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Histopathological effects in gills and liver of Sparus aurata following acute and chronic exposures to erythromycin and oxytetracycline

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Abstract

Due to their worldwide use and environmental persistence, antibiotics are frequently detected in various aquatic compartments. Their toxic properties raise environmental concerns to non-target organisms. Histopathology data is frequently applied in ecotoxicology studies to assess the effects of different classes of environmental stressors in fish, including antibiotics. Tissue alterations in gills and liver of gilthead seabream (Sparus aurata) individuals acutely (96 h) and chronically (28 days) exposed to environmentally relevant concentrations of the antibiotics erythromycin (ERY: 0.0002–200 μg/L) and oxytetracycline (OTC: 0.0004–400 μg/L), including a control non-exposed group, were evaluated. Several disorders (circulatory, regressive, progressive, and inflammatory) were observed in both organs of all exposed animals. The hereby obtained data showed a higher and significant increase in gill histopathological index of organisms acutely exposed to ERY and of those chronically exposed to OTC. In terms of categorical lesions, only a significant increase of regressive and progressive alterations occurred in gills after chronic exposure to OTC. For the liver, a significant increase in pathological index was also detected, as well as regressive changes, after chronic exposure to OTC. Furthermore, the present study indicates that most of the changes observed in gills and liver were of mild to moderate severity, which might be adaptive or protective, non-specific, and mostly reversible. Despite being observed, irreversible lesions were not significant in any of the fish organs analyzed. Although there were histological changes, gill apparatus was considered still functionally normal, as well as liver tissue, not supporting the occurrence of severe toxicity. In general, the observed histological changes were not stressor-specific, and toxicological mechanistic explanations for the alterations observed in gills and liver are presented. The obtained data showed that histopathological biomarkers can be successfully applied in ecotoxicological studies, evidencing their relevance, responsivity, and complementarity to other biochemical biomarker-based approaches.

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References

  • Abdel-Hameid N-AH (2007) Protective role of dimethyl diphenyl bicarboxylate (DDB) against erythromycin induced hepatotoxicity in male rats. Toxicol in Vitro 21(4):618–625

    Article  CAS  Google Scholar 

  • Ahmed MK, Al-Mamun MH, Parvin E, Akter MS, Khan MS (2013) Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, Tilapia (Oreochromis mossambicus). Exp Toxicol Pathol 65(6):903–909

    Article  CAS  Google Scholar 

  • Bano D, Young KW, Guerin CJ, Lefeuvre R, Rothwell NJ, Naldini L, Rizzuto R, Carafoli E, Nicotera P (2005) Cleavage of the plasma membrane Na/Ca exchanger in excitotoxicity. Cell 120:275–285

    Article  CAS  Google Scholar 

  • Barišić J, Dragun Z, Ramani S, Filipović-Marijić V, Krasnići N, Čož-Rakovac R, Kostov V, Rebok K, Jordanova M (2015) Evaluation of histopathological alterations in the gills of Vardar chub (Squalius vardarensis Karaman) as an indicator of river pollution. Ecotoxicol Environ Saf 118:158–166

    Article  CAS  Google Scholar 

  • Batchu SR, Panditi VR, O'Shea KE, Gardinali PR (2014) Photodegradation of antibiotics under simulated solar radiation: implications for their environmental fate. Sci Total Environ 470–471:299–310

    Article  CAS  Google Scholar 

  • Benzo CA (1987) Effects of oxytetracycline treatment on enzymes of hepatic glycogen metabolism in genetically diabetic (db/db) mice. Biochem Med Metab Biol 37(1):42–50

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34

    Article  Google Scholar 

  • Caballero MJ, Izquierdo MS, Kjørsvik E, Fernàndez AJ, Rosenlund G (2004) Histological alterations in the liver of sea bream, Sparus aurata L., caused by short- or long-term feeding with vegetable oils. Recovery of normal morphology after feeding fish oil as the sole lipid source. J Fish Dis 27:531–541

