Skip to main content
Log in

Effects of Dietary Exposure to Sulfamethazine on the Hematological Parameters and Hepatic Oxidative Stress Biomarkers in Nile Tilapia (Oreochromis niloticus)

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Sulfamethazine (SMZ) is one of the most commonly used sulfonamide compounds in fish farming, and its physiological effects on fish are unknown. SMZ was administered to juvenile Nile tilapia (Oreochromis niloticus) at a dose level of 422 mg kg−1 body weight, for a period of 11 days, via medicated feed. Fish were divided into two groups, the control group (CG) and the group fed with SMZ in feed. The administration of SMZ did not alter the erythrograms and leukograms of the Nile tilapia. The SMZ-fed group showed the same hepatic lipid peroxidation (LPO) concentration as the CG. Nonetheless, the oral administration of SMZ raised the hepatic catalase (CAT) and glutathione S-transferase (GST) activities, the increase probably being sufficient to prevent hepatic LPO production. The oral administration of SMZ affects the hepatic GST and CAT activities of Nile tilapia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aebi H (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, 3rd edn. Academic Press, London, pp 273–286

    Google Scholar 

  • Altinordulu S, Eraslan G (2009) Effects of some quinolone antibiotics on malondialdehyde levels and catalase activity in chicks. Food Chem Toxicol 4:2821–2823

    Article  Google Scholar 

  • Amend DF, Fryer JL, Pilcher KS (1967) Comparison of oregon pellet and fish-meat diets for administration of sulfamethazine to chinook salmon. Res Briefs 13:20–25

    Google Scholar 

  • Ankeli GO (1971) Furunculosis in the redspot salmon (Oncorhynchus rhodurus) and other salmonids in holding tanks. Can Vet J 12:136–138

    CAS  Google Scholar 

  • Bergsjo T, Nafstad I, Ingebrigtsen K (1979) The distribution of 35S-sulfadiazine and 14C-trimethoprim in rainbow trout Salmo gairdneri. Acta Vet Scand 20:25–37

    CAS  Google Scholar 

  • Boyd CE (1990) Water quality in ponds for aquaculture. Auburn University, Auburn

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Caipang CMA, Berg I, Brinchmann MF, Kiron V (2009) Short-term crowding stress in Atlantic cod, Gadus morhua L. modulates the humoral immune response. Aquaculture 295:110–115

    Article  CAS  Google Scholar 

  • Carraschi SP, Cruz C, Machado Neto MP, Castro NL, Gírio ACF (2011) Eficácia do florfenicol e da oxitetraciclina no controle de Aeromonas hydrophila em pacu (Piaractus mesopotamicus). Arq Bras Med Vet Zootec 63:579–583

    Article  CAS  Google Scholar 

  • CODEX (2016) Codex Alimentarius. Veterinary drug residues in food. http://www.fao.org/fao-who-codexalimentarius/standards/vetdrugs/veterinary-drug-detail/en/?d_id=57. Accessed 08 Mar 2016

  • Cogo AJD, Siqueira AF, Ramos AC, Cruz ZMA, Silva AG (2009) Utilização de enzimas do estresse oxidativo como biomarcadoras de impactos ambientais. Nat Online 7:37–42

    Google Scholar 

  • Defroirdt T, Sorgeloos P, Bossier P (2011) Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol 14:251–258

    Article  Google Scholar 

  • Di Giulio RT, Habig C, Gallagher EP (1993) Effects of black rock harbour sediments on indices of biotransformation, oxidative stress, and DNA integrity in channel catfish. Aquat Toxicol 26:1–22

    Article  Google Scholar 

  • EC (2002) European Community. Commission Decision 2002/657/EC. Implementing council directive 96/23/EC concerning the performance of analytical methods and the interpretation of results. Off J Eur Commun 221:8–36

    Google Scholar 

  • European Commission (2010) Commission Regulation (EU) n 37/2010, 22 December 2009, on pharmacologically active substances and their classification regarding maximum residue limits in foodstuffs of animal origin. http://ec.europa.eu/health/files/eudralex/vol5/reg_2010_37/reg_2010_37_en.pdf. Accessed 10 Sep 2015

  • FAO (2012) The state of world fisheries and aquaculture. http://www.fao.org/fishery/sofia/en. Acessed 23 Mar 2015

  • Ferreira AHC, Araripe MNBA, Monteiro CAB, Lopes JB, Hararipe HGA (2012) Uso de probióticos na aquicultura: revisão. Rev Electron Nutr 9:1965–1980

    Google Scholar 

  • Gül S, Belge-Kurutas E, Yildiz E, Sahan A, Doran F (2004) Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environ Int 30:605–609

    Article  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Oxford Claredon, New York

    Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo M (2011) Fish health aspects in grouper aquaculture. Aquaculture 320:1–21

