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

  • Sara Rodrigues
  • Sara C. Antunes
  • Bruno Nunes
  • Alberto Teodorico CorreiaEmail author
Research Article
  • 60 Downloads

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.

Keywords

Sparus aurata Acute and chronic exposures Erythromycin Oxytetracycline Tissue damages 

Notes

Funding information

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.

Compliance with ethical standards

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.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Abdel-Hameid N-AH (2007) Protective role of dimethyl diphenyl bicarboxylate (DDB) against erythromycin induced hepatotoxicity in male rats. Toxicol in Vitro 21(4):618–625Google Scholar
  2. 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):903–909Google Scholar
  3. 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 120:275–285Google Scholar
  4. 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 118:158–166Google Scholar
  5. 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 470–471:299–310Google Scholar
  6. 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):42–50Google Scholar
  7. 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 22:25–34Google Scholar
  8. 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 27:531–541Google Scholar
  9. 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 557–551Google Scholar
  10. 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):581–589Google Scholar
  11. 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):545–552Google Scholar
  12. 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 90:81–187Google Scholar
  13. 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 92:202–212Google Scholar
  14. Dębska J, Kot-Wasik A, Namieśnik J (2004) Fate and analysis of pharmaceutical residues in the aquatic environment. Crit Rev Anal Chem 34(1):51–67Google Scholar
  15. 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 TerritórioGoogle Scholar
  16. 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 12:246–253Google Scholar
  17. 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 85:97–177Google Scholar
  18. 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 13:105–116Google Scholar
  19. Gaw S, Thomas KV, Hutchinson TH (2014) Sources, impacts and trends of pharmaceuticals in the marine and coastal environment. Philos Trans R Soc B 369:20130572Google Scholar
  20. 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):763–766Google Scholar
  21. 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 35:792–800Google Scholar
  22. 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):120–129Google Scholar
  23. 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. 334–337:51–57Google Scholar
  24. 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 327–328:188–199Google Scholar
  25. 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):1287–1293Google Scholar
  26. 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):2071–2081Google Scholar
  27. Hall DA, Jackson DS (1983) International review of connective tissue research, vol 10. Academic Press Inc, New York, pp 333–378Google Scholar
  28. 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):25–32Google Scholar
  29. Himmelsbach M, Buchberger W (2005) Residue analysis of oxytetracycline in water and sediment samples by high-performance liquid chromatography and immunochemical techniques. Microchim Acta 151:67–72Google Scholar
  30. 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):227–232Google Scholar
  31. 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 601:1670–1681Google Scholar
  32. 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):166–171Google Scholar
  33. 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 115:205–219Google Scholar
  34. 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 24:5285–5292Google Scholar
  35. 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 490:914–920Google Scholar
  36. 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 9:67–72Google Scholar
  37. 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 34:34–45Google Scholar
  38. Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648Google Scholar
  39. 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 7:240–265Google Scholar
  40. 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 68:426–435Google Scholar
  41. Mohamed FA (2009) Histopathological studies on Tilapia zillii and Solea vulgaris from Lake Qarun, Egypt. World J Fish Mar Sci 1(1):29–39Google Scholar
  42. Monteiro SM, Rocha E, Fontaínhas-Fernandes A, Sousa M (2008) Quantitative histopathology of Oreochromis niloticus gills after copper exposure. J Fish Biol 73:1376–1392Google Scholar
  43. 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 138:326–344Google Scholar
  44. 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 490:59–72Google Scholar
  45. 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 357Google Scholar
  46. 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 48:4356–4362Google Scholar
  47. 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):365–377Google Scholar
  48. 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):228–232Google Scholar
  49. 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 68:371–381Google Scholar
  50. 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):667–678Google Scholar
  51. OECD (1992) Test no. 203: fish, acute toxicity test. OECD guidelines for the testing of chemicals, section 2. OECD Publishing, Paris, pp 9Google Scholar
  52. OECD (2000) Test no. 215: fish, juvenile growth test. OECD guidelines for the testing of chemicals. OECD, Paris, pp 16Google Scholar
  53. 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):903–912Google Scholar
  54. 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 42:41–44Google Scholar
  55. 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):180–195Google Scholar
  56. Pari L, Gnanasoundari M (2006) Influence of naringenin on oxytetracycline mediated oxidative damage in rat liver. Basic Clin Pharmacol Toxicol 98:456–461Google Scholar
  57. Peplow D, Edmonds R (2005) The effects of mine waste contamination at multiple levels of biological organization. Ecol Eng 24:101–119Google Scholar
  58. Ramzy EM (2014) Toxicity and stability of sodium cyanide in fresh water fish Nile tilapia. Water Sci 28:42–50Google Scholar
  59. 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 47:3455–3463Google Scholar
  60. 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):975–985Google Scholar
  61. 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):253–262Google Scholar
  62. 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):53–69Google Scholar
  63. 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 545–546:591–600Google Scholar
  64. 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. 26:104–117Google Scholar
  65. 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
  66. 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 53:164–176Google Scholar
  67. 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):141–150Google Scholar
  68. 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 30:327–334Google Scholar
  69. Secombes CJ, Chappell LH (1996) Fish immune responses to experimental and natural infection with helminth parasites. Annu Rev Fish Dis 6:167–177Google Scholar
  70. 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 29:31–35Google Scholar
  71. 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):519–529Google Scholar
  72. 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 16:54–57Google Scholar
  73. Soler F, Reja A, Garcia-Rubio L, Miguez MDP, Roncero V (1996) Anatomo-pathological effect of OTC in tench (Tinca tinca). Toxicol Lett 88:104Google Scholar
  74. 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. 144:55–60Google Scholar
  75. 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 58:757–764Google Scholar
  76. Sturgill MG, Lambert GH (1997) Xenobiotic-induced hepatotoxicity: mechanisms of liver injury and methods of monitoring hepatic function. Clin Chem 8(2):1512–1526Google Scholar
  77. 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):142–148Google Scholar
  78. 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):286Google Scholar
  79. Takashima F, Hibiya T (1995) An atlas of fish histology: normal and pathological features, 2nd edn. Kodensha Ltd., TokyoGoogle Scholar
  80. 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 205:185–196Google Scholar
  81. 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):708–717Google Scholar
  82. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149Google Scholar
  83. 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):1–12Google Scholar
  84. 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):9–27Google Scholar
  85. 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):e64020Google Scholar
  86. 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):785–799Google Scholar
  87. 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 55:299–304Google Scholar
  88. 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):297–325Google Scholar
  89. Wolf JC, Wolfe MJ (2005) A brief overview of nonneoplastic hepatic toxicity in fish. Toxicol Pathol 33:75–85Google Scholar
  90. 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):47–75Google Scholar
  91. 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 31:318–325Google Scholar
  92. 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 122:116–125Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sara Rodrigues
    • 1
    • 2
  • Sara C. Antunes
    • 1
    • 2
  • Bruno Nunes
    • 3
    • 4
  • Alberto Teodorico Correia
    • 2
    • 5
    Email author
  1. 1.Departamento de Biologia da Faculdade de Ciências da Universidade do Porto (FCUP)PortoPortugal
  2. 2.Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR)Terminal de Cruzeiros do Porto de LeixõesMatosinhosPortugal
  3. 3.Centro de Estudos do Ambiente e do Mar (CESAM), Campus de SantiagoUniversidade de AveiroAveiroPortugal
  4. 4.Departamento de Biologia da Universidade de AveiroAveiroPortugal
  5. 5.Faculdade de Ciências da Saúde da Universidade Fernando Pessoa (FCS-UFP)PortoPortugal

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