    Article  CAS  Google Scholar 

  • Casarett LJ, Klaassen CD, Amdur MO, Doull J (2008) Casarett and Doull’s toxicology: the basic science of poisons, 7th edn. McGraw-Hill, Health Professions Division, New York, pp 557–551

    Google Scholar 

  • Cengiz EI, Unlu E (2003) Histopathology of gills in mosquitofish Gambusia affinis after long-term exposure to sublethal concentrations of malathion. J Environ Sci Health B 38(5):581–589

    Article  CAS  Google Scholar 

  • Chaoui L, Kara MH, Faur E, Quignard JP (2006) Growth and reproduction of the gilthead seabream Sparus aurata in Mellah lagoon (north-eastern Algeria). Sci Mar 70(3):545–552

    Article  Google Scholar 

  • Chen H, Liu S, Xu XR, Liu SS, Zhou GJ, Sun KF, Zhao JL, Ying GG (2015) Antibiotics in typical marine aquaculture farms surrounding Hailing Island, South China: occurrence, bioaccumulation and human dietary exposure. Mar Pollut Bull 90:81–187

    Article  CAS  Google Scholar 

  • Costa PM, Diniz MS, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, Costa MH (2009) Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: a weighted indices approach. Aquat Toxicol 92:202–212

    Article  CAS  Google Scholar 

  • Dębska J, Kot-Wasik A, Namieśnik J (2004) Fate and analysis of pharmaceutical residues in the aquatic environment. Crit Rev Anal Chem 34(1):51–67

    Article  CAS  Google Scholar 

  • Decree-Law, 113/2013, de 7 de agosto. D.R. 151, Série I. Relativo à proteção dos animais utilizados para fins científicos. Ministério da Agricultura, do Mar, do Ambiente e do Ordenamento do Território

  • Doi AM, Stoskopf MK (2000) The kinetics of oxytetracycline degradation in deionized water under varying temperature, pH, light, substrate, and organic matter. J Aquat Anim Health 12:246–253

    Article  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  CAS  Google Scholar 

  • Fournie JW, Summers K, Courtney LA, Engle VD (2001) Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. J Aquat Anim Health 13:105–116

    Article  Google Scholar 

  • Gaw S, Thomas KV, Hutchinson TH (2014) Sources, impacts and trends of pharmaceuticals in the marine and coastal environment. Philos Trans R Soc B 369:20130572

    Article  Google Scholar 

  • Grenier D, Huot MP, Mayrand D (2000) Iron-chelating activity of tetracyclines and its impact on the susceptibility of Actinobacillus actinomycetemcomitans to these antibiotics. Antimicrob Agents Chemother 44(3):763–766

    Article  CAS  Google Scholar 

  • Guardiola FA, Cuesta A, Meseguer J, Martínez S, Martínez-Sanchez MJ, Perez-Sirvent C, Esteban MA (2013) Accumulation, histopathology and immunotoxicological effects of waterborne cadmium on gilthead seabream (Sparus aurata). Fish Shellfish Immunol 35:792–800

    Article  CAS  Google Scholar 

  • Guardiola FA, Gonzalez-Párraga P, Meseguer J, Cuesta A, Esteban MA (2014) Modulatory effects of deltamethrin-exposure on the immune status, metabolism and oxidative stress in gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 36(1):120–129

    Article  CAS  Google Scholar 

  • Guardiola FA, Cerezuela R, Meseguer J, Esteban MA (2012) Modulation of the immune parameters and expression of genes of gilthead seabream (Sparus aurata L.) by dietary administration of oxytetracycline. Aquaculture. 334–337:51–57

    Article  CAS  Google Scholar 

  • Guerra W, Silva-Caldeira PP, Terenzi H, Pereira-Maia EC (2016) Impact of metal coordination on the antibiotic and non-antibiotic activities of tetracycline-based drugs. Coord Chem Rev 327–328:188–199