    Article  Google Scholar 

  • Hormazabal V, Rogstad A (1992) Simultaneous determination of sulphadiazine and trimethoprim in plasma and tissues of cultured fish for residual and pharmacokinetic studies. J Chromatogr 583:201–207

    Article  CAS  Google Scholar 

  • Hrubec TC, Smith SA (2010) Hematology of fishes. In: Weiss DJ, Wardrop KJ (eds) Schalm’s veterinary hematology. Blackwell, Iowa, pp 994–1003

    Google Scholar 

  • Jemec A, Tišler T, Drobne D, Sepčić K, Jamnik P, Roš M (2008) Biochemical biomarkers in chronically metal-stressed daphnids. Comp Biochem Physiol 147(C):61–68

    Google Scholar 

  • Jiang ZY, Hunt JV, Wolf SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal Biochem 202:384–389

    Article  CAS  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantification. Met Mol Biol 32:9–15

    CAS  Google Scholar 

  • Li Q, Peng S, Sheng Z, Wang Y (2010) Ofloxacin induces oxidative damage to joint chondrocytes of juvenile rabbits: excessive production of reactive oxygen species, lipid peroxidation and DNA damage. Eur J Pharmacol 626:146–153

    Article  CAS  Google Scholar 

  • Livingstone DR, Lemaire P, Matthews A, Peters LD, Porte C, Fitzpatrick PJ, Forlin L, Nasci C, Fossato V, Wootton N, Goldfarb P (1995) Assessment of the impact of organic pollutants on goby (Zostersessor ophiocephalus) and mussel (Mytilus galloprovincialis) from the Venice Lagoon, Italy, biochemical studies. Mar Environ Res 39:235–240

    Article  CAS  Google Scholar 

  • Lundèn T, Bylund G (2002) Effect of sulphadiazine and trimethoprim on the immune response of rainbow trout (Oncorhynchus mykiss). Vet Immunol Immunopathol 85:99–108

    Article  Google Scholar 

  • Malvisi J, Della Rocca G, Anfossi P, Giorgetti G (1997) Tissue distribution and depletion of flumequine after in-feed administration in sea bream (Sparus aurata). Aquaculture 157:97–204

    Article  Google Scholar 

  • MAPA (2011) Ministério da Agricultura, Pecuária e Abastecimento do Brasil. Guia de validação e controle de qualidade analítica: fármacos em produtos para alimentação e medicamentos veterinários. http://www.agricultura.gov.br/arq_editor/file/Laboratorio/Guia-de-validacao-controle-de-qualidade-analitica.pdf

  • MAPA—Ministério da Agricultura, Pecuária e Abastecimento (2014) Plano Nacional de Controle de Resíduos, Instrução normativa SDA no 11, de 07 de maio de 2014. http://www.agricultura.gov.br/arq_editor/file/CRC/IN%2011%20-%20PNCRB%202014.pdf. Accessed 10 Sep 2015

  • McCarthy DH, Stevenson JP, Salsbury AW (1974) Combined in vitro of trimethoprim and sulphonamides on fish-pathogenic bacteria. Aquaculture 3:87–91

    Article  CAS  Google Scholar 

  • Natt MP, Herrick CA (1952) A new blood diluent for counting erythrocytes and leucocytes of the chicken. Poultry Sci 31:735–738

    Article  Google Scholar 

  • Nonaka CKV, Oliveira AMG, Paiva CR, Almeida MP, Resende CP, Moraes CGO, Botelho BG, Souza LF, Dias PG (2012) Ocurrence of antimicrobial residues in Brazilian food animals in 2008 and 2009. Food Addit Contam 29:526–534

    Article  CAS  Google Scholar 

  • Nunes B, Antunes SC, Gomes R, Campos JC, Braga MR, Ramos AS, Correia AT (2014) 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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Paschoal JAR, Bicudo ÃJA, Cyrino JEP, Reyes FGR, Rath S (2012) Depletion study and estimation of the withdrawal period for oxytetracycline in tilapia cultured in Brazil. J Vet Pharmacol Ther 35(1):90–96

    Article  CAS  Google Scholar 

  • Paschoal JAR, Quesada SP, Gonçalves LU, Cyrino JEP, Reyes FGR (2013) Depletion study and estimation of the withdrawal period for enrofloxacin in pacu (Piaractus mesopotamicus). J Vet Pharmacol Ther 36:594–602

    Article  CAS  Google Scholar 

  • Poirier LA, Doerge DR, Gaylor DW, Miller MA, Lorentzen RJ, Carciano DA, Kadlubar FF, Schwetz BA (1999) An FDA review of sulfamethazine toxicity. Regul Toxicol Pharmacol 30:217–222

    Article  CAS  Google Scholar 

  • Rigos G, Zonaras V, Nikoloudaki X, Cotou E, Henry M, Varo I, Alexis M (2013) Distribution and depletion of sulfadiazine after a multiple per os dosing in gilthead sea bream (Sparus aurata) fed two different diets. Medit Mar Sci 14(2):377–383

