibuprofen) on the marine clam Ruditapes philippinarum: an integrative and multibiomarker approach. Aquat Toxicol 208:146–156. https://doi.org/10.1016/j.aquatox.2019.01.004
doi: 10.1016/j.aquatox.2019.01.004
Trombini C, Kazakova J, Montilla-López A, Fernández-Cisnal R, Hampel M, Fernández-Torres R, Bello-López MÁ, Abril N, Blasco J (2021) Assessment of pharmaceutical mixture (ibuprofen, ciprofloxacin and flumequine) effects to the crayfish Procambarus clarkii: a multilevel analysis (biochemical, transcriptional and proteomic approaches). Environ Res 200:111396. https://doi.org/10.1016/j.envres.2021.111396
doi: 10.1016/j.envres.2021.111396
Vassalli QA, Caccavale F, Avagnano S, Murolo A, Guerriero G, Fucci L, Ausiò J, Piscopo M (2015) New insights into protamine-like component organization in Mytilus galloprovincialis' sperm chromatin. DNA Cell Biol 34:162–169
doi: 10.1089/dna.2014.2631
Vignet C, Cappello T, Fu Q, Lajoie K, De Marco G, Clérandeau C, Mottaz H, Maisano M, Hollender J, Schirmer K, Cachot J (2019) Imidacloprid induces adverse effects on fish early life stages that are more severe in Japanese medaka (Oryzias latipes) than in zebrafish (Danio rerio). Chemosphere 225:470–478. https://doi.org/10.1016/j.chemosphere.2019.03.002
doi: 10.1016/j.chemosphere.2019.03.002
Wills DE (1987) Evaluation of lipid peroxidation in lipids and biological membranes. In: Snell K, Mullock B (eds) Biochemical Toxicology: A Practical Approach. IRL Press, Washington, pp 127–150
Yilmaz G, Kaya Y, Vergili I, Beril Gönder Z, Özhan G, Ozbek Celik B, Altinkum SM, Bagdatli Y, Boergers A, Tuerk J (2017) Characterization and toxicity of hospital wastewaters in Turkey. Environ Monit Assess 189:55. https://doi.org/10.1007/s10661-016-5732-2
doi: 10.1007/s10661-016-5732-2
Zivna D, Sehonova P, Plhalova L, Marsalek P, Blahova J, Prokes M, Divisova L, Stancova V, Dobsikova R, Tichy F, Siroka Z, Svobodova Z (2015) Effect of salicylic acid on early life stages of common carp (Cyprinus carpio). Environ Toxicol Pharmacol 40:319–325. https://doi.org/10.1016/j.etap.2015.06.018
doi: 10.1016/j.etap.2015.06.018
Zivna D, Blahova J, Siroka Z, Plhalova L, Marsalek P, Doubkova V, Zelinska G, Vecerek V, Tichy F, Sehonova P, Svobodova Z (2016) The effects of salicylic acid on juvenile zebrafish Danio rerio under flow-through conditions. Bull Environ Contam Toxicol 97:323–330. https://doi.org/10.1007/s00128-016-1877-5
doi: 10.1007/s00128-016-1877-5

Auteurs

Giuseppe De Marco (G)

Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, 98166, Messina, Italy.

Sabrine Afsa (S)

Research Unit of Analysis and Process Applied to The Environment - APAE (UR17ES32) Higher Institute of Applied Sciences and Technology of Mahdia, University of Monastir, 5000, Monastir, Tunisia.

Mariachiara Galati (M)

Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, 98166, Messina, Italy.

Giulia Guerriero (G)

Department of Biology, University of Naples "Federico II", 80126, Naples, Italy.

Angela Mauceri (A)

Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, 98166, Messina, Italy.

Hedi Ben Mansour (H)

Research Unit of Analysis and Process Applied to The Environment - APAE (UR17ES32) Higher Institute of Applied Sciences and Technology of Mahdia, University of Monastir, 5000, Monastir, Tunisia.

Tiziana Cappello (T)

Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, 98166, Messina, Italy. tcappello@unime.it.

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