    Article  CAS  Google Scholar 

  • Gulkowska A, He Y, So MK, Yeung LW, Leung HW, Giesy JP, Lam PK, Martin M, Richardson BJ (2007) The occurrence of selected antibiotics in Hong Kong coastal waters. Mar Pollut Bull 54(8):1287–1293

    Article  CAS  Google Scholar 

  • Hadi AA, Aalwan SF (2012) Histological changes in gills, liver and kidney of fresh water fish, Tilapia zillii, exposed to aluminum. Int J Pharm Life Sci 3(11):2071–2081

    CAS  Google Scholar 

  • Hall DA, Jackson DS (1983) International review of connective tissue research, vol 10. Academic Press Inc, New York, pp 333–378

    Google Scholar 

  • He J, Guo S, Zhu F, Zhu J, Chen Y, Huang C, Gao JM, Dong QX, Xuan Y-X, Li C-Q (2013) A zebrafish phenotypic assay for assessing drug-induced hepatotoxicity. J Pharmacol Toxicol Methods 67(1):25–32

    Article  CAS  Google Scholar 

  • Himmelsbach M, Buchberger W (2005) Residue analysis of oxytetracycline in water and sediment samples by high-performance liquid chromatography and immunochemical techniques. Microchim Acta 151:67–72

    Article  CAS  Google Scholar 

  • Kim J-W, Ishibashi H, Yamauchi R, Ichikawa N, Takao Y, Hirano M, Koga M, Arizono K (2009) Acute toxicity of pharmaceutical and personal care products on freshwater crustacean (Thamnocephalus platyurus) and fish (Oryzias latipes). J Toxicol Sci 34(2):227–232

    Article  CAS  Google Scholar 

  • Kostić J, Kolarević S, Kračun-Kolarević M, Aborgiba M, Gačić Z, Paunović M, Višnjić-Jeftić Ž, Rašković B, Poleksić V, Lenhardt M, Vuković-Gačić B (2017) The impact of multiple stressors on the biomarkers response in gills and liver of freshwater breams during different seasons. Sci Total Environ 601:1670–1681

    Article  CAS  Google Scholar 

  • Lauriano ER, Calo M, Silvestri G, Zaccone D, Pergolizzi S, Cascio PL (2012) Mast cells in the intestine and gills of the sea bream, Sparus aurata, exposed to a polychlorinated biphenyl, PCB 126. Acta Histochem 114(2):166–171

    Article  CAS  Google Scholar 

  • Limbu SM, Zhou L, Sun SX, Zhang ML, Du ZY (2018) Chronic exposure to low environmental concentrations and legal aquaculture doses of antibiotics cause systemic adverse effects in Nile tilapia and provoke differential human health risk. Environ Int 115:205–219

    Article  CAS  Google Scholar 

  • Liu J, Lu G, Cai Y, Wu D, Yan Z, Wang Y (2017) Modulation of erythromycin-induced biochemical responses in crucian carp by ketoconazole. Environ Sci Pollut Res 24:5285–5292

    Article  CAS  Google Scholar 

  • Liu J, Lu G, Ding J, Zhang Z, Wang Y (2014) Tissue distribution, bioconcentration, metabolism, and effects of erythromycin in crucian carp (Carassius auratus). Sci Total Environ 490:914–920

    Article  CAS  Google Scholar 

  • Lunestad BT, Goksøyr J (1990) Reduction in the antibacterial effect of oxytetracycline in sea water by complex formation with magnesium and calcium. Dis Aquat Org 9:67–72

    Article  CAS  Google Scholar 

  • Madureira TV, Rocha MJ, Cruzeiro C, Rodrigues I, Monteiro RAF, Rocha E (2012) The toxicity potential of pharmaceuticals found in the Douro River estuary (Portugal): evaluation of impacts on fish liver, by histopathology, stereology, vitellogenin and CYP1A immunohistochemistry, after sub-acute exposures of the zebrafish model. Environ Toxicol Pharmacol 34:34–45