    Article  Google Scholar 

  • Rijkers GT, Van Oosteron R, Van Muiswinkel WB (1981) The immune system of cyprinid fish. Oxytetracycline and the regulation of the humoral immunity in carp. Vet Immunol Immunopathol 2:281–290

    Article  CAS  Google Scholar 

  • Saglam N, Yonar ME (2009) Effects of sulfamerazine on selected haematological and immunological parameters in rainbow trout (Onchorhynchus mykiss, Walbaum, 1792). Aquacul Res 40:395–404

    Article  CAS  Google Scholar 

  • Samanidou VF, Evaggelopoulou EN (2007) Analytical strategies to determine antibiotic residues in fish. J Sep Sci 30:2549–2569

    Article  CAS  Google Scholar 

  • Sanchez W, Palluel O, Meunier L, Coquery M, Porcher JM, Ait-Aissa S (2005) Copper-induced oxidative stress in three-spined stickleback, relationship with hepatic metal levels. Environ Toxicol Pharmacol 19:177–183

    Article  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress, molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  CAS  Google Scholar 

  • Scott P (1993) Therapy in aquaculture. In: Brown L (ed) Aquaculture for veterinarians. Pergamon Press, Oxford, pp 131–153

    Google Scholar 

  • Tavares-Dias M, Moraes FR (2003) Características hematológicas da Tilápia rendalli Boulenger, 1896 (Osteichthyes: cichlidae) capturada em “pesque pague” de Franca, São Paulo, Brasil. Biociência J 19:107–114

    Google Scholar 

  • Valarmathi S, Azariah J (2003) Effect of copper chloride on the enzyme activities of the crab Sesarma quadratum (Fabricius). Turk J Zool 27:253–256

    CAS  Google Scholar 

  • Varó I, Navarro JC, Rigos G, Del Ramo J, Calduch-Giner J, Hernández A, Pertusa J, Torreblanca A (2013) Proteomic evaluation of potentiated sulfa treatment on gilthead sea bream (Sparus aurata L.) liver. Aquaculture 376:36–44

    Article  Google Scholar 

  • Wedemeyer G, Yasutake WT (1977) Clinical methods for the assessment of the effects of environmental stress on fish health. US Fish Wildl Serv 89:18

    Google Scholar 

  • WHO (1990) Toxicological evaluation of certain veterinary drugs residues in foods. WHO Food Additives Series 25. World Health Organization, Geneva, pp 79–93. http://www.inchem.org/documents/jecfa/jecmono/v25je01.htm. Accessed 10 Sep 2015

  • WHO (1994) Toxicological evaluation of certain veterinary drugs residues in foods. WHO Food Additives Series 33. World Health Organization, Geneva, pp 91–103. http://www.inchem.org/documents/jecfa/jecmono/v33je07.htm. Accessed 10 Sep 2015

  • Wilhelm Filho D, Torres MA, Tribess TB, Pedrosa RC, Soares CHL (2001) Influence of season and pollution on the antioxidant defenses of the cichlid fish acará (Geophagus brasiliensis). Braz J Med Biol Res 34:719–726

    Article  CAS  Google Scholar 

  • Wood JW (1968) Diseases of Pacific salmon, their prevention and treatment. Washington Department of Fisheries, Olympia

    Google Scholar 

  • Wood EM, Yasutake WT, Johnson HE (1957) Acute sulfamethazine toxicity in young salmon. The Prog Fish Cultur 19(2):64–67

    Article  Google Scholar 

  • Xu W, Zhang G, Zou S, Li X, Liu Y (2007) Determination of selected antibiotics in the Victoria Harbour and the Pearl River, South China using high-performance liquid chromatography-electrospray ionization tandem mass spectrometry. Environ Pollut 145:672–679

    Article  CAS  Google Scholar 

  • Yildiz HY, Altunay S (2011) Physiological stress and innate immune response in gilthead sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax) exposed to combination of trimethoprim and sulfamethoxazole (TMP-SMX). Fish Physiol Biochem 37:401–409

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Funding for this study was provided by São Paulo Research Foundation (FAPESP; Grant # 2013/50452-5) and by the Brazilian National Council for Scientific and Technological Development (CNPq; Process No. 305390/2013-9). The authors sincerely thank the reviewers whose comments and suggestions helped to improve the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernanda Garcia Sampaio.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sampaio, F.G., Carra, M.L., Jonsson, C.M. et al. Effects of Dietary Exposure to Sulfamethazine on the Hematological Parameters and Hepatic Oxidative Stress Biomarkers in Nile Tilapia (Oreochromis niloticus). Bull Environ Contam Toxicol 97, 528–535 (2016). https://doi.org/10.1007/s00128-016-1837-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-016-1837-0

Keywords

Navigation