    Article  CAS  Google Scholar 

  • Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648

    Article  Google Scholar 

  • Mekkawy IAA, Mahmoud UM, Wassif ET, Naguib M (2012) Protective roles of tomato paste and vitamin E on cadmium-induced histological and histochemical changes of liver of Oreochromis niloticus (Linnaeus,1758). J Fisher Aqua Sci 7:240–265

    Article  CAS  Google Scholar 

  • Mela MR, Ventura F, Carvalho DF, Pelletier CE, Ribeiro CA (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicol Environ Saf 68:426–435

    Article  CAS  Google Scholar 

  • Mohamed FA (2009) Histopathological studies on Tilapia zillii and Solea vulgaris from Lake Qarun, Egypt. World J Fish Mar Sci 1(1):29–39

    Google Scholar 

  • Monteiro SM, Rocha E, Fontaínhas-Fernandes A, Sousa M (2008) Quantitative histopathology of Oreochromis niloticus gills after copper exposure. J Fish Biol 73:1376–1392

    Article  CAS  Google Scholar 

  • Moreno-González R, Rodriguez-Mozaz S, Gros M, Barceló D, León VM (2015) Seasonal distribution of pharmaceuticals in marine water and sediment from a Mediterranean coastal lagoon (SE Spain). Environ Res 138:326–344

    Article  CAS  Google Scholar 

  • Moreno-González R, Rodríguez-Mozaz S, Gros M, Pérez-Cánovas E, Barceló D, Leóna VM (2014) Input of pharmaceuticals through coastal surface watercourses into a Mediterranean lagoon (Mar Menor, SE Spain): sources and seasonal variations. Sci Total Environ 490:59–72

    Article  CAS  Google Scholar 

  • Mumford S, Heidel J, Smith C, Morrison J, MacConnell B, Blazer V, (2007) Fish histology and histopathology, 4th edn. U.S. Fish and Wildfife Service, National Conservation Training Center, West Virginia, pp 357

  • Nazeri S, Farhangi M, Modarres S (2017) The effect of different dietary inclusion levels of rutin (a flavonoid) on some liver enzyme activities and oxidative stress indices in rainbow trout, Oncorhynchus mykiss (Walbaum) exposed to oxytetracycline. Aquac Res 48:4356–4362

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lister A, Van der Kraak G, Lee LE, Van Meer T, MacKinnon MD, Dixon DG (2006) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water. Ecotoxicol Environ Saf 63(3):365–377

    Article  CAS  Google Scholar 

  • Noble D, Herchuelz A (2007) Role of Na/Ca exchange and the plasma membrane Ca2+- ATPase in cell function. Conference on Na/Ca exchange. EMBO Rep 8(3):228–232

    Article  CAS  Google Scholar 

  • Nunes B, Antunes SC, Gomes R, Campos JC, Braga MR, Ramos AS, Correia AT (2015a) Acute effects of tetracycline exposure in the freshwater fish Gambusia holbrooki: antioxidant effects, neurotoxicity and histological alterations. Arch Environ Contam Toxicol 68:371–381

    Article  CAS  Google Scholar 

  • Nunes B, Campos JC, Gomes R, Braga MR, Ramos AS, Antunes SC, Correia AT (2015b) Ecotoxicological effects of salicylic acid in the freshwater fish Salmo trutta fario: antioxidant mechanisms and histological alterations. Environ Sci Pollut Res 22(1):667–678

    Article  CAS  Google Scholar 

  • OECD (1992) Test no. 203: fish, acute toxicity test. OECD guidelines for the testing of chemicals, section 2. OECD Publishing, Paris, pp 9

    Book  Google Scholar 

  • OECD (2000) Test no. 215: fish, juvenile growth test. OECD guidelines for the testing of chemicals. OECD, Paris, pp 16

    Book  Google Scholar 

  • Oliveira R, McDonough S, Ladewig JC, Soares AM, Nogueira AJ, Domingues I (2013) Effects of oxytetracycline and amoxicillin on development and biomarkers activities of zebrafish (Danio rerio). Environ Toxicol Pharmacol 36(3):903–912

    Article  CAS  Google Scholar 

  • Olsson PE, Larsson A, Haux C (1996) Influence of seasonal changes in water temperature on cadmium inducibility of hepatic and renal metallothionein in rainbow trout. Mar Environ Res 42:41–44

    Article  CAS  Google Scholar 

  • Pal S, Kokushi E, Koyama J, Uno S, Ghosh AR (2012) Histopathological alterations in gill, liver and kidney of common carp exposed to chlorpyrifos. J Environ Sci Health B 47(3):180–195

    Article  CAS  Google Scholar 

  • Pari L, Gnanasoundari M (2006) Influence of naringenin on oxytetracycline mediated oxidative damage in rat liver. Basic Clin Pharmacol Toxicol 98:456–461

    Article  CAS  Google Scholar 

  • Peplow D, Edmonds R (2005) The effects of mine waste contamination at multiple levels of biological organization. Ecol Eng 24:101–119

    Article  Google Scholar 

  • Ramzy EM (2014) Toxicity and stability of sodium cyanide in fresh water fish Nile tilapia. Water Sci 28:42–50

    Article  Google Scholar 

  • Rašković B, Čičovački S, Ćirić M, Marković Z, Poleksić V (2016) Integrative approach of histopathology and histomorphometry of common carp (Cyprinus carpio L.) organs as a marker of general fish health state in pond culture. Aquac Res 47:3455–3463

    Article  Google Scholar 

  • Rašković B, Jarić I, Koko V, Spasić M, Dulić Z, Marković Z, Poleksić V (2013) Histopathological indicators: a useful fish health monitoring tool in common carp (Cyprinus carpio Linnaeus, 1758) culture. Cent Eur J Biol 8(10):975–985

    Google Scholar 

  • Rašković B, Poleksić V, Živić I, Spasić M (2010) Histology of carp (Cyprinus carpio L.) gills and pond water quality in semiintensive production. Bulg J Agric Sci 16(3):253–262

    Google Scholar 

  • Ribeiro OCA, Vollaire Y, Sanchez-Chardi A, Roche H (2005) Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat Toxicol 74(1):53–69

    Article  CAS  Google Scholar 

  • Rodrigues S, Antunes SC, Correia AT, Nunes B (2016) Acute and chronic effects of erythromycin exposure on oxidative stress and genotoxicity parameters of Oncorhynchus mykiss. Sci Total Environ 545–546:591–600

    Article  CAS  Google Scholar 

  • Rodrigues S, Antunes SC, Correia AT, Nunes B (2017b) Rainbow trout (Oncorhynchus mykiss) pro-oxidant and genotoxic responses following acute and chronic exposure to the antibiotic oxytetracycline. Ecotoxicology. 26:104–117

    Article  CAS  Google Scholar 

  • Rodrigues S, Antunes SC, Nunes BS, Correia AT (2015) Histological assessment of gills and liver of Oncorhynchus mykiss exposed to sublethal concentrations of the antibiotic erythromycin. Front Mar Sci Conference Abstract: XV European Congress of Ichthyology. https://doi.org/10.3389/conf.FMARS.2015.03.00203

  • Rodrigues S, Antunes SC, Nunes B, Correia AT (2017a) Histological alterations in gills and liver of rainbow trout (Oncorhynchus mykiss) after exposure to the antibiotic oxytetracycline. Environ Toxicol Pharmacol 53:164–176

    Article  CAS  Google Scholar 

  • Schwaiger J, Ferling H, Mallow U, Wintermayr H, Negele RD (2004) Toxic effects of the non-steroidal antiinflammatory drug diclofenac. Part I: histopathological alterations and bioaccumulation in rainbow trout. Aquat Toxicol 68(2):141–150

    Article  CAS  Google Scholar 

  • Schwaiger J, Fent K, Stecher H, Ferling H, Negele RD (1996) Effects of sublethal concentrations of triphenyltinacetate on raibow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 30:327–334

    Article  CAS  Google Scholar 

  • Secombes CJ, Chappell LH (1996) Fish immune responses to experimental and natural infection with helminth parasites. Annu Rev Fish Dis 6:167–177

    Article  Google Scholar 

  • Serezli R, Çagırgan H, Okumus I, Akhan SL, Balta F (2005) The effect of oxytetracycline on non-specific immune response in sea bream (Sparus aurata L. 1758). Turk J Vet Anim Sci 29:31–35

    CAS  Google Scholar 

  • Singh P, Singh L, Mondal S, Kumar S, Singh I (2014) Erythromycin-induced genotoxicity and hepatotoxicity in mice pups treated during prenatal and postnatal period. Fundam Clin Pharmacol 28(5):519–529

    Article  CAS  Google Scholar 

  • Smith P, Niland T, O'Domhnaill F, O'Tuathaigh G, Hiney M (1996) Influence of marine sediments and divalent cations on the activity of oxytetracycline against Listonella anguillarum. Bull Eur Assoc Fish Pathol 16:54–57

    Google Scholar 

  • Soler F, Reja A, Garcia-Rubio L, Miguez MDP, Roncero V (1996) Anatomo-pathological effect of OTC in tench (Tinca tinca). Toxicol Lett 88:104

    Article  Google Scholar 

  • Souid G, Souayed N, Haouas Z, Maaroufi K (2018) Does the phycotoxin okadaic acid cause oxidative stress damages and histological alterations to seabream (Sparus aurata)? Toxicon. 144:55–60

    Article  CAS  Google Scholar 

  • Stoyanova S, Yancheva VS, Velcheva I, Uchikova E, Georgieva E (2015) Histological alterations in common carp (Cyprinus carpio Linnaeus, 1758) gills as potential biomarkers for fungicide contamination. Braz Arch Biol Technol 58:757–764

    Article  CAS  Google Scholar 

  • Sturgill MG, Lambert GH (1997) Xenobiotic-induced hepatotoxicity: mechanisms of liver injury and methods of monitoring hepatic function. Clin Chem 8(2):1512–1526

    Google Scholar 

  • Suga N, Ogo M, Suzuki S (2013) Risk assessment of oxytetracycline in water phase to major sediment bacterial community: a water-sediment microcosm study. Environ Toxicol Pharmacol 36(1):142–148

    Article  CAS  Google Scholar 

  • Szarek J, Siwicki A, Wojtacka J, Kolman R, Babinska I, Zmysłowska I, Guziur J, Gesek M (2009) The effect of oxytetracycline and lysozyme dimer on the morphology of gills in Siberian sturgeon. J Comp Pathol 41(4):286

    Article  Google Scholar 

  • Takashima F, Hibiya T (1995) An atlas of fish histology: normal and pathological features, 2nd edn. Kodensha Ltd., Tokyo

    Google Scholar 

  • Traversi I, Gioacchini G, Scorolli A, Mita DG, Carnevali O, Mandich A (2014) Alkylphenolic contaminants in the diet: Sparus aurata juveniles hepatic response. Gen Comp Endocrinol 205:185–196

    Article  CAS  Google Scholar 

  • Valente L, Cornet J, Donnay-Moreno C, Gouygou J-P, Berge J-P, Bacelar M, Escórcio C, Rocha E, Malhão F, Cardinal M (2011) Quality differences of gilthead sea bream from distinct production systems in southern Europe: intensive, integrated, semi-intensive or extensive systems. Food Control 22(5):708–717

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149

    Article  Google Scholar 

  • Varadarajan R, Sankar HHS, Jose J, Philip B (2014) Sublethal effects of phenolic compounds on biochemical, histological and ionoregulatory parameters in a tropical teleost fish Oreochromis mossambicus (Peters). Int J Sci Res Publ 4(3):1–12

    Google Scholar 

  • Viluksela M, Hanhijarvi H, Husband RFA, Kosma V-M, Collan Y, Mannisto PT (1988) Comparative liver toxicity of various erythromycin derivatives in animals. J Antimicrob Chemother 21(Suppl. D):9–27

    Article  CAS  Google Scholar 

  • Wang J, Zhang P, Shen Q, Wang Q, Liu D, Li J, Wang L (2013) The effects of cadmium exposure on the oxidative state and cell death in the gill of freshwater crab Sinopotamon henanense. PLoS One 8(5):e64020

    Article  CAS  Google Scholar 

  • Wilson JM, Bunte RM, Carty AJ (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 48(6):785–799

    CAS  Google Scholar 

  • Wojtacka J, Szarek J, Babińska I, Andrzejewska A (2011) Modulating effect of lysozyme dimer (KLP-602) on the morphological pattern of hepatopancreas of Siberian sturgeon (Acipenser baeri, Brandth 1869) following oxytetracycline application. Bull Vet Inst Pulawy 55:299–304

    Google Scholar 

  • Wolf JC, Baumgartner WA, Blazer VS, Camus AC, Engelhardt JA, Fournie JW, Frasca S, Groman DB, Kent ML, Khoo LH, Law JM, Lombardini ED, RuehlFehlert C, Segner HE, Smith SA, Spitsbergen JM, Weber K, Wolfe MJ (2015) Nonlesions, misdiagnoses, missed diagnoses, and other interpretive challenges in fish histopathology studies: a guide for investigators, authors, reviewers, and readers. Toxicol Pathol 43(3):297–325

    Article  Google Scholar 

  • Wolf JC, Wolfe MJ (2005) A brief overview of nonneoplastic hepatic toxicity in fish. Toxicol Pathol 33:75–85

    Article  CAS  Google Scholar 

  • Yancheva V, Velcheva I, Stoyanova S, Georgieva E (2016) Histological biomarkers in fish as a tool in ecological risk assessment and monitoring programs: a review. Appl Ecol Environ Res 14(1):47–75

    Article  Google Scholar 

  • Yonar ME, Yonar SM, Silici S (2011) Protective effect of propolis against oxidative stress and immunosuppression induced by oxytetracycline in rainbow trout (Oncorhynchus mykiss, W.). Fish Shellfish Immun 31:318–325

    Article  CAS  Google Scholar 

  • Zena R, Speciale A, Calabrò C, Caló M, Palombieri D, Saija A, Cimino F, Trombetta D, Lo Cascio P (2015) Exposure of sea bream (Sparus aurata) to toxic concentrations of benzo[a]pyrene: possible human health effect. Ecotoxicol Environ Saf 122:116–125

    Article  CAS  Google Scholar 

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Funding

Sara Rodrigues and Sara C. Antunes received a Ph.D. fellowship (SFRH/BD/84061/2012) and a post doc grant (SFRH/BPD/109951/2015), respectively, by the Portuguese Foundation for Science and Technology (FCT). Bruno Nunes was hired through the Investigator FCT program (IF/01744/2013). This research was partially supported by the Strategic Funding UID/Multi/04423/2019 through national funds provided by FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020. This research was also financially supported for CESAM (UID/AMB/50017 - POCI-01-0145-FEDER-007638), to FCT/MCTES through national funds (PIDDAC), and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.

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Correspondence to Alberto Teodorico Correia.

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This method took into consideration the Portuguese animal welfare testing regulations (Decree-Law 113/2013) and is in agreement with the American Veterinary Medical Association Guidelines for the Euthanasia of Animals.

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Rodrigues, S., Antunes, S.C., Nunes, B. et al. Histopathological effects in gills and liver of Sparus aurata following acute and chronic exposures to erythromycin and oxytetracycline. Environ Sci Pollut Res 26, 15481–15495 (2019). https://doi.org/10.1007/s11356-019-04954-0

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